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Published bimonthly—January, March, May, July, Symposium Papers September, November 409 Anti-quality components in forage: Overview, significance, and economic impact by Copyright 2001 by the Society for Range Vivien Gore Allen and Eduardo Segarra Management 413 Structural anti-quality characteristics of range and pasture plants by Emilio A. INDIVIDUAL SUBSCRIPTION is by membership in Laca, Lisa A. Shipley, and Edward D. Reid the Society for Range Management. 420 Lignin and fiber digestion by Kenneth J. Moore and Hans-Joachim G. Jung LIBRARY or other INSTITUTIONAL SUBSCRIP- TIONS on a calendar year basis are $95.00 for the 431 Herbivore response to ani-quality factors in forages by K.L. Launchbaugh, F.D. United States postpaid and $112.00 for other coun- Provenza, and J.A. Pfister tries, postpaid. Payment from outside the United States should be remitted in US dollars by interna- 441 Animal health problems caused by silicon and other mineral imbalances by Henry tional money order or draft on a New York bank. F. Mayland and Glenn E. Shewmaker

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PRINTED IN USA Acting Managing Editor Associate Editors ELAINE E. GRINGS CAROLYN HULL SIEG JEFF BURWELL YUGUANG BAI USDA-ARS S.W. Science Complex 445 Union Blvd., Ste 230 Dept. Plant Sciences Fort Keogh-LARRL 2500 South Pine Knoll Lakewood, Colorado 80228 University of Saskatchewan Route 1, Box 2021 Flagstaff, Arizona 86001 (303) 986-3309 51 Campus Drive Miles City, Montana 59301 Fax: (303) 986-3892 Saskatoon, Saskatchewan FAISAL K. TAHA e-mail address: S7N 5A8 MARSHALL HAFERKAMP Director of Technical Programs [email protected] CANADA USDA-ARS Biosaline Agriculture Center Editor/Copy Editor Fort Keogh-LARRL P.O. Box 14660 GARY FRASIER/JO FRASIER ROBERT R. BLANK Route 1, Box 2021 Dubai, U.A.E. 7820 Stag Hollow Road USDA-ARS Miles City, Montana 59301 Loveland, Colorado 80538 920 Valley Road ALLEN TORELL e-mail address: Reno, Nevada 89512 MITCHEL McCLARAN New Mexico State University [email protected] University of Arizona Agricultural Economics Production Editor KLAAS BROERSMA 301 Biological Science East Box 3169 PATTY RICH Agriculture and Agri-Food Canada Tucson, Arizona 85721-0001 Las Cruces, New Mexico 88003 Society for Range Management 3015 Ord Rd. 3059A Hwy 92 Kamloops, British Columbia PAUL OHLENBUSCH MIMI WILLIAMS Hotchkiss, Colorado 81419-9548 V2B 8A9 CANADA Kansas State University USDA-ARS e-mail address: Department of Agronomy 22271 Chinsegut Hill Rd [email protected] JOE E. BRUMMER Throckmorton Hall Brooksville, Florida 34601-4672 Book Review Editor Mt. Meadows Res. Ctr. Manhattan, Kansas 66506 DAVID L. SCARNECCHIA P.O. Box 598 Dept of Natural Res. Sci. Gunnison, Colorado 81230 ROBERT PEARCE Washington State University Resources Concept Pullman, Washington 99164-6410 DAVID GANSKOPP 340 N. Minnesota St. e-mail address: USDA-ARS Carson City, Nevada 89703 [email protected] HC-71 4.51 HWY 205 Electronic JRM Editor Burns, Oregon 97720 MICHAEL H. RALPHS M. KEITH OWENS USDA-ARS Texas A&M University ROBERT GILLEN Poisonous Plant Lab Research Center USDA-ARS 1150 E 1400 N 1619 Garner Field Road Southern Plains Range Res. Sta. Logan, Utah 84341-2881 Ulvade, Texas 2000 18th Street e-mail address: Woodward, Oklahoma 73801 [email protected] J. Range Manage. 54: 314Ð321 July 2001 Ranching motivations in 2 Colorado Counties

HELEN IVY ROWE, E.T. BARTLETT, AND LOUIS E. SWANSON, JR.

Authors are research assistant and professor, Department of Rangeland Ecosystem Science and Chair and professor, Department of Sociology, Colorado State University, Fort Collins, Colo. 80523.

Abstract Resumen

The objectives of this Colorado study were to assess primary Los objetivos, bajo este estudio en el estado de Colorado, reasons ranchers choose to stay or sell the ranch, compare the fueron: a) determinar las razones más importantes de los pro- motivations for ranching between a traditional agriculturally ductores agrícolas para continuar con su unidad de producción o based county and a rapidly developing county, and assess venderla, b) comparar las aspiraciones de producción entre una whether factors such as length of tenure, fiscal dependency on agricultura tradicional regional y una agricultura especializada, ranching, and dependency on public lands play roles in decisions y c) determinar si factores como el tiempo de posesión, grávamen to sell. Personal interviews were conducted with 37 ranchers. fiscal y el uso de terrenos comunales son decisivos para vender While land use conversion occurs for a wide variety of reasons, las unidades de producción. El método de estudio fue por entre- lack of heirs and detrimental public policy were important rea- vistas personales realizándose 37 con productores agrícolas. Las sons given for selling ranches. Responses showed Routt County razones más importantes para la venta de la unidades de produc- (a rapidly developing county) ranchers were more likely to sell ción incluyen el cambio en el uso de la tierra, la falta de due to land use conversion related issues than Moffat County herederos y una política pobre sobre el uso de terrenos comu- ranchers (p = 0.056). Ranchers with a longer legacy on their land nales. Los resultados mostraron que los productores especializa- reported that profitability, having likely heirs, and continuing dos del Condado Routt fueron más propensos a la venta de las tradition enhanced their reasons to stay. Groups more “at risk” propiedades que los tradicionales del Condado Moffat (P=.056). of selling were non-homesteading ranchers close to retirement, Los productores agrícolas con muchos años en la explotación larger ranches, and ranchers dependent on ranching for income reportaron que las ganancias, la existencia de herederos, y la with declining profits. Large ranch owners experiencing land use tradición incrementa las razones para continuar produciendo. conflicts with non-ranchers and ranchers modestly dependent on Los grupos propensos para vender fueron productores próximos public forage experiencing changes in public policy regulations al retiro, productores grandes en la escala, y productores con and land use conflicts also indicated a higher proclivity to sell. ganancias descendentes. Además, fueron propensos de venta los Noting how groups of ranchers are impacted by different propietarios grandes con conflictos con otro tipo de productores changes can help refine community efforts related to land use y con productores agrícolas modestos dependientes de los cam- conversion and create more thoughtful policy measures. bios en la regulación de terrenos comunales para producción de forraje, y por conflictos con el uso de terrenos comunales. El factor más influyente en el ámbito de los productores agrícolas es el Key Words: rangeland policy, regulations, survey, public lands, impacto de cambios diversos que pueden ayudar a afinar los urban development, land use conversion esfuerzos comunitarios relacionados con cambios de uso de la tierra y con la creación de políticas de desarrollo más eficientes.

Colorado farm and ranch land has declined by over 600,000 ha since 1987 with over 80,000 ha lost to development and other uses in 1996 alone (Colo. Dept. of Agr. 1998). Land use conver- tradition, way of life, rancher image, and place attachment all sion from agriculture to development results not only in a loss of motivate ranchers to retain ownership (Smith and Martin 1972, agricultural production, but also fragments and degrades wildlife Harper and Eastman 1980, Grigsby 1980, Bartlett et al. 1989, habitat and reduces open space. The current political climate Gentner 1999, Liffman et al. 2000). Selling the ranch itself is a advocates the conservation of ranches to protect against fragmen- market transaction, but the land may represent a way of life, liveli- tation and support open space, agriculture, and ecological integri- hood, and family legacy, making the decision to sell difficult. ty (Liffman et al. 2000). By asking ranchers why they stay or Previous studies indicate that for some ranchers, financial man- leave, we discover the underlying causes of land use conversion agement tends to be a primary factor shaping a decision to stay in to better inform policy makers. ranching. Smith and Martin (1972) identify a group characterized by their conspicuous consumption and speculative attitudes. Such individuals buy ranches as an investment and plan to sell for a Motivations to continue ranching higher price. These investors enjoy the “rancher image” and Past research has indicated that factors other than profit or eco- lifestyle, often as absentee landowners, until land values rise and nomic incentives influence decisions that shape a ranch family’s reach a threshold that triggers a decision to sell. One group of 4 decisions to stay on the land. Researchers have found that family, defined by Bartlett et al. (1989) expressed a willingness to sell the ranch, but remained due to “difficulties in selling in current Manuscript accepted 20 Oct. 2000. market conditions.” This group rated land ethic and family life

314 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 slightly lower than the other groups. For Hart (1991, p. 35), in perhaps an over- Moffat had 1.5% (CSU Dept. of Agr. and this group it appears that economic con- statement to make a point, stresses the Res. Econ. 1995). siderations weigh more heavily in the sell impact of urbanization on agriculture: Recreationists flock to Routt County for or stay question. Young and Shumway “Urban expansion always wins, because outdoor pursuits including skiing at the (1991) support these findings, suggesting farmers are not able to pay urban costs for popular Steamboat Springs Ski Resort. The that factors including dependency on land. The basic question of land conver- tourism industry in Routt County supports ranch income, desire to increase net worth, sion is not whether, but when.” 147 related establishments for lodging, the perception of cattle production as a amusement/recreation, and eating/drinking. business venture, and the ability to obtain Moffat County has only 37 such business- off-ranch employment all increased the Hypotheses es. Population growth in Routt has been probability that ranchers would perceive double that in Moffat. Routt County had a themselves to be profit maximizers. For In the course of this research, several growth rate of 18.3% between 1990 and these kinds of ranchers, the business tends assumptions concerning ranchers’ reasons 1997, while Moffat County increased by to be a determining factor in decisions to either stay in or leave ranching were 8.9% (Yampa Valley Partners 1999). The over the fate of the ranch. considered. This paper addresses 5 alter- overall cost of living has also risen dispro- native hypotheses. portionately for the 2 counties according Motivations to sell a ranch 1. Raising a family and maintaining tradi- to a cost of living survey in Colorado. This Land use conversion issues, specifically, tion are primary determinants for stay- survey composed a numeric scale using 1 the “impermanence syndrome” and loss of ing in ranching. as the average for the state based on the “critical mass”, appear related to decisions 2. Due to greater development pressure, costs for 59 goods. Routt County ranks to sell or continue in ranching (Heimlich ranchers in an area undergoing rapid highest in the “above average” category at and Anderson 1987, Huntsinger and development will be more likely to sell 1.096, whereas Moffat falls into the “low” Hopkinson 1996, Hart 1991, Berry and Plaut than those in a more rural, agricultural cost of living category at .870 (Garner and 1978). Urbanization can lead to an “imper- area. Eckert 1999). Property values in Routt manence syndrome” among ranchers. This 3. Respondents with a longer legacy on County have leapt from $291.2 million in results in declining investment in agricul- the land will be less likely to sell. 1993 to $419.2 million in 1997. For the ture and reduction in intensity of manage- 4. Financial issues will be more important same years, Moffat County crept from ment and practices because ranchers to larger ranches and for those depen- $358.7 million to $367 million (Yampa become convinced that their land will be dent on ranch income for their liveli- Valley Partners 1999). These county dif- sold for non-agricultural uses (Heimlich hood. ferences allow us to compare the effects of and Anderson 1987). Speculation leads to 5. Federal public land and environmental growth between rapidly developing Routt idling farmlands or a conversion to other policies will affect public land depen- County and traditional Moffat County. types of agriculture that are less intensive dent ranchers more than ranchers with in time and capital (Berry and Plaut 1978, less public land. Study Sample Conklin and Lesher 1977). Hart (1991) A sampling frame of 242 Federal permit- found that as urbanization increased tees in the 2 counties was derived by com- around a ranch, succeeding generations Methods piling the Bureau of Land Management were more likely to sell. (BLM) and United States Forest Service Once a ranching community loses its Thirty-seven (37) personal interviews (USFS) permittee lists and condensing “critical mass” of ranchers, ranching may with public land ranchers in the Colorado duplicate listings. The sample size of 26 become less economically viable counties of Routt and Moffat were con- was calculated using a variance of .15 (Huntsinger and Hopkinson 1996, Hart ducted. Ranchers were randomly selected taken from Redmond et al. (1992), a study 1991, Heimlich and Anderson 1987, Berry from a compiled list of all of the federal relevant to the research presented here. The and Plaut 1978). As the numbers of agri- land grazing permittees of the 2 counties. sample was stratified into 7 strata based on culturalists declines, their political and number of AUMs and type of livestock economic clout erodes and non-farm pref- grazed on public land, increasing the sam- erences for community gain political legit- Study area ple size. Every effort was made to inter- imacy in local governance. New ordi- To evaluate the effects of urbanization view each of these ranchers, but replace- nances are passed designed to regulate we compare 2 counties, one experiencing ments were selected for those that refused, such things as noise of machinery and rapid development, Routt County, and the were not actively running their ranch, or tractors on roads. Demand for requisite other a traditional agricultural county, who lived too far outside the counties. suburban infrastructures by new residents Moffat County. Adjacent counties in the Thirty-seven personal interviews were can increase the tax load for ranchers northwestern corner of Colorado, these 2 completed. (Berry and Plaut 1978, Lisansky and Clark counties were selected for study based 1987). Fewer ranchers in an area makes it upon their relative proximity and similar cultural history, while differing in their Rancher Survey more difficult to pool labor and resources Drawing on questionnaires of Liffman at times of heavy work (Huntsinger and growth rates and level of development. et al. (2000), Gentner (1999), Smith and Hopkinson 1996). Furthermore, commer- Routt County comprises 60,000 ha and Martin (1972), and Bartlett et al. (1989), cial businesses that provide agricultural 49% of its land is either state or federally the authors constructed a survey exploring supplies and services are more likely to go owned. Moffat has 1.2 million ha with motivations for staying in ranching versus out of business as their ranching clients 63% of that in public ownership (Frank leaving ranching. The survey was pre-test- disappear (Flora et al. 1992, Danbom 1997). In 1992, Routt County had 3.4% 1995, Starrs 1998). income dependence on agribusiness, and ed on ranchers in Larimer County, Colo. The questionnaire consisted of 7 general

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 315 conceptual questions with 9 follow up The sample included a number of ranch- In addition to asking about motivations questions. The general questions covered ers that had public land in 1 of the coun- to continue ranching, we asked why ranch- the following categories of information: ties, but they resided either in the other ers stayed where they are rather than sell- quality of life, dependency on ranching for county or nearby across the Wyoming boring the ranch to buy another one else- income, motivating factors for continuing der. To refine the comparison, only Routt where. Responses to this were grouped in to ranch, factors influential in selling the County residents were considered in the 11 categories. The top answers for both ranch, motives for staying in the area, and Routt County category. Any rancher not counties combined (with 36 responses) public policy issues. Most questions were residing in Routt was placed in the Moffat indicated that tradition (50%) and attach- measured on a Likert scale with 1 indicat- County category (Table 1). ment to the ranch setting (39%) are both ing least important, 2 less important, 3 important reasons to continue ranching in moderately important, 4 more important, the area. The response “tradition” means and 5 most important. The authors chose Results and Discussion the rancher stays here because the ranch to group the Likert scale responses into has been in the family for 1 or more gener- either more important (4 and 5 answers) Hypothesis One: Motivations for ations. “Place attachment”, as defined by and less important (1, 2, and 3) to simplify the survey responses, encompasses love the comparisons. Follow up questions staying in ranching were asked if the rancher responded with a This research partly supported the first for life style and for the natural beauty of 4 or a 5 to any of the questions in the hypothesis. Family and tradition influences the area as well as simply not wanting to motivations to sell category. came out as important for over 50% of the leave. Ranchers develop a connection to The Federal Policy Impacts Section of sample. However, way of life outranked their ranch, the landscape, associated the questionnaire provided the indepen- family and tradition as reasons to continue wildlife, and the beauty of the area. The dent variables to test hypotheses 3 through ranching. The data also reveal that attach- Likert Scale responses support this enthu- 5, including the number of animal unit ment to the location of the ranch influences siasm for place attachment; 87% of the months (AUMs) and private land acres, ranchers to stay in agriculture. Profit ranchers rated living near natural beauty the degree of public land dependency, and ranked lower as a motivational factor. as more important. whether or not the rancher’s family home- Ranchers report that they stay in ranch- steaded in that county. Since 2 ranchers ing primarily because they enjoy the work Reasons for selling the ranch did not respond to the Federal Policy and way of life (Table 2). Over 50% of the The corollary to the first hypothesis, that Impacts Section, only 35 survey results respondents rated family and traditional deteriorating the quality of raising a fami- were used to test hypotheses 3 through 5. reasons as most important. Family and tra- ly or altering traditions would motivate For Hypothesis One, simple frequencies dition categories include: “A ranch is a ranchers to sell, is reflected in the respons- showed which factors ranchers chose as good place to raise your family”, consis- es (Table 2). Ranchers say that having no most important for staying or leaving tency with family tradition, culture and one to take over the ranch would be the ranching. Hypotheses 2 through 5 required values, living closer to family, “ranching most compelling reason to sell the ranch the use of the Chi-square statistic using is part of our Western heritage and should (57%). Having no one to take over the cross tabs. Due to difficulty in finding sig- be preserved”, “ranch has been in the fam- nificant differences with the small sample ranch incorporates both loss of family and ily for generations and you maintain it to size and the minimal consequences of tradition, since with no one to inherit the making a type I error, we considered dif- carry on the family tradition”, and to have ranch by definition indicates a severing ferences of p < 0.10 to be significant. a business to pass on to your children with family tradition. Of the 21 respon- (Table 2). dents that marked this factor as more/most important, 13 (62%) responded that it is Defining Groups To cross tab the groupings, continuous Table 1. Ranch characteristics, Routt and Moffat Counties, Colo., 1998. data was categorized for each hypothesis including homesteading history, county, Characteristics1 with characteristic dependence on ranching for income, size (%) of ranch by private acreage, size of ranch Dependent on ranching for livelihood 57 by number of AUMs, and dependence on Homesteaded 58 public lands. Ranches were re-categorized Rate quality of life great-excellent 87 under each group (Table 1). Private land Ranch in Routt County 24 acreages and AUMs were divided along Ranch in Moffat County 76 obvious splits in the data. Public land Small ranch: owns up to 1000 acres private land 37 dependency was determined by dividing Medium ranch: owns 1280Ð8000 acres private land 43 the number of public land AUMs by the Large ranch: own 15,000Ð80,000 acres private land 20 total number of AUMs, multiplied by a 2 hundred. Because public land dependency Small ranch: 90Ð707 total AUMs /year 40 had an even spread, we split it into quar- Medium ranch: 1068Ð8264 total AUMs/year 46 tiles and defined these groups as negligi- Large ranch: 14,604Ð39,412 total AUMs/year 14 ble, modest, moderate and high public Negligible public land dependency: 1Ð11% 23 land dependency. Homesteading and Modest public land dependency: 14Ð34% 26 dependency on ranching for income elicit- Moderate public land dependency: 35Ð62% 26 ed yes/no responses in the survey and High public land dependency: 69Ð96% 26 were categorized as such. 1Not all ranchers answered each category; thus, n varied from 35Ð37. 2Total AUMs includes federal, private, and privately leased forage, but does not include hay fed.

316 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 2. More important reasons to keep ranching or to sell responses listed in decreasing proportions, all respondents, 1999.

Survey Questions (n = 37) Responded 4/5 n You continue to ranch because: (%) You enjoy animal husbandry 97 37 You enjoy the ranching way of life 95 37 You like ranch work 89 34 A ranch is a good place to raise your family 87 37 Allows you to live near natural beauty 87 36 Ranching allows you independence 87 37 Owning land and a ranch is consistent with your family's traditions, culture and values 81 37 Living on a ranch allows you to live closer to your family 81 37 Ranching is part of our Western heritage and should be preserved 76 37 The ranch has been in the family for generations and you maintain it to carry on the family tradition. 57 37 You continue ranching so you will have a business to pass on to your children 50 36 It would be difficult to obtain a job outside the ranch 27 37 You own land and a ranch primarily for environmental purposes 25 36 Living on a ranch allows you to live closer to your friends 22 36 Profit 19 37 Conservation easements or land trusts made the property taxes and my debt more manageable. 18 28 Other 32 12 You would sell the ranch because: You have no one to pass the ranch on to 57 37 Public policy regulations. 49 37 You don't like the way the community is changing. 32 37 Ranching is no longer profitable, you start losing money 32 37 Increase in property value. 30 37 Land use conflicts with non ranchers 30 36 Nearby ranches being converted to other uses. 22 37 Retirement 11 36 Prefer to improve income through selling the ranch. 11 37 Perception that society no longer appreciates ranching 5 37 Prefer to improve income through an off-ranch job 0 36 Other 30 11 Why do you choose to stay here rather than sell the ranch and buy another one elsewhere? Ranch has been in the family for one or more generations 49 37 Place attachment 38 Moving does not solve problems in ranching 19 37 Good place to ranch 19 37 1For this open-ended question, percentages refer to response frequencies for each category. more/most likely that a family member on public lands (35%). Some of the fear of years. The ESA outranked the other will take over for them in the future. cuts is probably rooted in the BLM envi- issues, followed by elk management, Seven (33%) thought it would be moder- ronmental impact reports being done on water quality, multiple use, and water ate to very unlikely that a family member all allotments at the time of the interviews rights. Rancher comments revealed a neg- would take over and 1 (5%) did not know in summer 1999. Thirty percent of the 18 ative undercurrent towards the ESA. if it would be taken over by a family mem- respondents indicated concern about gov- Ironically these Federal policies may serve ber. Thus, roughly 19% (7/37) of the sam- ernment control over land use, usually to accelerate ranch sales, creating an even ple will likely sell the ranch because they range improvements, on both public and greater threat to policy goals aimed at lack viable heirs. private lands. Twenty percent cited multi- slowing land use conversion and preserv- Of particular significance to policy mak- ple-use as a threat. These respondents feel ing wildlife habitat. ers, public policy regulations were cited as that recreationists and hunters would Eleven people provided other reasons for the second most important reason to sell restrict their own ability to use the public why they would sell the ranch. Seven indi- (18 respondents or 49% of the sample lands by creating problems (trespass, van- cated that a loss of health would cause them marked more/most important). This ques- dalism, etc) and demanding more of the to sell the ranch. Other answers were aging, tion clearly implied federal not local poli- public land exclusively for themselves. county regulations, and loss of family. cies. The follow-up question asked these Though not evoked in the open-ended fol- 18 respondents which policies most con- low-up question, the Endangered Species cerned them. Answers were categorized Act (ESA) also seems to be a concern to Hypothesis 2: Routt County into 10 groups. The most frequent ranchers. Each respondent ranked a set of versus Moffat County response was cuts in allowed grazing use 5 issues according to which would most Ranchers in Routt County were more likely affect his or her ranch in the next 5 likely to sell their ranches due to land con-

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 317 Table 3. More important reasons for ranching or selling, Moffat versus Routt Counties, 1999. counties (Table 4). Significantly more ranchers in Routt than in Moffat County Survey questions County feel that ranch difficulties may exist on 1 Moffat (n=28) Routt (n=9) p-value any ranch, therefore moving will not Independent variables 2: (%) (%) resolve the problem. This finding may Did your family homestead in the area? 44 63 .329 reveal that Routt County ranchers perceive Do you depend on ranching for your income? 64 33 .103 their profession as more inherently You continue to ranch because: plagued with difficulty than do their more Owning land and a ranch is consistent with your traditional Moffat County neighbors. family’s traditions, culture and values 75 100 .096* Comparing the reasons ranchers contin- Living on a ranch allows you to live closer to your family 75 100 .096* ue may reveal interesting sets of character- It would be difficult to obtain a job outside the ranch 36 0 .036** istics for each county. Routt County Profit 25 0 .096* ranchers focus more on the family, and Conservation easements or land trusts made the less on profit (Table 3). Moffat County property taxes and my debt more manageable 10 43 .046** ranchers seem to care more about profit You would sell the ranch because: and are less concerned about family as a If you had no one to pass the ranch on to 54 67 .49 reason to ranch. Public policy regulations 50 44 .772 You don’t like the way the community is changing 29 44 .376 Hypothesis 3: Legacy on the Land Ranching is no longer profitable, you start losing money 39 11 .116 We hypothesized that respondents with a Land use conflicts with non ranchers 36 11 .16 longer legacy on the land would be less Increase in property value 32 22 .571 likely to sell. Respondents with a longer legacy on the land were defined as home- Nearby ranches being converted to other uses 14 44 .056* steaders; their family had originally home- Why do you choose to stay here rather than sell steaded in the area. To support this hypoth- the ranch and buy another one elsewhere? Been in the family for one or more generations 54 33 .145 esis, homesteaders would have marked fewer sell factors as more/most important Place attachment 36 44 .783 and more reasons to continue as more/most Moving does not solve problems in ranching 11 44 .029** important. In general this was not strongly Good place to ranch 22 11 .466 supported by the data. However, home- *, ** Significant at the 0.10 and 0.05 levels respectively. steaders considered themselves less likely 1 2 p-value results for x test. to sell the ranch at retirement (Table 4). 2For the independent variable questions, percentages refer to positive responses in each category. Relative newcomers to ranching may view the ranch as more of a profession from version issues than in Moffat County The question “Why do you choose to which to retire rather than a way of life that (Table 3). Routt County residents ranked stay here rather than sell the ranch and buy continues into retirement. “Nearby ranches being converted to other another one elsewhere?” elicited signifi- Homesteaders place more importance on uses” the second most common reason to cantly different responses between the 2 sell. This marked a significant difference economics, as measured by profit and dif- with Moffat, which marked this factor as seventh. Land use conversion influencing Table 4. More important reasons for homesteaders to sell or continue ranching, Routt and ranchers to sell supports the large body of Moffat Counties, 1999. literature indicating that urbanization causes ranchers to sell because of a lessen- Survey questions Homesteaders Non-homesteaders p-value1 ing expectation of the persistence of agri- (n=21) (n=15) culture as a viable use in an area, and the You continue to ranch because: (%) (%) loss of “critical mass” (Huntsinger and You continue ranching so you will have a Hopkinson 1996, Hart 1991, Heimlich and business to pass on to your children 65 33 .064* Anderson 1987, Berry and Plaut 1978, Living on a ranch allows you to live closer Conklin and Lesher 1977). to your family 67 100 .013** Also worthy of note were the reactions It would be difficult to obtain a job to easements and land trusts in the 2 coun- outside the ranch 38 7 .032** ties. Although rated low in both counties, significantly more people rated these as Profit 29 0 .023** important reasons to continue ranching in The ranch has been in the family for Routt County than in Moffat County generations and you maintain it to (Table 3). Generally, only the people hold- carry on the family tradition 81 20 .000*** ing land trusts themselves considered You would sell the ranch because: easements important. This result is per- Retirement 0 27 .014** haps not surprising considering land trusts Independent variable 2 are more common in Routt County. Do you depend on ranching for Locally based conservation policies your income? 62 47 .364** appear to have a positive influence on *, **, *** Significant at the 0.10, 0.05 and 0.01 levels respectively. 1p-value results for x2 test.. ranchers’ willingness to keep their land 2 from being developed. For the independent variable, percentages refer to positive responses in each category.

318 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 5. Significant correlations between independent variables using Pearson’s r-values. that as size of ranch increases, land use conflicts with non-ranchers become a Independent variables greater motivation to sell (Table 6). As County Dependency on ranching Homesteading Size (number of land around large ranches is converted to for income AUMs) non-ranching uses, resulting conflicts may Public land dependency Ð.325*3 influence larger ranch owners to sell. Size of ranch .349**2 Ð.430***3 (by number of AUMs) 2 3 4 Hypothesis 5: Public Lands Ranchers Size of ranch .485*** Ð.504*** .700*** Ranchers more highly dependent on (by number of acres public lands for forage did not show sig- of private land) nificantly more likelihood to sell due to *, **, *** Significant at the 0.10, 0.05 and 0.01 levels respectively. 1 public policy than those with lower depen- Homesteaders have a higher dependency on public land than non-homesteaders. 2Rancher in Routt County had fewer AUMs and owned less private land than ranchers in Moffat County. dency. It turns out, however, that it is the 3Larger ranches, as defined both by number of AUMs and number of private acres, are more dependent on ranching for modestly (14Ð34% of their total forage is their livelihood. 4 from public land) dependent ranchers who Ranches with large number of AUMs also held higher acreages of private land. are likely to sell due to public policy regulations and land use conflicts (Table 7). ficulty in finding a job off the ranch, as strongly about staying in ranching than This occurrence may be explained by sea- reasons to stay than do the more recent their counterparts. sonal dependence. Ranchers in the mod- non-homesteaders (Table 4). Perhaps estly dependent category have enough homesteaders ingrained in their successors Hypothesis 4: Financial Concerns dependency to be affected by changes but the paradigm of the ranch as a business The results tend to support the assump- may have fewer options in the face of such that needs to support the family needs. tion that owners of larger ranches and changes. These ranchers may depend on Members of older ranching families may ranchers more dependent on ranching for public forage for a specific period of time have less outside work experience or pro- their income are more concerned with when no other forage is available whereas fessional training which keeps them tied to profit. Ranches with more AUMs, more larger landholders may have more flexibil- the ranch. Newcomers to the trade may private land, and ranchers who declared ity. Another possibility is that ranchers in have more job options and financial themselves dependent on ranching for the modestly dependent category are self- resources, allowing them to be somewhat their income (3 highly correlated vari- selected (i.e., their fear of being harmed more economically sacrificial in their atti- ables, Table 5) stated that they would be by policy changes has already led them to tudes towards ranching. They know they much more likely to sell if the ranch start- reduce their public land). are giving up a higher standard of living ed losing money than their counterparts It stands to reason that public land for ranching and perhaps are more (Table 6). This same set of ranchers agrees dependent ranchers, many of whom are resigned to being “satisficers” (Smith and that difficulty in obtaining a job off of the homesteaders, would place more value on Martin 1972). ranch contributes to their reasons to con- tradition as a reason to continue on the Not surprisingly, homesteaders also find tinue ranching. Ranchers dependent on ranching also cited profit as a significantly ranch. The data shows a correlation passing the ranch on to children and main- more important reason to continue ranch- between homesteaders and increased taining tradition as reasons to stay (Table ing than non-dependent ranchers. dependency on public lands (Table 5). 4). Taken together, given a profit and will- Another finding, with strong implica- Further, public land dependent ranchers ing heirs, homesteaders may feel more tions for land use conversion policy, was

Table 6. More important reasons to sell reported by ranches of different sizes and income dependencies, Routt and Moffat Counties, 1999.

Survey questions AUM1 Dependency3 Acreage4 Small Medium Large p2 Low High p Small Medium Large p You continue to ranch because: (%) (%) (%) (%) (%) (%) (%) (%) Ranching is no longer profitable, you start losing money 14 25 100 .001*** 13 48 .024** 15 20 86 .002*** Perception that society no longer appreciates ranching 0 0 40 .002*** —5 — — 0 0 29 .014** Land use conflicts with non-ranchers 0 44 60 .007*** — — — 15 20 71 .019** Public policy regulations 21 69 60 .030** — — — — — — — You continue to ranch because: It would be difficult to obtain a job outside the ranch 21 19 80 .023** 6 43 .013** 8 33 57 .057* You enjoy animal husbandry 100 100 80 .062* — — — — — — — Allows you to live near natural beauty — — — — — — — 100 73 100 .049** Profit — — — — 19 29 .086*———— *, **, *** Significant at the 0.10, 0.05 and 0.01 levels respectively . 1Size of ranch categorized by the total number of AUMs, not including hay feed. 2p-value of given category for x2 test. 3Level of dependency on ranch income for their livelihood as defined by respondents. 4Size of ranch categorized by the number of owned private acres on the ranch. 5Non-significant values not included in this table.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 319 Table 7. More important reasons to stay or sell the ranch at different levels of dependence on pub- Decisions ranchers make about selling lic forage, Routt and Moffat Counties, 1999. their ranch directly affect the use of their land and can contribute to land use con- Levels of public land dependency version into subdivisions or other develop- Survey questions Negligible Modest Moderate High p-value ments. Conversely, if ranchers do not sell You continue to ranch because: their land, land use conversion is slowed. Owning land and a ranch is consistent with your family’s traditions, culture and values 50 89 100 78 .065* Diminished quality of ranch life, public policy regulations, the inability to pass the The ranch has been in the family for generations and you maintain it to carry 0 67 89 67 .002** ranch on to future generations, land use on the family tradition conversion and its associated conflicts, Ranching is part of our Western and, for some groups, loss of profitability, heritage and should be preserved 50 67 100 89 .064* may induce ranchers to sell. You would sell the ranch because: Land use conflicts with non-ranchers 0 56 22 33 .083* Public policy regulations 25 89 44 33 .036** Literature Cited *, **,Significant at the 0.10, and 0.05 levels respectively. 1p-value results for x2 test.. American Farmland Trust. 2000. The last roundup? How public policies facilitate rural rate tradition as an important factor for most important reason for selling a ranch, sprawl and the decline of ranching in staying on the ranch (Table 7). federal programs may inadvertently con- Colorado’s Mountain valleys, a summary report, 19 p. tribute to land use conversion by acceler- Bartlett, E. T., R. G. Taylor , J. McLean and ating the rate of ranch sales. J. G. Hof. 1989. Motivations of Colorado Conclusions The federal policies specified by ranch- ranchers with federal grazing allotments. J. ers as most pressing were cuts in grazing, Range Manage. 42:454Ð457. government regulations concerning land Berry, D. and T. Plaut. 1978. Retaining agri- Ranchers in northwestern Colorado use management, multiple use conflicts, cultural activities under urban pressure: a emphasize career fulfillment, tradition, and the Endangered Species Act (ESA). A review of land use conflicts and policies. place attachment and family as reasons recent study done in Routt County Policy Sci. 9:153Ð178. they intend to stay in agriculture. Profit (American Farmland Trust 2000) Colorado Department of Agriculture. 1998. and market factors rank relatively low as Colorado Agricultural Statistics Service described more subtle impacts that federal reasons to stay. Respondents list inheri- Report 1996-1997. Denver, Colo. policies are having on ranchers’ ability to tance issues as the most important reason Colorado State University (CSU), continue ranching in the face of increasing to sell, followed by public land policy reg- Department of Agricultural and Resource land use conversion. This American ulations, economic issues, and community Economics. 1995. Colorado's farm and food Farmland Trust (2000) study found that system: its contribution to the state economy change. Age and loss of health may also tax incentives for buying a second home, in 1992. Colorado State University be important reasons to sell. allowing 35-acre subdivided parcels to Cooperative Extension Resource Center, Generally, this study did not find that continue to be taxed at agricultural land executive summary of bulletin #551A. Fort rapid development alone would cause rates even given their weak ties to agricul- Collins, Colo. ranchers to sell, although land use conver- Conklin, H. E. and W. G. Lesher. 1977. ture, and zoning laws that permit subdivid- sion in developing counties might increase Farm-value assessment as a means for reducing land into 35-acre or greater parcels ranchers’ likelihood of selling. Land use ing premature and excessive agricultural dis- without a review process hastens land use conversion can lead to conflicts with investments in urban fringes. Amer. J. Agr. conversion from agriculture into residen- neighbors, a factor that large landowners Econ. 59(4):755Ð759. tial properties. Federal and local policies Danbom, D. B. 1995. Born in the country: a indicated would influence them to sell. supporting conservation easements help history of rural America. Johns Hopkins Homesteaders are less likely to sell the sustain commercial ranching but could be University Press, Baltimore, Md. ranch at retirement, and profit and heirs to strengthened. The American Farmland Flora, C. B., Jan L. Flora, Jacqueline D. inherit the ranch tends to bolster their con- Spears, Louis E. Swanson, Mark B. Trust study (2000) emphasizes that poli- viction to stay. Financial considerations Lapping and Mark L. Weinberg. 1992. cies designed to protect public lands are influential in decisions to continue in Rural communities legacy and change. increase development pressure on private agriculture for respondents with larger Westview Press, Boulder, San Francisco, and ranchlands by luring more recreationists to Oxford. ranches, dependence on ranching for an the area, while also limiting the potential Frank, T. 1997. Colorado land ownership sum- income, and with a higher dependence on supply of land for development. mary by county (acres) table. Colorado public lands. Modestly dependent rather Moreover, cutting grazing rights or sub- Department of Agriculture, Resource than highly dependent public land ranch- stantially increasing grazing fees “will Analysis Section. ers indicated an inclination to sell their Garner, E. H. and J. B. Eckert. 1999. Cost of almost certainly mean additional pressure ranch due to public policy regulations and living differences in Colorado: a summary of to subdivide and convert working ranches conflict with non-ranchers. county-level estimates for 1998. Dept. of into recreational properties” (American This research presents a potential irony Agr. Econ., Colorado State University Farmland Trust 2000, p. 14). The findings Cooperative Extension. for policy makers who advocate strong of this study in combination with the http://www.colostate.edu/Depts/CoopExt/PU environmental and other land-use pro- results found here should alert policy mak- BS/CONSUMER/xcm211.html. grams on both public and private land. ers to the potential vulnerability of ranch- Gentner, B. 1999. Characteristics of public Given the finding that respondents rank ers to an array of federal policies, both land grazing permittees. Masters Thesis. changes in public policy as the second Dept. of Agr. and Res. Econ., Oregon State overt and indirect. Univ., Corvalis, Ore.

320 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Grigsby, T. L. 1980. Today's riders of the pur- Liffman, R. H., L. Huntsinger and L. C. Starrs, P. 1998. Let the cowboy ride: cattle ple sage: symbols, values, and the cowboy Forero. 2000. To ranch or not to ranch: ranching in the American West. Johns myth. Rangelands 2:93Ð96. home on the urban range? J. Range Manage. Hopkins University Press, Baltimore, Md. Harper, W.M and C. Eastman. 1980. An 53:362Ð370. Yampa Valley Partners. 1999. Yampa Valley evaluation of goal hierarchies for small farm Lisansky, J. and G. Clark. 1987. Farmer-non- Partners community indicators project, 1999 operators. Amer. J. Agr. Econ. 62:742Ð747. farmer conflicts in the urban fringe: will report, l. Colorado Healthy Communities Hart, J. F. 1991. Farming on the edge: saving right-to-farm help? p. 219Ð230. In: William Initiative. Craig, Colo. family farms in Marin County, California. Lockeretz (ed.), Sustaining Agriculture Near Young, K. D. and C. R. Shumway. 1991. Univ of Calif. Press, Berkeley, Calif. Cities. Soil and Water Cons. Serv., Cow-calf producers' perceived profit maxi- Heimlich, R. E. and W. D. Anderson. 1987. Washington D.C. mization objective: a logit analysis. So. J. Dynamics of land use change in urbanizing Redmond, J. T., E. T. Bartlett, P. Gutierrez Agr. Econ. 23:129-36. areas: experience in the Economic Research and V. G. Carande. 1992. Costs of grazing Service, 135Ð154. In: William Lockeretz on federal lands and private leases: a 1991 (ed.), Sustaining Agriculture Near Cities. Colorado comparison. Dept of Rangeland Soil and Water Cons. Serv., Washington Ecosystem. Sci., Colorado State Univ. Coop. D.C. Exten., 28 p. Huntsinger, L. and P. Hopkinson. 1996. Smith, A. J. and W. E. Martin. 1972. Viewpoint: sustaining rangeland landscapes: Socioeconomic behavior of cattle ranchers a social and ecological process. J. Range with implications for rural community devel- Manage. 49:167Ð173. opment in the West. Amer. J. Agr. Econ. 54:217Ð225.

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JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 321 J. Range Manage. 54: 322Ð329 July 2001 Economic analysis of using sheep to control leafy spurge

DEAN A. BANGSUND, DAN J. NUDELL, RANDALL S. SELL, AND F. LARRY LEISTRITZ

Authors are research scientist, Department of Agribusiness and Applied Economics, North Dakota State University, Fargo, N.D., 58105, research specialist, Hettinger Research Extension Center, Hettinger, N.D., 58639, and research scientist and professor, respectively, Department of Agribusiness and Applied Economics, North Dakota State University, Fargo, N.D.

Abstract Resumen

Leafy spurge (Euphorbia esula L.), a widely established exotic, “Leafy spruge” (Euphorbia esula L.) Es una maleza exótica, noxious, perennial weed, is a major threat to rangeland and wild- perenne y nociva que esta ampliamente establecida y es una land in the Upper Great Plains. A deterministic, bioeconomic amenaza para los pastizales y de la parte superior de las model, incorporating relationships between sheep grazing and Grandes Planicies. Se desarrollo un modelo determinístico bioe- leafy spurge control, grass recovery, and forage consumption by conómico incorporando las relaciones entre el apacentamiento cattle, and expected costs and returns from sheep enterprises was de ovinos y el control de “Leafy spruge”, la recuperación de developed to evaluate the economic viability of using sheep to zacates, el consumo de forraje por bovinos y los costos y retornos control leafy spurge. Various scenarios were developed depicting esperados de la empresa de ovinos. El modelo se desarrollo para likely situations facing cattle ranches adding a sheep enterprise evaluar la viabilidad económica de utilizar ovinos para controlar for leafy spurge control. Two levels of flock profitability, one “Leafy spruge”. Se desarrollaron varios escenarios visualizando based on a level of proficiency achieved by established sheep escenarios posibles que enfrentan los ranchos de ganado bovino ranches and one substantially lower than typically achieved in y agregando una empresa ovina para el control de “Leafy the sheep industry, were combined with debt and no-debt to rep- spruge”. Dos niveles de rentabilidad del rebaño, uno basado en el resent best- and worst-case scenarios, respectively. In the best- nivel de eficiencia alcanzado por ranchos borregueros estableci- case situations, using sheep to control leafy spurge was economi- dos y uno substancialmente menor que la eficiencia típicamente cal in all of the scenarios examined. In the worst-case situations, lograda por la industria de ovinos, se combinaron con deuda y the economics of using sheep to control leafy spurge were mixed no deuda para representar el mejor y peor de los escenarios across the scenarios examined. Leafy spurge control with poor respectivamente. En todos los escenarios examinados, en las flock proficiency, high fence expense, and unproductive range- situaciones que representaron el mejor de los casos, el utilizar land generally was not economical. Situations with low fencing ovinos para controlar “Leafy spruge” fue económicamente costs, moderately productive rangeland, and poor flock profi- viable. En las situaciones del peor de los casos la economía de ciency resulted in less economic loss than no treatment. Actual utilizar ovinos para el control de “Leafy spruge”se mezclo a returns from leafy spurge control for most ranchers will likely través de los escenarios examinados. El control de “Leafy fall between the extremes examined. spruge” con una pobre eficiencia del rebaño, altos gastos de cer- cos y un pastizal improductivo generalmente no fue económico. Situaciones con bajos costos de cercado, pastizales moderada- Key Words: Euphorbia esula L., grazing, economics mente productivos y baja eficiencia del rebaño resultaron en menos perdidas económicas que el no tratamiento. Los retornos actuales del control de “Leafy spruge”en la mayoría de los ran- Leafy spurge (Euphorbia esula L.), first introduced in North chos probablemente caería entre los extremos examinados. America in the 19th century, was found in North Dakota in 1909, and was considered a threat to rangeland in the Upper Great Plains as early as 1933 (Hanson and Rudd 1933). The weed currently infests large amounts of untilled land in the Plains and established infestations on untillable land (Lym 1997). As a Mountain states and creates serious economic losses for land result, leafy spurge control must be approached as a long-term owners and ranchers (Leitch et al. 1996). The nature of leafy management problem since (1) the weed cannot be eradicated spurge and the detrimental effects of the weed on untilled land economically with current technology,1 (2) uncontrolled infesta- have been documented (Watson 1985, Lajeunesse et al. 1995, tions have detrimental long-term consequences for grazing land, USDA 1995). and (3) time lags often exist between treatments and returns. Current control technologies are ineffective in eradicating Although several control methods are available to land managers, each control approach has limitations in its applicability and Funding was provided by the Agricultural Research Service through the effectiveness in treating leafy spurge infestations. Grazing with Cooperative State Research Service of the U.S. Department of Agriculture and the sheep and goats, while known to be effective in controlling leafy North Dakota Agricultural Experiment Station. spurge since the 1930s (Helgeson and Thompson 1939, Helgeson The authors thank Drs. K. Sedivec and D. Kirby, Department of Animal and Range Sciences, and Dr. R. Lym, Department of Plant Sciences, North Dakota State University, Fargo, N.D. for development of model components used in the 1Leafy spurge has been eradicated using tillage activities in combination with study. fertilization in cropland (Lym and Messersmith 1993). These techniques are not Manuscript accepted 1 Oct. 2000. readily feasible in most grazing land situations.

322 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 and Longwell 1942), has lacked widespread adoption (Sedivec et al. 1995, Sell et al. 1999a). The apparent inability of biological agents to establish on many leafy spurge infestation sites (Bangsund et al. 1999), the economic and environmental restrictions and constraints associated with herbicides, and the ineffectiveness of cultural controls (e.g., mowing, burning) have led to a renewed interest by land owners in evaluating sheep grazing as a leafy spurge control method. Sheep will graze leafy spurge, and if used properly, reduce infestation density and prevent infestation spread over time (Helgeson and Longwell 1942, Johnston and Peake 1960, Bowes and Thomas 1978, Lacey et al. 1985, Sedivec et al. 1995). Since sheep will not eradicate leafy spurge and controlling leafy spurge with sheep requires grazing over several years, using sheep as a leafy spurge control must be considered a long-term management strategy. Preliminary research on the economic feasibility of using sheep to control leafy spurge has not evaluated the long- term benefits or costs of grazing control strategies (Sedivec et al. 1995, Williams et al. 1996). Since leafy spurge control must be approached as a long-term management problem, information on the economic feasibility of leafy spurge control methods must also be based on long-term treatment benefits and costs (Bangsund et al. 1996). A goal of this study was to provide economic information for assessing long-term Fig. 1. Economic evaluation model of the control of leafy spurge using sheep grazing. grazing control strategies for leafy spurge. Sell et al. (1999b) identified economic model design was adapted from Bangsund research remains sensitive to those key information on leafy spurge controls as et al. (1996). assumptions and relationships. one of the most desired types of weed con- The model included the relationship trol information sought by ranchers, local Model Development between leafy spurge control using sheep decision makers, and public land man- Documented effects of long-term sheep and forage recovery by cattle, sheep enter- agers in the Upper Great Plains. grazing on infestation canopy cover, rate prise budgets, leafy spurge growth (patch of spread, grass rejuvenation (i.e., increase expansion) component, and an economic in grass production within the infestation analysis component. Leafy spurge expan- Methods resulting from grazing controls), and cattle sion was based on a model adapted from grazing recovery rates (i.e., amount of Bangsund et al. (1993). Expected control A deterministic, simulation model was available grass cattle will consume upon was modeled as a function of time (i.e., developed to evaluate the economics of reduction in leafy spurge canopy cover) years grazed), assuming the same flock is using sheep to control leafy spurge and were not available. The relationships used used to graze leafy spurge annually, prop- determine which variables influence the in this study were developed from a com- er stocking rates are maintained, and graz- economic feasibility of various grazing bination of short-term data from unpub- ing controls are properly implemented strategies (Fig. 1). The economic feasibili- lished grazing trials and input from range (Fig. 2) (personal communication, Lym, ty of using sheep to control leafy spurge and weed scientists. Sufficient data from Kirby, Sedivec 1999). Control was defined was evaluated using selected scenarios grazing trials were not available to devel- as a percentage of the previous year’s which reflect likely situations facing cattle op control relationships over a 10-year canopy cover {e.g., canopy cover(year 2)- ranches adding a sheep enterprise for leafy period. To conduct a long-term economic [canopy cover(year 2) x control(year 2)] = spurge control. The annual difference evaluation of sheep grazing, it was neces- canopy cover(year 3)}. between treatment expenses, and the value sary to largely rely on the assumptions and The rate of infestation spread under of grazing outputs recovered and retained “best estimates” of range and weed scien- sheep grazing was modeled as a function through treatment were discounted over 10 tists. Until these relationships are refined of the number of years of control. Since years to provide a long-term perspective through additional grazing trials, much of the model can accommodate various rates for various control scenarios. General the economic analysis provided by this of expansion, reduction in the rate of

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 323 cover and grass production was based on the ability of leafy spurge to out compete native vegetation and create near monocultures (Watson 1985, Messersmith et al. 1985). Because leafy spurge control was based on the number of consecutive years of sheep grazing, the rate of forage consumed by cattle within the infestation was also modeled as a function of the number of years of sheep grazing (Fig. 5). Since sheep will not eradicate leafy spurge, forage consumption (as a percent of carrying capacity) by cattle within leafy spurge infestations was assumed to remain below that of uninfested rangeland. Some minor avoidance to grazing within the infestation may exist and grass production within the infestation would likely remain below that of uninfested rangeland, due to competition by leafy spurge roots. Grass production within the infestation was modeled to increase over time as infestation canopy cover was reduced; however, constraints on the increase in grass production were incorporated to prevent forage production from equaling the productivity of uninfested rangeland. The model assumes that cattle are properly stocked for the carrying capacity of the pasture.

Sheep Enterprises Fig. 2. Projected rate of leafy spurge expansion and leafy spurge canopy cover reduction with sea- Several possible sheep enterprise sce- sonal sheep grazing (personal communication, Lym, Kirby, and Sedivec 1999). narios were modeled after typical operations in western North Dakota (Nudell et spread was estimated as a percentage of that as leafy spurge infestations increase in al. 1998). Breeding stock was commercial actual spread (Fig. 2). Infestation spread canopy cover, grass production within -1 Western White-faced ewes and black- in the analysis was 0.6 m year . those infestations decreases (Fig. 4). The faced rams. Ewes were assumed to lamb The relationship between lost cattle relationship between leafy spurge canopy grazing capacity and infestation canopy cover was estimated from consultation with range scientists and was based on a linear function of canopy cover (Fig. 3). Grazing losses for cattle in leafy spurge- infested pastures stem from avoiding forage within infestations and from decreased herbage production within dense infestations (Lym and Messersmith 1985, Lym and Kirby 1987, Kronberg et al. 1993). Once a leafy spurge infestation represents about one-third of the canopy cover (top growth) within the patch, cattle grazing within the infestation has been eliminated. The model assumes that a 30% canopy cover would roughly translate to about 80 to 130 stems m-2. The approach for estimating the amount of forage consumed by cattle as a result of leafy spurge treatment was based on the amount of forage available within leafy spurge infestations (as a percentage of uninfested carrying capacity) and the amount of available carrying capacity that Fig. 3. Assumed reduction in cattle grazing within leafy spurge infestations (personal communica- cattle would utilize. The model assumes tion, Lym, Kirby, and Sedivec 1999).

324 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Fig. 4. Postulated relationship between grass production and leafy spurge Fig. 5. Assumed carrying capacity utilization by cattle within leafy spurge infestation canopy cover (personal communication, Lym, Kirby, and infestations controlled with seasonal sheep grazing (personal communi- Sedivec 1999). cation, Lym, Kirby, and Sedivec 1999). in February, with spring lambs fed during the management of the existing cattle es financed for 3 years. Annual interest the summer and marketed in the fall as enterprise. One scenario was based on rate was 10%. Thus, budgets for 8 combi- slaughter lambs. Replacements were flock proficiency equal to that of estab- nations of flock proficiency, size, and debt raised. Only ewes and rams were used for lished North Dakota sheep producers, were compiled. leafy spurge control. Sheep budgets were whereas the other scenario was based on The number of sheep needed for leafy prepared using an enterprise analysis pro- flock proficiency substantially less than spurge control generally decreases after gram for sheep producers (Hughes et al. typically achieved by established sheep the first 3 years and again after 7 years of 1997). producers (Table 1) (Nudell et al. 1998, a seasonal grazing control program Variations in the sheep enterprises were N.D. Farm and Ranch Business (Sedivec et al. 1995). Stocking rate reduc- limited to flock proficiency (e.g., lambing Management 1999). tions for sheep were estimated as a per- rate, weaning weight, death loss), size, Sheep enterprises were further catego- centage of the initial stocking rate. and debt. Because flock proficiency will rized by size and debt. Small flocks had 60 Budgets for each production scenario were likely vary depending upon the manage- ewes and large flocks had 200 ewes. Half estimated annually over a 10-year period ment ability, experience, animal hus- of the sheep enterprises had no debt, to accommodate changing flock size and bandry, and willingness and ability of meaning that breeding stock, facilities, and corresponding changes in debt (Table 2). ranchers and producers to devote equipment were either already available or Production coefficients, selling prices, and resources to flock management, 2 levels of purchased without financing. The enter- variable expenses per ewe were not adjust- flock proficiency were considered. The prises with debt had 50% of the equipment ed over the 10-year period. addition of a sheep enterprise for leafy and facility requirements financed for 5 Fencing expenses included modifying spurge control was assumed to not affect years and 50% of breeding stock purchas- an existing fence or constructing new fence. Material costs were based on 1999 Table 1. Sheep enterprise coefficients and characteristics. retail prices in western North Dakota. Modified fencing was based on adding 2 barb wires to an existing 3- or 4-wire Level of Flock Proficiency Characteristic/Coefficients Good Poor fence. New fence was based on 6 barb wires, including requirements for line and Selling characteristics Market lamb price ($ kg-1) 1.65 1.65 corner posts. Pastures were assumed to be Cull ewe price ($ kg-1) 0.77 0.77 relatively flat and square. Five percent of Cull ram price ($ hd-1) 50.0 50.0 total fencing expense was charged to the Wool price ($ kg-1) 1.10 1.10 enterprises annually. Market lamb weight (kg hd-1) 54.4 47.6 Several key assumptions were made in Lamb weaning weight (kg hd-1) 22.7 20.4 the preparation of the sheep budgets. Cull ewe weight (kg hd-1) 68.0 68.0 Economic charges (depreciation) were not -1 Wool production (kg ewe-1 year ) 4.5 4.5 included for machinery and equipment Flock Proficiency that generally overlaps with cattle produc- Conception rate (%) 100 100 tion (e.g., stock trailers, loader tractor, Lambing rate (%) 150 100 pickup). All pastures were assumed to Lamb death loss (%) 10 12 have water present in sufficient quantities Ewe death loss (%) 5 5.5 Replacement rate (%) 20 20 and available to sheep. Water maintenance Ewes per ram 33 33 and pasture expenses were not included. Selling prices for lambs, cull ewes, and

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 325 Table 2. Annual net revenues to unpaid labor, management, and equity per ewe for various sheep enterprise scenarios over a 10-year period, western North Dakota.

With Debt No Debt Small1 Large1 Small Large Fencing2 Fencing Fencing Fencing Years New Modify New Modify New Modify New Modify ------($) ------Good Proficiency ------1 & 2 23.55 28.85 39.94 41.00 30.57 33.80 44.41 45.06 3 15.48 20.78 31.57 32.63 22.49 25.72 36.05 36.70 4 & 5 19.36 28.19 30.28 32.05 24.94 30.33 31.66 32.74 6 24.94 30.33 31.66 32.74 24.94 30.33 31.66 32.74 7 19.53 24.92 26.66 27.74 19.53 24.92 26.66 27.74 8Ð10 14.56 22.65 29.67 31.29 14.56 22.65 29.67 31.29

------Poor Proficiency ------1 & 2 Ð12.12 Ð6.82 Ð4.56 Ð3.50 Ð5.22 Ð1.99 Ð0.18 0.47 3 Ð22.99 Ð17.69 Ð15.71 Ð14.65 Ð16.08 Ð12.85 Ð11.34 Ð10.69 4 & 5 Ð14.69 Ð5.86 Ð2.96 Ð1.19 Ð9.11 Ð3.72 Ð1.58 Ð0.50 6 Ð9.11 Ð3.72 Ð1.58 Ð0.50 Ð9.11 Ð3.72 Ð1.58 Ð0.50 7 Ð17.22 Ð11.83 Ð9.37 Ð8.29 Ð17.22 Ð11.83 Ð9.37 Ð8.29 8Ð10 Ð16.88 Ð8.79 Ð3.64 Ð2.02 Ð16.88 Ð8.79 Ð3.64 Ð2.02 1 Small flocks based on 60 ewes and large flocks based on 200 ewes. Flock reductions occurred in years 4 and 8. 2 New fencing expenses based on constructing a 6Ðwire fence, with requirements for line and corner posts. Modified fence included adding 2 barb wires to an existing 3Ð or 4Ðwire fence. New fence cost was estimated at $831 kmÐ1. Modified fence cost was estimated at $159 kmÐ1. wool represented a 5-year average of N.D. able. In the event that an existing grazing (N.D. Agricultural Statistics Service, vari- prices (N.D. Agricultural Statistics strategy results in more loss than without ous issues). Leafy spurge infestation Service, various issues). Net returns to control, a “do nothing” strategy or one canopy cover was limited to 5, 15, and unpaid labor, equity, and management for employing other methods (i.e., herbicides, 30%, which represented low (17% loss), the various sheep enterprises with debt biological agents, combined controls) moderate (50% loss), and high (100%) ranged from ($12.12) to $41.00 ewe-1 in might be optimal. grazing losses within the infestation, year 1 of the 10-year budgeting period A mixed-species, seasonal grazing respectively. Treatment benefits and costs (Table 2). Net returns for debt-free sheep approach was modeled based on sheep were discounted annually at 4%. enterprises ranged in year 1 of the 10-year grazing leafy spurge infested pastures for budgeting period from ($5.22) to $45.06 4 consecutive months. One ewe can be ewe-1 (Table 2). added per cow without reducing cattle Results production (Umberger et al. 1984, Glimp 1988, Nelson et al. 1992, Sedivec et al. Results from the model provided a Treatment Scenarios 1995). Adding sheep at a rate of 2.5 ewes The model was structured to assess -1 quantitative look at the long-term econom- ha of leafy spurge was assumed to not ic feasibility of adding a sheep enterprise control scenarios by (1) comparing only violate the rule of allowing one ewe per control costs with control benefits (i.e., to control leafy spurge under a variety of cow to a given pasture. The stocking rate plausible situations facing landowners in classic economic cost/benefit approach) for cattle was assumed to increase over and (2) determining potential overall loss- the Upper Great Plains. The model also time because of improved levels of leafy was used to assess the influence of the es with control (using sheep) vs losses spurge control. The change in forage pro- without control (i.e., least-loss or cost- magnitudes of various economic and phys- duction for cattle was measured in AUMs ical variables on returns from treatment. effective approach). Grazing scenarios and assumed (1) ranchers adjusted cattle where cumulative discounted annual bene- stocking rates or grazing duration to fits are greater than cumulative discounted accommodate the increase in grazing out- Benefit-Cost Analysis annual costs are economically feasible2. In put, (2) initial cattle stocking rates were For control scenarios including good the second approach, grazing scenarios appropriate for the land before leafy flock proficiency, positive net returns that are not economical (i.e., discounted spurge treatment, and (3) sheep stocking from leafy spurge control were substantial. costs greater than discounted benefits) rates were reduced over time. Total net returns (discounted treatment may still result in less economic loss than Although a number of scenarios were returns less discounted treatment costs) incurred without control. Under those con- used to evaluate the economics of using from leafy spurge control using sheep, ditions, using grazing controls would be sheep to control leafy spurge over a wide with rangeland carrying capacities of 0.5 economically advisable, provided more range of possibilities, several variables AUMs ha-1, ranged from $303 to $541 ha-1 economical control options were not avail- were held constant across all analyses. of leafy spurge over a 10-year period, Pasture size was limited to 141.6 ha. depending upon fencing obligations, debt, 2 Uncontrolled infestation spread was limit- and flock size. With rangeland carrying The concept of financial feasibility (i.e., con- -1 -1 straints on or availability of resources and cash flow ed to 0.6 radial m year and infestations capacities of 1.9 AUMs ha , total dis- needed for flock, equipment, building, and fencing were assumed to increase in canopy cover counted net returns from leafy spurge con- purchases) was not examined. Other constraints, such by 1.5% annually without treatment. trol ranged from $339 to $647 ha-1 of leafy -1 as availability of labor, were not addressed. Grazing outputs were valued at $15 AUM spurge over a 10-year period (Table 3).

326 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 3. Total discounted net returns per hectare over a 10-year period, control of leafy spurge using sheep under seasonal grazing.

20.2Ðha Infestation 101.2Ðha Infestation Infestation Canopy Cover (%) Infestation Canopy Cover (%) Carrying 5 15 30 5 15 30 5 15 30 5 15 30 Capacity ÐÐÐÐÐÐ Modified Fence ÐÐÐÐÐÐ ÐÐÐÐÐÐÐ New Fence ÐÐÐÐÐÐÐ ÐÐÐÐÐÐ Modified Fence ÐÐÐÐÐÐ ÐÐÐÐÐÐÐ New Fence ÐÐÐÐÐÐÐ ------($) ------AUMs haÐ1 ------good flock proficiency with no debt ------0.5 415 424 438 361 370 384 518 527 541 501 511 525 1.0 426 445 474 372 391 420 529 548 576 513 532 560 1.5 438 467 510 384 412 455 541 569 612 525 553 595 2.0 450 488 545 396 434 491 553 590 647 536 574 630

------good flock proficiency with debt ------0.5 376 386 400 303 313 327 488 497 511 466 475 489 1.0 388 407 436 315 334 363 499 518 547 478 496 525 1.5 400 428 471 327 355 398 511 539 582 489 517 560 2.0 412 449 507 339 377 434 523 560 617 501 538 595

------poor flock proficiency with no debt ------0.5 Ð68 Ð59 Ð45 Ð122 Ð113 Ð99 Ð26 Ð17 Ð2 Ð42 Ð33 Ð19 1.0 Ð57 Ð38 Ð9 Ð111 Ð92 Ð63 Ð14 4 33 Ð30 Ð12 17 1.5 Ð45 Ð17 26 Ð99 Ð70 Ð27 Ð3 25 68 Ð19 9 52 2.0 Ð33 5 62 Ð87 Ð49 8 9 46 103 Ð7 30 87

------poor flock proficiency with debt ------0.5 Ð106 Ð97 Ð82 Ð179 Ð170 Ð155 Ð55 Ð46 Ð31 Ð77 Ð67 Ð53 1.0 Ð94 Ð75 Ð47 Ð167 Ð148 Ð120 Ð43 Ð25 4 Ð65 Ð47 Ð18 1.5 Ð82 Ð54 Ð11 Ð155 Ð127 Ð84 Ð32 Ð4 39 Ð54 Ð26 17 2.0 Ð70 Ð33 24 Ð144 Ð106 Ð48 Ð20 17 74 Ð42 Ð5 52

For control scenarios including poor $163 ha-1 when comparing small with Factors Influencing Returns from flock proficiency, net returns from leafy large infestations. Control spurge control were sensitive to rangeland Many factors may influence the eco- productivity and leafy spurge canopy nomics of using sheep to control leafy cover. Total net returns from leafy spurge Least-loss Analysis Least-loss analysis compares economic spurge. One of the biggest factors influ- control, with rangeland carrying capacities encing returns from leafy spurge control, -1 losses incurred if a leafy spurge infestation of 0.5 AUMs ha , ranged from $(179) to when a sheep enterprise is added to an $(2) ha-1 of leafy spurge over the 10-year was uncontrolled to losses incurred with control. Where economic losses with treatment existing ranch, would be enterprise period, depending upon fencing obliga- are more than the economic losses incurred returns. When enterprise returns were pos- tions, debt, and flock size. With rangeland itive, discounted net returns from leafy -1 without control, the treatment program or carrying capacities of 1.9 AUMs ha , total strategy would not be recommended. spurge control were positive in all of the net returns from leafy spurge control treatment scenarios examined. In some -1 The good flock proficiency scenarios ranged from $(144) to $103 ha of leafy had positive enterprise returns, which cases, economic returns from leafy spurge spurge (Table 3). resulted in positive discounted net returns control were substantial. When sheep Generally, discounted net returns from from control. Thus, least-loss analyses enterprise returns were negative (because leafy spurge control were about $30 to $57 were not conducted for those scenarios. of assumed poor flock proficiency, Table -1 ha higher for scenarios having no debt vs Least-loss analyses were conducted for the 2), other factors determined the economics those with debt (Table 3). Over a 10-year poor flock proficiency scenarios. of control. period, net returns from leafy spurge con- Over a 10-year period, most sheep graz- Large infestations were more economi- -1 trol were $64 ha less for scenarios with ing scenarios with high rangeland produc- cal to treat than small infestations, based new fence vs modified fence scenarios tivity and high leafy spurge canopy cover on the fundamental assumptions used in -1 with small infestations and were $19 ha resulted in less economic loss than with no this study. Fencing costs per hectare were less with large infestations. Discounted net control (Table 4). Many of the grazing modeled to be less with larger infestations, -1 returns ha from leafy spurge control were scenarios with new fence and low leafy since overall pasture size was fixed across higher with large infestations (101.2 ha) vs spurge canopy cover would not be recom- infestation sizes. In reality, per ha fencing small infestations (20.2 ha) across all sce- mended, although most scenarios with costs for a 101.2-ha infestation could be new fence and high leafy spurge canopy narios. In a 10-year period, discounted net the same as for a 20.2-ha infestation. cover could be recommended for all but returns from large infestations compared Because some efficiencies in sheep pro- the least productive rangeland. In a 10- with small infestations increased by $42 to duction occur when moving from small $111 ha-1 for all scenarios with modified year period, none of the small flock scenarios would be recommended at range- flocks (e.g., 50 ewes) to larger flocks (e.g., fence. For all scenarios with new fence 200 ewes), enterprise returns improved over the same period, net returns from land carrying capacities of 0.494 AUMs ha-1 or less (Table 4). with flock size. Thus, lower per ewe fenc- leafy spurge control improved by $82 to ing costs and more favorable enterprise

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 327 Table 4. Least-loss analysis1 of the control of leafy spurge using sheep under seasonal grazing.

20.2Ðha Infestation 101.2Ðha Infestation Infestation Canopy Cover (%) Infestation Canopy Cover (%) Carrying 5 15 30 5 15 30 5 15 30 5 15 30 Capacity ÐÐÐÐÐÐ Modified Fence ÐÐÐÐÐÐ ÐÐÐÐÐÐÐ New Fence ÐÐÐÐÐÐÐ ÐÐÐÐÐÐ Modified Fence ÐÐÐÐÐÐ ÐÐÐÐÐÐÐ New Fence ÐÐÐÐÐÐÐ AUMs ha-1 ------poor flock proficiency with no debt ------0.5 no no no no no no no yes yes no no yes 1.0 no yes yes no no yes yes yes yes no yes yes 1.5 no yes yes no no yes yes yes yes yes yes yes 2.0 yes yes yes no yes yes yes yes yes yes yes yes

------poor flock proficiency with debt ------0.5 no no no no no no no no yes no no no 1.0 no no yes no no no no yes yes no no yes 1.5 no yes yes no no yes yes yes yes no yes yes 2.0 no yes yes no no yes yes yes yes yes yes yes 1In scenarios where discounted net returns from using sheep to control leafy spurge are negative, least-loss analysis indicates if using sheep grazing to control leafy spurge would result in less economic loss than if the leafy spurge infestation was left uncontrolled. A “yes” implies that the scenario will result in less economic loss than no treatment. A “no” implies that the scenario will result in more economic loss than no treatment. returns were major reasons that returns some scenarios that sheep grazing of leafy densities. Discounted net returns improved from control were more favorable with spurge would be uneconomical. when treatment scenarios were increased larger infestations. The added expense for new fence had a from 10- to 15-year periods. Returns in the Returns from control improved as leafy much greater effect on discounted net various periods would be sensitive to spurge canopy cover and the resulting for- returns for controlling small infestations changes in the discount rate. age suppression increased. As grazing (expense was divided among fewer ha). losses for cattle increase, potential returns For example, with small infestations, dis- from leafy spurge control also increase. counted net returns from control improved Conclusions This relationship directly influenced the about $64 ha-1 when compared to scenar- amount of grazing recovery that could be ios with modified fence. Similarly, with The basic premise for this study was expected from leafy spurge control. large infestations, returns from control -1 that sheep would be used to control leafy Returns from leafy spurge control improved by only $19 ha when compared spurge in rangeland by adding a sheep improved proportionally to changes in to scenarios with modified fence. enterprise to an existing ranch. Sheep grazing recovery. Since sheep grazing was grazing as a leafy spurge control method only evaluated using relatively large infes- Alternative Scenarios was economical across many enterprise tations, the value of grazing retention (i.e., Additional treatment scenarios were scenarios. In many of the scenarios with grazing output retained by preventing examined, although not presented for sake negative sheep enterprise returns, the ben- infestation spread) was a minor compo- of brevity. Twice-over rotational grazing efits of leafy spurge control outweighed nent of overall returns from treatment. systems were somewhat less economical the negative enterprise returns. Higher infestation densities and levels of than seasonal grazing strategies, due to In addition to economic criteria, other canopy cover would affect net returns reduced leafy spurge control and higher factors, such as labor and financial con- from leafy spurge control if grass recovery fencing costs (i.e., added cost for internal straints, need to be considered before and forage available within the infesta- fences). However, over a 10-year period, implementing a grazing control strategy. tions differed from the levels/relationships the difference between discounted net Even though returns may be positive for used in this study. returns from rotational and seasonal graz- many control scenarios, they may not be Returns from control were directly pro- ing strategies did not substantially influ- sufficient to adequately compensate for portional to rangeland productivity. Thus, ence the economics of using sheep to con- unpaid inputs. If these constraints do not holding all other factors constant, returns trol leafy spurge. prohibit adding a sheep enterprise to an were greater on more productive range- Leasing sheep for leafy spurge control existing ranch, the economics of using land. Similarly, holding all factors con- may be an alternative to adding a sheep sheep grazing to control leafy spurge stant, returns change as AUM values enterprise to an existing ranch. Lease rates appear favorable. change. -1 -1 above $1 head month did not provide The economics of using sheep to control Enterprise debt affected discounted net positive net returns in many of the control leafy spurge were sensitive to the grazing returns from leafy spurge control. The scenarios examined. Lease rates of $1 recovery rates assumed in this study. level of debt used in this study had suffi- head-1 month-1 would likely result in posi- Long-term research over a wide range of cient influence on returns from control tive net returns from control in many treat- treatment conditions is needed to refine (about $30 to $57 ha-1 over a 10-year peri- ment scenarios and provide less economic the control responses assumed in this od) to affect decisions regarding the eco- loss than no treatment across a range of study. Additional refinement in those rela- nomics of using sheep to control leafy treatment scenarios. tionships would add confidence to the spurge. The effects of added debt were Different time periods were also exam- study results. most influential in the poor flock profi- ined. Discounted net returns from treat- Several factors can influence costs and ciency scenarios. When enterprise returns ment were not as favorable in a 5-year returns from using sheep grazing to con- were negative, increased expense from period, largely because sheep grazing trol leafy spurge. As a result, a careful additional enterprise debt was sufficient in requires several years to reduce infestation

328 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 evaluation using site- and rancher-specific Kronberg, S.L., R.B. Muntifering, E.L. N.D. Agricultural Statistics Service. 1995- inputs would be recommended before Ayers, and C.B. Marlow. 1993. Cattle 1999. North Dakota agricultural statistics. implementing sheep grazing as a leafy avoidance of leafy spurge: A case of condi- N.D. Agr. Stat. Serv., N.D. State Univ., and spurge control method. tioned aversion. J. Range Manage. USDA, Fargo, N.D. 46(4):364Ð366. N.D. Farm and Ranch Business Lacey, C.A., P.K. Fay, R.G. Lym, C.G. Management. 1999. 1998 annual report. Messersmith, B.Maxwell, and H.P. Alley. N.D. Farm and Ranch Business Manage., Literature Cited 1985. The distribution, biology, and control Bismarck, N.D. of leafy spurge. Cooperative Ext. Circ. 309. Nudell, D., H. Hughes and T. Faller. 1998. Bangsund, D.A., F.L. Leistritz, and J.A. Mont. State Univ., Bozeman, Mont. Critical control points for profitability in Leitch. 1999. Assessing economic impacts Lajeunesse, S., R. Sheley, R. Lym, D. sheep production. N.D. Agr. Res., N.D. State of biological control of weeds: The case of Cooksey, C. Duncan, J. Lacey, N. Rees, Univ., Fargo, N.D. leafy spurge in the northern Great Plains of and M. Ferrell. 1995. Leafy spurge: biolo- Sedivec, K., T. Hanson and C. Heiser. 1995. the United States. J. Environ. Manage. gy, ecology, and management. Bull. No. W- Controlling leafy spurge using goats and 56:35Ð43. 1088. Mont. State Univ., Bozeman, Mont. sheep. Ext. Pub. R-1093. N.D. State Univ., Bangsund, D.A., J.A. Leitch, and F.L. Leitch, J.A., F.L. Leistritz, and D.A. Fargo, N.D. Leistritz. 1996. Economics of herbicide con- Bangsund. 1996. Economic effect of leafy Sell, R.S., D.A. Bangsund, and F.L. Leistritz. trol of leafy spurge (Euphorbia esula L.). J. spurge in the upper Great Plains: Methods, 1999a. Euphorbia esula: Perceptions by Agr. and Resource Econ. 21(2):381Ð395. models, and results. Impact Assessment ranchers and land managers. Weed Sci. Bangsund, D.A., R.K. Stroh, and J.A. Leitch. 14(4):419Ð433. 47:740Ð749. 1993. Leafy spurge patch expansion. Natur. Lym, R.G. 1997. The history of leafy spurge Sell, R.S., D.A. Bangsund, and F.L. Leistritz. Areas J. 13(2):131Ð132. control in North Dakota. N.D. Agr. Res.: 1999b. Perceptions of leafy spurge by ranch operators and local decision makers: An Bowes, G.G. and A.G. Thomas. 1978. N.D. State Univ., Fargo, N.D. Lym, R.G. and D.R. Kirby. 1987. Cattle for- update. Agr. Econ. Rep. No. 316. N.D. State Longevity of leafy spurge seeds in the soil aging behavior in leafy spurge (Euphorbia Univ., Fargo, N.D. following various control programs. J. Range esula)-infested rangeland. Weed Tech. Umberger, S.H., B.R. McKinnon, and A.L. Manage. 31:137Ð140. 1:314Ð318. Eller. 1983. Adding sheep to cattle for Glimp, H.A. 1988. Multi-species grazing and Lym, R.G. and C.G. Messersmith. 1993. Fall increased profits. Virg. Cooperative Ext. marketing. Rangelands. 10:275Ð278. cultivation and fertilization to reduce winter- Service Pub. 410-851. Virg. Cooperative Ext. Hanson, H.C. and V.E. Rudd. 1933. Leafy hardiness of leafy spurge (Euphorbia esula). Service, Blacksburg, Virg. spurge life history and habits. Agr. Exp. Sta. Weed Sci. 41:441Ð446. USDA. 1995. Purge spurge: Leafy spurge data- Bull. 226. N.D. Agr. Coll., Fargo, N.D. Lym, R.G. and C.G. Messersmith. 1985. base. CD-ROM Ver 3.0. USDA-ARS and Helgeson, E.A. and E.J. Longwell. 1942. Leafy spurge control and improved forage Mont. State Univ., Bozeman, Mont. Control of leafy spurge by sheep. N.D. Agr. production with herbicides. J. Range Watson, A.K. 1985. Integrated management of Exp. Sta. Bimonthly Bull. 4(5):10Ð12. Manage. 38:386Ð391. leafy spurge. p. 93Ð105. In: A.K. Watson Helgeson, E.A. and E.J. Thompson. 1939. Messersmith, C.G., R.G. Lym, and D.S. (ed.), Leafy spurge. Weed Sci. Soc. of Control of leafy spurge by sheep. N.D. Agr. Galitz. 1985. Biology of leafy spurge. p. 42- Amer., Champaign, Ill. Exp. Sta. Bimonthly Bull. 2(1):5Ð9. 56. In: A.K. Watson (ed.), Leafy spurge. Williams, K.E., J.R. Lacey, and B.E. Olson. Hughes, H., D. Nudell, and R. Egeberg. 1997. Weed Sci. Soc. of Amer., Champaign, Ill. 1996. Economic feasibility of grazing sheep SheepBud Ver. 1.01. N.D. State Univ., Nelson, J., D. Landblom, S. Silky, and T. on leafy spurge-infested rangeland in Fargo, N.D. Conlon. 1992. Multi species grazing of Montana. J. Range Manage. 49(4):372Ð374. Johnston, A. and R.W. Peake. 1960. Effect of native range in western North Dakota. p. selective grazing by sheep on the control of 42Ð46. In: T.C. Faller (ed.), Proceedings of leafy spurge (Euphorbia esula L.). J. Range western Dakota sheep day. Hettinger Res. Manage. 13:192Ð195. Ext. Center, Hettinger and N.D. State Univ., Fargo, N.D.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 329 J. Range Manage. 54: 330Ð337 July 2001 Dietary structural types of polygastric herbivores at different environments and seasons

ALICIA PELLIZA, PRISCILA WILLEMS, AND MARCELA MANACORDA

Authors are research technicians at the Instituto Nacional de Tecnología Agropecuaria (INTA), Estación Experimental Agropecuaria Bariloche, CC 277, (8400) San Carlos de Bariloche, Río Negro, Argentina. E-mail: [email protected]

Abstract Resumen

A classification of dietary structural types that represents dif- Se propone la clasificación de tipos estructurales de dietas, ferent arrangements of forage classes is proposed. It may be que representan diferentes ordenamientos de clases forrajeras especially useful for interpreting and comparing herbivore diets previamente definidas. La misma puede ser especialmente útil from different environments. As an example, a data set with the para interpretar y comparar la dieta de herbívoros en difer- botanical composition of 55 pooled fecal samples determined by entes ambientes. Como ejemplo se analizó un conjunto de datos microhistological analysis was analyzed. These samples came correspondiente a la composición botánica, determinada me- from 4 species of range herbivores (cattle, sheep, goat, and gua- diante el análisis microhistológico, de 55 muestras compuestas naco -Lama guanicoe-), from 9 different environments of de heces. Estas muestras provinieron de 4 herbívoros (bovino, Northern Patagonia (Argentina) during 3 seasons. Based on ovino, caprino y guanaco ÐLama guanicoe-), en condiciones plant characteristics related with the capacity of the animals to extensivas de pastoreo en 9 ambientes diferentes del norte de eat and digest each plant and with the occasional or permanent Patagonia, en 3 estaciones. En base a características de las presence of them in the vegetation, the information was grouped plantas relacionadas con la capacidad de los animales de co- into 5 forage classes: woody plants, perennial grasses, annual merlas y digerirlas y con la presencia ocasional o permanente grasses, grasslikes, and forbs. A principal component analysis of de las mismas, la información fue agrupada en cinco clases for- the grouped data was conducted. The graphic representations rajeras: plantas leñosas, gramíneas perennes, gramíneas evidenced the gradual changes in the structure of the data. Later, anuales, hierbas y graminoideas. A partir de los datos agrupa- working over the subspace defined by the 3 first principal com- dos se realizó un análisis de componentes principales. A través ponent axes, a hierarchical classification was performed that de sus representaciones gráficas se evidenciaron los cambios resulted in 9 dietary structural types. These types represented graduales en la estructura de los datos. Trabajando sobre el variation that resulted from the interaction of pasture differ- subespacio definido por los tres primeros ejes factoriales, se ences, species of herbivore and season. This concept is an hizo una clasificación jerárquica, para formar los grupos que abstraction developed from the experience, to extend its utility dieron origen a nueve tipos estructurales de dieta. Estos tipos beyond the particular cases. representan variaciones resultantes de la interacción de diferencias entre pasturas, especie de herbívoro y estación. Este con- cepto es una abstracción desarrollada a partir de la experien- Key Words: botanical diet composition, conceptualization, forage cia, para que su utilidad trascienda los casos particulares. classes, microhistological analysis, multivariate analysis, similarity of diets.

Indices of diversity, diet overlap and/or selectivity have been The diets of livestock and wildlife in the shrub, shrub-grass used to describe and compare the botanical composition of range steppes, and the mountain forests of Patagonia (Argentina) result herbivore diets in Patagonia (e.g., Bonvissuto et al. 1982, 1986, from the complex interaction between available forage and ani- Bonino et al. 1986) and by other authors in many other countries. mal species, their metabolic and reproductive status, the presence However, Scarnecchia (1996) pointed out, as did other authors of predators and especially the location of water, as pointed out cited in his work, that these indices have little general use in the as a generalization by O’Reagain and Swartz (1995). Herbivores science of range management. select diets from available forage in relation to their nutritional requirements (Hanley 1982). McInnis et al. (1990) applied hierarchical cluster analysis to the similarity indices to reveal patterns difficult to recognize in the matrix of similarity coefficients. Other multivariate methodolo- The authors wish to thank Ing. Agr. H.R. Taddeo for his helpful suggestions, gies such as principal component analysis and correspondence Ing. Agr. G.L. Bonvissuto, and Dr. M.S. Cid for the revision of the manuscript; the anonymous reviewers and the editor of the J.R.M. for the valuable contribution analysis have been used to analyze dietary information through their critical analysis; and Ms. S. García and Mr. V.C. Rocchi for their (Manacorda et al. 1996, Posse et al. 1996, Pelliza et al. 1997). help with manuscript preparation and graphic displays. This work was supported Conceptual models have been developed to explain foraging by the Instituto Nacional de Tecnología Agropecuaria (INTA), Estación behaviors. Senft (1987) stated that generalized models might be Experimental Bariloche. Manuscript accepted 12 Sept. 0000. useful to predict the response of the animal to changes in the composition of the plant communities or landscape mosaics.

330 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Hofmann (1989) classified ruminants into 3 feeding types: concentrate selectors, intermediate, and grass-roughage eaters. Provenza and Balph (1990) examined this classification and other models of diet- selection in ruminants, which are not mutually exclusive. They found that models based on morphophysiological characteristics and body size provide general predictions about foraging in unfamiliar environments and foraging in environments where the abundance and nutritional quality in dietary items vary temporally and spatially. Referring to mathematical models, Walker (1993) pointed out that the existence of several simulation models competing to explain foraging behavior suggests the difficulty in explaining diet selection by mathematical expressions. To interpret changes in vegetation in rangelands, Friedel et al. (1988) reduced a large number of species to a small number of “functional groups,” based on attributes selected according to their relevance for management. Similarly, defining forage classes according to the characteristics of the herbivores and the vegetation communities could enhance interpreting and comparing data from diets. The objective of this study was to develop a new method for describing and inter- Fig.1. Location of Pastures a to i in the Río Negro Province, Argentina (South America) with the phytogeographical provinces (Cabrera, 1976) and isolines of precipitation. Map adapt- preting diet information based on dietary ed from Ragonese & Piccinini (1969) and Muñoz & Garay (1985). structural types. This analysis is especially useful when studying diets from different Cabrera (1976) described the phytogeo- The plant species identified were classi- environments. The usefulness of this pro- graphical regions and provinces of fied as belonging to 1 of the following 5 cedure is demonstrated by analyzing diets of 4 polygastric herbivores grazing in dif- Argentina and Soriano (1956) subdivided “forage classes” based on morphological ferent environments of Northern one of the provinces in districts. The phy- and anatomical characteristics, related to Patagonia. togeographical areas for Río Negro the capacity of the herbivores to eat and province are described in Table 1 and their digest them, and their perennial or locations presented in Figure 1. Diets of ephemeral availability: Materials and Methods cattle, sheep, goat, and guanaco (Lama 1. Woody plants (WP): stems and roots Study area guanicoe) located in 9 pastures distributed with secondary structure, characterized The Río Negro Province, Argentina, is across the Rio Negro Province were used by lignified cellular walls included in the vast region known as in this study (Fig.1). 2. Forbs (F): without secondary structure Patagonia. It has an area of 203.013 km2 and with high digestibility and extends 758 km from the Andes 3. Perennial grasses (PG): without sec- Mountains to the Atlantic Ocean and 485 Analysis of diets A minimum of 15 fecal samples from ondary structure with lignified cellular km between 37¡ and 42¡ of south latitude walls (Fig.1). It has a moderately cold climate in each of 4 herbivore species (cattle, sheep, goat, guanaco) were collected, when pre- 4. Annual grasses (AG): without sec- the west and varies to warm-temperate ondary structure with less lignified cel- toward the northeast (Soriano 1983). sent, in each pasture during the summer, winter, and spring of 1991. Following 6 lular walls than PG Mean annual precipitation, in part as 5. Grasslike plants (G) (Juncaceae and snow, decreases from more than 2,000 years of drought, the annual rainfall during the study was slightly greater than the Cyperaceae families): without sec- mm in a forest dominated strip in the west ondary structure and digestibility simi- to 150 mm in the central area, and increas- mean (Unpublished data, Bustos). The feces were pooled to obtain 55 composite lar to the PG. es again to 300 mm on the east of the Hanley (1982) showed that woody Province. More than half of the Río Negro samples, each one of them corresponding to each combination of pasture, season, plants (WP) offer easily digestible forage Province has a mean annual precipitation with good nutritive quality in their buds, lower than 200 mm (Fig. 1). Strong, con- and animal species, which is referred to flowers, and fruits. Similarly, Somlo et al. stant winds prevail from the west year- hereafter as a diet. Samples were analyzed (1985, 1997) reported that in our study long (Muñoz and Garay 1985, Bustos microhistologically according to Holechek 1996). Most of Río Negro Province range- and Vavra (1981), determining percentage area WP had good nutritive quality. lands are in the semiarid environments, of frequency in accordance with Holechek Perennial grasses constituted an abundant with extensive grazing units. and Gross (1982). and permanent forage, while the annual

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 331 Table 1. Characterization of the phytogeographical regions, provinces and districts in the study area.

Region Province District Description Pastures Forests with tree species of austral distribution, mainly of the genus Nothofagus (Cabrera 1976). Grazing predominates in the forest of the deciduous “Ñire”, Nothofagus antarctica, with grasses and a AUSTRAL Subantártica forbs in the understorey. There are meadows with grasslike plants as: Juncus spp., Carex spp. and Eleocharis spp., grasses as Poa pratensis and forbs as Trifolium repens (Manacorda et al. 1996).

Characterized by tussock grasses (Stipa spp., Poa ligularis) and cushion-like shrubs as Mulinum spinosum and Senecio spp. Occidental District (Soriano 1956). There are meadows characterized by Juncaceae, b, c, d Cyperaceae and perennial grasses, such as Juncus spp., Carex spp. and Festuca pallescens, respectively (Boelcke 1957). Within those meadows, there are areas with the halophytic grass Distichlis spp. (Nicora 1978), towards the east (Marcolin et al. 1978). Patagónica ------Plateaus and mountains of the center of the Río Negro Province with an NEO altitude superior to 816 m. (Ragonese and Piccinini 1969). The dominant TROPICAL Central District species are: Chuquiraga avellanedae and Nassauvia glomerulosa among e shrubs and Stipa spp. among grasses. Prosopis denudans and other shrubs are sporadically present (Soriano 1956). ------Xerophile, sandy and halophile steppes predominate, with short-shrubs, succulent and ephemeral species. The characteristic community is the del Monte “Jarillal” (pastures h and i), an association of Larrea spp., with Monttea aphylla, Bouganvillea spinosa and other plants (Cabrera 1976). f, g, h, i In the salinized depressions (pastures f and g) a community characterized by halophytic shrubs of the genus Atriplex spp. dominates (Morello 1958). grasses (AG) have occasional presence. due to the union made in that particular and herbivore. Figure 2a shows the first Grasslike plants are restricted to meadows. step, relative to the total variance of the factorial plane of the PCA made on the data. The objective of this analysis was to dietary space (accounting for 47 and 28% Statistical analysis create the groups, characterizing them by of the total variation by axes 1 and 2, To obtain dietary structural types, the the biological interpretation of the factori- respectively), and Figure 2b presents the data were grouped into the 5 forage class- al axes employed. The groups were factorial plane of the variable space (i.e., es and analyzed. They were arranged in a obtained by cutting the dendrogram with a forage class). Woody plants were separat- matrix A={a }, for i=1,...,55; j=1,...,5; continuous line, not necessarily straight, ed from perennial grasses and grasslikes ij according to Benzécri (1992). The dendro- on the first PCA axis, with their estimated being the element aij the percentage of the forage class “j” in the diet “i.” Principal gram was cut at a subjective level, which correlation coefficients r being: rWP,PG = component analysis (PCA) was performed was established to get groups with a bio- Ð0.83 and rWP,G = -0.67. Figure 3 shows on this matrix to represent the data in a logical meaning in order to define the the dendrogram corresponding to the clus- space of reduced dimensions with optimal dietary structural types. Data analysis was ter analysis made with the diets described properties (Lebart et al. 1995). The results conducted using SAS (1988). by the scores given by the first 3 axes of of PCA allowed evaluating the similarity the PCA, and the resulting 9 groups that of diets, expressed through their proximity Definition of dietary structural types were identified. The botanical composition in the vectorial space. Diets with closer The dietary structural types represent of these groups, at forage class level, was scores (coordinates of diets in the factorial different arrangements of the 5 forage used to develop the 9 dietary structural axes) are more similar. These scores are a classes. The terms a) characterized, b) types defined in Table 3. linear combination of the original dietary accompanied, and c) associated were used Cluster analysis grouped 64% of the composition data that maximizes the vari- to define the proportion of the diet that the diets into structural types I, II, III, IV, and ation in these resultant scores with the forage classes represented. A forage class V based on the proportion of perennial restriction that the different sets of princi- characterized a group of diets if it com- grasses or woody plants in the diet (axis 1, pal component scores are not correlated to prised the majority of those diets, whereas Fig. 2b). This first component accounted each other. This PCA also describes the a forage class was considered accompany- for differences between the Monte and the correlation structure of the variables. ing if it was in a lower proportion. When other 2 phytogeographical provinces. The Next a hierarchical classification was the majority of the diets of a group had 2 perennial grass-woody plant gradient was carried out, according to the criterion of forage classes in similar proportions, they also seen in structural types VI, VII, VIII, minimal variance, working over the sub- were defined as associated. and IX, which were separated along the space defined by the first 3 principal com- second principal component axis based on 2 the occurrence of forbs and annual grasses ponents. The semipartial R was the statis- Results tic used to evaluate the change produced (axis 2, Fig 2b) and by perennial grasses Table 2 shows the plant species or genus and grasslikes (axis 3, which was used in in the k-th step. This statistic expresses the identified with values greater than 10%, magnitude of the increment in variability the classification). The group defined as grouped by forage class, pasture, season the structural type IX is more heteroge-

332 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 The location of diets from pastures b and c on the first principal component axis (Fig. 2a) shows that most of the grazing in the Patagónica Province, Occidental District (Table 1), occurs in the meadows Bonvissuto et al. 1996. The diets of the 4 herbivores in pastures b and c contained a high proportion of perennial grasses with different proportions of grasslikes. In the Central District of the Patagónica Province and in the Monte, the steppes become predominant (Table 1), with different combinations of shrubs with perennial and/or annual grasses. Thus, in the dietary structural types of pastures e, f, g, h, i, woody plants were especially important, combined with different proportions of the other forage classes, apart from grasslikes. This tendency is more evident in sheep, goat, and guanaco diets than in cattle diets. The communities of the Phytogeographical Subantárctica Province (Table 1) have a variety of perennial grasses, woody plants, grasslikes, and forbs available. Therefore, in all seasons, the diets of sheep and cattle, corresponding to pasture a, were characterized by an association of all the forage classes considered, excluding the annual grasses. It can also be noted (Fig. 2a) that there are dietary structural types defined almost exclusively by diets corresponding to one pasture: type VII by pasture a and types I and VI by pasture b. Those pastures always containing grasslikes have greater forage availability than the pastures of the steppes. Given the geographical location effect in the graphical diet distribution, the results also show a seasonal effect. It is especially evident in the dietary structural types V, mostly defined by summer diets, and in types VIII and IX, which are defined almost exclusively by spring diets (Fig. 2a.). In both cases, this remark is related with the seasonal foraging availability: in the first case, by woody plants that include Fig 2. First factorial plane of the Principal Component Analysis of diet composition data, fruits, and in the latter, by the presence of expressed in 5 forage classes, of 4 different herbivores from 9 pastures and 3 seasons. (a) annual grasses (Tables 2 and 3). Representation of the dietary space. Labels of the diets: CATTLE: ■ summer, ■ spring, ❏ winter; SHEEP: summer, spring, † winter; GOAT: l summer, l spring, m winter; Other authors (Bonino et al. 1986, GUANACO: n summer, n spring, o winter. The letter inside represents the pasture. The per- McInnis et al. 1990, Manacorda et al. centages of the total inertia explained by each axis are expressed between parenthesis. The 1996) found a relationship between the diets that belong to each Dietary Structural Type (in roman numbers) are enclosed by a shut results of dietary studies and animal dotted line. (b) Representation of the variables (forage classes). species considered, although subordinated to the influence of the plant community. In this group of samples, 2 known tendencies neous than the others, but it was taken as a large amount of grasslikes (16%); and in were evident: a) Cattle tended to have single cluster because of the availability of the latter, forbs were present (12%) and diets characterized by grasslikes and the annual grasses, which characterized it, there were fewer woody plants. These 2 perennial grasses, with minor influence of is more variable than the other forage diets appear in italics in Figure 2a and are woody plants and b) the other herbivores, classes. Two of the 55 diets analyzed did indicated by an asterisk in Figure 3. In especially goat, tended to have dietary pat- not correspond completely to the charac- Figure 4, the contribution of each forage terns with a strong component of woody terizations given to the structural types IV class in every diet is represented, showing plants (Figs. 2a, 2b, and 4). and VIII, so they were excluded. In the the different diet compositions that charac- first case, the diet was the only one with a terize the defined dietary structural types.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 333 Table 2. Plant species contributing 10% or more to the diets of 4 different herbivores in Northern Patagonia, Argentina. Diets are grouped by herbivore, pasture and season.

Pastures a b c d e f g h i Seasons UWP UWP UWP UWP UWP UWP UWP UWP UWP Woody Plants Acantholippia seryphiodes ...... L ...... Adesmia spp ...... G ...... Atriplex spp ...... C S S S . . . Berberis spp. . C . . . . .G ...... L L . . S . .S . Bredemeyera microphylla ...... G L . . . . Capparis atamisquea ...... G ...... S . . Cassia aphylla ...... C C S S S ...... Condalia microphylla ...... G G . . . S . . Cyclolepis genistioides ...... G . . . S . S . . S Chuquiraga spp...... L...... L L . L . S . S . S S . C . G . . Lycium spp ...... G . . . . L ...... Maytenus boaria S ...... Monttea aphylla ...... G . . . Mulinum spinosum ...... L G ...... Nardophyllum spp...... L...... Nassauvia glomerulosa ...... G ...... Prosopidastrum globosum ...... S L . . . Prosopis spp...... C C . . . . G G . G G .

L L . L L . S S . S S . S S . Retanilla patagonica ...... L ...... Schinus spp...... G ...... GGG . GG . S . . LL Senecio spp. . . . L ...... Verbena spp...... L G . G . . .L ...... Annual Grasses Schismus spp...... G . . G L L . L L . S S . S S . S S . Grasses Distichlis spp...... C . . . . . S ...... G ...... Festuca pallescens . . . C . C C . . L L L . . L . S S S S S . Poa spp. (P.pratensis+ C C . C CC C ...... P.lanuginosa+ P.ligularis) L L L G . . . . L S S S S S S S S . . . S Setaria spp...... S Sporobolus rigens ...... S ...... Stipa spp. (S.tenuis + S.speciosa) ...... G G G . G ...... G . . G G L . . . L . L L L L L . . L L S S . S S S S S S S S . . C C C C . Forbs Blechnum spp. . S ...... Erodium cicutarium ...... G Sphaeralcea spp...... G Trifolium repens C ...... Verbascum thapsus S. . Grasslikes Carex spp. . . . C C C C ...... Eleocharis spp. C . . . . S ...... S...... Juncus spp. . . . . C CC C ...... G . . S . . Seasons are: U = sUmmer W = Winter P = sPring Herbivores species are: C = Cattle G = Goat L = guanaco (Lama guanicoe) S = Sheep

334 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 could be seen, sometimes evidencing gradual changes. Instead, the classification methods, as cluster analysis, try to find discontinuities in the data, obtaining groups of similar individuals as a result. In Figure 2a, the groups that are clearly different can be separated from the others that, even when having more similarities within groups than between groups, show a slow and gradual change in the dietary composition. The biological meaning of the identified clusters in this study was based on the biological interpretation of each principal axis. In an extensive work on most of Patagonia, Pelliza et al. (1997) employed a similar methodology (multiple correspondence analysis and cluster analysis), with the objective of systematizing the results of a dietary survey in the dominant production systems of the principal environments of Patagonia. Starting with dietary information from more than 300 fecal samples representing 10 monogastric and polygastric herbivores, in 3 seasons they defined 20 dietary types or patterns and Fig. 3. Dendrogram of the cluster analysis based on the first three factorial axes of the PCA. presented them in cartographic form. The The numbers are semipartial R square. Bold numbers represent the result from the last union that originate the clusters shown with bold lines. Soft numbers result from the present work proposes to extract directly unions above the last ones considered. The dotted line shows where the dendrogram was from the dietary information the conceptu- cut. C = Cattle, G = Goat, L = guanaco (Lama guanicoe), S = Sheep. P = sPring, U = alization of dietary structural type. These sUmmer, W = Winter. Pastures = a to i. Dietary structural types = I to IX. Asterisks corre- types, in the sense proposed here, are a spond to diets that were excluded from those patterns. generalization that integrates the particular cases, helping in the interpretation of the Discussion and Conclusions different herbivores diet by creating a variation found in the real situations. In Frequently, the lists of genus and/or matrix of similarity indices. In our study Nature only the variation is real and the plant species obtained through the survey the mean seasonal percentage composition named “types” are statistical abstractions on rangelands or through the analysis of of the 5 forage categories in the diets of 4 (Unpublished work, Valverde). The range herbivore diets, are not enough to different herbivores was reduced to a dietary structural types defined here do not understand the complex animal-plant matrix of first 3 principle component differ conceptually from the dietary types interaction. To get a more integral inter- scores. But here PCA was not used merely or patterns of Pelliza et al. (1997). The dif- pretation, plants generally are grouped as a transformation technique, it was ferent terminology was used to avoid con- into functional categories that are indepen- mainly used to reduce the data dimension, fusions due to the meaning given to these dent of taxonomic classification. Different allowing their distribution to be shown in terms in other works (McInnis et al. 1990, functional groupings based on research graphics. Possible structures of the data Owen-Smith 1993). objectives or characteristics of available forage have been proposed by Bonvissuto Table 3. Dietary structural types defined by cluster analysis of the scores obtained from the first 3 et al. (1996), Posse et al. (1996), and principal component axes of the PCA made on diet composition data expressed in 5 forage class- Friedel et al. (1988), among other authors. es, of 4 different herbivores from 9 pastures and 3 seasons. The forage classes proposed here are useful for the interpretation of the diet infor- Dietary Description Structural mation from different environments. Types This study differs from McInnis et al. (1990) in the objective and in methodolog- I Diets characterized by perennial grasses ical aspects. In this case, the objective is II Diets characterized by perennial grasses accompanied by woody plants. III Diets characterized by perennial grasses associated with woody plants. not only the classification of diets, but also IV Diets characterized by woody plants accompanied by perennial grasses. the interpretation and the comparison of V Diets characterized by woody plants. the foraging response of herbivores in dif- VI Diets characterized by grasslikes associated with perennial grasses. ferent environments. About the transfor- VII Diets characterized by perennial grasses associated with woody plants, accompanied by mation applied to the original dietary com- grasslikes and forbs. position data prior to the classification of VIII Diets characterized by woody plants, accompanied by perennial grasses and annual grasses. the diets using cluster analysis, McInnis et IX Diets characterized by annual grasses associated with woody plants, accompanied by al. (1990) reduced the matrix of mean sea- perennial grasses with a variable presence of forbs. sonal percentage botanical composition of

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 335 Fig. 4. Forage classes composition of diets grouped on the defined Dietary Structural Types (I to IX). C = Cattle, G = Goat, L = guanaco (Lama guanicoe), S = Sheep. P = sPring, U = sUmmer, W = Winter. Pastures = a to i.

With respect to the interpretation of studies, to develop more complex concep- Cabrera, A. 1976. Regiones Fitogeográficas plant-herbivore interaction, Senft (1987) tual models of dietary selection. Argentinas. Enciclopedia Argentina de suggested that there might be basic pat- Agricultura y Jardinería. Segunda Ed. Tomo II. Ed. Acme S.A.C.I., Buenos Aires: 81 pp. terns of this interaction that are indepen- Friedel, M.H., G.N. Bastin, and G.F. dent of vegetation type and perhaps of Literature Cited Griffing. 1988. Range assessment and mon- plant species, and that those patterns could itoring in arid lands: the derivation of func- differ with level of ecological organiza- Benzécri, J.P. 1992. Correspondence Analysis tional groups to simplify vegetation data. J. Environ. Manage., 27:85Ð97. tion. In this work, it was found that some Handbook. Ed. Marcel Dekker, Inc., N.Y. Hanley, T.A. 1982. The nutritional basis for of the dietary structural types were not Boelcke, O. 1957. Comunidades herbáceas del independent of the structural and specific food selection by ungulates. J. Range norte de Patagonia. Rev. Inv. Agric. XI(1). Manage. 35(2):146Ð151. characteristics of the vegetation of each Bonino, N., G. Bonvissuto, A. Pelliza Hofmann, R.R. 1989. Evolutionary steps of region, although they were conditioned to Sbriller, and R. Somlo. 1986. Hábitos ali- ecophysiologial adaptation and diversifica- animal characteristics, as discussed by mentarios de los herbívoros en la zona cen- tion of ruminants: a comparative view of Hanley (1982). Thus, this approach helps tral del área ecológica Sierras y Mesetas their digestive system. Oecologia, in setting up the interaction between the Occidentales de Patagonia. Rev. Arg. Prod. 78:443Ð457. herbivore morphophysiology and the veg- Anim. 6 (5-6):275Ð287. Holechek, J. and B. Gross. 1982. Evaluation Bonvissuto, G., E. Moricz, O. Astibia, and J. of different calculation procedures for micro- etation type. There are cases, in which the De Anchorena. 1982. Resultados prelimi- histological analysis. J. Range Manage. 35 same herbivore has similar diets in differ- nares sobre los hábitos dietarios de ovinos en (6):721Ð723. ent environments, whereas in other cases, un pastizal semidesértico de Patagonia. Holechek, J.L. and M. Vavra. 1981. The different herbivores at different environ- IDIA, INTA, Buenos Aires, Suplemento effect of slide and frequency observation ments have similar diets. 36:243Ð253. numbers on the precision of microhistologi- The concept of structural types defined Bonvissuto, G., R. Somlo, A. Pelliza Sbriller, cal analysis. J. Range Manage. 34 in this study fulfills the characteristics and E. Moricz. 1996. Dieta estacional de (4):337Ð338. ovinos restrictos a un mallín en Sierras y Lebart, L., A. Morineau, and M. Piron. cited by Scarnecchia (1996) for any con- 1995. Statistique exploratoire multidimen- ceptualization: it is an abstraction devel- Mesetas Occidentales—Patagonia. Rev. Arg. de Prod. Anim. 16(1):35Ð44. sionnelle. Ed.Dunod, Paris. oped from the experience attempting to Bustos, C. 1996. Climodiagramas de locali- Manacorda, M., R. Somlo, A. Pelliza generalize the information so that its use dades seleccionadas de la Provincia de Río Sbriller, and P. Willems. 1996. Dieta de transcends the particular cases. The types Negro. Comunicación Técnica Nº 16— ovinos y bovinos en la región de los bosques de ñire (Nothofagus antarctica) de Río Negro based on the contribution of forage classes Agrometeorología. INTA EEA Bariloche. y Neuquén. Rev. Inv. Agr., INTA, Buenos in the diets may be integrated in future Aires, 26(1):137Ð146.

336 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Marcolin, A., G. Durañona, R. Ortiz, E. Owen-Smith, N. 1993. Evaluating optimal diet Senft, R.L. 1987. Domestic herbivore foraging Sourrouille, M. Latour, and G. Larrama. models for an African browsing ruminant, tactics and landscape pattern. Symposium on 1978. Caracterización de mallines en un área the kudu: how constraining are the assumed Plant-Herbivore Interactions, USDA-Forest del Sudoeste de la Provincia de Río Negro. constraints?. Evolutionary Ecol., 7:499Ð524. Serv. Intermoun. Res. Station. Gen. Tech Comunicación Técnica Nº 13, Pastizales Pelliza, A., P. Willems, V. Nakamatsu, A. Rept, INT - 222:137-140. Naturales. INTA EEA Bariloche. Manero et al. 1997. Atlas dietario de her- Somlo, R., G. Durañona, and R. Ortiz. 1985. McInnis, M.L., L.L. Larson, and M. Vavra. bívoros patagónicos. INTA-GTZ-FAO, Valor nutritivo de especies forrajeras 1990. Classifying herbivore diets using hier- Bariloche. ISBN 950-9853-88-7. Ed.: R. patagónicas. Rev. Arg. Prod. Anim. 5(9-10): archical cluster analysis. J. Range Manage. Somlo. 589Ð605. 43(3):271Ð274. Posse, G., J. Anchorena, and M. Collantes. Somlo, R., L. Cohen, H. Giorgetti, O. Morello, J. 1958. La Provincia Fitogeográfica 1996. Seasonal diets of sheep in the steppe Montenegro, and G. Rodriguez. 1997. del Monte. Opera Lilloana II, Instituto region of Tierra del Fuego, Argentina. J. Tablas de valor nutritivo de especies forra- Miguel Lillo, Tucumán. Range Manage. 49(1):24Ð30. jeras patagónicas. 2 Monte Pampeano. Muñoz, E. and A. Garay. 1985. Provenza, F. and D. F. Balph. 1990. Comunicación Técnica Nº 65 - Recursos Caracterización climática de la Provincia de Applicability of five diet-selection models to Naturales-Pastizales Naturales. INTA EEA Río Negro. Comunicación Técnica Nº 14. various foraging challenges ruminants Bariloche. Rec Naturales, Agrometeorología. INTA encounter, p. 423Ð459. In: R. N. Hughes Soriano, A. 1956. Los distritos florísticos de la EEA Bariloche. (ed.), NATO ASI Series Vol G 20, Springer- Provincia Patagónica. Rev. Inv. Agr., Tomo Nicora, E. 1978. Flora Patagónica. Parte III. Verlag, Berlin Heidelberg. X, 4:323Ð342. Gramineae, Colección Científica del INTA Ragonese, A. and B. Piccinini. 1969. Límite Soriano, A. 1983. Deserts and semi-deserts of Tomo VIII. Ed. Correa, M. INTA, Buenos entre el Monte y el Semidesierto Patagónico Patagonia, p.423Ð460. In: Temperate Deserts Aires. en las Provincias de Río Negro y Neuquén. and Semi-deserts, Ed. N.E. West. Elsevier O’Reagain, P.J. and J. Schwartz. 1995. Dietary Boletín Soc. Arg. Bot. 11(4): 299–302. Scientific Publishing Co, Amsterdam. selection and foraging strategies of animals on SAS. 1988. SAS/STAT User’s guide.Release Walker, J.W. 1993. Nutritional models for rangeland. Coping with spatial and temporal 6.03 Ed. Sas Inst.Inc.Cary, N.C. grazing animals. BÚVÍSINDI, ICEL. AGR. variability, p. 407Ð423. In: M. Journet, E. Scarnecchia, D.L. 1996. Viewpoint: Concept SCI. 7: 45Ð57. Grenet, M-H. Farce, M. Theriez, and C. design in range management science. J. Demarquilly (eds.). Proc. IVth Int. Symp. Range Manage. 49(5):421Ð424. Nutr. of Herbivores, INRA Editions, Paris.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 337 J. Range Manage. 54: 338Ð347 July 2001 Cattle use of foothills rangeland near dehydrated molasses supplement

DEREK W. BAILEY, G. ROBERT WELLING, AND ERIC T. MILLER

Authors are assistant professor and former research technicians, Northern Agricultural Research Center, Montana State University, Star Route 36 Box 43, Havre, Mont. 59501. This study was funded in part by NRI Competitive Grants Program/USDA, Award 9703712. The authors would like to thank David Cameron and the staff of the Dana Ranch and Steve Roth and the staff of the IX Ranch for their cooperation in this study.

Abstract Resumen

Strategic supplement placement has been shown to be an effec- La colocación estratégica del suplemento ha mostrado ser una tive tool to lure cattle to underutilized rangeland. The goal of this herramienta efectiva para atraer el ganado hacia áreas subuti- study was to determine where cattle grazed when supplement lizadas del pastizal. La meta de este estudio fue determinar was placed in foothills rangeland. The study was conducted in 4 donde apacienta el ganado cuando el suplemento se coloca en los pastures in northern Montana that were dominated by cool-sea- pastizales de pie de montaña. El estudio se condujo en cuatro son grasses. For 2-week periods beginning in October 1998 and potreros del norte de Montana dominados por zacates de ending in January 1999, dehydrated molasses blocks (30% CP) estación fría. Por periodos de 2 semanas, iniciando en Octubre were placed in locations within 3 pastures that were steeper and de 1998 y terminando en Enero de 1999, se colocaron bloques de further from water. Forage utilization was measured at the time melaza deshidratada (30% PC) en lugares dentro de los 3 of supplement placement and again at removal. Increases in for- potreros que eran áreas con pendiente pronunciada y lejos del age utilization during each period (14%) were similar (P > 0.1) at agua. La utilización del forraje se midió al momento de colocar distances of 30 to 600 m from supplement, and increases were el suplemento y nuevamente al remover los bloques. Los incre- additive across periods. Forage utilization was evaluated in a mentos en la utilización del forraje durante cada periodo fueron fourth pasture during August and September 1999 at distances similares (14%) (P>0.1) en las distancias de 30 y 600 m del suple- of 50 to 3,000 m from the supplement. Forage use declined (P < mento y el aumento fue aditivo a través de los periodos. La uti- 0.01) at further distances from supplement, and forage use at dis- lización del forraje se evaluó en un cuarto potrero durante tances less than 600 to 800 m from supplement was greater than Agosto y Septiembre de 1999 a distancias de 50 y 3,000 m del the average of all measurements collected throughout the pas- suplemento. El uso del forraje disminuyo (P < 0.01) conforme la ture. During the autumn and early winter at the 2 pastures locat- distancia del suplemento fue mayor y el uso del forraje a distan- ed near Havre, Mont., 53% of the cows were observed within 600 cias menores de 600 a 800 m del suplemento fue mayor que el m of supplement and 47% were observed at greater distances promedio de todas las medidas colectadas a través del potrero. from supplement. Eighty-one of the 159 cows grazing the 2 pas- Durante el otoño e inicios de invierno en los 2 potreros localiza- tures near Havre (245 and 330 ha) were fitted with Global dos cerca de Havre, Mont., el 53% de las vacas se observaron Positioning System (GPS) tracking collars. The collared cows dentro de una distancia de 600 m del suplemento y 47% restante spent 37% of their time within 600 m of supplement. Uniformity se observó a distancias mayores. A 81 de las 159 vacas que of cattle grazing can be enhanced by the placement of dehydrat- apacentaban en los 2 potreros cerca de Havre (245 y 330 ha) se ed molasses supplement in rugged topography, and the area les colocó un collar de restero de un Sistema de Posicionamiento influenced can include distances up to 600 m from supplement. Global (GPS). Las vacas con collar gastaron el 37% de su tiempo dentro de 600 m del suplemento. En áreas de topografía escabrosa la uniformidad del apacentamiento del ganado se Key Words: distribution, grazing, behavior, utilization puede mejorar con la colocación de suplemento de melaza deshidratada y el área influenciada puede incluir distancia hasta de 600 m del suplemento. Uneven livestock grazing distribution is often associated with many resource concerns on rangelands. Increasing the uniformity of grazing and preventing concentrated heavy grazing in local- ized areas is one of the principles of rangeland management (Bell supplements are available in containers (blocks weighing up to 1973). In addition to management practices such as developing 113 kg) that can be transported to rugged rangeland and then self water, salting, fencing and herding (Cook 1966, Bailey and fed. Most containers last up to 2 weeks before they are emptied Rittenhouse 1989), strategic placement of supplement has been and should be replaced to maintain intake. Bailey and Welling used to modify livestock grazing distribution (Martin and Ward (1999) showed that cattle spent more time and grazed more for- 1973, McDougald et al. 1989). Most commercially available sup- age in pasture areas where dehydrated molasses supplement was plements fed to cattle are palatable and potentially could be used provided than in similar control areas where no supplement was to lure aimals to underutilized rangeland. Dehydrated molasses provided. Although it was more effective in moderate terrain (10Ð20% slopes), strategic supplement placement noticeably changed livestock grazing patterns in steeper terrain (15Ð30% Manuscript accepted 10 Oct. 2000. slopes) at greater distances from water. Ongoing work in

338 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 California (Mel George, personal commu- Anderson pasture (48¼ 22'44"N 109¼ steeper slopes, vegetation was dominated by nication) also suggests that dehydrated 37'21"W) is approximately 330 ha bisect- rough fescue and bluebunch wheatgrass. molasses supplement can modify cattle ed with a perennial stream (Bull Hook Elevation in the pasture varied from 1,100 grazing patterns. Creek). Topographic relief varies from to 1,460 m. Soils were primarily shallow Although previous and ongoing research 1,055 to 1,222 m. Both pastures were to deep loams with some areas of clays. has demonstrated that strategic supple- dominated by Kentucky bluegrass (Poa ment placement can be effective, several pratensis L.), bluebunch wheatgrass Supplement placement aspects of this practice are not known. (Pseudoregnaria spicata [Pursh] A Love), Thackeray Ranch. Dehydrated molasses Protocols for its practical use are not in rough fescue (Festuca scabrella Torr.), supplement (30% CP) was placed at a rate place and should be developed. and Idaho fescue (Festuca idahoensis of 1 barrel (113 kg-block) per 20 cows Experimental procedures used in the past Elmer). Soils were primarily shallow clays (Table 1). In each pasture, 8 barrels were (Bailey and Welling 1999) would not be and gravelly loams. placed in pairs (2 barrels/site) about 30 m practical for range livestock producers. Dana Ranch. The Dana Ranch is located apart, similar to the Bailey and Welling The effect of strategic supplement place- 35 km south of Cascade, Mont. in rugged (1999) study. Salt blocks (23 kg, >99 to ment on livestock grazing distribution foothill rangeland near the Big Belt 99.9% NaCl) were placed at 2 of the 4 should be evaluated throughout the year. Mountains. Two study areas were estab- supplement sites. The 4 supplement sites Bailey and Welling (1999) studied the lished within a 4,900 ha pasture. Study (site = 1 pair of barrels) were arranged in a effects of dehydrated molasses supplement areas were approximately 325 ha in size rectangular pattern about 200 to 250 m on grazing distribution during the autumn and located about 2.5 km from each other. between sites (Fig. 1). Supplement was and winter (October to January) when the One area was identified as Coyote (47¼ not placed near water nor within extreme forage was mature and dormant, but this 01'38"N 111¼ 29'35"W) and the other was terrain (>40% slopes). In the Rakes Draw practice also may be effective during late identified as Pine Coulee (47¼ 00'30"N pasture, supplement was placed in areas summer (August and September). To con- 111¼ 30'00"W). The 2 study areas were classified as difficult using the criteria of duct economic evaluations of this practice, evaluated simultaneously. Relief in the Bailey and Welling (1999). Terrain classi- the area impacted by supplement place- pasture varied from 1,220 to 1,680 m, but fied as difficult was the usable area (<40% ment must be estimated. Bailey and elevations in the study areas varied from slopes) that contained the steeper slopes or Welling (1999) found that forage use was 1,490 to 1,680 m. Study areas were domi- was further from water than the moderate similar at distances of 20 to 200 m from nated by timothy (Phleum pratense L.), or easy terrain. Easy terrain was the gentle supplement. To determine the area impact- rough fescue, and Kentucky bluegrass. terrain near water. In the Anderson pas- ed by a single placement, forage use must Soils in the study area were primarily deep ture, supplement was placed only in areas be evaluated at distances further from sup- to shallow loams. classified as difficult in the Bailey and plement. IX Ranch. The IX Ranch is located in Welling (1999) study. Objectives of this study were to: 1) the Bear’s Paws Mountains, approximate- Every 2 weeks, previously used supple- develop and evaluate a practical approach ly 30 km east of Big Sandy, Mont. (48¼ ment barrels were removed and full sup- for strategic placement of dehydrated 04'55"N 109¼ 51'30"W). The study was plement barrels were placed in an adjacent molasses supplements during late summer, conducted in a pasture (approximately area at least 250 m from the previous loca- autumn and early winter, 2) estimate the 2,020 ha) containing gentle and rugged tion (Fig. 1). Supplement was provided to distance that cattle grazing distribution topography. Vegetation on gentler slopes cattle in the Rakes Draw pasture for three, was affected by supplement placement. In (5 to 15% slopes) was dominated by 2-week periods (periods 1 to 3, 9 October this study, effect of supplement was ini- Kentucky bluegrass with significant quanti- 1998 to 26 November 1998) and in the tially evaluated at distances of 30 to 600 m ties of bluebunch wheatgrass, western wheat- Anderson pasture for four, 2-week periods from supplement, and distances of 30 to grass (Pascopyrum smithii Rydb.(Love)), (periods 4 to 7, 26 November 1998 to 19 3,000 m were examined later. prairie junegrass (Koeleria macrantha January 1999). (Ledeb.) Schult.) , and blue grama (Bouteloua The supplement placement pattern used gracilis (H. B. K.) Lag. ex Griffiths). On in this study was based on previous expe- Methods rience (Bailey and Welling 1999). The Table 1. Nutrient concentration and ingredients purpose of placing new supplement in of the dehydrated molasses supplement used Study sites in the study. nearby underutilized areas was to facilitate The study was conducted at 3 locations cattle finding new supplement sites and to in northern Montana: Thackeray Ranch, Nutrient Level allow managers to progressively move supplement through underutilized sections Dana Ranch, and IX Ranch. Forage mea- (%) surements were collected at all locations, Crude protein 30.0 of a pasture. Travel time to place supple- but animal behavior observations were Not more than 12% equivalent ment and remove empty barrels was collected only at the Thackeray Ranch, crude protein from non-protein reduced because new barrels were placed near Havre, Mont. nitrogen near empty barrels that needed to be Thackeray Ranch. The Thackeray Crude fat 4.0 picked up. Ranch is located in the Bear’s Paw Crude fiber 2.5 Dana Ranch. Ten dehydrated molasses Mountains 30 km south of Havre, Mont. Ingredients: Molasses products, animal fat (preserved with supplement barrels (Table 1) were placed ethoxquin), plant protein products, animal protein prod- Two pastures were used at this study site, ucts, processed grain by-products, urea, monocalcium in each study area (i.e., Coyote and Pine Rakes Draw and Anderson. The Rakes phosphate, dicalcium phosphate, calcium carbonate, mag- Coulee) at the Dana Ranch (20 total). Draw pasture (48¼ 21'29"N 109¼ 34'31"W) nesium oxide, sulfur, vitamin A acetate, D-activated ani- Supplement was placed in a rectangular mal sterol, vitamin E supplement, zinc sulfate, manganous is approximately 245 ha with elevations oxide, ferrous sulfate, copper carbonate, calcium iodate, pattern similar to that used at the varying from 1,150 to 1,320 m. The sodium selenite. Thackeray Ranch with the additional 2

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 339 Fig. 1. Diagrams of the Anderson and Rakes Draw pastures. Fencelines are indicated by “x”. Two open gates allowed cattle access to the 2 sections of the Rakes Draw pasture. Eight supplement barrels were placed during each 2-week period. In the Anderson pasture, cattle watered in Bull Hook Creek that bisects the pasture. Most cattle watered at the location marked primary watering location. In the Rakes Draw pasture cattle watered at the primary watering location. The secondary water location provided enough water for only 40 to 50 of the 159 cows in the pasture. barrels placed in the middle of the rectangu- were placed and previously placed barrels 1998 and ending 15 December 1998. lar supplement area. Salt blocks (described were removed every 2 weeks. The study Supplement was placed only in terrain previously) were placed at 3 of the 5 sites was conducted for three, 2-week periods classified as difficult (Bailey and Welling (pair of barrels). New supplement barrels in each study area beginning 4 November 1999).

340 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 tions. Two of the ranches (Dana and IX) were large commercial cow-calf operations (>1,500 AU) that utilized extensive rangeland pastures. Cattle were treated at least annually for external parasites and may or may not have been treated for internal parasites. Treatment for internal parasites did not affect performance of rangeland beef cows in northern Montana (Bailey et al. 1997). Vaccination programs were based on recommendations from local veterinarians. Thackeray Ranch. A total of 159 cow- calf pairs of Hereford and Tarentaise breeding were provided dehydrated molasses supplement for 2 weeks before the study (14 September 1998 to 30 September 1998) to reacquaint them with the supplement. These cows had 1 year’s previous experience with dehydrated molasses supplement in the Bailey and Welling (1999) study. Mean cow weight during the study was 590 kg. Cow age averaged 5 year and varied from 3 to 8 year. Calves were weaned on 1 October 1998 at the Thackeray Ranch, and the study began on 9 October 1998 in the Rakes Draw pasture. Cows were moved from the Rakes Draw to the Anderson pasture on 26 November 1998. Cows were moved from Anderson pasture and the study ended on 19 January 1999. Dana Ranch. Approximately 1200 non- lactating cows with Angus and Angus x Hereford breeding were placed in the pas- Fig. 2. Map of a portion of the pasture at the IX Ranch where the study was conducted. The ture on 4 November 1998. Although the map was adapted from a 7.5-minute topographic map. Contour intervals are 12 m. The study ended on 15 December 1998, cattle pasture fence is indicated by a dotted line ( …. ). The north-south lines where vegetative remained in the pasture until mid-March measurement transects were collected are indicated by dashed lines ( ---- ). Dark cylinders 1999. Cattle had been exposed to dehy- indicate the approximate locations of supplement barrel pairs. Barrels were placed in 2 drated molasses supplement for 4 consecu- general locations in each of 3 periods. tive years before this study, including the Bailey and Welling (1999) study in 1997. IX Ranch. The IX Ranch study was con- rectangular pattern. Loose salt (99 to IX Ranch. Cow-calf pairs (n = 824) with ducted after completing the studies at the 99.9% NaCl) was placed in 2 separate Hereford and Red Angus breeding grazed Thackeray and Dana Ranches. The proto- locations roughly 200 m from water. the study pasture from 12 August 1999 to col was changed slightly to facilitate mea- The study was designed so that supple- 23 September 1999. Cattle had not been surement of forage utilization at distances ment would be moved along benches in a exposed to dehydrated molasses supple- further from supplement and to fit the ter- south to north direction. The benches con- ments prior to the study. To initially train rain and management goals of the ranch. tained similar topography and vegetation the cattle, 12 barrels of dehydrated At the beginning of each period (10 to 14 (Fig. 2). The benches were considered molasses supplement were placed near days), new dehydrated molasses supple- easy to moderate terrain based on the cri- water (100 to 400 m) in separate pastures ment barrels (Table 1) were placed, and teria used by Bailey and Welling (1999), from 1 August 1999 to 12 August 1999. previously placed supplement barrels were but they have historically received little removed. Period 1 began 12 August 1999 grazing use (Steve Roth, personal commu- and ended 29 August 1999, period 2 began nication). During period 3, supplement Forage measurements 30 August 1999 and ended 12 September was placed on steeper terrain (> 20% Thackeray and Dana Ranches. Forage 1999, and period 3 began 13 September slopes) near the west bench. use was measured before placement and 1999 and ended 23 September 1999. after supplement removal at 2 randomly During each period, supplement (8 to 12 Cattle selected locations within the rectangular barrel pattern. Measurements also were barrels) was placed in each of 2 general The protocol for this study was obtained at distances of 200, 300, 400, 500 locations (Fig. 2). Eight to 12 barrels were approved by the Institutional Animal Care and 600 m from supplement (Fig. 3). The placed in each location. Similar to the and Use Committee of Montana State 200-, 400-, and 600-m measurements were Thackeray and Dana Ranch studies, sup- University. Management was typical of repeated in 2 directions away from the rec- plement barrels were placed in pairs in a northern Montana rangeland cattle opera-

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 341 Ryan Butte (Fig. 2). Forage use measurements were also collected in a line west of the supplement placed on the southern slope of Ryan Butte and included steeper slopes (> 20%). In addition, forage utilization was observed at 14 randomly-selected locations throughout the entire pasture. All of these additional forage utilization measurements were collected using the protocol described above.

Grazing behavior—Thackeray Ranch Horseback observations. The location of cows within the study pastures was recorded 2 times per week by observers on horseback, usually once in the morning and once in the afternoon. Pastures were divided into map units (1 to 6 ha), based on slope, aspect, elevation, and distance to water. The number of cows in each map unit was recorded during each observation. Average distance from supplement and water were calculated by measuring Fig. 3. Example of forage utilization and stubble height measurements in period 3 (third bar- the distance from the map unit to supple- rel placement) in the Rakes Draw pasture. Utilization/stubble height transects began at ment and water locations on scaled maps. distances of 200, 300, 400, 500, and 600 m from supplement as indicated by the end of the In addition, the number of cows at supple- arrow. In addition, 2 transects (identified as “In”) were completed inside the rectangular ment barrels (< 30 m) was recorded. barrel pattern. GPS collars. Cattle were fitted with Lotek GPS 2000 collars (Lotek tangular supplement placement pattern 1). Forage measurements for the supple- Engineering, Newmarket, Ontario) that along the contour. The measurements 300 ment placed during period 6 were collect- record the location of cattle within 5 to 12 and 500 m from supplement were collected at the beginning of period 6 and the end m (Moen et al. 1997). Seven to 12 collars ed along a line perpendicular to the 200-, of period 7. were available to track cattle. At the 400-, and 600-m measurements. Forage Standing crop was measured before beginning of the study, 4 randomly select- measurements at each interval consisted of grazing by clipping to ground level ran- 2 ed cows were fitted with collars that were measuring the stubble height of 20 grass domly placed 0.09 m plots. Clipped for- powered with disposable batteries capable plants along a 40-m transect (2 m between age was separated into current year’s of recording and storing 3,000 locations. plants). The beginning and end of each growth of grass and forbs and the previous These 4 cows were tracked at 10-minute transect was marked with plastic surveyor year’s standing vegetation (standing dead). intervals for 10 days (7 days during period flags to help ensure that measurements Forage was dried for 48 hours at 50¼ C and 1 and 3 days in period 2). At the end of before and after supplement placement weighed. Clipped grass samples were period 1, cattle were tracked with collars were collected in the same location. The ground to pass a 1-mm screen and ana- powered by rechargeable batteries capable slope at each transect was recorded using lyzed for nitrogen content using a micro- of recording and storing 500 to 1,000 loca- an inclinometer. Observers were trained to kjeldahl process (AOAC 1990). tions during mild to moderate tempera- measure the intervals between transects IX Ranch. Forage measurements were tures. At cold temperatures (consistently and measure the 2-m intervals between identical to those used for the Thackeray <Ð12¡C) collars with rechargeable batter- stubble height readings using steps so that and Dana Ranches except for the follow- ies generally recorded and stored 150 to the measurements could be collected in a ing differences. Forage use was measured 300 locations. Because of the variation in reasonable amount of time. Stubble every 200 m along 2 south to north lines collar performance, locations were sam- heights were converted to forage utiliza- that roughly bisected each of the benches pled with several sampling schedules. tion levels using height-weight curves where the supplement was placed (Fig. 2). Initial performance of the rechargeable (Cook and Stubbendieck 1986). Ungrazed This allowed forage use to be evaluated at batteries allowed sampling intervals to be heights were measured before grazing distances of 30 to over 3,000 m from sup- changed to every 5 minutes during the day when supplement was first placed in the plement. Intervals were estimated by pac- and every 10 minutes at night. Later as pastures. Height-weight curves were ing or by an odometer and were not performance declined, the sampling inter- developed for major species (Kentucky marked. At each interval, stubble height of val was changed back to every 10 minutes. bluegrass, rough fescue, and timothy) and 15 plants was measured along a 30 m tran- During the last 2 periods in late December published relationships (US Forest Service sect (1 plant every 2 m). and January, the schedule was changed to 1980) were used for other grasses. At the end of the final period, additional every 15 minutes during the day and every In the Anderson pasture, deep snow- forage utilization measurements were col- 30 minutes at night to extend battery life drifts prevented retrieval of supplement at lected along 2 lines running east and west during cold weather. the end of period 6. Additional supplement across the pasture, perpendicular to the A total of 81 randomly-selected cows was placed in a new location (opposite north-south lines (Fig. 2). These 2 lines were tracked during the study. Collars side of the pasture) during period 7 (Fig. were south of the steeper terrain found on

342 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 effect of supplement placement. Distance to supplement, distance to water and slope were used as independent variables. Separate simple regression models also were used to individually evaluate effects of distance to supplement, distance to water and slope on forage utilization. Distance to supplement in the final use analyses refers to distance to nearest supplement during any of the 3 periods. Grazing behavior—Thackeray Ranch. Distances that cattle were observed from supplement (horseback and GPS data) were analyzed using chi-square procedures (Lehner 1979). The observed frequencies of cattle located at 200-m increments from supplement were compared to expected values using a goodness of fit Fig. 4. Standing crop of current year’s growth of grasses and forbs and previous years’ vege- test. Expected values were determined by tation (standing dead) at the Thackeray Ranch (Rakes Draw and Anderson pastures), multiplying the proportion of the pasture Dana Ranch (Coyote and Pine Coulee sites) and IX Ranch. Standing dead vegetation could that each incremental distance comprised not be distinguished at the Dana Ranch and forage was pooled into grass and forbs. by the total number of cows observed at all distances from supplement. The size were placed on sets of cows 9 different to supplement, distance to water and (ha) of each incremental distance from times. For each set of cows (7 to 12 ani- slope. Data from each period were ana- supplement was estimated using a mals), individual cow locations usually lyzed separately to determine if the rela- planimeter within the geographical infor- were recorded for 4 or 5 days. Then col- tionships were consistent from the begin- mation system (ArcViewTM, ESRL, lars were removed, and the data were ning to the end of grazing in the pasture. Redlands, Calif. Each cow location downloaded to a computer. Batteries were In addition to evaluating changes in for- recorded by an observer was considered recharged, and collars were prepared and age use from the beginning to end of a an observation. For the horseback obser- placed on another set of cows. These period, all use observations collected at vations, each pasture was analyzed sepa- cycles from placement on 1 set of cows to the end of period 3 were examined in a rately. For GPS collar data, each cow dur- placement on the next set took 7 to 9 days. separate analysis to determine the overall ing a period was considered an observa- The location of supplement barrels were recorded with an 8-channel, L-Band GPS receiver with ± 1 m positional accuracy (Omnistar, Houston, Tex.). Locations of fence boundaries, gates, water and terrain features were also mapped with this GPS receiver.

Statistical analyses Forage measurements—Thackeray and Dana Ranches. Changes in forage use and stubble height from the beginning to the end of a period (before supplement placement and after removal) were regressed on distance to supplement and slope (SAS 1985). Distance to water was not included in these analyses because it was highly correlated with distance to supplement. Changes in forage use also were regressed on distance to supplement alone. The 4 study sites (Anderson and Rakes Draw pastures and Coyote and Pine Coulee areas) were analyzed separately and included data from all periods. Forage measurements—IX Ranch. Similar statistical procedures were used for the IX Ranch data except that distance Fig. 5. Scatter plot of changes in forage utilization versus distance from supplement in the to water was added to the multiple regres- Rakes Draw and Anderson pastures at the Thackeray Ranch and Coyote and Pine Coulee sion model. Changes in forage use and study areas at the Dana Ranch. Changes in forage utilization were not related (P > 0.05) to stubble height were regressed on distance distance to supplement.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 343 Fig. 6. Scatter plot of changes in forage utilization and distance to supplement during periods 1, 2, and 3 at the IX Ranch. Changes in forage utilization were related (P < 0.05) to distance to supplement during all periods. tion, and data for a cow during a period 2,230 kg ha-1 (Fig. were averaged. Some cows (n = 24) were 4). This pasture had Fig. 7. Scatter plot of final utilization values and distance to supple- observed in 2 periods, and the data from not been grazed ment, distance to water and slope at the IX Ranch. each period was considered a separate since July 1997 and observation. The rationale for considering contained a large ha-1 with a large forb component and little them separate observations was that the quantity of previous years’ vegetation standing dead vegetation. supplement was placed in different loca- (standing dead). The Anderson pasture had Forage generally was dormant during tions during each period (Fig. 1). been grazed for 10 days in May 1998 and autumn 1998 at the Thackeray and Dana the total standing crop was about 1170 kg Ranches and the nutritive value as mea- -1 ha . Little standing dead vegetation was sured by crude protein (CP) was consis- Results observed in the Anderson pasture. Mean tently low. Crude protein concentration of standing crop at the Dana Ranch was 2,180 grass at the Dana Ranch was 4.5% in the -1 Vegetation measurements kg ha . We were unable to distinguish Coyote study area and 5.7% in the Pine Initial forage conditions. At the standing dead at the Dana Ranch, and any Coulee study area at the beginning of the Thackeray Ranch, mean total standing standing dead vegetation was pooled into study (4 November 1998). At the end of crop (current year’s growth of grass and the grass and forb categories. At the IX the study (17 December 1998), forage CP forbs) in the Rakes Draw pasture was Ranch, mean standing crop was 1,790 kg concentration in the 2 study areas aver-

344 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 GPS collar observations Collared cows spent about 17% of their time within 200 yards of supplement in the Rakes Draws pasture and about 16% of their time in the Anderson pasture (Fig. 9). Cattle use of the areas between 0 to 200, 201 to 400, 401 to 600, and greater than 600 m from supplement was not different from what would be expected by chance (P > 0.05). Collared cows spent 40% and 33% of their time within 600 m of supplement in the Rakes Draw and Anderson pastures, respectively (Fig. 9).

Discussion

Forage utilization Utilization levels. During the autumn Fig. 8. Mean number of cattle at varying distances from supplement observed by horseback and winter at the Thackeray and Dana observers. Expected values reflect the proportion of the pasture that the incremental dis- Ranches, areas within 600 m of dehydrat- tance from supplement represents and the number of cattle observed. A total of 159 cattle ed molasses received grazing use by cattle grazed in both pastures. Grazing patterns differed from expected values (P < 0.05). even though the supplement sites were located on some of the steepest terrain and aged 4.1%. In the Rakes Draw pasture slope (P = 0.09) in the multiple regression furthest areas from water. The mean during October 1998, mean CP concentra- analysis. Individual regressions of changes increase in forage utilization in this study tion of the current year’s grass growth was in forage utilization on distance to supple- (14 percentage points) was similar to the 6.5% and 4.4% for the bottoms and slopes, ment, distance to water and slope (simple 11 percentage point increase observed by respectively. In the Anderson pasture dur- linear regression, Fig. 7), were similar to Bailey and Welling (1999) in the same or ing November 1998, mean CP concentra- the multiple regression analyses except similar pastures. tion of the current year’s grass was 5.4%. that the relationship between forage uti- Forage utilization measurements show Forage utilization—Thackeray and lization and slope was no longer important that cattle continued to forage in previous- Dana Ranches. In all study areas, changes (P = 0.47). ly grazed areas as long as the areas in forage utilization and stubble height remained within 600 m of supplement. In were similar (P > 0.05) at all distances this study supplement was usually moved from 30 to 600 m (Fig. 5). Slope of terrain Cattle observations—horseback to an adjacent area 250 to 400 m from the where vegetation was measured did not Observations near barrels. In the Rakes first location (Fig. 1). Since change in for- influence (P > 0.1) change in forage use or Draw pasture, the mean number of cows age utilization was consistent at all dis- stubble height. The mean increase in for- observed at the 8 supplement barrels was tances from supplement, forage utilization age utilization was 14 percentage points 12, or 1.5 cows per barrel. In the Anderson increased 20 to 30 percentage points dur- during a period, but individual forage-uti- pasture, the mean number of cows ing a month (2 periods) when supplement lization measurements varied by more observed at barrels was 6, or 0.75 cows was nearby. So long as forage utilization than 20 percentage points at every dis- per barrel. The number of cows observed is less than acceptable levels (40 to 55%), tance measured in every study area (Fig. at all 8 barrels ranged from 0 to 24 total placing supplement adjacent to under- 5). Stubble heights decreased by an aver- animals or 0 to 3 cows per barrel in Rakes grazed sites will likely encourage cattle to age of 20 cm within a period. Draw. The range of cows at all 8 barrels in graze nearby. Forage utilization—IX Ranch. Using the the Anderson pasture was 0 to 20 cows, or Slope and distance to water. In contrast 0 to 2.5 cows per barrel. The number of multiple regression model, changes in for- to other studies (Valentine 1947, Mueggler cows observed at the barrels was similar age utilization and stubble height were 1965, Cook 1966), slope and distance to (P > 0.1) in the morning and afternoon. related (P < 0.01) to distance from supple- water did not consistently affect forage uti- Entire pasture observations. During the ment (30 to 3,000 m) during periods 2 and lization. Utilization measurements were 3, but in period 1 there was no relationship study, an average of 86% of the herd was observed. Cattle were not distributed uni- not collected in areas where slopes exceed- (P > 0.1). Changes in forage utilization ed 40%. At the IX Ranch where distance to and stubble height were not related (P > formly (P < 0.001) across pastures (Fig. 8). In both the Rakes Draw and Anderson water was used as a variable, the pasture 0.1) to distance to water and slope during was well watered, and cattle had to travel any period. If distance to water and slope pastures, 18% of cows were within 200 m of supplement, and these areas made up less than 800 m to reach water in most of were removed from the model, changes in the pasture. forage utilization decreased (P < 0.01) as 10% and 7% of the pasture acreage, distance from supplement increased in all respectively. In the Rakes Draw pasture, 3 periods (Fig. 6). 58% of the cows were observed within Area affected by supplement Final forage utilization (end of period 3) 600 m of supplement (38% of the pasture). For economic analyses of supplement decreased with distance to supplement (P In the Anderson pasture, 38% of the cows placement on cattle grazing distribution, < 0.001), distance to water (P = 0.02) and were observed within 600 m of supple- the extent of effects of supplement placement (26% of the pasture). ment must be estimated. The relationships

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 345 Thackeray and Dana Ranches was relatively consistent for distances up to 600 m. We expected a decline in forage use at 300 to 600 m from supplement. An additional study was conducted at the IX Ranch to estimate the furthest distance beyond which supplement would not affect cattle grazing patterns. Unlike the results observed at Thackeray and Dana Ranches, forage use decreased linearly with increasing distance from supplement at the IX Ranch. Forage measurements were collected at distances greater than 2,000 m from supplement at the IX Ranch but at the other ranches measurements were not collected at distances greater than 600 m from supplement. When observations greater than 600 m from supplement were excluded from the analyses of IX Ranch data, the relationship between change in forage utilization and distance to supplement was not important Fig. 9. Average use of terrain at varying distances from supplement by GPS collared cows in the (P > 0.1) for any period. Rakes Draw and Anderson pastures. Values are averages of individual collared cows (n = 81). At the IX Ranch during period 1, the Expected values reflect the proportion of the pasture that the incremental distance from sup- predicted change in forage utilization plement represents. Grazing patterns did not differ (P > 0.05) from expected values. equaled the average measured change in forage utilization at 815 m from supple- between changes in forage use and dis- tle grazing patterns. Bailey and Welling ment. At distances greater than 815 m tance from supplement at all 3 locations (1999) found forage use was relatively from supplement, the predicted change in (ranches) were used to estimate the dis- consistent for distances from 20 to 200 m forage use was less than the average tance to which 8 to 12 barrels (907 to from supplement. In contrast to our initial observed. Thus, grazing distribution was not affected at distances of greater than 1,361 kg) of supplement might affect cat- expectations, overall forage use at the 815 m from supplement during period 1.

Fig. 10. Locations of cow 9013 the last 4 days of period 1 and the first 2 days of period 2 in the Rakes Draw pasture. Locations were recorded at 10 minute intervals using GPS collars.

346 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 For period 2, the predicted change in for- of the cattle were gathered from the west- Bell, H.M. 1973. Rangeland management for age utilization equaled the average mea- ern half of the pasture, and less than 20% livestock production. Univ. Oklahoma Press, sured change in forage utilization at 638 m were found on the eastern half (Steve Norman, Okla. from supplement. For period 3, predicted Roth, personal communication). At the Cook, C. 1966. Factors affecting utilization of change in forage use equaled the average end of this study, the majority of the cattle mountain slopes by cattle. J. Range Manage. 19:200Ð204. observed change in forage use at 725 m (over 55%) were gathered on the eastern from supplement. During all 3 periods at Cook, C.W. and J. Stubbendieck. 1986. half of the pasture. This anecdotal obser- Range research: basic problems and tech- the IX Ranch, cattle were not lured to vation is consistent with the vegetative areas further than 600 to 800 m from sup- niques. Soc. Range Manage., Denver, Colo. measurements that show that cattle grazed plement. The consistency of the response DelCurto, T., M. Porath, M. McInnis, P. to supplement from 30 to 600 m at the more near supplement placed in the east- Momont, and C. Parsons. 1999. Management ern half of the pasture. strategies for optimal beef cattle distribution Thackeray and Dana Ranches and the esti- and use of mountain riparian meadows, p. mated end of influence after 600 m at the 119Ð129. In: K.L. Launchbaugh, K.D. Sanders IX Ranch suggests that the area that cattle Conclusions and Implications and J.C. Mosley (eds.), Grazing behavior of were lured to graze by a single placement livestock and wildlife. Idaho For., Wildlife and of supplement included areas up to 600 m, Range Exp. Sta. Bull. # 70, Univ. of Idaho, but the effect of supplement on grazing When dehydrated molasses supplement Moscow, Ida. patterns rapidly declined at distances was placed in rugged foothills rangeland, Lehner, P.N. 1979. Handbook of ethological greater than 600 m and ended before 800 cattle grazed nearby areas relatively evenly methods. Garland STPM Press, New York, m from supplement. for distances of 0 to 600 m from supple- N.Y. ment. If evaluated at distances greater than Martin, S.C. and D.E. Ward. 1973. Salt and meal-salt help distribute cattle use on semi- Effective seasons of use 600 m, forage use declined linearly with desert range. J. Range Manage. 26:94Ð97. Previous work with dehydrated increasing distances from supplement. McDougald N.K., W.E. Frost and D.E. molasses supplement to modify grazing Placement of 8 to 12 barrels (113 kg/barrel) Jones. 1989. Use of supplemental feeding distribution was conducted during the of dehydrated molasses supplement affects locations to manage cattle use on riparian autumn and winter (Bailey and Welling cattle grazing patterns for distances up to areas of hardwood rangelands, p. 124Ð126. 1999). Results from this study using non- 600 m, but the influence rapidly declines Proc. California Riparian Systems Conference, lactating cows during the autumn and win- beyond 600 m. Supplement should not be Davis, Calif., USDA For. Serv. Gen. Tech. ter resulted in similar grazing patterns expected to lure cattle to areas beyond 600 Rep. PSW-110. Washington, D.C. observed in the earlier study. At the IX to 700 m from placement. Moen, R., J. Pastor and Y. Cohen. 1997. Ranch, the decline in forage use at dis- Placing dehydrated molasses supple- Accuracy of GPS telemetry collar locations tances further from supplement demon- ment in undergrazed rangeland was an with differential correction. J. Wildl. strated that dehydrated molasses supple- effective tool to modify cattle grazing dis- Manage. 61:530Ð539. ment can effect grazing patterns of cow- Mueggler, W.F. 1965. Cattle distribution on tribution during late summer, autumn, and steep slopes. J. Range Manage. 18:255Ð257. calf pairs during August and September. winter. Supplement should be placed in Many concerns with livestock grazing in SAS. 1985. SAS user’s guide: Statistics. SAS undergrazed rangeland within a limited Inst., Inc. Cary, N.C. riparian and other areas occur during late area (5 to 15 ha in this study). When the summer (DelCurto et al. 1999). U.S. Forest Service Rocky Mountain Forest supplement is consumed, new supplement and Range Experiment Station. 1980. should be placed in an adjoining under- Utilization gauge: an instrument for measur- Cattle location grazed area. All cattle used to evaluate ing the utilization of grasses. American Observations of cattle location corre- dehydrated molasses supplement in this Slide-Char Corp., Wheaton, Ill. sponded well with vegetative measure- study had been exposed to the supplement Valentine, K.A. 1947. Distance from water as ments. Horseback observations showed before the study began. Supplement may a factor in grazing capacity of rangeland. J. that 18% of the cows were observed with- not be effective if cattle are not exposed to Forest. 45:749Ð754. in 200 m of supplement and that cattle the supplement before it is placed in used areas further than 600 m from sup- undergrazed rangeland. plement less than expected by chance. Less than 20% of the cows were observed within 200 m of the primary water source. Literature Cited Data from GPS collars also showed that cattle distributed themselves relatively evenly from 0 to 600 m from supplement AOAC. 1990. Official methods of analysis (e.g., Fig. 10). In the Bailey and Welling (14th ed.) Association of Official Analytical (1999) study about 30% of the cattle were Chemists. Washington, D.C. observed in the areas (subunits) with sup- Bailey, D.W. and L.R. Rittenhouse. 1989. plement and only 3% were observed in Management of cattle distribution. Rangelands 11:159Ð161. control areas. Control areas were separat- Bailey, D.W. and G.R. Welling. 1999. ed from areas with supplement in the Modification of cattle grazing distribution Bailey and Welling (1999) study. In the with dehydrated molasses supplement. J. Rakes Draw pasture, cattle utilized almost Range Manage. 52:575Ð582. all of the difficult terrain near supplement, Bailey, D.W., D.C. Anderson, and D.E. about 25% of the total area. Historically, Doornbos. 1997. Comparison of ivermectin this area of the pasture had received little and conventional external parasite control in grazing use by cattle. young beef cows. Prof. Anim. Sci. At the IX Ranch, cattle historically used 13:129Ð132. the western half of the pasture. Over 80%

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 347 J. Range Manage. 54: 348Ð355 July 2001 Complementary grazing of native pasture and Old World bluestem

ROBERT L. GILLEN AND WILLIAM A. BERG

Authors are rangeland scientist and soil scientist (retired), USDA-ARS, Southern Plains Range Research Station, 2000 18th Street, Woodward, Okla., 73801.

Abstract Resumen

Native pasture and Old World bluestems (Bothriochloa spp.) Las praderas nativas y los zacates “Old World bluestems” have contrasting herbage production characteristics that suggest (Bothriochloa spp.) tienen características de producción de forra- potential for incorporation into a complementary forage system. je contratantes que sugieren un potencial para incorporarlos en We compared 2 yearling beef production systems consisting of sistemas complementarios de producción de forraje. Durante 5 either native pasture (Native) or Old World bluestem combined años comparamos dos sistemas anuales de producción de carne with native pasture (Old World bluestem-Native) over 5 years. consistentes de pradera nativa (Nativa ) o “Old World bluestem” Crossbred steers (initial weight 257 kg) grazed only native pas- combinado con pradera nativa (“Old World bluestem”- Nativa). ture in the Native system, but alternated between Old World Novillos cruzados (peso inicial de 257 kg) apacentaron solo bluestem and native pastures in the Old World bluestem-Native pradera nativa en el sistema Nativa y en el sistema “Old World system. Production system had no effect on the frequency of any bluestem’-Nativa alternaron entre “Old World bluestem” y plant species in the native pastures (P > 0.16) even though stock- pradera nativa. El sistema de producción no tuvo efecto en la ing rate in the growing season was increased 31% in the Old frecuencia de ninguna de las especies de la pradera nativa (P > World bluestem-Native system. Peak standing crop of Old World 0.16) a pesar de que en el sistema “Old World bluestem”- Nativa bluestem averaged 4640 kg ha-1 but did not differ between the la carga animal se incremento en 31% durante la estación de cultivars ‘WW-Iron Master’ and ‘WW-Spar’ (P = 0.16). crecimiento. El pico de máxima producción de forraje en pie del -1 Individual steer gain was higher in the Native system during the “Old World bluestem” promedio 4,640 kg ha , pero no difirió Winter (P < 0.01) and Early Native (P = 0.03) management peri- entre los cultivares ‘WW-Iron Master’ y ‘WW-Spar’ (P = 0.16). ods, but was greater in the Old World bluestem-Native system La ganancia individual por novillo fue mayor en el sistema when steers were grazing Old World bluestem in June and July Nativa (P < 0.01) durante el invierno y durante los periodos de (P < 0.001). Over the entire season, steers in the Native system manejo tempranos(P = 0.03), pero fue mayor en el sistema “Old gained 13.5 kg head-1 more than steers in the Old World World bluestem”- Nativa cuando los novillos apacentaron en bluestem-Native system. Total livestock production was greater “Old World bluestem”en Junio y Julio (P < 0.001). A lo largo de in the Old World bluestem-Native system (77 versus 47 kg ha-1, P la estación completa, los novillos en el sistema Nativa ganaron -1 < 0.01). Relative economic returns between the 2 systems were 13.5 kg cabeza mas que los novillos del sistema “Old World dependent on the marginal value of livestock gain and the rela- bluestem”-Nativa. La producción total fue mayor en el sistema -1 tive costs of production for the 2 types of pasture. With average “Old World bluestem”- Native (77 versus 47 kg ha , P < 0.01). costs for native pasture of $17 ha-1 and for Old World bluestem Los retornos económicos relativos entre los dos sistemas fueron pasture of $62.10 ha-1, the Native system was often more prof- dependientes del valor marginal de la ganancia del ganado y los itable, even though livestock production per ha was much higher costos relativos de producción para los dos tipos de sistema. Con -1 -1 with the Old World bluestem-Native system. Lower costs for costos promedio de $17 ha en la pradera nativa y de $62.10 ha native pasture and high values of livestock gain favored the en la pradera de “Old World bluestem”, el sistema Nativa fue Native system. mas rentable, a pesar de que la producción del ganado por ha fue mucho mas alta en el sistema “Old World bluestem”- Nativa. Los bajos costos de la pradera nativa y el alto valor de la ganancia del ganado favorecieron al sistema Nativa. Key Words: mixed prairie, complementary forages, Old World bluestem, Bothriochloa, livestock performance Complementary forage systems combine different types of forages in an effort to overcome deficiencies in seasonal production and nutrient content that are inherent in any single forage. Major advantages of complementary forage systems include more effi- The authors wish to thank Dan Persons, Rick Hurst, Ron Charmasson, Lonnie Parsons, and Jim Bradford for livestock management and vegetation sampling. cient use of each individual forage, improved range condition, Contribution from the USDA-Agricultural Research Service. All programs and and higher overall stocking rates. The complementary forage sys- services of the U.S. Department of Agriculture are offered on a nondiscriminatory tem is one of the few grazing management methods that can sub- basis without regard to race, color, national origin, religion, sex, age, marital sta- stantially increase livestock production from forage-livestock tus, or handicap. Manuscript accepted 1 Oct. 2000. systems in the Great Plains (Launchbaugh et al. 1978, Sims and Bailey 1995).

348 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Old World bluestems (Bothriochloa cover of sand sagebrush to less than 5% grazed native pasture for the entire grazing spp.) and native pasture have potential as on the study pastures. All study pastures season. In the Old World bluestem-Native components of a complementary forage were contiguous. system, steers grazed Old World bluestem system. Old World bluestems are highly The second pasture type was a monocul- during the Winter and Old World productive warm-season grasses that ture of the introduced grass Old World Bluestem periods and native pasture in the respond well to nitrogen fertilization (Berg bluestem (Bothriochloa ischaemum L.). Early Native and Late Native periods. 1990). However, 70% of their growth Two different cultivars of Old World Stocking rates for the native pastures occurs during the month of June and nutri- bluestem, ‘WW-Spar’ and ‘WW-Iron were based on a moderate stocking rate of tive value declines rapidly (White and Master,’ were studied. The WW-Spar pas- 3.9 ha steer-1 for 320 days or about 53 Dewald 1996). Old World bluestem starts tures were seeded in 1980 and the WW- steer-days ha-1 (Sims and Gillen 1999). Our rapid growth about 4 weeks later than Iron Master pastures were seeded in 1983. stocking rate was also 53 steer-days ha-1 native pasture. Native mixed prairies are Both cultivars were seeded on Pratt fine with a land allowance of 3.2 ha steer-1 and dominated by warm-season grasses but sandy loams. Prior to seeding to Old a grazing season of 253 days. This stock- also have a moderate component of cool- World bluestem, these fields supported ing rate should maintain plant vigor over season grasses including annual bromegrass- monocultures of various forage grasses or years. Information on forage and livestock es (Bromus spp.) and, on sandy soils, Texas short-term (3 year) production of winter production on Old World bluestem over a bluegrass (Poa arachnifera Torr.) wheat since 1940. Old World bluestem range of stocking rates is not available. Integration of Old World bluestem and pastures were located within 1 km of the However, the stocking rate chosen for this native pasture could allow the capture of rangeland pastures. study has been tested for this environment the short-term, high productive potential The Old World bluestem pastures were and determined to be sustainable over of Old World bluestem and the earlier spring burned each spring in early to mid April to years (Berg and Sims 1995). growth of native prairie into a more feasible remove dead standing forage. We did not Six yearling beef steers were allocated production system for stocker cattle. burn these pastures in the spring of 1996 to each experimental unit for the Native Our objective was to compare steer pro- because of low precipitation and high fire system and 12 steers were allocated to duction systems based wholly on native danger throughout the spring. Nitrogen each Old World bluestem-Native unit. pasture or a combination of native and Old was applied at a rate of 67 kg N ha-1 as Steers were typical crossbred yearlings World bluestem pastures. Specific inter- ammonium nitrate in the third or fourth (Bos taurus x B. indicus, maximum 1/8 B. ests centered on the impact on the native week of April each spring. Broadleaf indicus) originating in north-central or pastures and on livestock production, the weeds, primarily horseweed [Conyza south Texas. Steers were randomly allo- performance of 2 cultivars of Old World canadensis (L.) Cronq.], were controlled cated to treatment groups such that aver- bluestem, and the relative net returns from with 0.56 kg ha-1 2,4-D on 13 June 1995 age initial weights were equal among the 2 systems. and with 0.84 kg ha-1 2,4-D on 13 June experimental units. Weight classes within 1997. No cultural practices were applied the original steer herd were proportionate- to the rangeland pastures. ly represented in the treatment groups. Materials and Methods Experimental treatments consisted of 2 Initial weights averaged 257 kg (SD = 12 basic production systems. The first system kg). Steers were weighed on each manage- contained only native pasture (Native). ment date after being held for 18 hours This study was conducted from 1993 The second system combined Old World without feed or water. Steers were implant- through 1997 at the USDA-ARS Southern bluestem and native pasture (Old World ed with Synovex-S1 (Ft. Dodge Animal Plains Range Research Station in north- bluestem-Native). Within the Old World Health, Overland Park, Kan.) at the start of west Oklahoma (36¡ 35'N, 99¡ 35'W, elev. bluestem-Native system, there were 2 sub- grazing and again in early May. We fed a 630 m). The regional climate is continen- systems differing only in the variety of 38% crude protein cube to the steers at a tal. Average annual precipitation is 560 Old World bluestem they contained. One rate of 1.7 kg head-1 day-1 from the start of mm with 72% falling during the sub-system contained WW-Spar and the grazing until about mid April. Actual prac- AprilÐSeptember growing season. second contained WW-Iron Master. There tice was to feed 3.9 kg head-1 of supple- Average monthly temperatures are 2.3¡C were 2 replications of each of the 3 sys- ment 3 times per week. Steers were treated in January and 28¡C in July. Minimum tems or subsystems for a total of 6 experi- for internal parasites with Ivomec1 (Merial and maximum recorded temperatures are mental units. The experimental units for Limited, Iselin, N.J.) in early May. They Ð27¡C and 45¡C. the Native treatment were approximately had unlimited access to block salt. All pro- Two major types of pastures were 20 ha in size. Each experimental unit for cedures for animal care and management included in this study. The first type con- the Old World bluestem-Native treatments were in accordance with accepted guide- sisted of native sand sagebrush (Artemisia consisted of a 20-ha rangeland pasture lines (Consortium 1988). filifolia Torr.)-mixed prairie growing on matched with a 2.6-ha Old World In the winter of 1994, all steers on the deep sandy soils on gently undulating, sta- bluestem pasture. Old World bluestem-Native units were bilized dunes (Berg 1994). Pratt soils The grazing season was divided into 4 grouped together as a single herd and (sandy, mixed thermic Psammentic periods. Average dates for these periods grazed Old World bluestem pastures that Haplustalfs) were on the lower slopes and were: a) Winter, 21 December to 15 were not in the study for 55 days (49% of more level areas, and Tivoli soils (mixed, March (84 days); b) Early Native, 15 the Winter period). In 1996, severe thermic Typic Ustipsamments) occurred March to 9 June (86 days); c) Old World on the upper slopes. A mixture of tall, Bluestem, 9 June to 30 July (51 days); and mid, and short warm-season grasses domi- 1 d) Late Native, 30 July to 31 August (32 Names are necessary to report factually on available data, nated the vegetation. Applications of 2,4- however, the USDA neither guarantees nor warrants the days). The total grazing season averaged D (2,4-dichlorophenoxyacetic acid) in the standard of the product, and the use of the name by USDA 253 days. In the Native system, steers implies no approval of the product to the exclusion of oth- 1970’s and 1980’s had reduced canopy ers that may also be suitable.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 349 drought in the early growing season randomized analysis of variance with (HeadN x Sale WeightN x Sale PriceN) Ð delayed grazing on the Old World bluestem repeated measures. Variety of Old World [HeadN x (CostNp x 3.2 ha)] = until June 21. Abundant precipitation in bluestem was the whole plot independent (HeadON x Sale WeightON x July and August resulted in high production variable and year was the repeated inde- Sale PriceON) Ð {HeadON x of Old World bluestem and the steers were pendent variable. [(CostNp x 1.6 ha) + (CostOWBp left on the Old World bluestem units until Steer gains were analyzed as a com- x 0.2 ha)]}. (4) the end of the grazing season, August 28. pletely randomized analysis of variance Equation 4 can be further simplified by This eliminated the late summer grazing with repeated measures. Production sys- assuming the 2 production systems will period on rangeland for the Old World tem was the independent variable and year produce the same number of steers. This bluestem-Native steers. Because of these was the repeated variable. Gain per head will require different total land areas. The inconsistencies in grazing management, was analyzed separately for each manage- equation can then be rearranged and steer gains for 1994 and 1996 were exclud- ment period and for the entire season. reduced to: ed and only gains from 1993, 1995, and Gain per ha was analyzed for each forage 1997 were used in the analyses. type within production system and over all (Sale WeightN x Sale PriceN) - (Sale Frequency sampling was conducted in production systems. WeightON x Sale PriceON) = (1.6 x the native pastures to determine the effects The main focus of the economic analy- CostNp) Ð (0.2 x CostOWBp). (5) of production system on plant species sis was to determine the factors that favor The left hand side of this equation is the composition. Four transects consisting of one production system over the other in difference in total sale price between a 50 quadrats (0.1 m-2) were located in each terms of net returns (NR). steer from the Native system and a steer pasture for a total of 200 quadrats per pas- NR = GIÐ LiP Ð LiVC Ð LaC, (1) from the Old World bluestem-Native sys- ture. The distances between transects and tem. This quantity can also be expressed quadrats were calculated to allow uniform where, as a function of the difference in weights spacing across the pastures and quadrats GI = gross income between the 2 types of steers and the mar- were located by pacing. The first sample LiP = livestock purchase costs ginal value of gain: was taken in October 1993, at the end of LiVC = livestock variable costs of (Sale WeightN x Sale PriceN) - (Sale the first year of treatment. Presence or production LaC = land costs. WeightON x Sale PriceON) = (Sale absence in the quadrats was recorded for weightN Ð Sale WeightON) x Value all plant species. A second sample was These terms can be rewritten as GI = Head x Sale Weight x Sale of Gain (6) taken in late September 1996, after 4 The value of gain is inversely related to years of treatment. Presence or absence of Price LiP = Head x Purchase Weight x the difference between the price per kg of 25 plant species was recorded. The species lighter versus heavier animals. As the dif- list for the second sample was based on Purchase Price -1 ference between the unit price of lighter the 25 most common plant species from LiVC = Head x Variable costs head LaC = Head x [(CostNp x haNp and heavier animals becomes smaller, the the first sample. -1 head ) + (CostOWBp x value of gain approaches the actual sale Peak standing crop of Old World -1 haOWBp head )], price. As the difference in unit price bluestem was determined at the end of the increases, the value of gain decreases. The summer grazing period for Old World where, subscript N = native pasture marginal value of gain is always lower bluestem. One plot measuring 1.3 x 4.9 m p than the sale price as long as lighter- was harvested with a sickle bar mower at a subscript OWBp = Old World bluestem pasture. weight steers are worth more per kg than height of 7 cm within each of 5 exclosures heavier-weight steers. This is the most per experimental unit. The exclosures If net returns are equal for the 2 production systems, common price structure in the U.S. beef were moved each year. Forage samples cattle market. Substituting this alternative were dried at 60¡C. Only data from the GIN Ð LiPN Ð LiVCN Ð LaCN = expression into equation 5 results in: years 1993 and 1995 to 1997 were includ- GI ÐLiP Ð LiVC Ð LaC , (2) ON ON ON ON (Sale weight Ð Sale Weight ) x ed in the analyses because data from 1994 where, N ON were lost. Value of Gain = (1.6 x CostNp) subscript N = Native production system Ð0.2 x Cost ). (7) Frequency of plant species within the subscript ON = Old World bluestem- OWBp rangeland units was analyzed with a com- Native system. Sale weights of the steers from each sys- pletely randomized analysis of variance We assumed that livestock purchase and tem are biological responses dependent on with repeated measures (Milliken and variable costs would be similar between the treatments themselves. The economic Johnson 1984). Production system was the the systems. This assumption is warranted advantage of one production system over whole plot independent variable and year because the type of animal, period of own- the other is also dependent on 3 external was the repeated independent variable. ership, and livestock management (other factors: the value of gain, the cost of The variance due to production system than grazing management) are essentially native pasture, and the cost of Old World was further partitioned into orthogonal identical between systems. This reduces bluestem pasture. The value of gain for the contrasts of Native versus Old World equation (2) to type of steers used in this study averaged bluestem-Native and WW-Spar versus $1.20 kg-1 at the Oklahoma City WW-Iron Master (within Old World GIN Ð LaCN = GION Ð LaCON (3) Stockyards from 1985 to 1995. The mini- bluestem-Native). A probability level of P Making substitutions for GI and LaC for mum value of gain was $0.60 kg-1 and the = 0.10 was used to declare significant each production system results in: maximum was $1.50 kg-1. We used these treatment effects. values of gain and systematically varied Peak standing crop of Old World the cost of rangeland from $12 to $26 ha-1. bluestem was analyzed with a completely At each combination of these 2 factors, we

350 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 then solved for the cost of Old World bluestem that would equalize returns between the 2 production systems.

Results and Discussion

Weather Precipitation during the study period was close to or higher than the long-term average with 2 exceptions (Fig. 1). The June to July period in 1994 was well below average. While precipitation totals for 1996 were above average, the distribution was highly skewed. Only 36 mm were received during the October 1995 to April 1996 period. This is a record low and is only 17% of the average of 213 mm for this period. Later that year, 488 mm (2.6 times the average amount) were received in the months of July, August, and September.

Species Composition of Native Pastures Production system had no impact on the Fig. 1. Precipitation at the Southern Plains Experimental Range, Harper County, Okla., dur- frequency of any plant species in the ing the study period. Average precipitation calculated over the period 1940 to 1998. rangeland pastures (P = 0.16 to 0.98, Table 1). There were no interactions responded to abundant precipitation in of 3,200 ± 548 kg ha-1 in 1997 to a high of between production system and year (P = July and August of 1996. 6,270 ± 620 kg ha-1 in 1996 when aver- 0.12 to 0.90). Growing season stocking Species decreasing over years included aged over cultivars. Gillen et al. (1999) rates were higher on the native pastures in Texas bluegrass, Scribner’s dicanthelium, measured peak standing crops of 4580 kg the Old World bluestem-Native system western ragweed, annual buckwheat, cam- ha-1 for WW-Iron Master growing on an compared to the Native system, 50.5 ver- -1 phorweed, and plantago. Texas bluegrass Enterprise fine sandy loam (coarse-silty, sus 38.5 AUD ha , but this increase did and Scribner’s dicanthelium are both cool- mixed, thermic Typic Ustochrept). Berg not affect plant populations. This may be season grasses and their decrease may be a (1990, 1993) reported annual production attributable to the rest period of 51 days in reflection of the severe winter-spring of 2,840 kg ha-1 for WW-Spar growing on the Old World bluestem-Native system drought just prior to the second sample a Woodward sandy loam (coarse-silty, while the steers grazed Old World period. This drought was probably also mixed, thermic Typic Ustocrept) in this bluestem in June and July. responsible for the decreases in forb same region and 2,945 kg ha-1 from WW- Species that did not change in frequency species. Three of these species, annual Iron Master growing on a Carey loam over years included sand bluestem, switch- buckwheat, camphorweed, and plantago, (fine silty, mixed, thermic, Typic grass, little bluestem, sand lovegrass, sand are annuals and susceptible to adverse Argiustoll). Precipitation in the May to paspalum, and purple threeawn. All of spring growing conditions. Camphorweed August period was 5Ð30% above average these are warm-season grasses and all and plantago were essentially absent in the for all of these studies and nitrogen fertil- except purple threeawn would be consid- second sample (Table 1). izer rates were comparable. The maximum ered palatable decreasers. Populations of production potential for these grasses may dominant warm-season grasses on the cen- be higher than previously thought. tral and southern Great Plains have gener- Old World Bluestem Standing Crop ally not been affected or have increased Standing crop of Old World bluestem slightly with intensive early stocking was similar (P = 0.16) for WW-Iron Steer Gain Master (4,790 ± 1,350 kg ha-1) and WW- Winter gains were greater for steers on (Owensby et al. 1988, Olson et al. 1993, -1 Gillen and Sims 1999). Perennial threeawn Spar (4,480 ± 1,190 kg ha ) when aver- native pastures compared with those on increased moderately as stocking rates aged over years. There was no interaction Old World bluestem (Table 2). This result- -1 were reduced in west central Oklahoma but between variety and year (P = 0.80) indi- ed in average daily gains of 0.34 kg head -1 its reaction to grazing has been mixed in cating a consistent response over years. day for steers on the Native system and -1 -1 other studies (Gillen et al. 2000). WW-Iron Master produces about 50% 0.19 kg head day for steers on Old Sideoats grama, sand dropseed, fall more forage than WW-Spar when growing World bluestem. Stocking density was 16 witchgrass, sand sedge, windmillgrass, on calcareous, iron-deficient soils (Berg et times higher in the Old World bluestem blue grama, sandbur, and sand sagebrush al. 1986). pastures. Forage standing crop was not The average peak standing crop over measured but was probably no more than all increased over years, regardless of -1 treatment (Table 1). All are warm-season years and cultivars was 4,640 kg ha . Old 3 to 4 times higher in the Old World species except sand sedge. Sandbur is a World bluestem standing crop was affect- bluestem pastures. This resulted in a high- warm-season annual grass that may have ed by year (P < 0.01) ranging from a low er grazing pressure in the Old World

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 351 Table 1. Plant frequency (%) in rangeland pastures as affected by production system and year and P-values from analyses-of-variance.

Production Plant Frequency P-values Species System 1993 1996 Treatment Year Trt xYear ------(%) ------Sand bluestem Native 21.7 28.8 0.79 0.30 0.60 (Andropogon hallii Hack.) OWB-Native 25.4 28.0 Switchgrass Native 16.0 18.8 0.56 0.34 0.60 (Panicum virgatum L.) OWB-Native 11.8 14.1 Little bluestem Native 11.7 12.5 0.98 0.33 0.83 [Schizachyrium scoparium (Michx.) Nash] OWB-Native 11.0 13.5 Sand lovegrass Native 6.1 11.3 0.38 0.50 0.50 [Eragrostis trichodes (Nutt.) Wood] OWB-Native 4.7 4.5 Sand paspalum Native 10.5 13.5 0.24 0.16 0.38 (Paspalum setaceum Michx.) OWB-Native 17.0 20.9 Sideoats grama Native 6.7 7.5 0.68 0.06 0.37 [Bouteloua curtipendula (Michx.) Torr.] OWB-Native 2.9 7.3 Sand dropseed Native 40.3 47.0 0.90 0.09 0.42 [Sporobolus cryptandrus (Torr.) Gray] OWB-Native 38.3 47.8 Purple threeawn Native 1.8 5.5 0.29 0.74 0.36 (Aristida purpurea Nutt.) OWB-Native 1.6 0.5 Fall witchgrass Native 8.9 19.5 0.90 0.04 0.42 [Digitaria cognata (J.A. Schultes) Pilger] OWB-Native 9.5 18.4 Texas bluegrass Native 63.5 37.8 0.28 0.02 0.43 (Poa arachnifera Torr.) OWB-Native 51.9 29.3 Sand sedge Native 6.9 28.5 0.98 0.01 0.52 (Cyperus schweinitzii Torr.) OWB-Native 6.7 28.9 Scribner’s dicanthelium Native 7.4 5.0 0.74 0.06 0.13 [Dicanthelium oligosanthes (J.A. Schultes) Gould] OWB-Native 6.7 4.4 Windmillgrass Native 11.0 19.0 0.30 0.01 0.61 (Chloris verticillata Nutt.) OWB-Native 4.4 16.0 Blue grama Native 54.9 69.0 0.96 0.01 0.17 [Bouteloua gracilis (Willd. ex Kunth) Lag. ex Griffiths] OWB-Native 50.3 70.1 Sandbur Native 7.2 21.5 0.16 0.01 0.33 (Cenchrus carolinianus Walt.) OWB-Native 16.7 38.5 Western ragweed Native 72.5 4.3 0.26 0.01 0.69 (Ambrosia psilostachya DC.) OWB-Native 64.6 1.9 Annual buckwheat Native 7.9 1.8 0.72 0.07 0.51 (Eriogonum annuum Nutt.) OWB-Native 9.9 1.9 Camphorweed Native 5.6 0.3 0.81 0.06 0.90 [Heterotheca subaxillaris (Lam.) Britt. & Rusby] OWB-Native 17.2 0.0 Plantago Native 14.8 0.0 0.25 0.04 0.41 (Plantago patagonica Jacq.) OWB-Native 17.9 0.0 Sand sagebrush Native 1.0 1.8 0.49 0.01 0.12 (Artemisia filifolia Torr.) OWB-Native 1.5 2.8 bluestem pastures that reduced the oppor- was one-half the stocking density of steers been growing rapidly for about 4 weeks tunity for selective grazing. Selectivity in the Old World bluestem-Native system. when this management period began while was also favored in the native pastures by Steer gains are often less sensitive to the Old World bluestems were just begin- the greater variety of plant species present. stocking density during the spring period ning rapid vegetative growth. In addition, Marston et al. (1993) found crude protein because forage quality is uniformly high the Old World bluestems were fertilized content of steer diets was higher in native (Owensby et al. 1988, Olson et al. 1993). with nitrogen, which has been shown to pastures compared to Old World bluestem However, earlier studies of intensive early increase forage crude protein content during this period but in vitro organic mat- stocking at this same location also report- (Berg and Sims 1995). Diets of steers ter digestibility was higher in Old World ed reduced steer growth when stocking grazing nitrogen-fertilized Old World bluestem pastures. Winter gains did not densities were increased in the early por- bluestem were higher in crude protein and differ between the 2 cultivars of Old tion of the growing season (Gillen and in vitro organic matter digestibility than World bluestem (Table 2). Sims 1999). diets of steers grazing native pasture dur- Steers in both production systems The steers grazed different forage types ing June and August in west-central grazed native pasture in the Early Native during the Old World bluestem manage- Oklahoma (Gunter et al. 1992). management period. Steers in the Native ment period. Gains for Native steers were Steers grazing WW-Iron Master gained system again gained more weight than less than for Old World bluestem-Native more than steers grazing WW-Spar during steers in the Old World bluestem-Native steers (Table 2). Average daily gains for the Old World bluestem management peri- system (Table 2). This resulted in respec- steers grazing native pasture, WW-Iron od (Table 2). On 7 sample dates over 3 tive average daily gains of 0.85 and 0.70 Master, and WW-Spar, were 0.89, 1.09, years, Sims et al. (1983) reported that kg head-1 day-1 from the 2 systems. and 0.94 kg head-1 day-1. Forage quality WW-Iron Master was always higher than Although steers in both systems were was likely higher in the Old World or equal to WW-Spar in crude protein con- grazing the same pasture type, the stock- bluestem pastures during this period. The tent with an overall mean of 8.0% for ing density for steers in the Native system dominant warm-season native grasses had WW-Iron Master and 7.6% for WW-Spar.

352 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 2. Individual steer gain for different management periods. Average dates: a) Winter, 21 Dec. to 15 Mar.; b) Early Native, 15 Mar. to 9 Jun.; c) Old World Bluestem, 9 Jun. to 30 Jul.; and d) Late Native, 30 Jul. to 31 Aug. All steers grazed native pastures during the Early and Late Native periods. Steers in the Old World bluestem-Native systems grazed Old World bluestem during the Winter and Old World bluestem periods. Numbers in parentheses represent 1 standard deviation.

Management period Production system Winter Early native Old World bluestem Late native Total ------kg steer-1 ------Native 28 74 45 14 161 (10) (19) (5) (10) (22) ‘WW- Iron Master’ - Native 17 62 56 18 152 (7) (24) (5) (10) (19) ‘WW- Spar’ - Native 15 59 48 22 144 (9) (23) (6) (8) (23) P-Values for contrasts Native vs. Old World bluestem Systems <0.01 0.03 <0.01 0.25 0.05 Old World bluestem cultivars 0.38 0.34 <0.01 0.15 0.14

WW-Iron Master also had greater or equal rates so there was little potential to bluestem in a relatively short, intensive in vitro dry matter digestibility on 6 of 7 increase gain per ha. With an overall mean grazing period can be seen when these dates with an overall mean of 62.6% for of 47 kg ha-1, the gains from native pasture gains are compared to the 200 kg ha-1 WW-Iron Master and 61.4% for WW-Spar are similar to the 42 kg ha-1 reported from gains produced by continuous grazing of (Sims et al. 1983). This advantage in nutri- earlier stocking rate studies at this location Old World bluestem from December to ent concentration may explain the higher (Sims and Gillen 1999). September (Sims et al. 1983). The steer gains on WW-Iron Master. Production per ha was not different increase was largely attributable to the For the final management period, Late between cultivars of Old World bluestem concentration of steer grazing during the Native, all steers were again on native pas- within the Old World bluestem-Native portion of the grazing season when quality ture. There was no difference in steer systems (P = 0.17, Fig. 2) or for the total of Old World bluestem was highest. gains for Native or Old World bluestem- system area (P = 0.69). Gain per ha was Total livestock production per ha Native steers (Table 2) or between steers about 6.5 times higher on Old World increased by 64% with the Old World that had grazed on the different cultivars bluestem than native pasture. At 306 kg bluestem-Native system compared to the of Old World bluestem (Table 2). Average ha-1, gains from Old World bluestem were Native system (P < 0.01, Fig. 2). The daily gains were 0.45 and 0.62 kg head-1 not greatly different than the 270 kg ha-1 increase in production was strictly due to day-1 for the Native and Old World reported from earlier work at this same the addition of the Old World bluestem bluestem-Native systems, respectively. location (Berg and Sims 1995, Gillen et al. since production per ha from the native There were no interactions for steer gain 1999). The value of using Old World portion of each system was not different. (P > 0.08) between production system and year for any management period. Total gains over all management periods averaged 13.5 kg head-1 greater for the Native system (Table 2) over the Old World bluestem-Native system and did not differ between sub-systems of Old World bluestem-Native. This difference was attributable to the Winter period when gains were 12 kg head-1 higher for the Native system. Growing season gains (combined over the last 3 management periods) were not different between production systems (P = 0.70). Winter gain was only 13% of total gain but was important in subsequent economic analyses. Livestock production per ha from the native portion of each system was not different (P = 0.89, Fig. 2). To increase gain per ha on native pasture, stocking rate must usually be increased because gain per head is near maximum under moderate stocking rates. With the ratio of native:Old World bluestem used in this study, stocking rate for the native pasture in the Old Fig. 2. Livestock production from the different forage types and the total land area in the 2 World bluestem-Native system actually production systems. Within forage type, production systems with different letters are sig- decreased 5% below moderate stocking nificantly different (P < 0.05). Bars denote 1 standard deviation.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 353 were 0.75 to 66.5. The average ratio was 3.7. The cost of Old World bluestem that maintained equal returns between production systems was linearly and positively related to the cost of native pasture (Fig. 3A). As the cost of native pasture increased, the cost of Old World bluestem could also increase and still maintain equal returns. For each $1 ha-1 increase in the cost of native pasture, Old World bluestem could increase $8 ha-1 because 1 ha of Old World bluestem substituted for 8 ha of native pasture in the Old World bluestem-Native system. At a value of gain of $1.20 kg-1 and a cost of native pasture of $17 ha-1, returns were greater for the Old World bluestem-Native system only if the cost of Old World bluestem was less than 3.3 times the cost of native pasture (Fig. 3B). As the cost of native pasture increased, the competitive advantage increased for Old World bluestem. At a native pasture cost of $26 ha-1, Old World bluestem could cost 4.9 times as much as native pasture. As the value of gain increased, the economic penalty for lower steer gains in the Old World bluestem-Native production system also increased. This means a pro- ducer could not afford to pay as much for land costs for Old World bluestem in the Old World bluestem-Native system (Fig. 3A). Conversely, as the value of gain declined, the cost of Old World bluestem could increase. Higher values of gain (narrow price differentials) favor the Native system while lower values of gain (wide price differentials) favor the Old World bluestem-Native system. If native pasture costs $17 ha-1 and value of gain is $1.50 kg-1, returns are only greater for the Old Fig. 3. Relative economic returns between the Native and Old World bluestem-Native pro- World bluestem-Native system if the cost duction systems. A) The effects of value of gain and land costs. B) The effects of value of of Old World bluestem is less than $36 ha-1 gain and ratio of land costs. The lines represent equal returns between the 2 systems. The Native system has greater net returns in the upper left portion of the figures and the Old or 2.1 times greater than the cost of native World bluestem-Native system has greater economic returns in the lower right portion of pasture (Fig. 3B). However, if the value of -1 the figures. gain is $0.60 kg , the cost of Old World bluestem can increase to $96 ha-1 or 5.6 -1 -1 times the cost of native pasture. For each Total system stocking rate was 53 AUD ha with a range of $2.50 to $111.20 ha . -1 -1 $0.01 kg decrease in value of gain, the ha in the Native system compared to 90 In addition to rent, costs associated with -1 allowable cost of Old World bluestem AUD h in the Old World bluestem- the management practices used for the Old increases $0.67 ha-1. The ratio of allowable Native system, an increase of 69% for the World bluestem pastures in this study land costs was less sensitive to value of complementary system. (Kletke and Doye 1998) include nitrogen gain as the cost of native pasture increased fertilization (average $28.00 ha-1, range (Fig 3B). $19.10 to $40.20 ha-1) and weed control Economic Comparisons The lower season-long gain of 13.5 kg every second year (average $6.50 ha-1, The relative economic response between head-1 in the Old World bluestem-Native range $5.00 to $11.90 ha-1). This resulted systems was dependent on the manage- system was a key factor in the analysis. At in an average total cost for Old World ment costs for the 2 forage types. To frame a value of gain of $1.20 kg-1, the ratio of bluestem of $62.10 ha-1 with a range of the following discussion, regional rental land costs that equalizes net returns ranges - $26.60 to $163.20 ha-1. Rent averaged only rates for native pasture averaged $16.70 ha from 1.3 to 5.2. If steer gains had been 1 -1 44% of the total cost of Old World with a range of $2.50 to $37.0 ha (Doye similar between systems, the allowable bluestem. Ratios of land costs (Old World et al. 1999). Regional rental rates for Old ratio of land costs increases to 8 and is not World bluestem pasture averaged $27.70 bluestem:native) based on the extremes

354 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 dependent on value of gain. The Winter Literature Cited Kletke, D. and D.G. Doye. 1998. Oklahoma management period accounted for much of farm and ranch custom rates, 1997-98. Okla. the difference in steer gains. One approach Coop. Ext. Serv. Curr. Rep. CR-205. to improving gains for the Old World Berg, W.A. 1990. Old World bluestem Launchbaugh, J.L., C.E. Owensby, F.L. bluestem-Native system would be to put responses to nitrogen fertilization. J. Range Schwartz, and L.R. Corah. 1978. Grazing Manage. 43:265Ð270. management to meet nutritional and func- half the steers on native pasture during the Berg, W.A. 1993. Old World bluestem tional needs of livestock, p. 541Ð546. In: Winter period. In this study, native pasture response to fire and nitrogen fertilizers. J. Hyder, D. N. (ed.), Proc. 1st Int. Rangeland in the Old World bluestem-Native system Range Manage. 46:421Ð425. Congress, Denver, Colo. was not utilized in the Winter period. Berg, W.A. 1994. Sand sagebrush- mixed Marston, T.T., S.A. Gunter, F.T. McCollum Since the stocking density of steers on prairie, p. 99. In: T. N. Shiflet (ed.), III, and R.L. Gillen. 1993. A comparison of native pasture would be equal between the Rangeland Cover Types of the United States. midgrass prairie and Old World bluestem 2 production systems, gains should at least Soc. Range Manage., Denver, Colo. during winter and early spring, p. 363Ð366. be equalized on half of the steers. With the Berg, W.A. and P.L. Sims. 1995. Nitrogen In: 1993 Animal Science Research Report. fertilizer use efficiency in steer gain on Old resulting lower stocking density on Old Okla. Agr. Exp. Sta. P-933, Stillwater, Okla. World bluestem. J. Range Manage. Milliken, G.A. and D.E. Johnson. 1984. World bluestem, gains might also improve 48:465Ð469. for the steers still grazing Old World Analysis of messy data. Lifetime Learning Berg, W.A., C.L. Dewald, and P.I. Coyne. Publications, Belmont, Calif. bluestem. 1986. Selection for iron-efficient Old World Olson, K.C., J.R. Brethour, and J.L. bluestems. J. Plant Nutr. 9:453Ð458. This economic analysis was based on Launchbaugh. 1993. Shortgrass range vege- Consortium. 1988. Guide for care and use of relative returns between the 2 production tation and steer growth response to intensive- agricultural animals in agricultural research systems. Actual profitability for either sys- early stocking. J. Range Manage. and teaching. Consortium for Developing a tem depends on many other factors such as Guide for the Care and Use of Agricultural 46:127Ð132. purchase and sales prices, marketing Animals in Agricultural Research and Owensby, C.E., R. Cochran, and E.F. Smith. arrangements, death loss, feed costs, and Teaching. Champaign, Ill. 1988. Stocking rate effects on intensive-early many others. However, these factors Doye, D.G., D. Kletke, and B.L. Fischer. 1999. stocked Flint Hills bluestem range. J. Range would generally affect both systems. Oklahoma pasture rental rates: 1998Ð99. Okla. Manage. 41:483Ð487. Given average values for livestock gain of Coop Ext. Serv. Curr. Rep. CR-216. Sims, P.L. and D. Bailey. 1995. Calf produc- $1.20 kg-1, and average costs for native Gillen, R.L. and P.L. Sims. 1999. Intensive tion by Angus-Hereford and Brahman- Hereford cows on two native rangeland for- pasture of $17 ha-1, the Old World early stocking of southern mixed grass prairie, USA, p. 499Ð500. In: Eldridge, D., age systems. J. Anim.. Sci. 73:2893Ð2902. bluestem-Native system was economically and D. Freudenberger (eds.). Proc. 6th Sims, P.L. and R.L. Gillen. 1999. Rangeland competitive as long as the ratio of land International Rangeland Congress, and steer responses to grazing in the southern costs was 3.3. Since the average ratio of Townsville, Australia. plains. J. Range Manage. 52:651Ð660. land costs was 3.7, the Native system was Gillen, R.L., J.A. Eckroat, and F.T. Sims, P.L., C.L. Dewald, and S. Cowles. often more profitable, even though the McCollum III. 2000. Vegetation response to 1983. Advancements with Old World livestock production per ha was much stocking rate in southern mixed-grass prairie. bluestems, p. 4Ð11. In: Wiedemann, H. T., higher with the Old World bluestem- J. Range Manage. 53:471Ð478. and J. F. Cadenhead (eds.). Proc. Range and Native system. Conditions further favoring Gillen, R.L., W.A. Berg, C.L. Dewald, and Pasture Seeding in the Southern Great Plains. P.L. Sims. 1999. Sequence grazing systems the Native system included low costs for Texas A&M Univ. Res. and Ext. Center, on the southern plains. J. Range Manage. Vernon, Tex.. native pasture and a high marginal value 52:583Ð589. White, L.M. and C.L. Dewald. 1996. Yield of livestock gain. When value of gain is Gunter, S.A., F.T. McCollum III, and R.L. and quality of WW-Iron Master and cau- low, the Old World bluestem-Native sys- Gillen. 1992. Midgrass prairie range versus casian bluestem regrowth. J. Range Manage. tem would likely be more profitable at Plains bluestem pasture for stocker cattle, p. 49:42-45. almost any cost level for native pasture. 426Ð433. In: 1992 Animal Science Research Report. Okla. Agr. Exp. Sta. MP-136, Stillwater, Okla.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 355 J. Range Manage. 54: 356Ð361 July 2001 Upland erosion under a simulated most damaging storm

S. J. LINSE, D. E. MERGEN, J. L. SMITH, AND M. J. TRLICA

Authors are environmental engineer, Western Water Consultants, 611 Skyline Road, Laramie, Wyo. 82070; research associate, Rangeland Ecosystem Science Department, Colorado State University, 5212 Kissing Camel Drive, Colorado Springs, Colo. 80904; professor emeritus of Civil Engineering, University of Wyoming, Laramie, Wyo. 82071; and professor of Rangeland Ecosystem Science, Colorado State University, Ft. Collins, Colo. 80523.

Resumen Abstract A 2 year study was conducted to determine the effects of sur- Se condujo un estudio de 2 años para determinar los efectos de face cover and roughness on sediment yield from plots subjected la cobertura superficial y la rugosidad en la producción de sedi- to a simulated most damaging storm. This storm, based on long mento de parcelas sujetas simulación de la tormenta mas dañina. term sediment records from 3 Wyoming streams, produced Esta tormenta, basada en registros de largo plazo de la produc- approximately 18 mm of precipitation in 15 min with an intensity ción de sedimento de 3 corrientes de Wyoming produjo aproxi- of 97 mm hour-1. The rainfall simulator covered 2 plots; each 0.6 madamente 18 mm de precipitación en 15 minutos con una by 2 m. Plots were on 9% slopes with highly erosive soils (silt and intensidad de 97 mm hora-1. El simulador de lluvia cubrió 2 fine sand texture) on native rangeland in 3 areas of Wyoming. parcelas, cada una de 0.6 x 2 m. Las parcelas se localizaron en Cover and surface roughness were measured with a point frame. tres áreas de Wyoming en pastizales nativos con pendientes del Sediment production typically peaked approximately 120 sec 9% y suelos altamente erosivos (textura de limo y arena fina). La after runoff started and reached steady state within 6 min. Plots cobertura y rugosidad de la superficie se midieron con un marco with no cover (tilled) seldom produced runoff due to high infil- de puntos. La producción de sedimento típicamente estuvo en su tration and the short duration rainfall. Sediment yield was mod- mas alto punto a los 120 segundos después de que inicio el escur- erately correlated with total cover for total cover less than 30%, rimiento y alcanzo el estado de equilibrio dentro de 6 minutos. and sediment yield decreased to 0.1 tonnes ha-1 (assumed allow- Las parcelas sin cobertura (con labranza) raramente produjeron able soil loss) or less for greater than 30% cover. There was a escurrimiento debido a la alta infiltración y a la corta duración weak correlation between surface roughness and sediment yield, de la lluvia. La producción de sedimento se correlaciono moder- and surface roughness was slightly correlated with total cover. adamente con la cobertura total en coberturas menores al 30% y These results suggested that maintaining at least 30% total cover la producción de sedimento disminuyo a 0.1 ton ha-1 (perdida de could control sediment yields from short duration-intense suelo que se asume permitida) o menos en coberturas mayores al storms. Experimental results also indicated considerably higher 30%. Hubo un a correlación débil entre la rugosidad de la super- sediment yields than those predicted by the Revised Universal ficie y la producción de sedimento y la rugosidad de la superficie Soil Loss Equation or a modified version of that equation. se correlaciono ligeramente con la cobertura total. Estos resultados sugieren que manteniendo al menos 30% de cobertura total se podría controlar la producción de sedimiento de tormentas de Key Words: sediment yield, surface cover, surface roughness, corta duración-alta intensidad. Los resultados experimentales eolian sediment, RUSLE, non-point source pollution, water qual- también indicaron producciones de sedimento considerable- ity mente mas altas que las predichas por la Ecuación Universal de Perdida de Suelo Revisada o una versión modificada de esa ecuación. Sediment contaminates more kilometers of Wyoming’s rivers and streams than any other non-point source (Hogan 1988), a situation typical in many western states (Heady and Child 1994). Runoff and sediment transported with runoff from rangelands of vegetation also affects the spatial and temporal variation of also transports biological and chemical pollutants into rivers and runoff and erosion (Weltz and Wood 1986, Blackburn and Wood streams while removing vital plant nutrients. Thus, erosion 1990). Eolian sediment deposition, which is influenced by the decreases range productivity (Binkley and Brown 1993), and pol- same factors (Skidmore 1994), may be an important source of lutants accumulate in water supplies, which reduces water quality sediment from rangelands during precipitation events. Wind (Hogan 1988). speeds of 40 km hour-1 (less than twice the average daily wind Vegetation cover, plant life form (grasses, forbs, shrubs), speed on many rangelands) cause erosion at approximately the ground cover, soils, and topography influence runoff and erosion same rate as many precipitation events, but windstorms occur (Simanton et al. l991, Benkobi et al. 1994). The type and amount more frequently (Skidmore 1994). Rangeland runoff and erosion are controlled by a complex combination of soil, plant, microtopographic, and hydrologic This research was funded by the State of Wyoming Department of Environmental Quality, Non-point Source Program. interactions (Seyfried 1991, Weltz and Blackburn 1995). For At the time of this research, the first author was Graduate Assistant, Department example, the spatial arrangement of vegetation and plant life of Civil Engineering, University of Wyoming. form affects litter and roughness of the soil surface (Blackburn et Manuscript accepted 2 Sept. 2000. al. 1992) thereby affecting runoff and sediment filtration (Weltz

356 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 et al. 1992) and soil properties (Naeth et al. uses are grazing, recreation, and oil and The most damaging storm was defined 1991). Coppice dunes, which may be par- gas production. The drainage contributes as the storm that produced the greatest tially formed by deposition of eolian sedi- approximately 0.8% of the mean annual average annual stream sediment load. ment, are associated with surface rough- flow of the Bighorn River, but also con- Using records for 3 Wyoming watersheds, ness and aggregate stability, and by influ- tributes 75% of the annual sediment load Huffsmith (1988) showed that most dam- encing infiltration, influence runoff and (Cooper 1979). aging storms produced 16 to 19 mm of erosion (Blackburn et al. 1990). Eolian Ten Mile Creek has the same average rainfall with return periods of approxi- sediment typically has the same texture rainfall and temperature as Fifteen Mile, mately 2 years. Branson et al. (1981) con- (silt and fine sand) as soils which are high- but has greater canopy cover. Soil in the cluded that many rangeland storms pro- ly susceptible to rainfall erosion. While area is an Uffens-Rairdent complex. duced less than 17 mm of rainfall, had there is ample evidence in the literature of Vegetation consists of wheatgrasses durations of less than 60 min, and reached the impact of precipitation events on runoff (Agropyron spp.), needle-and-thread peak intensity in less than 10 min. Using a and erosion, there is little information to (Stipia comata Trin.&Rupr.), and big relationship presented by Linsley et al. show the impact of vegetation and soil sur- sagebrush (Artemisia tridenta Nutt.) with (1982), the minimum duration for such face characteristics on sediment yield limited blue grama and pricklypear cactus. storms is approximately 7 min. Assuming caused by a “most damaging storm”. Primary historical use is for grazing, but 15 min duration and using an analysis pre- The objective of this research was to there was no evidence of grazing before sented by Haan et al. (1994), the intensity evaluate the effects of cover and surface the simulations were run. should be approximately 100 mm hour-1. roughness on the sediment yield caused by Beaver and Jack Creeks are in the In preliminary tests, it was observed that a simulated most damaging storm. Stratton Sagebrush Hydrology Study Area. plot runoff and sediment yield stabilized Sediment yield was defined as the amount Soils belong to the Youga series, mixed within 6 min or less with a simulator rain- of soil detached from an area which Argic Cryboroll. Beaver Creek receives an fall intensity of 97 mm hour-1. Therefore, passed a downslope point (Ponce 1989), annual precipitation of 381 mm, has an the simulator operating parameters repre- and the most damaging storm was defined annual average temperature of 5¡C, and sented a reasonable compromise of the as the rainfall event which caused the was being grazed at the time of the simu- most damaging storm. greatest average annual sediment load for lations. Jack Creek receives an average 3 Wyoming streams (Huffsmith 1988). It annual precipitation of 516 mm, has an Cover and Surface Roughness average annual temperature of 5¡C, and was hypothesized that sediment yields Surface cover was the controlled vari- has not been grazed since 1960. produced by a most damaging storm able in this research, and plots were select- Vegetation consists of big sagebrush and would be greater and more sensitive to ed at the 3 study sites over the range of 0 grasses such as fescues (Festuca spp.), cover than those predicted by the Revised to 100% cover. Cover and surface rough- Universal Soil Loss Equation (Renard et blue grasses (Poa spp.), and needle grasses (Stipa spp.). Litter cover, which was ness were measured using the point frame al. 1994) or a modified version of that method (Bonham 1989). The point frame equation (Benkobi et al. 1994). often several cm thick, influenced cover and surface roughness at this site. covered an entire plot and contained 100 equally spaced pins (20 rows and 5 columns). Pin height was measured rela- Methods Rainfall Simulator tive to the frame top using a digital The rainfall simulator was a 0.2 scale micrometer, and surface roughness was Study Site model of the “Swanson type” simulator calculated as the standard deviation of the Three upland range sites were selected (Laflen et al. 1991) which covered 2 plots, pin elevations (Renard et al. 1994). Cover for this research; Fifteen Mile drainage each 0.6 by 2 m. Pearce et al. (1998) type was calculated based on the cover west of Worland, Wyo. (108¡20'W, found that sediment yields from plots of (plant canopy, litter, rock, etc.) touched on 44¡11'N), provided the least cover, Ten this size were more sensitive to cover and the first hit of 50 pins. Mile Creek north of Worland, Wyo. surface roughness than from larger (3 by (108°8’W, 44°21'N), provided intermediate 10 m) Swanson plots. Simulator nozzles 1 Field Experimental Procedure cover, and areas along Beaver and Jack (Veejet 9570, Spraying Systems Inc. ), Specific plots were selected on 9% Creeks south of Rawlins, Wyo. (107¡7'W, and operating parameters were selected slopes and by visual observation of cover. 41¡27'N), provided the greatest cover. Soil based on laboratory calibration and nozzle A frame, which outlined both simulator types were different at the 3 sites; however, manufacturer’s data. Using these results, plots and located the center of the simula- surface soils at all sites had similar texture. the nozzles were located on a radius of 1.6 tor, was then placed on the ground parallel Vegetative and cover differences were m and height of 2.9 m. This configuration, to the slope and sheet metal plot bound- evaluated in terms of height, total cover, with an operating pressure of 42 kPa, pro- aries were driven approximately 3 cm into canopy cover, litter, rock, and biomass. duced a relatively uniform spray pattern the soil. After collecting surface soil sam- Fifteen Mile Drainage receives a mean over the plot areas. The median drop size ples adjacent to the plots and surface annual precipitation of 203 mm and has an (2 mm) was within values discussed by roughness and cover data, covered collec- average annual temperature of 7¡C. Soils Lal and Elliot (1994) for high intensity tion pans were placed at the lower end of belong to the Greybull-Persayo associa- storms. Measured drop maximum velocity each plot, the plots were covered with averaged 7.4 m sec-1 compared to 6.5 m plastic, and the simulator was started. The tion. The drainage is sparsely vegetated -1 with saltbush (Atriplex spp.), pricklypear sec for natural raindrops falling in still air plastic was removed (time = 0) and the cactus (Opuntia spp.), blue grama (de Ploey and Gabriels 1980). times at which runoff started were recorded. Runoff samples were collected for 10 (Bouteloua gracilis (H.B.K.) Lag.), and 1Use of trade names is for information purposes sec at times of 30, 60, 90, 120, 150, 180 various shrubs. Steeply sloped badlands sec, and at each 60 sec thereafter follow- cover much of the area. Primary historical only and does not constitute endorsement by the authors or their employers. ing the start of runoff.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 357 Eighteen simulations were run at Fifteen Mile with canopy cover ranging from 6 to 43% and surface roughness ranging from 1.5 to 15.7 mm; 12 simulations were run at Ten Mile with canopy cover ranging from 5 to 62% and surface roughness ranging from 5.3 to 17.6 mm; and 8 simulations were run at Beaver and Jack Creeks with canopy cover ranging from 29 to 73% and surface roughness ranging from 8 to 35 mm. Simulations were also run on tilled plots (no cover) at Ten Mile and Beaver and Jack Creeks. Plots were not tilled at Fifteen Mile because of the presence of an erosion pavement. Tilled plots seldom produced runoff and were therefore excluded from the analysis. Seven plots identified as outliers were also excluded from the analysis (Belsley 1991).

Laboratory Analyses The volume of runoff and mass of sediment collected in each sample (10 sec runoff) were determined by drying and weighing. Sieve and hydrometer analyses (ASTM D-442-63) were used to determine Fig. 1. Sediment mass in 10 sec runoff samples for a simulation with 26% total cover. The the texture of the surface soil on each sim- general shape of this curve is typical of most simulations, although the peak value ulation site. Although soil texture differed decreased as total cover increased. somewhat between the 3 sites, the soils had very little clay (maximum of < 7% boundaries were driven rather than dug in. Cover finer than 0.002 mm) and approximately Surface soils were susceptible to desicca- With 7 data points deleted as outliers, 30% silt and fine sand (0.002 to 0.1 mm). tion and surface sealing because there was regression analysis indicated that total These soils are highly erosive (Goldman et considerable fine sand and silt; however, cover explained 74% of the variability in al. 1986). The overall average soil texture tilled plots did not exhibit surface sealing. sediment yield for total cover < 30% (Fig. was 4% clay, 17% silt and 79% sand. Eolian sediment deposition would 2). However, regression analysis was not depend on wind characteristics, topograph- significant for total cover > 30% (r2 = ic features, and vegetation height, diversi- 0.01) (Fig. 3). A possible explanation of Results and Discussion ty, and morphological characteristics. In these results is that micro-channel net- addition to accumulation on the ground works, which controlled sediment trans- Sediment Yield surface, eolian sediment would be deposit- port off the plots, were better developed Sediment mass in 10 sec runoff samples ed on plant leaves and stems and would be on plots with total cover < 30%, and net- was plotted as a function of time after washed off at the beginning of rainfall works improved as total cover decreased runoff started. A typical simulation is events. The accumulation of eolian sedi- from 30%. However, for plots with total shown in Figure 1. In all simulations, peak ment would also depend on the frequency cover > 30%, micro-channel networks sediment mass was observed 120 to 180 of rainfall events of magnitude sufficient to were less developed and more random. sec after runoff started and sediment mass transport sediment off the site. Devine et Thus, sediment transport off plots with decreased to a relatively steady value al. (1998) reported that spring time sedi- total cover > 30% was decreased and sedi- within approximately 6 min. For plots ment yields observed in New Mexico ment yields were more random. Given the with total cover < 30%, the steady value might have resulted from wind deposition short duration of the simulated storm used was generally less than 15% of the peak of fine sediment. Higher wind blown dust in this study and the relatively small sedi- value. Highly erodible surface soil was levels during winter and spring were also ment yields, it is unlikely that micro-chan- flushed off the plot and then rainfall ero- reported by Pease et al. (1998). The texture nel networks were altered significantly by sion occurred at a relatively constant rate. of eolian sediment, silt and fine sand the rainfall simulations. Schreiber and Renard (1978) and Wilcox (Skidmore 1994), is typical of the texture On plots at Beaver and Jack Creeks with and Wood (1988) reported similar initial of the surface soils in this research. total cover > 70%, litter cover explained flushing. Possible explanations for this Although this discussion is subjective, it 56% of the variability in sediment yield. response include disturbance caused by offers an explanation for high stream sedi- Few if any raindrops reached the soil sur- installing plot boundaries, desiccation of ment loads produced by short duration-high face of these plots because of the high lit- the soil surface during dry periods, surface intensity storms which occur at approxi- ter cover, and only 1 plot which had total sealing during the intense storm, and accu- mately 2 year intervals. The time interval cover > 30% had a sediment yield greater mulated deposition of eolian sediment. between these storms is sufficient for accu- than 0.1 tonnes ha-1, the assumed allow- Soil disturbance caused by installing plot mulation of eolian sediment in areas adja- able soil loss (Fig. 3). This value was boundaries was minimal because the plot cent to streams under climatic conditions selected as 5% of the soil loss tolerance (2 typical of many western rangelands.

358 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 yields than did others. An attempt to use SY point frame pin elevations to predict plot micro-topography and identify micro-channel networks was unsuccessful. Note that the pin spacing was approximately 5 cm.

Revised Universal Soil Loss Equation Analysis Using cover, soil, storm characteristics, and surface roughness, sediment yields were estimated using the Revised Universal Soil Loss Equation and a modified version of that equation (Benkobi et al. 1994). Results are shown in Figure 4, and compared with sediment yields determined from the simulations. Sixteen plots with sediment yields > 0.1 tonnes ha-1 and plots with no measured sediment loss were not included in this figure. The Revised Universal Soil Loss Equation and modified version predicted very low sediment yields compared to simulation sediment yields although the modified version predicted slightly greater values than did the Revised Universal Soil Loss Equation. For total cover > 70%, the comparison improved; however, sediment yields were Fig. 2. Sediment yields (SY) for total cover (TC) less than or equal to 30%. The regression generally very low. Neglecting the flush- line is statistically significant (p < 0.01). Allowable soil loss was assumed to be 5% of the ing of fines would reduce sediment yield soil loss tolerance. values by approximately 60%; however, tonnes ha-1) for this soil (Morgan 1987). Sediment yields decreased for plots with total cover > 30%, and were very low for total cover > 70%, with the exception of 4 plots with total cover = 100%. Runoff from these plots transported litter, which affected the sediment determination.

Surface Roughness Surface roughness reflects the undula- tions of the soil surface and the surface cover, and is related to the effectiveness of the surface to influence sediment yield (Renard et al.1994). Regression analysis indicated that total cover accounted for only 19% of the variability in surface roughness, and surface roughness was weakly correlated to sediment yield (r2 = 0.06). In this study, cover was the decision variable rather than surface roughness; thus surface roughness was less significant. A possible explanation for the variability of sediment yield with surface roughness may be that plots with similar surface roughness had more or less developed micro-channel networks to transport sediment. Surface roughness did not reflect the degree of micro-channel development, and thus some plots with similar surface roughness produced much greater sediment Fig. 3. Sediment yields for total cover greater than 30%. The relationship is not statistically significant. Allowable soil loss was assumed to be 5% of the soil loss tolerance.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 359 were much higher than those predicted by the Revised Universal Soil Loss Equation or a modified version of that equation. However, the comparison improved for total cover values greater than 70%. The silt and fine sand soil texture of the surface soil and the flushing of fines were partially responsible for differences between sediment yield values measured on simulation plots and predicted values. The relative degree of micro-channel development on the plots may also have contributed to these differences.

References Cited Belsley, D.A. 1991. Conditioning diagnostics collinear and weak data in regression. John Wiley, New York, N.Y. Benkobi, L., M.J. Trlica, and J.L. Smith. 1994. Evaluation of a refined surface cover subfactor for use in RUSLE. J. Range. Manage. 47:74Ð78. Binkley, D. and T.C. Brown. 1993. Forest practices as non-point sources of pollution in North America. Water Res. Bull. 29:729Ð739. Blackburn, W.H. and M.K. Wood. 1990. Influence of soil frost on infiltration of shrub Fig. 4. Sediment yields predicted using the Revised Universal Soil Loss Equation (RUSLE) coppice and dune interspace soils in south- and a modified version of that equation (RRUSLE) (Benkobi et al. 1994), as a function of eastern Nevada. Great Basin Nat. 50:41Ð46. total cover for a most damaging storm. Sediment yields from the simulations are included Blackburn, W.H., F.B. Pierson, and M.S. -1 for comparison; however, 16 simulations with sediment yields greater than 0.1 tonnes ha Seyfried. 1990. Spatial and temporal influ- and 7 plots identified as outliers are not included. Allowable soil loss was assumed to be 5% ence of soil frost on infiltration and erosion of the soil loss tolerance. of sagebrush rangelands. Water Res. Bull. 26:991Ð997. measured values would still be consider- storm which was defined as the storm that Blackburn, W.H., F.B. Pierson, C.L. ably greater than predicted values. produced the maximum average annual Hanson, T.L. Thurow, and A.L. Hanson. Blackburn et al. (1992) concluded that sediment load in 3 Wyoming streams. 1992. The spatial and temporal influence of erosion and runoff models were inade- Sediment yields were evaluated in terms vegetation on soil surface factors in semiarid rangelands. Trans. ASAE 35:479Ð486. quate for rangelands because model para- of cover and roughness on 9% slopes hav- Bonham, C.D. 1989. Measurement of terrestrial meters did not adequately account for ing highly erosive surface soils. vegetation. Wiley Interscience, New York, N.Y. rangeland variability. In this study, para- Sediment mass eroded from the plots Branson, F.A., G.F. Gifford, K.G. Renard, meters were evaluated in detail yet the was characterized by a high initial rate as and R.F. Hadley. 1981. Rangeland hydrolo- Revised Universal Soil Loss Equation and loose sediment was flushed from the sur- gy. Range Sci. Ser. No. 1. Kendall/Hunt modified version of that equation predict- face and a lower approximately steady Publ. Co. Dubuque, Iowa. ed very low sediment yields compared to level typical of longer duration-less Cooper, C. 1979. 208 water quality manage- measured values. The degree of micro- intense storms. It is plausible that the ment plan, Big Horn Basin, Wyoming, DEQ channel development on the plots and the source of most of the sediment flushed Regional Planing Office, Basin, Wyo. de Ploey, J. and D. Gabriels. 1980. Measuring resulting sediment transport capability from the plots was accumulated eolian soil loss and experimental studies. In: M.J. may have been a factor in this comparison sediment deposition. Kirkby and R.P.C. Morgan (eds.) Soil ero- and in Blackburn’s study. Micro-channel Assuming an allowable soil loss of 0.1 sion. John Wiley, New York, N.Y. networks are not considered in current tonnes ha-1 (5% of the allowable soil loss Devine, D.L., M.K. Wood, and G.B. Donart. rangeland erosion and runoff models. tolerance for the soil), 30% total cover 1998. Runoff and erosion from a mosaic provided adequate erosion protection for tobosograss and burrograss community in the most damaging storm. Sediment yields northern Chihuahuan desert grassland. J. Summary and Conclusions decreased moderately for greater than 30% Arid Environ. 39:11Ð19. total cover and were very low for greater Goldman, S.J., K. Jackson, and T.A. Burztynsky. 1986. Erosion and sediment than 70% total cover. The influence of Rainfall simulations were used to evalu- control handbook. McGraw-Hill, New York, cover on the relative development of ate soil erosion from 3 undisturbed upland N.Y. micro-channel networks and thus on sedi- Wyoming range sites. A 0.2 scale (2 plots, Haan, C.T., B.J. Barfield, and J.C. Hayes. ment transport off the plots, may explain each 0.6 x 2 m) “Swanson type” simulator, 1994. Design hydrology and sedimentology these results. was used to simulate a most damaging for small catchments. Academic Press, San Sediment yields from simulation plots Diego, Calif.

360 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Heady, H.F. and R.D. Child. 1994. Rangeland Pearce, R.A., G.W. Frasier, M.J. Trlica, Skidmore, E.L. 1994. Wind erosion. In: R. Lal ecology and management. Westview Press, W.C. Leininger, J.D. Stednick, and J. L. (ed.) Soil erosion research methods. 2nd ed. Boulder, Colo. Smith. 1998. Sediment filtration in a mon- St. Lucie Press, Delray Beach, Fla. Hogan, D.W. 1988. Wyoming statewide water tane riparian zone under simulated rainfall. J. Weltz, M.A. and W.H. Blackburn. 1995. quality assessment report. Wyoming DEQ Range Manage. 51:309Ð314. Water budget for south Texas rangelands. J. Cheyenne, Wyo. Pease, P.P., V.P. Tchakerian, and N.W. Range Manage. 48:45Ð52. Huffsmith, R.L. 1988. Alternative sediment Tindale. 1998. Aerosols over the Arabian Weltz, M.A. and M.K. Wood. 1986. Short control in surface mine reclamation. MS Sea: geochemistry and source areas for aeo- duration grazing in central New Mexico: Thesis, University of Wyoming, Laramie, lian desert dust. J. Arid Environ. 39:477-496. effects on sediment production. J. Soil Water Wyo. Ponce, V.M. 1989. Engineering hydrology Cons. 41:262Ð266. Laflen, J.M., W.J. Elliot, J.R. Simanton, C.S. principles and practices. Prentice-Hall, Weltz, M.A., A.B. Arslan, and L.J. Lane. 1992. Hydraulic roughness coefficients for Holzhey, and K.D. Kohl. 1991. WEPP soil Englewood Cliffs, N.J. native rangelands. J. Irrig. Drain. Eng. erodibility experiments for rangelands and Renard, K.G., J.M. Laflen, G.R. Foster, and 118:776Ð790. cropland soil. J. Soil Water Cons. 46:39Ð44. D.K. McCool. 1994. The revised universal Wilcox, B.P. and M.K. Wood. 1988. Lal, R. and W. Elliot. 1994. Erodibilty and soil loss equation. In: R. Lal (ed.) Soil ero- Hydrologic impacts of sheep grazing on erosivity. In: R. Lal (ed.) Soil erosion sion research methods. 2nd ed. St. Lucie steep slopes in semiarid rangelands. J. research methods. 2nd ed. St. Lucie Press, Press, Delray Beach, Fla. Range. Manage. 41:303Ð306. Delray Beach, Fla. Schreiber, H.A. and K.G. Renard. 1978. Linsley, R.K., M.A. Kohler, and J.L.H. Runoff water quality from varying land uses Paulhus. 1982. Hydrology for engineers. 3rd in southeastern Arizona. J. Range Manage. ed. McGraw-Hill, New York, N.Y. 31:274Ð279. Morgan, R.P.C. 1987. Soil erosion and conser- Seyfried, M.S. 1991. Infiltration patterns from vation. Longman Sci. Tech. Publ. Essex, simulated rainfall on a semiarid rangeland England. soil. J. Soil Sci. Soc. Amer. 55:1726Ð734. Naeth, M.A., A.W. Bailey, D.J. Luth, D.S. Simanton, J.R., M.A. Weltz, and H.D. Chanasyk, and R.T. Hardin. 1991. Grazing Larson. 1991. Rangeland experiments to impacts on litter and soil organic matter in parameterize the water erosion prediction project model: vegetation canopy cover mixed prairie fescue grassland ecosystems of effects. J. Range Manage. 44:276Ð282. Alberta. J. Range. Manage. 44:7Ð12.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 361 J. Range Manage. 54: 362Ð369 July 2001 Restoring tallgrass prairie species mixtures on leafy spurge-infested rangeland

ROBERT A. MASTERS, DANIEL D. BERAN, AND ROCH E. GAUSSOIN

Authors are field development biologist, Dow AgroSciences, 3618 South 75th Street, Lincoln, Nebr. 68506, market development specialist, BASF, 1422 57th, Place, Des Moines, Iowa, and extension turfgrass specialist, Department of Agronomy and Horticulture, University of Nebraska, Lincoln, Nebr. 68583. At time of this research, Masters was rangeland scientist, USDA-ARS, 344 Keim Hall, University of Nebraska, Lincoln, Nebr. 68583 and Beran was research assistant, Department of Agronomy and Horticulture, University of Nebraska, Lincoln, Nebr. 68583.

Abstract Resumen

Leafy spurge (Euphorbia esula L.) reduces northern Great El “Leafy spurge (Euphorbia esula L.) reduce la capacidad de Plains rangeland carrying capacity. Treatment strategies were carga de los pastizales del norte de las Grandes Planicies. Se evaluated that suppressed leafy spurge and facilitated establish- evaluaron estrategias de tratamiento que suprimen el “Leafy ment of mixtures of native grasses and legumes on range sites spurge” y facilitaron el establecimiento de mezclas de zacates near Mason City and Tilden, Nebr. Glyphosate at 1,600 g a.i. nativos y leguminosas en sitios de pastizal cercanos a Mason (active ingredient) ha-1 was applied with or without imazapic at City, Nebr. En Octubre de 1995 se aplico Glifosato en dosis de 140 or 210 g a.i. ha-1 in October 1995. In April 1996, standing crop 1600 g i.a. (i.a. = ingrediente activo) con y sin Imazapic en dosis was burned or mowed. Mixtures of native grasses [big bluestem de 140 o 210 g i.a. ha-1. En Abril de 1996 el forraje en pie fue (Andropogon gerardii Vitman), indiangrass (Sorghastrum nutans segado o quemado y después se plantaron mezclas de zacates (L.) Nash), switchgrass (Panicum virgatum L.), little bluestem nativos [“Big bluestem” (Andropogon gerardii Vitman), (Schizachyrium scoparium (Michx.) Nash), and sideoats grama “Indiangrass” (Sorghastrum nutans (L.) Nash), “Switchgrass” (Bouteloua curtiplendula (Michx.) Torr.)] were then planted with (Panicum virgatum L.), “Little bluestem” (Schizachyrium scopari- or without native legumes [leadplant (Amorpha canescens (Nutt.) um (Michx.) Nash), and “Sideoats grama” (Bouteloua curtiplen- Pursh), Illinois bundleflower (Desmanthus illinoensis (Michx.) dula (Michx.) Torr.)] con y sin leguminosas nativas MacM.), and purple prairieclover (Petalostemum purpureum [“Leadplant” (Amorpha canescens (Nutt.) Pursh), “Illinois (Vent.) Rybd.)] at 440 pls m-2 into a non-tilled seedbed. Imazapic bundleflower” (Desmanthus illinoensis (Michx.) MacM.), and was applied at 70 g a.i. ha-1 in June 1996 to half the plots that had “Purple prairieclover” (Petalostemum purpureum (Vent.) Rybd.)] been treated with imazapic in October 1995. Frequency, dry mat- a una densidad de 440 SPV m-2 en camas de siembra sin labran- ter yield, and leafy spurge density were measured 14 to 16 months za. En Junio de 1996 a la mitad de las parcelas que en Octubre after planting. Leafy spurge density and yield were least, and fre- de 1995 habían sido tratadas con Imazapic se les aplico Imazapic quencies and yields of the planted grasses usually were greatest a una dosis de 70 g i.a ha-1. Después de 14 a 16 meses de la siem- where imazapic had been applied with glyphosate in October bra se midió la frecuencia, densidad y rendimiento de materia 1995. Purple prairieclover was the only planted legume to persist seca de “Leafy spruge”. La densidad y rendimiento de "Leafy 14 months after planting, and yields were greatest where imaza- spurge" fueron menores y las frecuencias y rendimientos de los pic was applied with glyphosate. Imazapic applied in June 1996 zacates plantados usualmente fueron mayores en las áreas donde usually did not improve planted species yields or leafy spurge se aplico Imazapic con Glifosato en Octubre de 1995. La única control. Total vegetation yields were greater where imazapic was leguminosa que persistió después de 14 meses de la siembre fue applied with glyphosate at both sites and where native species el “Purple prairieclover” y los rendimientos fueron mayores were seeded at Mason City. Vegetation suppression with fall- donde se aplico Imazapic con Glifosato. El Imazapic aplicado en applied herbicides and removal of standing crop enabled success- Junio de 1996 usualmente no mejoro los rendimientos de las ful establishment of desirable species, increased forage yields, and especies plantadas o el control de "Leafy spurge”. Los suppressed leafy spurge. rendimientos totales de la vegetación fueron mayores donde se aplico Imazapic con Glifosato, esto fue similar en ambos sitios y donde las especies nativas se sembraron en Manso City. La Key Words: Prescribed fire, grassland restoration, imazapic, supresión de vegetación con herbicidas aplicados en otoño y la glyphosate, warm-season grasses, cool-season grasses, legumes, remoción de la vegetación en pie permitio el establecimiento exi- invasive plants toso de especies deseables, incrementó los rendimientos de forraje y suprimió el “Leafy spurge”.

Research was funded in part by American Cyanamid, Monsanto, University of Nebraska Foundation-Arthur Sampson Range and Pasture Management Endowment Fund, and United States Environmental Protection Agency. The authors thank Kevin Leafy spurge (Euphorbia esula L.) is an invasive noxious weed Grams, Fernando Rivas-Pantoja, and Ken Carlson for their assistance with plot that alters the function and structure of North American range- installation and sampling. This paper is a joint contribution of the USDA-ARS and land ecosystems. Leafy spurge was introduced from Eurasia into the Nebraska Agriculture Research Division Journal Series No. 13133. Manuscript accepted 30 Sept. 00. the northern Great Plains and prairie provinces of Canada in the

362 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 late 1800s (Watson 1985) and now infests the search for a single control technology sulfometuron {2-[[[[(4,6-dimethyl-2-pyrim- more than 1 million ha in North America to development of integrated strategies idinyl)amino]carbonyl]amino]sulfonyl]ben (Dunn 1979). This invasive plant displaces composed of multiple technologies used in zoic acid} in the fall and burned the fol- native species (Belcher and Wilson 1989) sequences and combinations that optimize lowing spring before tallgrasses were and reduces livestock carrying capacity weed control and rangeland improvement planted into the herbicide-suppressed sod (Lym and Kirby 1987). Leafy spurge inva- (Scifres 1987). A goal of rangeland weed without tillage. These studies demonstrate siveness is attributed to its ability to repro- management should be to improve degrad- that leafy spurge-infested rangeland can be duce from seed, adventitious shoot buds ed rangeland communities so they are less improved in the short-term by planting on the crown and roots (Raju 1985), and susceptible to invasion by weeds (Masters monoculture stands of desirable forage the lack of natural enemies in North et al. 1996, Sheley et al. 1996, Masters grasses; however, the rate of leafy spurge America (Harris et al. 1985). High seed and Nissen 1998). Invasive plants appear recovery and management required to yields and viability and rapid seedling to be a symptom of management problems maintain monoculture grass stands, while development enable new infestations to that must be corrected before sustained suppressing leafy spurge, has not been establish quickly (Selleck et al. 1962). progress can be made toward controlling determined. Past management practices appear to have weeds and improving rangeland produc- The focus of our rangeland improve- hastened leafy spurge establishment and tivity. Removing a weed species with ment research effort was to develop inte- spread in the Great Plains (Masters et al. chemical or biological controls may only grated management strategies that sup- 1996). provide an open niche for another undesir- press leafy spurge and associated vegeta- Chemical and biological controls have able species unless desirable species are tion, and facilitate planting and establish- been the primary means to manage leafy present to occupy the vacated niche. In ment of multiple native warm-season grass spurge. Long-term control of leafy spurge many instances, rangeland vegetation has and legume species. Conceptually, multi- is possible with picloram (4-amino-3,5,6- deteriorated to the point that desirable species assemblages should more fully use trichloro-2-pyridinecarboxylic acid) applied species are either not present or in such resources on degraded rangeland and more at 2.2 kg a.i. (active ingredient) ha-1 or low abundance that plant community completely preempt resource use by less greater rates (Lym and Messersmith 1985). recovery may not occur without revegeta- desirable species, including leafy spurge. The high cost of this treatment and con- tion with desirable species. The purpose of this study was to deter- cerns about surface water and groundwater Approaches that include herbicide appli- mine if application of herbicides followed contamination precludes picloram use on cation and establishing monoculture by mowing or burning the herbaceous large infestations. Application of 2,4-D stands of introduced or native perennial standing crop could enhance establishment [(2,4-dichlorophenoxy)acetic acid] + grasses have been used successfully to of planted mixtures of native species and picloram at 1.1 + 0.28 kg a.i. ha-1 or 2,4-D suppress leafy spurge and improve forage reduce leafy spurge productivity. alone at 2.2 kg a.i. ha-1 provides short-term production on rangeland. In Wyoming, Glyphosate and imazapic were the herbi- control of leafy spurge and reduces seed seedbed preparation consisted of multiple cides selected to suppress leafy spurge and production. Imazapic {2-[4,5-dihydro-4- applications of glyphosate [N-(phospho- existing resident vegetation. Glyphosate methyl-4-(1-methyl-ethyl)-5-oxo-1H-imi- nomethyl)glycine] in spring and summer controls cool-season grasses that are dazol-2-yl]-5-methyl-pyridine carboxylic followed by tillage before planting intro- actively growing at the time of applica- acid}, applied in the fall for 2 consecutive duced cool-season grasses (Ferrell et al. tion, but provides no residual weed con- years at 140 g a.i. ha-1 controlled more 1998). Introduced cool-season grasses trol. Imazapic provides residual control of than 90% of the leafy spurge 11 to 12 were planted in a tilled seedbed following leafy spurge, annual grasses, and broadleaf months after the second application application of glyphosate and 2,4-D in plants that would interfere with establish- (Masters et al. 1998). The efficacy of North Dakota (Lym and Tober 1997). The ment of planted species. Imazapic is toler- imazapic results from high absorption, planted grasses that were most effective in ated by a number of warm-season grasses preferential translocation to roots and suppressing leafy spurge were ‘Bozoisky’ (Rivas-Pantoja et al. 1997, Beran et al. adventitious shoot buds, and slow rate of Russian wildrye [Psathyrostachys juncea 2000), forbs (Beran et al. 1999a) and metabolism of this herbicide by leafy (Fisch.) Nevski] and ‘Luna’ pubescent legumes (Beran et al. 1999b). Herbaceous spurge (Thompson et al. 1998). Biological wheatgrass [Elytrigia intermedia (Host) standing crop was removed to reduce the control agents used against leafy spurge Beauv.] in Wyoming, and ‘Rebound’ quantity of the plant residue that would include goats (Lym et al. 1997), sheep smooth bromegrass (Bromus inermis L.) otherwise interfere with no-till of planting (Landgraf et al. 1984), and insects and ‘Reliant’ intermediate wheatgrass desirable native species into the herbicide- (Hansen et al. 1997). Flea beetles reduced [Thinopyrum intermedium (Host) Barkw. suppressed sod. leafy spurge densities at some sites in & D.R. Dewey] in North Dakota. In North Dakota, but these reductions did not Nebraska, monoculture stands of native have a positive effect on grass yields warm-season grasses, big bluestem Materials and Methods (Kirby and Carlson 1998). Establishment (Andropogon gerardii Vitman), indian- of flea beetle populations has been highly grass [Sorghastrum nutans (L.) Nash], and Experiments were established on leafy variable in the northern Great Plains and switchgrass (Panicum virgatum L.), estab- spurge-infested rangeland near Mason factors responsible for this uneven success lished on leafy spurge-infested rangeland City (41¡ 17' N, 99¡ 17' W) and Tilden have not been identified (Lym 1998). increased herbage yields by more than City (42¡ 00’ N, 97° 53’ W), Nebr. The Historically, rangeland weed manage- 40% and reduced leafy spurge density and distance between the sites is about 150 ment research has emphasized develop- yield (Masters and Nissen 1998). The sites km, and Mason City and Tilden are locat- ment of chemical and biological control were treated with imazapyr {2-[4,5-dihydro- ed in south-central and northeastern tactics. There is growing recognition that 4-methyl-4-(1-methylethyl)-5-oxo-1H-imi- Nebraska, respectively. These sites occur rangeland weed research should shift from dazol-2-yl]-3-pyridinecarboxylic acid} and in the mixed-grass prairie region of the

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 363 central Great Plains. Soil at Mason City threeawn, sand dropseed, buffalograss, and legume mixture, were planted in sepa- was a Uly silt loam (mixed, mesic, Typic and blue grama) by imazapic applied in rate sub-subplots, and no species were Haplustoll) and at Tilden was a Thurman June 1996 would further enhance estab- planted in the third sub-subplot. Equal fine sand (mixed, mesic, Udorthentic lishment of the planted species. Leafy numbers of pure live seed of each species Haplustoll). The flora at both sites was spurge and cool-season grasses were were included in each mixture to achieve a dominated by leafy spurge, Kentucky growing, and warm-season grasses were seeding rate of 440 pls m-2. The grass bluegrass (Poa pratensis L.), and smooth dormant when herbicides were applied in species in the grass or grass and legume bromegrass. Warm-season grasses at October. Leafy spurge and cool-season mixtures were big bluestem, indiangrass, Mason City included buffalograss grasses were flowering, while warm-sea- switchgrass, little bluestem [Schizachyrium [Buchloe dactyloides (Nutt.) Engelm.], tall son grasses were vegetative when herbi- scoparium (Michx.) Nash], and sideoats dropseed [Sporobolus asper (Michx.) cide was applied in June. Herbicides were grama [Bouteloua curtipendula (Michx.) Kunth], and red threeawn (Aristida applied in a total delivery volume of 187 Torr.]. Legumes in the grass and legume longiseta Stued.). At Tilden, warm-season liters ha-1 at 3 km hour-1 and at 250 kPa mixture were leadplant [Amorpha grasses included sand bluestem with a tractor-mounted, compressed-air- canescens (Nutt.) Pursh], Illinois bundle- (Andropogon halli Hack.), big bluestem, pressurized sprayer. Methylated seed oil flower [Desmanthus illinoensis (Michx.) sand dropseed [Sporobolus cryptandrus and 28% urea ammonium fertilizer, each MacM.], and purple prairieclover (Torr.) A. Gray], and blue grama at 1.25% (v/v), were included in spray (Petalostemum purpurea Vent.). Seed [Bouteloua gracilis (H.B.K.) Lag. ex solutions to optimize foliar uptake of her- mixtures were planted directly into the sod Steud.]. Both sites had a management histo- bicides. with no tillage on 11 April 1996 at Mason ry of moderate to heavy continuous grazing At each site, there were 3 different City and 26 April 1996 at Tilden using a by cattle during spring and summer. Sites planting treatments per sub-subplot. Two 7-row plot drill with an 18-cm spacing were not grazed or hayed during the study. seed mixtures, grass mixture only or grass between rows at a 1.3-cm depth. Native Experiments at both sites were designed as a randomized complete block arranged as a split-split plot with 4 replications per treatment combination. Standing crop management schemes were the main plot (10- by 48-m at Mason City and 16- by 30-m at Tilden), herbicides were the subplot (8- by 5-m in size), and native plant mixtures were the sub-subplot (8- by 1.6- m in size) treatments. At Mason City, the standing crop on 4 main plots was mowed to a 10 cm stubble height followed by removal with a dump rake on 3 April 1996 and was removed from the remaining 4 main plots by burning on 4 April 1996. At Tilden, the Kentucky bluegrass thatch that remained after mowing and raking the standing crop on 4 of the 8 main plots on 8 April 1996 was too heavy to allow pene- tration of the grass drill double disk open- ers during planting. This thatch layer was reduced on 9 April 1996 with a self-pro- pelled dethatcher followed by raking. Standing crop was removed from the remaining main plots by burning on 17 April 1996. Main plots at both sites were burned according to Masters et al. (1990). Herbicide treatments were applied to separate subplots in October 1995 and June 1996. Glyphosate at 1600 g a.i. ha-1 was applied alone or in combination with imazapic at 140 or 210 g a.i. ha-1 on 3 October 1995 at Mason City and 11 October 1995 at Tilden. Imazapic was applied at 70 g a.i. ha-1 on 19 June 1996 at Mason City and 17 June 1996 at Tilden to half the number of plots that had been treated with imazapic in October 1995. This treatment was used to determine if additional suppression of leafy spurge and less desirable warm-season grasses (red Fig. 1. Monthly precipitation for 1995 through 1997 and 30 year averages at Mason City and Tilden, Nebr.

364 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 plant mixtures were planted without tillage spurge density was determined by record- City and Tilden during this period in 1997. to reduce soil erosion, soil water loss, and ing the number of live shoots emerging Leafy spurge density and yield in cost of seedbed preparation. from the soil surface within quadrats August 1997 were usually reduced where Frequency and herbage dry matter yield placed in each sub-subplot during harvest. imazapic was applied with glyphosate were measured between 14 and 16 months Data from each site were analyzed sepa- (Table 1). At Mason City, leafy spurge after planting. Measurements were taken rately using the general linear model pro- density averaged 147 shoots m-2 where no the year after planting because establish- cedure (SAS 1996). Frequency, density, herbicide was applied and 62 shoots m-2 ment of perennial plants from seed is best and yield data were tested by analysis of where imazapic at 210 g ha-1 was applied determined after plants have survived a variance using a split-split plot model. with glyphosate. At Tilden, leafy spurge period of dormancy during the winter Response variables were analyzed within densities averaged ≥ 97 shoots m-2 where (Cook and Stubbendieck 1986). Both sites site because several variables had signifi- no herbicide or glyphosate was applied. were burned in mid-spring 1997 to reduce cant (P ≤ 0.05) site interactions and het- In contrast, leafy spurge densities were interference of standing dead herbage with erogeneous error variances as indicated by reduced to ≤ 14 shoots m-2 where imazapic vegetation sampling. Hartley’s F-max test (Hartley 1950). was applied with glyphosate. At both sites, Frequency was measured because it Planted species and leafy spurge yield data leafy spurge yields were reduced more integrates pattern and abundance were log transformed (Lentner and Bishop than 65% where imazapic was applied (Goldsmith and Harrison 1976), 2 impor- 1993). Data from significant (P ≤ 0.05) with glyphosate compared with yields tant attributes when determining planted highest order interactions are presented where no herbicide was applied. Imazapic species establishment. Frequencies were with means separated using Fisher’s- pro- reapplied in June 1996 did not provide determined in mid-June 1997 using a 90- tected LSD (alpha = 0.05) (Ott 1977). additional reduction in leafy spurge densi- by 90-cm (0.81 m2) metal frame parti- ty or yield compared with imazapic tioned into a grid of twenty-five, 18- by applied in October 1995. The amount of 18-cm, cells. The frame was placed over Results and Discussion imazapic applied in June may have been the center 5 rows at 2 locations within insufficient to provide additional leafy each subplot. Presence or absence of a Annual precipitation at National spurge control. seeded grass or legume in each cell within Oceanographic and Atmospheric At Mason City, native grass frequency the frame was recorded. Frequency within Administration stations within 15 km of was influenced by herbicide and standing each frame was calculated by dividing the the study sites during 1995, 1996, and crop treatments (Table 2). Native grass number of cells that contained at least 1 1997 ranged from 2 to 10% above the 30- frequencies where no herbicide or only seeded species by 25 and then multiplying year average near Mason City and from glyphosate was applied were 11% or less by 100 to convert the calculated propor- 30% below average to 29% above average compared with frequencies that exceeded tion to a percentage. For this study, a near Tilden (Fig. 1). April through August 34% where imazapic was applied with threshold frequency above which estab- encompasses the time that the perennial glyphosate. Native grass establishment lishment of the planted grasses was con- native grasses and legumes were planted was successful (≥ 32%) only where imaza- sidered successful was determined. and period of peak production of the vari- pic was applied with glyphosate. Launchbaugh and Owensby (1970) report- ous vegetation components. Cumulative Frequencies were greater where the ed that >10 plants m-2 were needed for precipitation from April through August residue was mowed and raked before successful grass establishment in the cen- 1996 near Mason City was 408 mm and planting. Residue that remained after tral Great Plains. We estimated that a near Tilden was 368 mm. Cumulative pre- mowing and raking could have ameliorat- planted grass frequency of 32% (≥ 1 grass cipitation was 401 and 286 mm at Mason ed the seedbed environment, dampening plant in 8 of the 25 cells within the grid used to determine frequency) was about Table 1. Leafy spurge density and yield at rangeland sites near Mason City and Tilden, Nebr. in -2 August 1997 that were treated with herbicides, burned or mowed, and seeded with grass or grass equivalent to 10 plants m . This is a con- 1, 2 servative estimate, since it is based on the and legume mixtures. presence of only 1 seeded grass plant in each of 8 cells within the frequency grid. Rate Mason City Tilden Herbicide Fall Spring Density Yield3 Density Yield3 Dry matter yield of selected components -1 -2 -1 -2 -1 of the vegetation and leafy spurge shoot (g a.i. ha ) (no. m ) (kg ha ) (no. m ) (kg ha ) density were determined in early August Non-Treated 0 0 147 340 a 117 240 a 1997. Dry matter yields were determined Glyphosate 1600 0 125 250 b 97 150 a by harvesting vegetation within two, 0.25- Imazapic + 140 0 82 120 c 14 60 b m2 quadrats within each sub-subplot. glyphosate 1600 0 Vegetation within each quadrat was Imazapic + 140 70 59 100 c 4 10 c clipped to a 2-cm stubble height, separat- glyphosate 1600 0 ed, oven-dried at 60¡ C to a constant Imazapic + 210 0 62 120 c 8 10 c weight, and weighed. Vegetation was sep- glyphosate 1600 0 arated into the following categories: big Imazapic + 210 70 34 50 c 1 0 d bluestem; switchgrass; indiangrass; little glyphosate 1600 0 bluestem; sideoats grama; purple LSD (0.05) 65 — 22 — prairieclover; leadplant; Illinois bundle- 1Herbicides were applied in October 1995 (Fall) and June 1996 (Spring). Burn and mow treatments were applied and flower; leafy spurge; warm-season grasses grass and grass and legume mixtures were planted in April 1996. 2Measured attributes are averaged across burn and mow treatments and planting treatments. (not including planted grasses); cool-sea- 3Means followed by the same letter within a column are not significantly different (P ≤ 0.05). Non-transformed means son grasses; and forbs (not including are presented, but mean separation test is based on analysis of log transformed data. planted legumes or leafy spurge). Leafy

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 365 Table 2. Frequency of planted native grasses (NG) and purple prairieclover (PPC) in June 1997 at rangeland sites near Mason City and Tilden, Nebr. that were treated with herbicides, burned (B) or mowed (M), and seeded with grass (G) or grass and legume mixtures (GL).1

Tilden Mason City NG Rate NG2 B M Herbicide Fall Spring B M PPC3 G GL G GL PPC3 (g a.i. ha-1) ------(%) ------Non-Treated 0 0 0 1 0 0 1 0 0 0 Glyphosate 1600 0 0 11 4 33 51 33 33 4 Imazapic + 140 0 34 69 26 79 29 58 61 11 glyphosate 1600 0 Imazapic + 140 70 45 73 20 57 63 68 45 11 glyphosate 1600 0 Imazapic + 210 0 48 63 18 65 63 49 53 12 glyphosate 1600 0 Imazapic + 210 70 53 68 19 69 50 61 59 15 glyphosate 1600 0

LSD (0.05) ----- 12 ----- 8 ------16 ------8 1Herbicides were applied in October 1995 (Fall) and June 1996 (Spring). Burn and mow treatments were applied and grass and grass and legume mixtures were planted in April 1996. 2Native grass frequencies are averaged across grass and grass and legume mixture treatments. 3Purple prairieclover frequencies are averaged across burn and mow treatments. variations in temperature extremes and bluestem, indiangrass, and little bluestem there was no difference in big bluestem soil water loss, compared with areas where yields at Mason City were greater where yields where glyphosate was applied with the residue was consumed by fire. imazapic was applied than where no herbi- or without imazapic (Table 4). When At Tilden, native grass frequency was cide or only glyphosate was applied assessing yields of the various species influenced by the interaction of herbicide, (Table 3). Sideoats grama and switchgrass within the planted mixtures it is important residue, and planting treatments (Table 2). yields were very low, regardless of herbi- to note that these data reflect species com- Native grass frequencies where no herbicide treatment. Sideoats grama yields may position early in the development of these cide was applied were 1% or less com- have been low because this mid-grass is plant stands. The distribution and compo- pared with frequencies that usually not as productive and may not have been sition of species will likely change as the exceeded 32% where glyphosate was as competitive as the planted tallgrasses. stands mature under prevailing climate applied with or without imazapic. In a few Low yields of switchgrass may reflect its and management regimes. instances, grass frequencies were lower susceptibility to imazapic as reported by Purple prairieclover was the only where the grass and legume mixture had Masters et al. (1996). At Tilden, indian- legume to persist 14 months after planting been planted compared with where only grass yields were greatest where imazapic at both study sites. Frequency of purple the grass mixture was planted. This could was applied with glyphosate, whereas prairieclover was ≥ 18% and 11% where have been because more grass seeds were planted in the grass mixture compared Table 3. Yield of big bluestem (BB), indiangrass (IN), little bluestem (LB), sideoats grama (SG), with the grass and legume mixture. The switchgrass (SW), and purple prairieclover (PPC) and combined yield of grass (G) and grass -2 total seeding rate was 440 pls m per mix- and legume (GL) mixtures in August 1997 at a rangeland site near Mason City, Nebr. that was ture, which was 88 pls m-2 for each of the treated with herbicides, burned (B) or mowed (M), and seeded with grass or grass and legume 5 species planted in the grass mixture and mixtures.1, 2 55 pls m-2 for each of the 8 species (5 grasses and 3 legumes) in the grass and Rate Planted species3 4 legume mixture. Herbicide Fall Spring BB IN LB SG + SW PPC Combined yield Imazapic applied with glyphosate (g a.i. ha-1) ------(Mg ha-1) ------improved combined yields of the planted Non-Treated 0 0 0 a 0 a 0 a 0 a 0 a 0 a species in the grass mixture or grass and Glyphosate 1600 0 0.1 b 0.1 b 0 a 0 a 0 a 0.3 b legume mixture at both study sites (Tables Imazapic + 140 0 0.8 c 1.6 c 0.3 b 0.1 a 0.6 b 3.0 c 3 and 4). Combined yields ranged from glyphosate 1600 0 -1 3.0 to 4.6 Mg ha at Mason City and 1.9 Imazapic + 140 70 0.9 c 2.1 c 0.3 b 0 a 0.2 b 3.5 c to 3.0 Mg ha-1 at Tilden where imazapic glyphosate 1600 0 was applied with glyphosate. In contrast, Imazapic + 210 0 0.8 c 1.8 c 0.5 b 0 a 0.3 b 3.3 c yields were 0.3 Mg ha-1 at Mason City and glyphosate 1600 0 -1 1.2 Mg ha at Tilden where only Imazapic + 210 70 1.1 c 2.9 c 0.3 b 0 a 0.4 b 4.6 c glyphosate was applied, and 0.3 Mg ha-1 or glyphosate 1600 0 less at both sites where no herbicide was 1Herbicides were applied in October 1995 (Fall) and June 1996 (Spring). Burn or mow treatments were applied and grass or grass and legume mixtures were planted in April 1996. applied. Big bluestem and indiangrass 2 were the dominant grasses in the planted Means followed by the same letter within a column are not significantly different (P ≤ 0.05). Non-transformed means are presented, but mean separation test is based on analysis of transformed data. stands. They comprised more than 60% of 3Planted grass yields are averaged across planted grass and grass and legume mixtures and burn and mow treatments. the combined yields where imazapic was Prairieclover yields are averaged across burn and mow treatments. 4 applied with glyphosate at both sites. Big Combined yields are averaged across planted grass and grass and legume mixtures and burn and mow treatments.

366 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 4. Yield of big bluestem (BB), indiangrass (IN), little bluestem (LB), sideoats grama (SG), ranged from 0.6 to 0.8 Mg ha-1 where switchgrass (SW), and purple prairieclover (PPC) and combined yield of grass (G) and grass imazapic was applied with glyphosate and and legume (GL) mixtures in August 1997 at a rangeland site near Tilden, Nebr. that was treat- -1 ed with herbicides, burned (B) or mowed (M), and seeded with grass or grass and legume mix- were < 0.3 Mg ha where no herbicide or tures.1, 2 only glyphosate was applied. Yields of the warm-season grasses were less than 0.2 -1 Rate Planted species3 Mg ha where grass or grass and legume Herbicide Fall Spring BB IN SG + LB PPC Combined yield4 mixtures were planted and were 1.3 Mg +SW ha-1 where no species were planted. This (g a.i. ha-1) ------(Mg ha-1) ------response of the resident warm-season Non-Treated 0 0 0 a 0.1 a 0.2 a 0 a 0.3 a grasses resulted from remnant native Glyphosate 1600 0 0.4 b 0.2 a 0.5 a 0.2 b 1.2 b grasses at Tilden that were released after Imazapic + 140 0 0.5 b 0.9 b 0.4 a 0.1 b 1.9 c leafy spurge and other resident vegetation glyphosate 1600 0 was suppressed by the herbicides. Imazapic + 140 70 0.8 b 1.3 b 0.7 a 0.3 b 3.0 c Total vegetation yield (planted species glyphosate 1600 0 yield + resident vegetation yield) respons- Imazapic + 210 0 0.6 b 0.9 b 0.8 a 0.2 b 2.4 c es to the treatments varied by site. At glyphosate 1600 0 Mason City, the interaction of herbicide Imazapic + 210 70 0.7 b 1.4 b 0.5 a 0.2 b 2.6 c and planting treatments was significant (P glyphosate 1600 0 ≤ 0.05) (Table 5). Yields, ranging from 2.0 1Herbicides were applied in October 1995 (Fall) and June 1996 (Spring). Burn or mow treatments were applied and to 2.7 Mg ha-1, were similar across planti- grass or grass and legume mixtures were planted in April 1996. ng treatments where no herbicide or only 2Means followed by the same letter within a column are not significantly different (P ≤ 0.05). Non-transformed means are presented, but mean separation test is based on analysis of transformed data. glyphosate was applied. In contrast, total 3Planted grass yields are averaged across planted grass and grass and legume mixtures and burn and mow treatments. yields from imazapic-treated areas were Prairieclover yields are averaged across burn and mow treatments. -1 4 greater and ranged from 4.1 to 7.0 Mg ha Combined yields are averaged across planted grass and grass and legume mixtures and burn and mow treatments. where grass or grass and legume mixtures were planted, while yields where no imazapic was applied with glyphosate at Effects of herbicides on yields of resi- species were planted ranged from 2.3 to Mason City and Tilden, respectively dent cool- and warm-season grasses and 3.2 Mg ha-1. These substantive yield (Table 2), compared with 4% or lower fre- forbs were inconsistent at both sites. At increases provide evidence for the sup- quencies where no herbicide or only Mason City, cool-season grass yields pression of existing vegetation by imaza- -1 glyphosate was applied. Purple prairieclover ranged from 0.8 to 1.3 Mg ha where pic applied with glyphosate, which facili- yields were greater at both sites where her- imazapic was applied with glyphosate tated establishment of the planted species. -1 bicides had been applied and contributed at compared with 1.0 Mg ha or more where Moreover, increased dry matter yield most 20% and usually less than 10% to the glyphosate or no herbicide was applied. where the planted grasses were successful- combined herbage yield (Tables 3 and 4). Warm-season grass and forb yields were ly established demonstrates that the pro- Illinois bundleflower was common at both not affected by herbicides and ranged ductivity of the leafy spurge-dominated -1 sites within the first 3 months after planting, from 0.3 to 0.5 Mg ha . At Tilden, cool- plant community was far lower than the but did not persist. Leadplant was rarely season grass yields were not affected by potential for the site. observed during the study. herbicide treatments and ranged from 0.3 Total vegetation yield at Tilden was -1 Successful establishment of only 1 of to 0.8 Mg ha . Warm-season grass yields influenced by herbicides, but not by plant- the 3 planted legume species in this study highlights potential problems using native legumes in rangeland revegetation pro- Table 5. Total yield of vegetation on rangeland sites near Mason City and Tilden, Nebr. in August 1997 that were treated with herbicides, burned or mowed, seeded with grass (G) or grass and grams. High cost, low availability, and 1 variable quality of native legume seeds legume mixtures (GL) or not seeded (NS). further constrain their use. Legumes may Rate Mason City2 improve N availability in degraded range- 2 land ecosystems, while providing a sus- Herbicide Fall Spring G GL NS Tilden -1 -1 tainable and higher quality forage (g a.i. ha ) ------(Mg ha ) ------resource. Posler et al. (1993) found that Non-Treated 0 0 2.1 2.0 2.3 1.1 certain legumes native to the central Great Glyphosate 1600 0 2.3 2.4 2.7 2.3 Plains, e.g., Illinois bundleflower, round- Imazapic + 140 0 4.1 5.0 2.4 3.0 head lespedeza (Lespedeza capitata glyphosate 1600 0 Michx.), and catclaw sensitivebriar Imazapic + 140 70 4.7 5.8 3.2 4.0 [Mimosa quadrivalvis var. nuttallii (DC.) glyphosate 1600 0 LS. Beard ex Barneby], improved forage Imazapic + 210 0 4.8 5.1 2.7 3.2 yield and crude protein content when glyphosate 1600 0 seeded with native warm-season grasses. Imazapic + 210 70 7.0 4.7 3.0 3.3 Clearly, more information is needed about glyphosate 1600 0 native legume compatibility with warm- LSD (0.05) ------1.2 ------0.9 season grasses, contribution to nitrogen 1 fixation, seed production, and establish- Herbicides were applied in October 1995 (Fall) and June 1996 (Spring). Burn and mow treatments were applied and grass and grass and legume mixtures were planted in April 1996. ment methods before they can be recom- 2Measured attributes are averaged across burn and mow treatments. mended for use in rangeland improvement 3Measured attributes are averaged across planting treatments and burn and mow treatments. strategies.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 367 ing treatments. Total yields where imaza- productivity and nitrogen use were greater Cook, C.W. and J.L. Stubbendieck. 1986. pic was applied with glyphosate ranged in more diverse plant species mixtures Range research: Basic problems and tech- from 3.0 to 4.0 Mg ha-1 compared with a than less diverse mixtures. This supports niques. Soc. for Range Manage., Denver, yield of only 1.1 Mg ha-1 where no herbi- the concept that differences in resource Colo. cide was applied (Table 5). Total yields use by multiple plant species allows more Dunn, P.H. 1979. The distribution of leafy spurge (Euphorbia esula) and other weedy were increased where imazapic was diverse plant communities to more fully use -1 Euphorbia spp. in the United States. Weed applied at 70 g a.i. ha in June 1996 com- resources than less diverse plant communi- Sci. 27:509Ð516. pared to yields where glyphosate was ties and improve overall productivity (Frank Ferrell, M.A., T.D. Whitson, D.W. Koch, applied in October 1995. Total yields on and McNaughton 1991, McNaughton 1993, and A.E. Gade. 1998. Leafy spurge areas treated with imazapic at 140 g a.i. Naeem et al. 1994). More diverse grassland (Euphorbia esula) control with several grass ha-1 combined with glyphosate in October communities also should be more resilient species. Weed Technol. 12:374Ð380. 1995 were greatest where imazapic was (Tilman and Downing 1994) and better able Frank, D.A. and S.J. McNaughton. 1991. applied again in June 1996. Perhaps sup- to sustain stable ecosystem processes over a Stability increases with diversity in plant pression of certain species in the resident range of disturbances, e.g., grazing, fire, and communities: empirical evidence from the 1988 Yellowstone drought. Oikos vegetation caused by the June 1996 imaza- periodic droughts, and return to a desirable 62:360Ð362. pic treatment favored some of the planted state once disturbances moderate. Goldsmith, F. B. and C. M. Harrison. 1976. or resident species. The reasons for this Our goal was to provide rangeland man- Description and analysis of vegetation. p. positive response were not evident from agers with strategies that extend beyond 85Ð155 In S. B. Chapman, ed. Methods in yields of the planted species (Tables 3 and controlling undesirable vegetation and plant ecology. Halstead Press, New York, 4) or resident vegetation components. lead to restoring degraded rangeland com- N.Y. Imazapic and glyphosate were essential munities by reintroducing desirable native Hansen, R.W., R.D. Richard, P.E. Parker, components of treatments applied before plant mixtures. Establishing mixtures of and L.E. Wendel. 1997. Distribution of bio- planting to improve establishment of desirable species, as demonstrated in this logical control agents of leafy spurge native grass and legume stands on the study, represents an important step in the (Euphorbia esula L.) in the United States: 1988Ð1996. Biol. Control 10:129Ð142. leafy spurge-infested grasslands evaluated process of recapturing the productive Harris, P., P. H. Dunn, D. Schroeder, and R. in this study. Applying these herbicides potential of leafy spurge-infested sites in Vonmoos. 1985. Biological control of leafy together reduced leafy spurge and other the central Great Plains. Once these desir- spurge in North America. p. 79Ð92 In: A. K. resident vegetation, which facilitated able species establish, management sys- Watson, ed. Leafy Spurge Monograph No. 3. establishment of the planted native species tems must be used that shift the competi- Weed Sci. Soc. Amer. Champaign, Ill. in less than 2 years. Planted species yields tive advantage to desirable species and Hartley, H.O. 1950. The maximum F-ratio as were increased substantially and leafy away from invasive species. Chemical and a short-cut test for heterogeneity of variance. spurge density and yield were reduced by biological controls will continue to be Biometrika. 37:308Ð312. imazapic applied with glyphosate com- important components of these manage- Kirby, D. R. and R. B. Carlson. 1998. Leafy spurge control with flea beetles (Aphthona pared with glyphosate applied alone or no ment systems because of the continued spp.). Proc. Western Soc. Weed Sci. 51:130. herbicide. Increases in total yields where threat leafy spurge will pose to these Landgraf, B.K., P.K. Fay, and K.M. native species were seeded at Mason City restored communities. The strategy devel- Havstad. 1984. Utilization of leafy spurge and where imazapic was applied with oped in this study has the potential to pro- (Euphorbia esula) by sheep. Weed Sci. glyphosate at Tilden indicate that the inher- vide the means to redirect the successional 32:348Ð352. ent productivity of the site was not being trajectory of the leafy spurge-infested Launchbaugh, J.L. and C.E. Owensby. 1970. fully expressed by the plant community communities towards a more desirable Seeding rate and first year stand relationships dominated by leafy spurge, Kentucky blue- community comprised of native prairie for six native grasses. J. Range Manage. grass, and smooth bromegrass. These yield flora with improved carrying capacity and 23:414Ð417. increases reflect the considerable contribu- native plant diversity, and decreased leafy Lentner, M. and T. Bishop. 1993. Experimental design and analysis. Valley tion of the warm-season native plants, spurge abundance. Book Co., Blacksburg, Virg. which appeared to use site resources more Lym, R.G. 1998. The biology and integrated efficiently than the cool-season plants that management of leafy spurge (Euphorbia dominated the leafy spurge-infested com- Literature Cited esula) on North Dakota rangeland. Weed munities. This strategy took less than 2 Technol. 12:367Ð373. Lym, R.G. and D.R. Kirby. 1987. Cattle for- years to substantively improve the forage Beran, D.D., R.E. Gaussoin, and R.A. aging behavior in leafy spurge (Euphorbia resource and reduce leafy spurge. These Masters. 1999a. Native wildflower estab- esula)-infested rangeland. Weed Technol. plant stands should be evaluated over sev- lishment with imidazolinone herbicides. 1:314Ð318. eral years to determine changes in species HortSci. 34:283Ð286. Lym, R.G. and C.G. Messersmith. 1985. Beran, D.D., R.A. Masters, and R.E. composition and productivity, and rate of Leafy spurge control with herbicides in Gaussoin. 1999b. Grassland legume estab- leafy spurge recovery. North Dakota: 20 year summary. J. Range lishment with imazethapyr and imazapic. Established mixtures of native species Manage. 38:149Ð154. Agron. J. 91:592Ð596. have the potential to more fully utilize Lym, R.G. and D.A. Tober. 1997. Competitive Beran, D.D., R.A. Masters, R.E. Gaussoin, F. grassland resources and preempt resource grasses for leafy spurge (Euphorbia esula) Rivas-Pantoja. 2000. Establishment of big use by leafy spurge and the other less reduction. Weed Technol. 11:787Ð792. bluestem and Illinois bundleflower mixtures Lym, R.G., K.K. Sedivec, and D.R. Kirby. desirable species. By maximizing resource with imazapic and imazethapyr. Agron. J. 1997. Leafy spurge control with angora goats capture, the more diverse reestablished 92:460Ð465. and herbicides. J. Range Manage. grassland community could be more resis- Belcher, J.W. and S.D. Wilson. 1989. Leafy 50:123Ð128. tant to invasion by less desirable species. spurge and the species composition of a Masters, R.A. and S.J. Nissen. 1998. mixed-grass prairie. J. Range Manage. Tilman et al. (1996) determined that plant Revegetating leafy spurge (Euphorbia esula 42:172Ð175.

368 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 L.)-infested grasslands with native tallgrass- Ott, L. 1977. An introduction to statistical Sheley, R.L., T.J. Svejcar, and B.D. es. Weed Technol. 12:381Ð390. methods and data analysis. Duxbury Press, Maxwell. 1996. A theoretical framework for Masters, R.A., D.D. Beran, and F. Rivas- Belmont, Calif. developing successional weed managmeent Pantoja. 1998. Leafy spurge (Euphorbia Posler, G.L., A.W. Lenssen, and G.L. Fine. strategies for rangeland. Weed Technol. esula L.) response to AC 263,222. Weed 1993. Forage yield, quality, compatibility 10:766Ð773. Technol. 12:602Ð609. and persistence of warm-season grass- Thompson, W.M., S.J. Nissen, and R.A. Masters R.A., R. Stritzke, and S.S. Waller. legume mixtures. Agron. J. 85:554Ð560 Masters. 1998. AC 263,222 absorption and 1990. How to conduct a prescribed burn and Raju, M.V.S. 1985. Morphology and anatomy fate in leafy spurge (Euphorbia esula). Weed prescribed burning checklist. Nebr. Coop. of leafy spurge. p. 26Ð41. In: Watson, A.K. Sci. 46:510Ð513. Ext. Serv. EC 90Ð121. (ed.) Leafy spurge. Weed Sci. Soc. Monogr. Tilman, D. and J.A. Downing. 1994. Masters, R.A., S.J. Nissen, R.E. Gaussoin, 3. Champaign, Ill. Biodiversity and stability in grasslands. D.D. Beran, and R.N. Stougaard. 1996. Rivas-Pantoja, F., R.A. Masters, and D.D. Nature 367:363Ð365. Imidazolinone herbicides improve restoration Beran. 1997. Influence of planting date and Tilman, D., D. Wedin, and J. Knops. 1996. of Great Plains grasslands. Weed Technol. herbicides on native tallgrass establishment. Productivity and sustainability influenced by 10:392Ð403. Soc. Range Manage., Rapid City, S.D. Abstr. biodiversity in grassland ecosystems. Nature McNaugton, S.J. 1993. Biodiversity and func- p. 63. 379:718Ð720. tion of grazed ecosystems. p. 311Ð382 In: SAS Institute, Inc. 1996. SAS user’s guide: Watson, A.K. 1985. Introduction—The leafy Schulze, E.D. and H.A. Mooney, eds. statistics. Version 6 ed. SAS Inst., Cary, N.C. spurge problem. p. 1Ð7 In: Watson, A.K. Biodiversity and ecosystem function. Scifres, C.J. 1987. Decision-analysis approach to (ed.) Leafy spurge. Weed Sci. Soc. Monogr. Springer-Verlag, Berlin. brush management planning: Ramifications for 3. Champaign, Ill. Naeem, S, L.J. Thompson, S.P. Lawler, J.H. integrated range resources management. J. Lawton, and R.M. Woodfin. 1994. Range Manage. 40:482Ð490. Selleck, G.W., R.T. Coupland, and C. Declining biodiversity can alter the perfor- Frankton. 1962. Leafy spurge in mance of ecosystems. Nature 368:734Ð737. Saskatchewan. Ecol. Monogr. 32:1Ð29.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 369 J. Range Manage. 54: 370Ð377 July 2001 Statistical analyses of fluorometry data from chloroform filtrate of lamb feces

A. MUKHERJEE1, D.M. ANDERSON2, D.L. DANIEL3, L.W. MURRAY3, G. TISONE4, E.L. FREDRICKSON2, R.E. ESTELL2, G.D. RAYSON5, AND K.M. HAVSTAD2

1Former graduate student, New Mexico State University, University Statistics Center, Las Cruces, N.M 88003-0003 (U.S.A.), 2research scientist, USDA, Agricultural Research Service, Jornada Experimental Range, Box 30003, NMSU, Dept. 3JER, Las Cruces, N.M. 88003-00033, statistician, New Mexico State University, University Statistics Center, Las Cruces, N.M. 88003-0003, 4president/physicist, TW Research Associates, 10212 Chapala Pl. NE, Albuquerque, N.M. 87111, 5associate professor, New Mexico State University, Department of Chemistry and Biochemistry, Las Cruces, N.M. 88003-0003.

Resumen Abstract Accurately identifying the botanical composition of free-rang- El identificar en forma certera la composición botánica de la ing animal diets remains a challenge. Currently accepted proce- dieta de animales en libre pastoreo sigue siendo un reto. Los pro- dures are time consuming, many requiring painstaking sample cedimientos actualmente aceptados consumen mucho tiempo y preparation while none produce data useful for real-time man- muchos requieren una laboriosa preparación de la muestra, agement. Automated procedures focusing on detection of chemi- mientras que ninguno produce datos útiles en términos de mane- cal and/or physical plant properties using specific molecules jo real de tiempo. Los procedimientos automatizados enfocados a called fluorophores offers possibilities for determining the la detección de propiedades físico-químicas de las plantas medi- species composition of herbivore diets. This study was designed ante el uso de moléculas especificas llamadas fluroforos ofrecen to evaluate fluorometry techniques in herbivore diet determina- posibilidades alentadoras para determinar la composición de tions using fecal samples obtained from 13 lambs fed a basal diet especies de la dieta de los herbívoro. Este estudio se diseño para of tobosa hay (Pleuraphis mutica Buckley), and containing 4 dif- evaluar las técnicas de flurometría en la determinación de la ferent levels (0, 10, 20, and 30%) of tarbush (Flourensia cernua D dieta de herbívoros utilizando muestras fecales obtenidas de 13 C.) leaf material. Chloroform (CHCl3) filtrate obtained from the corderos alimentados con una dieta basal de heno de toboso lamb’s feces was exposed to UV light from a xenon arc lamp. (Pleuraphis mutica Buckley) y conteniendo cuatro diferentes This caused fluorophore molecules in the filtrate to have their niveles (0, 10, 20, y 30%) de hojas “Tarbush” (Flourensia cernua outer shell electrons move to a higher energy state as a result of D C.). Un filtrado de cloroformo (CHCL3) obtenido de las heces UV light excitation. After excitation by UV light at 310, 320, 330, de los corderos se expuso a la luz ultravioleta (UV)de una lam- 340, 350, and 355 nm, the fluorophores returned to their ground para de arco de xenón. Esto causo que los electrones de las state giving off light (fluorescence). This fluorescence intensity órbitas exteriores de las las moléculas de los fluoroforos del fil- (counts) varied and when captured using appropriate electronics, trado cambiaran a un estado de alta energía resultante de la produced 1,024 pairs of light intensities (counts) and fluorescent excitación por la luz UV. Después de la excitación por la luz UV wavelengths between 175 and 818 nm in 0.63 nm increments. a 310, 320, 330, 340 y 350 nm, los fluoroforos regresaron a su Previous research indicated differences among diets could be estado inicial quedando sin fluorescencia. Esta intensidad de flu- determined using distinct peaks in the red and blue regions of the orescencia (conteos) variaron, cuando son capturados con los visible light spectrum and a univariate (1 variable at a time) aparatos apropiados, produjeron 1,024 pares de intensidades de analysis. This research demonstrates the entire fluorescence data luz (conteos) y longitudes de onda fluorescente entre 175 y 818 set can be used to determine differences among diets using multi- nm con incrementos de 0.63 nm. La investigación previa indica variate statistics. Sequences of 5 increasingly complex statistical que la diferencia entre dietas pude ser determinada utilizando techniques were used to distinguish among diets: 2-dimensional distintos picos en las regiones azul y roja del espectro de luz visi- plots, polynomial regression models, confidence interval plots, ble y un análisis univariado (1 variable a la vez). Esta investi- discriminant analysis, and 3-dimensional plots. Two-dimensional gación demuestra que el conjunto completo de los datos de fluo- plots indicated 2 spectral fluorescence peaks, 1 in the blue-green rescencia puede ser utilizado para determinar diferencias entre (420Ð600 nm) and 1 in the red (640Ð720 nm) region of the visible las dietas mediante el uso de estadística multivariada. Se uti- lizaron las secuencias de 5 técnicas estadísticas que incrementan en complejidad para distinguir entre las dietas: gráficas bidi- Trade names used in this publication are solely for the purpose of providing spe- mensionales, modelos de regresión polinomial, gráficas de inter- cific information. Mention of a trade name does not constitute a guarantee, valos de confianza, análisis discriminante y gráficas tridimen- endorsement, or warranty of the product by the U.S. Department of Agriculture, New Mexico State University or Sandia National Laboratories over other products sionales. Las gráficas bidimensionales indicaron 2 picos de espec- not mentioned. tro de fluorescencia, 1 en la región azul-verde (420–600 nm) y 1 The authors express sincere appreciation to Dr. Perry Gray, research scientist en la región roja (640–720 nm) del espectro visible. Debido a la with the Pulsed Power and Laser Initatives Department Sandia National naturaleza asimétrica de estos picos se desarrollaron polinomi- Laboratory, Albuquerque, N.M. for generating the spectral signatures from the ales de quinto orden para diferenciar entre 4 dietas. La confia- sheep feces. Manuscript accepted 7 Oct. 2000. bilidad estadística fue alta cuando se discrimino entre dietas que

370 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 spectrum. Because of the asymmetrical Diets are currently determined using materials will emit fluorescence if excited nature of these peaks, fifth-order polyno- various techniques. Probably the oldest with the proper excitation wavelength mials were developed to differentiate and least automated technique is that of (Brach et al. 1977). Excitation is accom- among the 4 diets. Statistical reliability direct observation of foraging animals plished with an energy source, such as a was high when discriminating between (Bjugstad et al. 1970). The bite count pro- xenon arc lamp or laser. This source, when diets containing no tarbush leaf and the cedure, as it is frequently called, is still focused at specific wavelengths and diets containing 30% tarbush leaf; howev- used (Doherty et al. 1999); yet, it is often directed at a material, excites outer shell er, it was not possible to statistically sepa- inappropriate for some animal species and electrons from a ground state to a higher rate diets containing intermediate (10 and landscapes, and is always of concern sci- energy state. After excitation the electrons 20%) amounts of tarbush leaf material entifically because of the ever-present fall back to their ground state, many in a from each other or from the 2 extremes (0 effect of observer influence. All other ani- cascade fashion, and give off energy in the and 30% tarbush leaf). These results suggest spectral signatures arising from fluo- mal-based techniques require sampling form of heat and light. The light emitted as rometry data may be useful for differenti- digesta from 1 or more locations along the a result of excitation has a longer wave- ating among botanical composition diets digestive tract (Holechek et al. 1984). The length than the excitation light and is that differ in plant form, but that a multi- microhistological technique is the predom- termed fluorescence or more generally variate approach may require large sam- inant method currently used for identify- luminescence. This emitted light, when ple sizes. ing dietary botanical composition of free- captured by a photo diode array, produces ranging animals (Bennett et al. 1999, a unique spectral fluorescence fingerprint. Bontti et al. 1999), with feces being the These fluorophores and their unique indi- Key Words: Cattle, botanical composition, most commonly used samples since they vidual fluorescence characteristics form fluorescence, xenon fluorometry, fecal flu- represent a broad spatial and temporal the basis for identification. The objective orophores range of dietary intakes (Norbury and of this research was to evaluate several Sanson 1992). Plant fragments too small statistical approaches using the entire no contenían hojas de “Tarbush” y dietas to identify taxonomically, the overestima- spectral fingerprint to determine differ- conteniendo 30% de hojas de “Tarbush”; tion of indigestible materials and the ences among fluorophores in a chloroform sin embargo, no fue posible separar underestimation of readily digested mate- filtrate of feces from lambs fed differing estadísticamente las dietas que contenían rials such as leaf material, are just some of diets. cantidades intermedias (10 a 20%) de the problems that beset microhistological hojas de “Tarbush”, no se pudieron sepa- analysis. A major limitation to this tech- rar entre ellas o de las otras 2 dietas nique as a management tool is the amount Materials and Methods extremos (0 y 30% de hojas de “Tarbush”. of time required for sample preparation Estos resultados sugieren que firmas and analysis thus preventing its usefulness Feces from 13 ruminally cannulated espectrales que surgen de los datos de la Polypay x Rambouillet lambs were fed a flurometría pueden ser útiles para difer- in making real-time management decisions. Two recent automated techniques basal diet of tobosa (Pleuraphis mutica enciar entre la composición botánica de Buckley) hay with 0, 10, 20, and 30% tar- dietas que difieren en la forma de la plan- for determining botanical composition of animal diets having shorter analytical time bush (Flourensia cernua D C.) leaf was ta, pero se puede requerir un análisis mul- added to provide 4 dietary treatments. The tivariado para tamaños de muestra requirements are near infrared reflectance feces collected were taken in conjunction grandes spectroscopy (NIRS); (Garcia-Criado et al. 1991, Walker et al. 1998) and laser with a metabolism study previously induced fluorescence (LIF); (Anderson et reported by King et al. (1996). Collection Determining the components compris- al. 1996, 1998). Although NIRS (Foley et of the samples used in these fluorometry ing free-ranging herbivore diets is crucial al. 1998) and fluorometry (Lakowitz 1983, analyses and the sample preparation pro- to evaluating the nutritional well being Guilbault 1990), of which LIF is one type, cedures has been previously described by and implementing herbivore management both rely on molecular properties, they Anderson et al. (1996) who used laser- as well as maintaining positive plant rela- differ in several important ways (Table 1). induced fluorescence (LIF) to establish tionships within ecological communities. differences among these same diets. Therefore, it is essential for managers to This study differed from previous not only know what kind and amount of The Fluorometric Technique research (Anderson et al. 1996) in 3 ways. Fluorometry involves capturing light forages are available, but also which First, chloroform (CHCl3), an organic species are actually being eaten. emitted from an excited molecule. All polar solvent having a dipole moment

Table 1. Comparison of near infrared reflectance spectroscopy (NIRS) and fluorometry.

Characteristics NIRS Fluorometry Measures Vibrational energies (>700 nm) Electron transitions (190 to 800 nm) Pattern recognition Focuses on blended chemical structures Focuses on specific chemical structures (many 2D response curves) (specific 2D curves to 5D1 response surfaces) Sample state Choice of specific solvents required (many Many polar & non-polar solvents available materials absorb) (fewer materials fluoresce) Post processing data Complex algorithms “trainable” for indirect Simple algorithms “trainable” for indirect determination of determination of alternative characteristics alternative characteristics 1Fluorescence lifetime represents the fourth dimension and rotational anisotropy* (the rate at which the fluorophore rotates in a liquid or gaseous solvent based on the fluorophore’s size and the solvent’s viscosity) represents the fifth dimension. * Lakowitz, J. R. 1983. Principles of Fluorescence Spectroscopy. Plenum Press, New York, NY.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 371 slightly less than that of water, containing had 5 nm resolution. A calibrated D2 lamp ate component to the problem of distin- fecal pellet filtrate was exposed to UV was used to determine the response of the guishing among diets by using more than light from a xenon arc lamp instead of a detector system in the spectral range 200- 1 response at a time. The sequence of the laser. Second, the continuous fluorescence 400 nm. The spectrum of the D2 lamp was 5 interrelated statistical techniques is now spectrum for 6 excitation wavelengths calibrated by the manufacturer in accor- discussed in detail. (310, 320, 330, 340, 350, and 355 nm) dance with the National Institute of was used to determine differences among Standards and Technology (NIST) stan- Two-dimensional Plots the diets instead of only evaluating indi- dards. The relative output of the xenon Fluorescent light intensity (counts) was vidual peak features. Third, the fecal pel- lamp through the monochromator was plotted against fluorescent wavelengths lets were exposed at room temperature to measured using an Ophir Model PD-300- for each of the 6 excitation wavelengths chloroform for 24 hours, a shorter period UV colorimeter. using the GPLOT procedure in SAS (SAS of time than previously used, before the Five excitation wavelengths (310, 320, Institute 1990b, 1990c). All data were CHCl3 extract was filtered through No. 4 330, 340, and 350 nm) were selected for plotted on the same scale to help visually Whatman Filter Paper. All pellets were evaluation by 1 author (Tisone) based on distinguish similarities and differences intact and immediately removed before fil- his experience with fluorescence spectra. among the 4 tarbush leaf treatments and to tration except for one, a 100% tobosa diet These 5 wavelengths produced the most decide on appropriate regression models. fecal pellet in which the pellet had been visually prominent and distinct fluores- Because of the consistent bimodal nature ground through a Wiley mill to pass a 40- cence features from among the 200 to 400 of the x-y plots with individual peaks of mesh (0.5 mm) screen before being placed nm range of excitation wavelengths asso- different magnitudes in the blue-green and in the chloroform. We did not consider the ciated with response surfaces. A sixth red regions of the visible spectrum across physical condition of the fecal material to excitation wavelength (355 nm) was also all diets and animals, we decided to fit a be of concern since Anderson et al. (1996) selected, corresponding to the single exci- polynomial to each of these regions for demonstrated similar spectral signatures tation wavelength previously used to pro- each of the 6 excitation wavelengths. A using feces from these same lambs when duce LIF on samples of this same fecal fifth-order polynomial was chosen comparing ground and intact sheep fecal material as previously reported (Anderson because of slope asymmetry among the pellets. For this study, fecal pellets from et al. 1996). Light intensity counts at each individual peaks. only 13 of the original 16 lambs were excitation wavelength were measured at available (King et al. 1996, Anderson et fluorescent wavelengths between 175 and al. 1996). Lambs 1Ð3 received only the 818 nm in 0.63 nm increments. This Polynomial Regression Models basal diet consisting of tobosa hay, lambs resulted in a total of n = 1,024 pairs, each The fifth-order polynomial regression 4Ð6 received a diet consisting of 90% consisting of a fluorescent wavelength and model (Neter et al. 1996) is given by tobosa hay and 10% tarbush leaf, lambs an intensity count. 2 3 4 5 Yi = §0 + §1Xi + §2Xi + §3Xi +§4Xi +§5Xi ∈ 7Ð9 received a diet consisting of 80% In previous work, Anderson et al. (1996) + i , (1) tobosa hay and 20% tarbush leaf and used LIF information from distinct peaks where Yi is the intensity count at fluores- lambs 10Ð13 received a diet consisting of in the red and blue-green regions of the cent wavelength i, for i = 1 to 1,024, 70% tobosa hay and 30% tarbush leaf. visible light spectrum to conduct statistical §0, §1,…,ß5 are (unknown) regression Fecal filtrate was prepared and evaluat- analyses. Responses were analyzed by parameters, ed using a fluorometer at Sandia National analysis of variance using intensity counts th Xi is the i fluorescent wavelength Laboratory, Albuquerque, N. M. The fluo- and wavelengths for each peak and the which is a fixed constant and ranges from rometer had as an excitation source a 150 red/blue count ratio. In addition, only uni- 175 to 818 nm, watt, high-pressure xenon arc lamp (Oriel variate (i.e., 1 response at a time) statisti- 2 5 Xi , ….Xi are the higher powers of flu- Model 68805 arc lamp with xenon bulb cal analyses were conducted. orescent wavelengths, and Model 6254). White light from the xenon This study examined the 4 dietary treat- ∈ i are errors which are independent and lamp was focused into an F/4, 1/8 meter ments using the entire spectrum of fluores- identically distributed as N( 0, σ2). double monochromator (CVI Model 120, cence light intensities, necessitating a The REG procedure in SAS (SAS 200Ð400 nm range, 5 nm steps, 7 nm more complex statistical sequence requir- Institute 1989b) was used to model the bandwidth) to reduce scattered light out- ing 5 analyses. First, bivariate plots of data. There were 13 fitted models for each side of the pass band of the monochroma- light intensities versus fluorescence wave- of the 6 excitation wavelengths and 2 tor. Light from the monochromator was lengths were examined to decide on regions of the visible spectrum (blue, then imaged into the center of an RF- appropriate regression models. Next, green, or red), 1 for each lamb, with each 3010-T FUV ultraviolet quartz sample cell regression models were fitted and the fit- model containing 6 regression coeffi- (Spectrocell, Oreland, Penn). Scattered ted regression coefficients were extracted cients. These regression coefficients were light and fluorescence from the chloro- for use in the next 3 statistical techniques output for use in succeeding statistical form filtrate was detected at 90 degrees to to discriminate among diets. Given that a analyses. the incident excitation source. Excitation regression model is a good fit, the regres- light was imaged into the entrance slit of sion coefficients contain all statistical an F/4, 1/8 meter imaging spectrometer information about the shape of the Confidence Interval Plots (ISA Jobin Yvon, Edison, N. J., 200Ð700 response curve. Thus, the dimensionality Confidence interval plots represent a nm range, 5 nm resolution). A 1,024-ele- of the problem was reduced from 2n (in univariate statistical technique. After poly- ment intensified Reticon array (Model this case 2,048) down to k = the number of nomials models were fitted, similarities 1420, EG&G Princeton Applied Research, regression coefficients. In addition, 2 of and differences among the 4 tobosa diet Trenton, N.J.) detected the light at the the last 3 techniques (discriminant analysis models were examined using the individ- image plane. The detection spectrometer and 3-dimensional plots) add a multivari- ual regression coefficients (e.g., we compared intercepts for all 13 models of sam-

372 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 ples in chloroform). To statistically com- class means. The individual is then pre- ber of variables that could be examined at pare regression coefficients, it was neces- dicted to belong to the class for which the one time using discriminant analysis. sary to have information about the reliabil- individual has the highest probability of ity or precision of the estimates. belonging. Three-dimensional Plots Therefore, confidence intervals incorpo- Pairwise generalized-squared distances Finally, 3-dimensional plots of the poly- rating information from both the regres- are a unitless measure of the distances nomial regression coefficients were used sion coefficient and its variability were between class means—again, scaled rela- to study the spatial relationships among used to compare coefficients for a particu- tive to the variability in each variable. The the 4 diet treatments graphically (JMP lar term (e.g., the intercept) across diets. magnitudes of these squared distances can software, SAS Institute 1995). All subsets To view these diet comparisons graphical- give insight into the potential for separat- of 3 coefficients were picked and plotted ly, confidence interval plots for each term ing 2 treatments. on 3 axes. Changing the orientation of the were constructed (intercept, linear term, To evaluate how well the discriminant axes (i.e., by rotating the axes at different etc.) for each excitation wavelength. analysis classified an individual, cross-val- angles) helped in understanding how the Identifiers for the 13 lambs fed with the 4 idation was used. In the cross-validation lambs were assigned to the various classi- diets were represented along the vertical procedure, 1 of the individuals is deleted fications, and which variables effectively (Y) axis, and first-order regression coeffi- while the remaining individuals are used separated the treatment groups spatially. cient estimates with their 95% confidence to build the discriminant function. The This provides information regarding the intervals were plotted on the horizontal deleted individual is then classified based utility of including each of the variables (X) axis. For each fluorescent region on this new discriminant function. This (regression coefficients) in the discrimi- (blue, green or red) within each excitation process is repeated for each individual in nant analysis. After choosing the coeffi- wavelength, there were 6 such plots, 1 for the data set, and the number of mis-speci- cients that facilitated separation of the each regression coefficient. The plots were fications are totaled to obtain the misclas- observations, the discriminant function constructed using the PLOT procedure in sification rates for each class analyses were performed again, using the SAS (SAS Institute 1990a). These plots In these data, there were 4 classes (c = DISCRIM procedure in SAS. Using vari- provided a subjective, graphical way to 4) representing the 4 diets, 6 classification ables that do not add useful information compare the treatments univariately (i.e., 1 variables (the intercept and the 5 estimated reduces the ability of many procedures to regression coefficient at a time). regression coefficients from the fifth-order correctly distinguish among individuals Discriminant analysis was used to com- polynomial model), and n = 13 lambs (4 from different treatments. pare treatments using all coefficients at the for 70% tobosa mixed with 30% tarbush same time to distinguish more objectively leaf, and 3 each for the remaining three among treatments. diets). Discriminant analysis was used to Results and Discussion develop classification rules, classify each Discriminant Analysis lamb using cross-validation, and then determine if a lamb was properly classi- Two-dimensional Plots Discriminant analysis, also known as Initially, plots of the fluorescent intensi- discriminant function analysis, is a multi- fied into the correct diet class, all based on the values of the polynomial regression ty counts versus fluorescent wavelengths variate technique designed to address were evaluated. In general, the feces from problems arising due to classification. In coefficients. The DISCRIM procedure of SAS (SAS Institute 1989a) was used to all 13 lambs at all 6 excitation wave- plant taxonomy, discriminant analysis has lengths had a sharp distinct tall peak in the been used to classify an individual into 1 perform these analyses. Having 13 observations limited the num- red (640Ð720 nm) and a relatively short of several related species (Morrison 1976, broad peak in the blue-green (420Ð600 Johnson and Wichern 1988). In general, data from individuals from several known, mutually exclusive classes are used to develop rules (discriminant functions) which will then allow classification of an unknown individual into 1 of the classes. Implementation of discriminant analysis involves several steps. First, a statistical metric distance to the sample mean of each class (Mahalanobis distance) is determined for every individual in the data set. These distances are based on the individual’s multivariate measures and are scaled relative to the variability associated with each variable. The individuals’ true classi- fications and these metric distances are then used to develop formulas for estimating the probability that any individual belongs to a particular class. Using these formulas, the probability that an individual (whose classification is unknown) belongs Fig. 1. Two dimensional plots of a raw fluorescence signature obtained from chloroform fil- to a class can be estimated for each class trate excited with a xenon light at 355 nm, obtained from lamb 1’s feces representing a based on the individual’s distances to the 100% tobosa hay diet. Plot represents fluorescence intensity (counts) vs. fluorescence wavelengths between 420 and 720 nm.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 373 gested a fifth-order polynomial model would capture most of the peak curvatures in both the red and blue-green regions of the fluorescence spectrum, including a commonly visible “shoulder” in the red region between 700 and 720 nm. Because of the magnitude of the X-values (fluorescent wavelengths), there was severe collinearity (linear relationships) among the predictors, X, X2, …X5. That is, there were high pairwise correlations between X and X2, etc. This caused the polynomial regressions to be unstable, and resulted in the regression procedure incorrectly reporting coefficient estimates that were “biased” and “not unique.” This is a common computational problem with polynomial models and was solved by centering the data at 0 (by subtracting the mean of the range of wavelengths) and scaling the range of the data to be approximately between Ð2 and +2 (by dividing by an appropriate constant) (Aiken and West 1991). For example, for the 420 to 600 nm range, the origin was shifted by subtracting 510 and the resulting deviations were divided by 45. For each of the replicates at the excitation wavelengths of 310, 330, and 355 nm, a fifth-order polynomial equation was developed. After scaling, the fitted models had high R-square values, ranging from 0.908 to 0.998. Most of the regression coefficients were significant at the 5% level (e.g., of the 13 fitted models for the blue-green region at 355 nm, only 4 of 78 Fig. 2. Two dimensional plots of a raw fluorescence signature obtained from chloroform fil- regression coefficients were not signifi- trate excited with a xenon light at 355 nm, obtained from lamb 1’s feces representing a cant, see Table 2). 100% tobosa hay diet. Plot (A) is the same data as for Fig. 1 but only for the blue-green Summaries from the fitted model with region (420Ð600 nm) of the visible spectrum. Plot (B) represents a fifth-order polynomial estimated regression coefficients, Mean superimposed over the blue-green region of the fluorescence spectrum. Square Error, and R-square for the blue- green and red regions at excitation wave- nm) region of the visible spectrum. This The sharp peaks (high counts) in the red length 355 nm are given in Table 2. Figure bimodal characteristic was similar to that region, were possibly from chlorophyll a 2B is a plot of the same data from Figures previously reported by Anderson et al. (Krause and Weis 1984, Lang et al. 1991) 1 and 2A with the fitted polynomial model (1996) for these same feces when excited and the relatively low peaks (low counts) from Table 2 superimposed. with Laser-Induced Fluorescence. Figure 1 in the blue-green region were from fluo- depicts the fecal spectral signature from rophores possibly associated with cell wall Confidence Interval Plots lamb 1 fed only the basal diet consisting bound ferulic acid (Lichtenthaler and These plots visually depict how the 4 of tobosa hay, excited at 355 nm over the Schweiger 1998). Therefore, the 2 regions diets differed or were similar with respect range 420 to 720 nm. Figure 2A is from were modeled separately. to each term in the model. Coefficients the same data for only the blue-green that were similar had overlapping 95% region. The curves were bimodal among Polynomial Regression Models confidence intervals while coefficients all plots of the 6 different excitation wave- Polynomial regression is used when the that were different had non-overlapping lengths. true curvilinear response function is a 95% confidence intervals. The latter was Of the 6 excitation wavelengths for polynomial function, but can also be used the case for all regression coefficients which data were collected, only the when the curvilinear response is unknown except the fourth-order term. The control extreme and middle excitation wave- or complex, because a polynomial curve is diet (0% tarbush leaf) and the diet contain- lengths (310, 330, and 355 nm) were used often a good approximation of the true ing 30% tarbush leaf material, were readi- in further statistical procedures. As the function (Neter et al. 1996). In this study, ly distinguishable most of the time (for the other 3 excitation wavelengths were at polynomial regression was used because blue-green region at 355 nm, 5 out of 6 intermediate levels (320, 340, and 350), the true curvilinear response was confidence intervals plots were readily they should not contribute much additional unknown. The 2-dimensional plots sug- distinguishable). Five of the 6 plots from information in the diet characterizations.

374 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 samples excited at 355 nm in the blue- Table 2. Estimated regression coefficients of fluorescence data in the blue-green (420Ð600 nm)1 green region indicated separation of the and red (640Ð720 nm)1 regions of the visible spectrum obtained from the excitation of chloro- control diet from the diet containing the form filtrate of lamb fecal pellets excited with a xenon lamp focused at 355 nm using four diets differing in tarbush leaf content with mean square error (MSE) and coefficient of determination maximum amount of tarbush leaf material 2 α (30%), while neither of the other 2 diets (R ). Regression coefficients without “ns” below the number are significant ( = 0.05). containing 10% and 20% tarbush leaf Tarbush Regression coefficients 420 to 600 nm material were visually distinguishable in leaf in a any of the 6 plots. The models developed basal diet Linear Quadratic Cubic Quartic Quintic for the blue-green region of the fluores- of tobosa cence spectrum showed more visual sepa- hay Lamb Intercept X X2 X3 X4 X5 MSE R2 ration than the models depicting the red (%) region. Similar results were obtained for 0 1 538.5 Ð471.6 83.6 190.6 Ð37.5 Ð20.0 2769.8 0.950 the other excitation wavelengths. 0 2 673.3 Ð578.3 Ð108.6 180.6 Ð39.9 Ð17.6 3321.8 0.972 Plots of confidence intervals for each 0 3 531.1 Ð410.9 92.2 130.3 Ð34.2 Ð10.7 1946.4 0.964 regression term suggested a possibility of 10 4 869.1 Ð795.2 10.9 373.5 Ð41.7 Ð44.9 5499.7 0.961 ns separating the control diet from the diet 10 5 894.7 Ð775.7 Ð39.8 420.4 Ð33.1 Ð56.6 7452.2 0.940 containing 30% tarbush leaf material. To 10 6 1173.3 Ð993.8 Ð91.3 503.4 Ð31.3 Ð66.9 9968.8 0.955 illustrate, Figure 3 shows a plot of the 20 7 922.8 Ð777.4 7.3 332.8 Ð38.0 Ð38.4 4674.6 0.969 95% confidence intervals for the first- ns order regression coefficient estimates for 20 8 858.2 Ð759.4 Ð181.7 518.8 Ð4.4 Ð81.3 8776.6 0.926 excitation wavelength 355 nm with emis- ns 20 9 1362.8 Ð1089.9 Ð38.7 439.6 Ð32.1 Ð54.3 6603.2 0.980 sion in the blue-green spectral region. The 30 10 1671.6 Ð1319.6 Ð230.6 623.1 Ð12.9 Ð82.9 9882.2 0.977 vertical axis identifies the 13 lambs and 30 11 1364.8 Ð1339.0 Ð155.4 754.9 Ð39.5 Ð106.2 17674.0 0.952 the diets to which they had been randomly 30 12 1262.2 Ð1108.3 0.4 456.6 Ð51.8 Ð52.1 7382.3 0.977 assigned. This plot shows the first-order ns coefficients are reasonably differentiated 30 13 1578.0 Ð1296.4 Ð115.3 585.4 Ð41.7 Ð72.5 10668.0 0.975 between the 70% and 100% tobosa diets, Regression coefficients 640 to 720 nm but not differentiated between the 80% and 90% tobosa diets. The extreme diets 0 1 16984 13552.0 Ð4186.6 Ð6147.6 221.6 816.7 309413 0.995 0 2 11825 7191.7 Ð4017.1 Ð3382.7 435.9 460.9 45696 0.998 are generally differentiated from the mid- 0 3 13844 9634.1 Ð4230.0 Ð4546.9 392.6 623.7 83045 0.997 10 4 15021 12690.0 Ð2870.1 Ð5613.3 7.3 729.0 385263 0.992 ns 10 5 14882 13094.0 Ð2645.5 Ð5733.7 Ð56.8 733.0 380007 0.992 ns 10 6 11349 6807.9 Ð3352.6 Ð3175.1 Ð319.3 440.9 70632 0.996 20 7 15333 11412.0 Ð4140.8 Ð5288.1 292.3 712.8 209464 0.995 20 8 8164 7997.7 249.6 Ð2990.6 Ð427.6 326.8 351623 0.983 ns 20 9 9066 4798.7 Ð3092.1 Ð2291.9 353.7 319.5 23722 0.998 30 10 10036 5350.6 Ð3354.6 Ð2571.9 375.9 359.9 24450 0.998 30 11 11945 9004.7 Ð2249.7 Ð3932.5 7.0 508.4 192165 0.993 ns 30 12 14341 10765.0 Ð3970.5 Ð5196.9 303.3 725.7 227452 0.994 30 13 9699 6125.5 Ð2886.0 Ð3087.8 277.5 444.4 41928 0.997 1Weast, R.C. (Ed). 1967 Handbook of Chemistry and Physics, 48th ed. CRC Press, Cleveland, Ohio, pp. E-133.

dle diets, but not completely. For example, mensional space, as opposed to the confi- the confidence intervals for lamb 12 (con- dence-interval plots that examined 1 suming 30% tarbush leaf) and lamb 9 dimension at a time. In this approach, the (consuming 20% tarbush leaf) overlap. 13 lambs fed the 4 diets were treated as This and similar plots suggest that first- observations and the 6 regression coeffi- order regression coefficient estimates are cients were treated as variables. Each of useful in separating lamb diets consisting the 3 excitation wavelengths (310, 330, of 30% tarbush leaf content from diets not and 355 nm) was individually evaluated Fig. 3. First-order regression coefficient esti- containing tarbush leaf. However, at inter- for both the blue-green and red regions of mates of fluorometry data obtained from mediate levels of tarbush leaf, it is not the visible spectrum. The number of lambs chloroform filtrate of fecal samples from apparent that the first-order coefficients sampled (13) was not high compared to 13 different lambs fed a basal diet of tobosa hay containing 4 levels (0, 10, 20, assist in separating diets—at least with the number of variables (6); therefore, no and 30%) of tarbush leaf. The middle ver- these sample sizes. sharp demarcation was possible between tical line on each symbol represents the intermediate diets. However, it was possi- linear coefficient point estimate, while the Discriminant Analysis ble with discriminant analysis to delineate outer vertical lines represent the 95% con- Among the 4 dietary treatments, dis- between control diets and those containing fidence interval. The diets having esti- 30% tarbush leaf material. mates that are furthest apart are the most criminant function analysis provided a means for detecting differences in multidi- Pairwise generalized squared distances statistically dissimilar. and misclassification rates give insight and

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 375 Table 3. Misclassification results from discriminant analysis performed on polynomial regression Conclusions coefficients obtained from fluorometry data of fecal chloroform filtrate differing in tarbush leaf content exposed to 355 nm xenon light. The values represent number of lambs classified incorrectly into a particular diet category by the discriminant analysis procedure when using spectral It was possible to discriminate 30% dif- 1 1 characteristics from both the blue-green (420Ð600 nm ) and red (640Ð720 nm ) regions of the ferences (0% and 30%) but not smaller visible spectrum. differences (10% and 20%) among chloroform filtrates from lamb feces that differed Wavelength in tarbush leaf content using a series of 2- Tarbush leaf 420 to 640 nm 640 to 720 nm in a basal diet 30 20 10 0 30 20 10 0 dimensional plots, confidence interval of tobosa hay plots, discriminant analysis, and 3-dimen- (%) ------(Count------(Count)------sional plots. Statistically, feces from con- 30 3 1 0 0 2 2 0 0 trol lambs fed no tarbush leaf material 20 0 0 2 1 1 1 1 0 (0%) had bimodal spectral signatures 10 0 3 0 0 1 1 1 0 between 400 and 800 nm that were differ- 0 0 0 0 3 0 1 0 2 ent from feces obtained from lambs that 1Weast, R.C. (Ed). 1967 Handbook of Chemistry and Physics, 48th ed. CRC Press, Cleveland, Ohio, pp. E-133. had been fed the basal diet but which contained 30% tarbush leaf material. However, lambs fed a tobosa hay basal diet contain- help to illustrate our conclusions. The gen- also provided in Table 3. Misclassification ing 10% and 20% tarbush leaf material eralized squared distance between the con- results for the red and blue-green regions could not be statistically separated. trol diet and the diet containing 30% tar- of the visible spectrum for excitation Univariate analyses on single-peak infor- bush leaf material, 106.62, was much larg- wavelengths 310 and 330 nm were also mation in Anderson et al. (1996) similarly er than the distances between the other calculated but are not reported. distinguished between the control and 30% treatments, ranging between 5.48 and tarbush leaf material in diets but also dis- 41.58. Misclassification rates in Table 3 Three-dimensional Plots tinguished among intermediate diets. (listed for analysis of the blue-green and Based on the 3-dimensional plots of These single peaks were in the blue and red regions of the visible spectrum at an polynomial regression coefficients taken 3 red regions of the visible spectrum and excitation wavelength of 355 nm) show at a time, it was observed that regression made it possible to discriminate among the that all 3 lambs fed the control diet con- coefficients for the fourth-order term were 4 diets in a linear fashion (a = 0.05). taining no tarbush leaf (100% tobosa hay) giving the least useful information to Multivariate techniques are, in general, were correctly classified, and 3 out of the graphically separate the regression coeffi- more powerful than analogous univariate 4 lambs fed the diet containing 30% tar- cients. Therefore, the decision was made techniques but do require larger sample bush leaf were correctly classified. Cross- to replace the quartic term with a new sizes to compensate for simultaneously fit- validation (the CROSSLIST option in the variable, the red-to-blue count intensity ting more parameters. In this set of analy- DISCRIM procedure in SAS 1989a) indi- ratio. This decision was based on the pre- ses, the number of observations (lambs) cated the lambs fed the diets containing vious work by Anderson et al. (1996, was small (n = 13) relative to the number 10% and 20% tarbush leaves were likely 1998), who found the red-to-blue count of variables and groups being used (t = 6, to be misclassified—in general inter- ratio to be useful in distinguishing among c = 4). The small sample size likely result- changeably. This indicated there was no materials when using maximum fluores- ed in the inability of multivariate analyses sharp spectral separation at the excitation cence intensity values. The maximum to separate the 10% and 20% tarbush leaf wavelength evaluated between the diets intensity of both blue-green and red diets from the 2 extreme diets. However, containing 10% and 20% tarbush leaf regions was found for each of the lamb’s these analyses do provide information material. 13 data sets and the ratio of these 2 maxi- about the entire fluorescence spectrum, Out of 7 misclassifications given in mum peak intensities was calculated using summarizing that information in just 6 Table 3, five were strongly misclassified, the MEANS procedure in SAS (SAS regression coefficients for each lamb and with maximum classification probabilities Institute 1990a). After including this new spectral region. In situations where more greater than 0.95. For example, for 1 lamb variable (an intensity ratio) and deleting animals are available from which to obtain fed 10% tarbush leaf which was misclassi- the fourth-order regression coefficient, fecal samples, we expect this sequence of fied to the diet containing 20% tarbush discriminant function analysis was again statistical techniques will be able to distin- leaf, the maximum classification probabil- performed. Unfortunately, the addition of guish among diets. ity was 0.97 while the probability of cor- the red-to-blue maximum count intensity These results suggest fluorometry in rectly classifying that lamb was much ratio did not improve diet separation. For conjunction with multivariate statistical lower at only 0.02. Two of the misclassifi- all cases (i.e., for both red and blue-green techniques show promise in distinguishing cations were borderline with a maximum regions and for each of the excitation among fecal samples representing differ- classification probability of 0.55, but with wave lengths 310, 330, and 355 nm), sepa- ent diets, especially if numbers of animals only a slightly lower probability (0.45) for ration of the extreme diets (those contain- sampled remains relatively large. It is the being correctly classified to the diet con- ing no tarbush leaf and those containing opinion of the authors that 20 to 30 ani- taining 10% tarbush leaf. Even with the 30% tarbush leaf) was possible only for mals allocated among the 4 diets would small sample size for each treatment, it the red region at 310 nm. The 2 intermedi- have substantially improved our ability to was still possible to separate the control ate diets containing 10% and 20% tarbush discriminate among the different diets. diet from the diet containing 30% tarbush leaf material were still indistinguishable in leaf material. The misclassification results all cases. Future Work from the red region of the visible spectrum Calibration procedures following NIST for an excitation wavelength of 355 nm are standards should be conducted to evaluate

376 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 long term instrument stability by compar- Foley, W.J., A. McIlwee, I. Lawler, L. SAS Institute Inc., 1990c. SAS / GRAPH Ð ing data taken from sub samples of a sin- Aragones, A.P. Woolnough, and N. Software: Ref. Ver. 6, 1st ed., Vol. 2, Cary gle sample that are randomly evaluated Berding. 1998. Ecological applications of NC: SAS Institute Inc., 664 pp. over time. Furthermore, a set of reference near infrared reflectance spectroscopy Ð a SAS Institute Inc., 1995. JMP Statistics and standards representing the materials being tool for rapid, cost-effective prediction of the Graphics Guide, Ver. 3.1, Cary NC: SAS evaluated should be periodically evaluated composition of plant and animal tissues and Institute Inc., 593 pp. aspects of animal performance. Oecologia. Walker, J.W., D.H. Clark, and S.D. McCoy. to determine if spectral output changes 116:293Ð305. 1998. Fecal NIRS for predicting percent among runs. 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JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 377 J. Range Manage. 54: 378Ð381 July 2001 A proposed method for determining shrub utilization using (LA/LS) imagery

MARK C. QUILTER AND VAL JO ANDERSON

Authors are environmental practices specialist, Utah Department of Agriculture and Food, PO Box 146500, Salt Lake City, Utah 84114-6500; and professor, Botany and Range Science Department, Brigham Young University, Provo, Utah 84602.

Abstract Resumen

Utilization of plant above ground biomass has continued to be La utilizaciónde la biomasa vegetal aérea continua siendo un a critical yet difficult assessment in rangeland monitoring. Shrub criterio critico pero difícil de evaluar en el monitoreo de pastiza- size and woody structure further compound the measurement of les. El tamaño del arbusto y la estructura leñosa componen las shrub biomass utilization. This study was designed to determine medidas de la utilización de biomasa de arbustos. Este estudio se the potential utility of low altitude / large scale (LA/LS) imagery diseño para determinar la utilidad potencial de las imágenes de in assessing shrub utilization. A near monoculture of Ceriotoides baja altitud/amplia escala (LA/LS) para evaluar la utilización de lanata (Pursh) J.T. Howell (winterfat) located in the western arbustos. Para evaluar la técnica se utilizó una población casi desert shrubland of Utah was used to evaluate this technique. pura de Ceriotides lanata (Pursh) J.T.Howell (winterfat) localiza- Four, 3.1 by 3.1 m plots were identified and the shrubs within the da en un matorral desértico de Utah. Se identificaron 4 parcelas plots were defoliated by hand-picking at about 10% intervals de 3.1 x 3.1 m y los arbustos dentro de ellas fueron defoliados with imagery of the plots obtained between pickings. Imagery manualmente en intervalos aproximados del 10% y en ellas se was obtained using a radio controlled airplane (drone) fitted with tomaron imágenes entre defoliación y defoliación. Las imágenes a 35 mm camera. Images were evaluated using image processing se obtuvieron utilizando un aeroplano controlado por radio software and the resulting reflectance data correlated with defo- (zumbido) equipado con una cámara de 35 mm. Las imágenes se liation percentages (weight basis) for each plot. Reflectance data evaluaron utilizando programas de computadora para procesar from images correlated highly with defoliation percentages (r2 > imágenes y los datos de reflectancia resultantes se correla- 0.9). This technique of using LA/LS imagery shows promise for a cionaron con los porcentajes de defoliación (en base a peso)de quick and accurate tool in assessing utilization of shrubs. cada parcela. Los datos de reflectancia de las imágenes se cor- relacionaron altamente con los porcentajes de defoliación (r2 > 0.9). Esta técnica de utilizar imágenes LA/LS promete ser una Key Words: remote sensing, vegetation inventory, photography herramienta rápida y certera para evaluar la utilización de arbustos. Plant utilization is commonly measured as part of a sustainable natural resource management plan. Many utilization techniques have been developed and used on rangelands, some of which are in forests. When leaves and small stems are removed there are complex and require extensive experience. After significant fewer bright and dark specks in the image and the image texture review of browse utilization techniques, Bonham (1989) conclud- becomes “soft” or “fuzzy”. It is proposed that by measuring this ed that, “Estimation of browse utilization is one of the most diffi- change in texture caused by defoliation (grazing) the amount of cult vegetation characteristics to determine” The object of this foliage removed can be estimated. research was to develop a simple, fast, and inexpensive method of measuring shrub utilization using low altitude/large scale (LA/LS) imagery. Methods and Materials Walker and De Vore (1985) described how LA/LS imagery is effective in discerning shadows of small objects in archeological work. Shadows produce “texture” in images. Leaves, stems, and A near monoculture of winterfat (Ceriotoides lanata (Pursh) flowers all produce shadows and bright spots depending on how J.T. Howell) was selected for study during the summer of 1995 in they are lighted by the sun. This produces dark and light spots on Rush Valley, Tooele County, Utah"). Using a 1-m circular images. With lots of small objects, such as leaves and stems inter- quadrat with 15 replications, the canopy cover of winterfat on the cepting light (bright) and casting shadows (dark) an image will site covering 50 ha was estimated to be about 35%. Three, 3.1 by have a “salt and pepper” appearance or texture. Olthof and King 3.1 m plots were delineated adjacent to each other in the most (1997) found using this textural information in LA/LS imagery uniform stand of winterfat. A wooden stake marked each corner increased their ability to accurately estimate the Leaf Area Index of each plot. Yellow nylon line was attached to the stakes and marked the perimeter of the plots. To make identification of plot Research was funded in part by the Utah Department of Agriculture and Food. corners easier to see in images, paper plates, measuring 23 cm in Authors wish to thank Jim Walker and Wally Barrus for technical assistance with diameter were centered on each stake at a height of 45 cm. construction and operation of the drone. Plots were defoliated by hand to simulate grazing. The plots Manuscript accepted 20 Sept. 2000. were picked 10 times removing approximately 10% of current

378 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 year’s growth each time. At the end of 10 picking events all of the current years growth was removed. The harvested plant materials were placed in separate paper sacks for each plot and picking event. After drying in a forced air dryer at 38¡C for 7 days, weights were obtained for each plot and picking event. After each picking event a white paper plate was placed between plots to document picking periods (the first picking event had 1 plate, the second 2, the third 3, etc.). Plots were then photographed from the air. Two drones were used to photograph the plots. One drone was fitted with 2 digital cameras; one, was a 3 color (Red, Blue, and Green) sensor and the other a black and white sensor which was filtered with a wratten 25 filter to record reflected near infra-red (NIR) light. This drone was flown before the first picking and after each of the 10 pickings. It was intended that vegetation indexes could be obtained from the red and NIR bands of the digital cameras and provide measurements of defoliation. The second drone was fitted with a 35 mm SLR film camera and loaded with a 36-exposure roll of Kodak Gold ISO 200 film. Pictures acquired with this drone were intended primarily to document the work and only flown during the 2nd, 4th, 5th, and 9th pickings. The work was done on 12 July 1995 between 1000 hours and 1200 hours. This period of time would provide the best sun angle (almost vertical) for aerial photographs. The drones flew at an altitude Fig. 1. Aerial images of winterfat study plots in Utah’s west desert: a). Lightly Defoliated (2 122 m. Drone pilots were directed by the picking events, about 20% defoliation); b). Heavily Defoliated (9 picking events, about ground crew when to trigger their cameras 80% defoliation). by signaling when the drones were directly over the plots. The images from the dig- The TIFFs were imported into image vegetation which created them (see Figs. ital cameras were viewed at the site on a processing software package (IDIRSI, 1a. and 1b). After visually analyzing the laptop computer. It was found that none of Clark University 1995) for image analysis. images, it was decided that the most effi- the digital images recorded the plots. It This analysis produced red, blue, and cient method to interpret them was to eval- was determined that the automatic expo- green bands from each TIFF image. All uate reflectance profiles for each plot and sure sequence of the digital cameras was images were colored balanced to match picking event. Reflectance profiles show not consistent between cameras or expo- the first image by selecting the same area the amount of reflected light recorded in sures. Therefore we were unable to time in each image and using IDRISI's regres- an image as a profile with high reflectance the cameras' exposures and obtain usable sion procedure to obtain slope and y inter- values (white objects) forming peaks and digital images of the plots. cept values to adjust color. To balance the low reflectance values (shadows) forming Film from the drone was developed at a effect of time on shadows the images were valleys (see Figs. 2a and 2b). Profiles were commercial film processor. Differences balanced using a linear stretch routine in selected on diagonal lines of the plots as between the early pickings and later pick- IDRISI. This procedure also neutralized marked by paper plates at the corners. ings were apparent in the photographs. It effects of harsh shadows caused by direct This ensured that each profile was of the was determined that we would evaluate sunlight. same area in each image for each plot. The the photographs. One image from each of The difference between the early and profile's y-axis records the gray scale the 4 photographed picking events were late images (non-defoliated vs. defoliated) reflectance from 0 (dark shadow) to 215 selected and enlarged to 20.3 by 25.4 cm. was depicted in the photograph's texture. (bright reflectance of white light) for the Enlarged photographs were then scanned Non-defoliated plots had many variations paper plates. The x-axis was the distance in a flat bed color scanner set at a resolu- in shadow and light making the image from corner to corner. tion of 900 dots per inch. The images were speckled. Photographs of defoliated plots Profiles were evaluated by determining cropped to show just the plots and saved appeared soft and somewhat fuzzy, the percentage of the line that has a Grey in a tagged-image file format (TIFF) for because the many variations of shadow Scale Reflectance value of 21.5 or higher. computer processing. and light were removed by removing the This is the reflectance level of soft shad-

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 379 a b

Fig. 2. Reflectance profile of winterfat study plots in Utah’s west desert area after: a). 2 picking events (about 20% defoliation); b). 9 picking events (about 80% defoliation). The value of 215 represents total reflectance (bright white) where 0 is no reflectance (deep shadow). Line intercept values are measured as a percent reflectance running between points “A” and “B” along the reflectance value of 21.5. Fig. 2a shows more shadows than Fig. 2b which has very little shadow along the “AB” line. ows caused by small twigs, leaves, and The total dry weight of plant material vegetation cover or browse available. diffuse objects. (The value of 21.5 was removed from each plot was determined After visually studying aerial photographs determined by querying the reflectance by summing all dry weights from each of treated plots, it was apparent that there values of soft shadows in the images.) picking event for the plot. Percent dry were changes due to successive defoliation Reflectance values below 21.5 are harsh weights for each picking event was then (compare Fig. 1a. Lightly Defoliated and shadows from large stems, rocks, and calculated based on the total plant material Fig. 1b. Heavily Defoliated). The most other solid objects. Vertical lines were removed from the plot up to and including notable changes were in the textural char- first drawn at the plot corners. The high the current picking event (“Percent acteristics of the defoliated plots (Fig. 1b). reflectance values (215), which are flat, Utilization”). Areas outside of the treated plots have a were produced by the paper plates and “Percent Reflectance” values were then rough, specked appearance. The defoliated identify the plot corners. Next, a line is regressed against the corresponding plots appear soft or fuzzy because shad- drawn parallel to the x-axis at the y-value “Percent Utilization” values of the picked ows have been removed by defoliation. of 21.5. The total length of the gray area vegetation for corresponding plots and Percent Reflectance had high positive that intercepted the line at 21.5 was mea- picking events using Pearson’s Correlation correlation with Percent Utilization (Fig. sured and divided by the total length of procedures (Conover 1980). 3, r2 = 0.9365). This indicates that pho- the line to give a “Percent Reflectance”. tographs using this methodology can be Percentages were used to negate the dif- used to measure utilization in winterfat ferences in scale of the different pho- Results and Discussion communities. Of significance for the range tographs. Profiles were determined for manager, is the area of the curve between each plot in the 4 photographs producing The purpose of this project was to find a 20 and 80 percent utilization. It is in this 12 profiles. simple method of measuring changes in range that critical decisions are made as to when livestock are removed from the

Fig. 3. Reflectance plotted against percent utilization with the Fig. 4. Reflectance plotted against percent utilization (between 20 respective regression equation, line and strength. and 80%) with the respective regression equation lines and strengths.

380 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 range site. The best exponential fit in this flights would be made throughout the Literature Cited critical range has an even higher correla- grazing season or seasons to measure uti- tion value (Fig. 4, r2 = 0.9805). lization of the site. Bonham, Charles D. 1989. Utilization. This study demonstrates the value of Measurements For Terrestrial. John Wiley and using LA/LS imagery in measuring shrub Sons. NY, NY. utilization in winterfat communities. This Conclusions Clark University. 1995. IDRISI For Windows, procedure could likely be extended to Version 1.0 Reference Manual. IDRISI Project, other shrub and herbaceous communities. This work demonstrates that LA/LS Clark University, Worcester, Mass. A recommended procedure would be to Conover, W. J. 1980. Practical Nonparametric may be a useful tool in range management Statistics 2nd edition. John Wiley and Sons, N.Y., place several pairs of posts to designate to accurately measure utilization of desert N.Y. permanent transect lines. Next a small shrubs. The LA/LS imagery could become Olthof, Ian and Douglas J. King. 1997. Evaluation enclosure would be needed next to each a primary method for measuring utiliza- of Textural Information IN Airborne CIR Digital transect line. This enclosure would serve tion and change in rangeland areas. Since Camera Imagery for Estimation of Forest Stand as a control to adjust images taken at vari- the method measures change in shadow, Leaf Area Index. Proceed. of The First North ous times as well as provide an undis- which in turn is related to the vegetative American Symp. on Small Format Aerial Photog. cover, the method has promise for measur- pg 154Ð165. ASPRS. Bethesda, Md. turbed site for comparisons. At the time of Walker, James W. and Steven L. De Vore. photographing the posts would be fitted ing change in any vegetated area. Unlike 1995. Low Altitude Large Scale Reconnaissance: with a white highly reflective target to many of the traditional utilization methods A Method of Obtaining High Resolution Vertical delineate transects on the images. Profiles of monitoring, this method requires little Photographs for Small Areas, Revised Edition. would then be obtained and processed as time, is non-destructive, and the data is Interagency Arch. Serv., Div. of Partnerships and discussed in this paper. Consecutive permanently recorded. Outreach, Rocky Moun. Reg. Office, Nat. Park Serv., Denver, Co.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 381 J. Range Manage. 54: 382Ð389 July 2001 Low density of prickly acacia under sheep grazing in Queensland

FLEUR TIVER, MIKE NICHOLAS, DARREN KRITICOS, AND JOEL R. BROWN

The first author is senior lecturer in ecology, School of Environmental Management, University of South Australia, Mawson Lakes, South Australia 5095. At the time of the research, she was a research scientist, CSIRO Division of Tropical Crops & Pastures, Davies Laboratory, Aitkenvale, Townsville, Queensland 4814. The 2nd author is a research officer, CSIRO Division of Tropical Agriculture, Davies Laboratory, Aitkenvale, Townsville. At the time of writing the 3rd author was a doctoral student at the Cooperative Research Centre for Tropical Pest Management, Gehrmann Laboratories, University of Queensland, Brisbane, and is now a post-doctoral research fellow, Cooperative Research Centre for Weed Management Systems, CSIRO Entomology, GPO Box 1700, Canberra ACT 2601, Australia. The 4th author is a senior research scientist with the USDA/NCRS, Jornada Experimental Range, PO Box 32003, MSC 3JER, New Mexico State University, Las Cruces, N.M 88003-8003, USA. At the time of the research he was a project officer, CSIRO Division of Tropical Crops & Pastures, Davies Laboratory, Aitkenvale, Townsville, Queensland.

Abstract Resumen

Populations of an introduced woody weed, prickly acacia En 4 sitios de la región central de Queensland se muestrearon (Acacia nilotica (L.) Delile ssp. indica (Benth.) Brenan syn. poblaciones de una maleza leñosa introducida, “Prickly acacia” Acacia arabica (Lam.) Willd. ssp. indica Benth.), were surveyed (Acacia nilotica (L.) Delile ssp indica (Benth.) brenan syn Acacia at 4 sites in central Queensland. There is a significantly lower arabica (Lam) Willd. ssp indica Benth.). Dentro de poblaciones frequency of plants of < 3 m in height within populations which que han sido apacentadas por ovinos hay una frecuencia signi- have been grazed by sheep, indicating that browsing by sheep ficativamente menor de plantas de < 3 m de altura, indicando reduces regeneration. There were higher losses of seedlings at a que el ramoneo por ovinos reduce la regeneración. Hubo may- sheep-grazed site than at cattle-grazed sites. These results sup- ores perdidas de plántulas en los sitios apacentados por ovinos port previous assertions that prickly acacia is regenerating more que en los sitios apacentados por bovinos. Estos resultados successfully on cattle properties, because cattle both disperse avalan afirmaciones previas respecto a que el “Prickly acacia” se seeds and are less effective herbivores. In regions of low annual esta regenerando mas exitosamente en los ranchos que son rainfall, prickly acacia is capable of forming dense stands (up to explotados con bovinos porque dispersan las semillas y son her- 2,700 shrubs ha-1) in lowland landscape types. Stands are less bívoros menos efectivos. En regiones de baja precipitación anual dense in upland landscapes (maximum of 718 shrubs ha-1). Of el “Prickly acacia”es capaz de formar poblaciones densas (hasta -1 most concern is that in regions of high annual rainfall prickly 2,700 arbustos ha ) en tipos de paisaje de tierras bajas. Las acacia can form extremely dense thickets across most landscape poblaciones son menos densas en terrenos altos (máximo 718 -1 types (up to 3,400 shrubs ha-1). We suggest that prickly acacia is arbustos ha ). La preocupación mas frecuente es que en regiones most likely to become a management problem on cattle proper- de alta precipitación anual el “Prickly acacia” forme poblaciones ties, and an extreme problem in high annual rainfall areas. The extremadamente densas en la mayoría de los tipos de paisaje -1 inclusion of sheep in livestock rotations may be an effective con- (hasta 3,400 arbustos ha ). Sugerimos que el “Prickly acacia” es trol measure in the Mitchell Grasslands, but this may not always mas probable que llegue a ser un problema de manejo en las be possible. A high priority is to prevent prickly acacia from propiedades de bovinos y un problema extremo en áreas con alta expanding its range into equivalent high rainfall areas within precipitación anual. La inclusión de ovinos en las rotaciones de Queensland, and also in the Northern Territory, northern New ganado puede ser una medida de control efectiva en los pastiza- South Wales, and Western Australia. This could be achieved by les Mitchell, pero esto no siempre es posible. Una alta prioridad quarantining livestock which have come from infested properties es el evitar la expansión del rango del “Prickly acacia” a áreas until seeds have passed through the digestive tract, after about 6 equivalentes de alta precipitación dentro de Queensland, del days. Management strategies at the property level should aim to Territorio del Norte, del norte del Nuevo Sur de Galeso y el oeste prevent further spread of prickly acacia by controlling cattle de Australia. Esto se puede lograr cuarentenando el ganado que movements between paddocks during periods when cattle are viene de propiedades infestadas hasta que las semillas hayan ingesting pods and seeds. pasado a través de tracto digestivo, aproximadamente después de 6 días. Se deben promover estrategias de manejo a nivel de propiedad para prevenir la dispersión del “Prickly acacia” mediante el control de los movimientos de ganado entre potreros con The authors wish to thank the following landholders for access to land and assis- bovinos que están consumiendo vainas y semillas. tance with historical grazing information: Mr Gordon Smith of Bowen; Messrs Mic and Cec Burry of Giru; Alan Davidson of Nocoleche Station, Hughenden; Management and staff of Marathon Station, Richmond; Mr and Mrs K.J. Cameron Key Words: Life-stage profiles, rainfall, population dynamics, of Allaru Station, Richmond; Mr and Mrs B. Fells of Garomna Station, Julia Creek, regeneration, cattle, woody weeds and Trevor Mitchell of the Queensland Department of Lands, Hughenden. Marnie McCulloch and Debbie Atkins of the Queensland Department of Primary Industries Prickly acacia (Acacia nilotica (L.) Delile ssp. indica (Benth.) in Bowen provided assistance in locating sites. Funding for this project was provid- Brenan syn. Acacia arabica (Lam.) Willd. ssp. indica Benth.) ed by a CSIRO Multi-Divisional Project as part of the Tropical Agri-Export Program. Tony Grice and Jim Noble critically reviewed the manuscript. was introduced into the Mitchell Grass Plains of western Manuscript accepted 16 Sept. 2000. Queensland in the 1890s as a source of shade and fodder (Barker

382 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 1996). From western Queensland, prickly Cattle pass about 81% of ingested seed the climate of the Pacific Ocean and east- acacia has spread as far as Cooktown in far intact of which 15% are germinable ern Australia (Nicholls 1991). During north Queensland, south to Coonamble in (Harvey 1981), giving 41% germinability 1974 much of the low-lying country in New South Wales, west to the Barkly from those ingested (Barker 1996). Sheep western Queensland was flooded for Tablelands and Arnhem Land in Northern pass < 1% of prickly acacia seeds intact of weeks and local pastoralists report that Territory and east to the coast of which 33% are germinable (Harvey 1981, there was a mass germination of prickly Queensland, an area approaching 4 million Carter et al. 1991, Barker 1996). Sheep acacia following these floods. Pods are km2. It is now listed as a category 1 weed tend to regurgitate large numbers of seeds indehiscent, so the seeds remain in the for northern Australia, that is: a terrestrial during ingestion of the pods (35%) and pods unless consumed by herbivores. We species which has extensive continental rumination (14%) (Carter and Cowan have observed that pods are capable of distribution and is capable of destroying an 1993) hence depositing the seeds close to floating for up to 30 hours in water with ecosystem (Humphries et al. 1991). source and contributing little to increased 67% subsequent germination so the floods Rapidly increasing populations of both range of prickly acacia. Cattle have been may have served a dual purpose of dis- native and exotic shrubs, often called shown to disperse the seeds of mesquite persing seeds and also scarifying them by “woody weeds”, which cause disruption of (Prosopis) in North America (Brown and softening the seed-coat and leaching ecosystems and reduction of rangeland Archer 1987). The gut bacterial flora of growth inhibitors. productivity have been well documented large herbivores has been shown to in the USA (Hennessy et al. 1983, Archer destroy larvae of beetles from the family The Study Area 1989, 1984, Brown and Archer 1989), Bruchidae which would otherwise con- Eight sites in prickly acacia stands were southern Africa (Skarpe 1990, Holmes and sume the seeds in which they are present chosen in central Queensland; locations Cowling 1997) as well as in Australia (Miller 1994). This means that large herbi- and rainfall are shown in Fig. 1 and Table (PNSW 1901, Moore 1969, Harrington et vores not only act as dispersal agents, they 1. Average annual rainfall data from the al. 1984, Humphries et al. 1991). Efforts also protect the seed from one of the nearest recording centres to each site to control shrubs by clearing and poison- potentially most important predators. The (Giru, Bowen, Hughenden, Richmond and ing have generally proved unsuccessful process of digestion also scarifies the Julia Creek) were obtained from the and uneconomic. Such methods are expen- seeds, thus increasing germinability of Australian Bureau of Meteorology, and sive for the degree of control achieved, deposited seeds and further increasing the had been collected for 60Ð100 years, and there is only a short to medium term potential of large herbivores to spread depending on the time of establishment of benefit in increased livestock returns per prickly acacia. the recording stations at these centres hectare, particularly on properties where The objective of this study was to sur- (ABM 1996). Two high rainfall (989 and stocking rates are low regardless of shrub vey existing populations of prickly acacia 1,164 mm) sites were near the coast south densities. Control strategies are more like- and to determine if the species of livestock of Townsville (Giru and Bowen). It is very ly to be implemented if they are economi- used for rangeland enterprises (sheep and difficult to determine the original vegeta- cal and aligned with existing management cattle) are each associated with differences tion at these sites because of the large practices, and more likely to be successful in seedling survival and population densi- degree of alteration to the vegetation cover if based on ecological principles ties of prickly acacia. through cultivation for sugar cane, intro- (Harrington 1979, Adamson and Fox duction of pasture species for cattle-graz- 1982, Jacoby 1985). Any alteration in the Materials and Methods ing, and invasion by woody weeds includ- establishment of new individuals into the ing prickly acacia and others such as population can have dramatic effects on paloverde (Parkinsonia aculeata L.). The the long-term survival of plant populations Background sites appear to have originally been tea- (Harper 1977). The survivorship of Prickly acacia was deliberately intro- tree (Melaleuca spp.) swampy woodlands. seedlings is crucial to shrub regeneration duced to western Queensland at least by The remaining 6 sites were at inland, low so it is logical to examine this portion of 1926, when it was recommended as a annual rainfall (420Ð487 mm) areas in the life cycle of a plant when developing a shade and fodder species by the central western Queensland between management strategy. Queensland Department of Agriculture Hughenden and Julia Creek. These sites A widespread change from sheep to cat- and Stock (Barker 1996). It was not listed were originally open plains dominated by tle-based enterprises in the Richmond as a significant exotic in western Mitchell grass (Astrebla spp.). The land- Shire may have contributed to the increase Queensland in 1938 (Blake 1938). holders supplied information on grazing of prickly acacia since 1973/74 (Carter Although prickly acacia became natural- histories for the previous 20 years or 1994). Originally, leases in the western ized along creeks and boredrains (artificial more. The 2 coastal sites (Giru and districts were only legally permitted to drains where artesian water from the Great Bowen) and one of the Hughenden sites carry sheep. This requirement was relaxed Artesian Basin is channelled for live- (Marathon Station) have been exclusively during the 1960s and 70s and increased stock), it did not appear to cause wide- grazed by cattle for ≥ 25 years. The cattle prices encouraged many landholders spread concern until the 1970s. There remaining Hughenden site (Nocoleche to switch from sheep to cattle-based enter- were several above-average rainfall years Station) is grazed by cattle. The 2 sites at prises. Both sheep and cattle are known to in the early 1970s, including 1973 and Richmond (Allaru Station) are grazed pre- eat the pods of prickly acacia but cattle 1974 when the annual rainfall was around dominantly by sheep, with very occasional chew seeds very ineffectively compared to twice the average (ABM 1996). These access by cattle to the site. The 2 sites at sheep, pass a larger proportion of viable periods of high rainfall are associated with Julia Creek (Garomna Station) have been seeds in their dung and hence are more La Niña phases of the El Niño-Southern grazed by sheep only, and one was effective dispersal agents than sheep. Oscillation (ENSO) patterns which control unstocked during the seedling study.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 383 plant was still present with the rings intact. Where rings were scattered and the seedling missing from its recorded position, it was assumed that the seedling had been either trampled or grazed, thus allowing the rings to come off. These seedlings were recorded as missing since it was usually not possible to determine with certain- ty whether they had been trampled or grazed. Cohorts were followed until July 1995. The experiment was located oppor- tunistically rather than by design. It is therefore not replicated and the results were not statistically analysed, but presented in summarized format only.

Results

Population Densities Densities of prickly acacia at 6 sites are Fig. 1. The study area in central Queensland (inset) showing the location of 8 sites in prickly given in Table 2. Prickly acacia can form acacia (Acacia nilotica ) populations. The sites at Giru, Bowen, and Hughenden are grazed very dense stands, especially in high annu- by cattle, and the sites at Richmond and Julia Creek are grazed by sheep. The coastal sites, al rainfall regions of coastal Queensland Giru and Bowen have about double the annual rainfall (around 1000 mm ) of the inland such as Bowen (3,381 shrubs ha-1). sites (around 450 mm) (see Table 1). Extremely dense stands were also recorded at Giru (5,059 shrubs ha-1), a high rain- Population Structures & Population Seedling Survival fall site which had been chained approxi- Densities Following rain in January 1995, cohorts mately 15 years previously (C. Burry pers. Size structure profiles of each popula- of acacia seedlings were observed at Giru, comm.). At the high annual rainfall sites, tion were developed from 20 individuals Bowen, Nocoleche, Allaru, and Garomna shrub densities were highest on well- located by a “random walk” transect North. At each site over 60 seedlings were drained sites (uplands and plains) whereas method (Kent and Coker 1992, Silvertown located and their positions recorded using a poorly drained floodzone supported and Lovett-Doust 1993) and the results a measuring tape placed between 2 perma- lower density shrubs ha-1. Prickly acacia plotted as frequency distributions. nent marking stakes. has also formed dense stands at low annu- Differences between sheep and cattle Seedling location was recorded as a pair al rainfall in the Mitchell grasslands of grazed sites were analysed by t-test. At 6 of coordinates, distance along the tape in inland Queensland, but only in and adja- of the sites, the height of the nearest tree m and distance and direction at right cent to boredrains (shallow earth channels within each of the 4 compass quadrants angles from the tape in cm. Seedlings built to carry water flowing from was measured each 20 m along a 400 m were tagged with plastic poultry leg-rings. uncapped artesian bores for livestock) and transect, giving a size profile for each pop- Two rings were placed on each plant, in in creeklines which receive extra water ulation based on 80 individuals per site. different combinations of 6 colours so that from surface flow. Densities were as high Density of prickly acacia at each land- individuals could be found and identified as 1,150 shrubs ha-1 on the bank of a bore- scape type within each site was calculated easily. The cohorts were visited every 3 drain at Allaru North but on upland land- as follows. The distance to each of the weeks and individuals which had died due scapes the maximum was 354 shrubs ha-1 trees in each quadrant was measured using to desiccation recorded. In this case, the at Marathon. a point-centred quarter plotless sampling technique. These were later used to calcu- Table 1. Locations (recorded by GPS) and precipitation data of 8 prickly acacia (Acacia nilotica) late plant densities (D) using the formula: sites in central Queensland.Rainfall data were obtained from the Australian Bureau of 20 4 Meteorology (ABR 1996). D = 20 / ∑ ( ∑ d m, n / 4 )2 (1) m = 1 n = 1 Site Coordinates Nearest Rainfall Median Years of Recording Station Rainfall Rainfall Records where d is the distance to the trunk of the (mm) (years) nearest tree in each quadrant n, and m is Giru 20¡ 28'14" S 147¡ 7' 5" E Giru PO 1164 1929Ð1993 the tree number (Cottam and Curtis 1956, Bowen 20¡ 3' 45" S 148¡ 12' 23" E Bowen PO 988 1871Ð994 Greig-Smith 1983). Differences in popula- Nocoleche 20¡ 54' 39" S 144¡ 10' 33" E Hughenden PO 483 1884Ð1994 tion densities between sites and landscape Marathon 20¡ 54' 44" S 143¡ 34' 00" E Richmond PO 425 1890Ð1994 types within sites were analysed by Allaru North 20¡ 45' 16" S 143¡ 09' 10" E Richmond PO " " ANOVA. Allaru South 20¡ 46' 8" S 143¡ 9' 10" E Richmond PO " " Garomna North 20¡ 40' 7" S 141¡ 47' 28" E Julia Creek PO 422 1913Ð994 Garomna South 20¡ 42' 8" S 141¡ 50' 51" E Julia Creek PO " "

384 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 2. Mean densities (shrubs ha-1) of prickly acacia (Acacia nilotica) at 6 sites in northern losses were caused by grazing. Seedling Queensland. Densities differ significantly (F = 6.84, df = 5, 113, p = 0.0001) by anova. Numbers losses were between 16 and 23 % at cattle- of trees within each landscape type are shown in brackets. Densities between coastal sites (Giru grazed sites. Most mortality appeared to and Bowen are significantly different from those at the inland sites (Nocoleche, Marathon, be due to trampling because there were Allaru North and Garomna North) (t = 4.182, df = 117, p = 0.0001). hoofmarks present in most cases and the rings were often found kicked some dis- Site Landscape type Density Site Mean (n = no. of trees) tance away. Losses to grazing, presumably by insects, were very low (3%) at the site (shrubs ha-1) Giru upland/plain (n = 10) 5059 which was ungrazed by sheep or cattle for floodzone (n = 7) 220 the duration of the study, Garomna North. swamp (n = 3) 2642 3696 Bowen upland/plain (n = 20) 3381 3381 Discussion and Conclusions Nocoleche bank (n = 4) 339 creek (n = 5) 497 floodplain (n = 1) 610 Prickly acacia populations are capable upland/plain (n = 10) 181 313 of reaching extremely high densities (over Marathon puddle/gilgai (n = 6) 192 3,000 shrubs ha-1) on high annual rainfall bank (n = 5) 354 (> 900 mm year-1) sites where they have creek (n = 2) 64 upland/plain (n = 6) 354 272 formed impenetrable thickets, presenting a serious management problem. Populations Allaru North bore-drain (n = 4) 1039 of this density were not recorded in the bank of drain (n = 6) 1150 -1 upland/plain (n = 10) 253 679 low annual rainfall (< 500 mm year ) Garomna North creek-bed (n = 7) 613 rangelands to the west, the highest densi- bank (n = 3) 385 ties recorded in boredrains are about one upland (n = 9) 80 359 fifth (just over 1,000 shrubs h-1) of those

Population Structures Population profiles show a higher frequency of individuals between 100 and 300 cm high at cattle-grazed as compared with sheep-grazed sites (Figs 2 and 3). This is also apparent when expressed as a percentage of the total population (Table 3) and is statistically significant by t- test (p = 0.0284). The few individuals under 300 cm present at the 4 sheep-grazed sites were heavily browsed and dwarfed, and may have been considerably older than expected for those height classes. These are indistinguishable from recent recruits in the histograms, highlighting a problem of using height as a surrogate for age. The browsed dwarfs were particularly noticeable at Garomna (both North and South) and Allaru South. In many cases these had died. Individuals between 100 and 300 cm high were almost entirely absent from the remaining sheep-grazed site (Allaru North). Individuals below 300 cm at the cattle-grazed sites (Giru, Bowen, Nocoleche and Marathon) showed little sign of browsing.

Seedling Survival Prickly acacia seedling losses were highest at the sheep-grazed site, Allaru North (88%) (Fig. 4). Some plants were missing from their recorded positions and this could have been due to either tram- Fig. 2. Height structure profiles of prickly acacia (Acacia nilotica) populations at 4 cattle- pling or grazing. However in some cases grazed sites in central Queensland. Data are frequency percentages, height classes are as follows: 1 = 0 - 100 cm; 2 = 101 - 200 cm etc) Rainfall and grazing histories are: Giru (high the nipped off stem of the seedling was rainfall, cattle), Bowen (high rainfall, cattle), Nocoleche (low rainfall, cattle), Marathon located, indicating that at least some of the (low rainfall, cattle).

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 385 1976, Crisp 1978, Miller and Halpern 1998, Tiver and Andrew 1997), and by other herbivores (Myster and McCarthy 1989). As observed in Lange and Purdie’s (1976) A. papyrocarpa Benth. study, sheep-browsed dwarves may survive as stunted, non-reproductive individuals for months or even years before finally suc- cumbing. Previous studies of Acacia nilotica have concluded that neither sheep nor goats had any effect on juveniles (Carter and Cowan 1993). Grazing induced mortality may only occur when years of biomass reduction by repeated browsing are combined with drought conditions, a process not detectable in short-term grazing trials. Milton (1994) attributed mortality of populations of 3 species of shrubby Asteraceae to factors other than defoliation, but the study indicated that grazing could have a substantial effect on growth form and reproductive success. Similarly, grazing by prairie dogs (Cynomys spp.) limits recruitment of Prosopis glandulosa in grasslands of southwestern North America (Weltzin et al. 1997). It appears that the lower regeneration of prickly acacia at sheep-grazed sites is due to a combination of trampling and grazing Fig. 3. Height structure profiles of prickly acacia (Acacia nilotica) populations at 4 low rain- of young seedlings, and browsing and fall sheep-grazed sites in central western Queensland. Data are frequency percentages, stunting of juveniles as long as their height classes are in metres. Rainfall and grazing histories are: Allaru North (sheep, some canopies remain within browse range. The cattle), Allaru South (sheep, some cattle), Garomna North (sheep only), Garomna South reintroduction of sheep, either alone or in (sheep only). a grazing rotation with cattle, could be a useful control measure for prickly acacia from high rainfall areas. However, the stage, which may eventually lead to death in western Queensland, at least preventing high percentages of individuals in the low- of the plant. Continuous browsing over a further increases in density and spread on est size classes on cattle-grazed properties number of years would inevitably reduce already infested properties. Unfortunately at low annual rainfall indicate a rapid rate photosynthetic area, limit growth, and pre- sheep do not thrive in the wet humid con- of regeneration in recent years, so we prevent the formation of an extensive root ditions which prevail on the coast, so dict increases in both density and area system, presumably making these individ- alternative methods of control will be infested by prickly acacia on cattle proper- uals more drought-susceptible. required there. ties in central western Queensland unless This is the first direct evidence of sheep Anecdotal evidence that prickly acacia appropriate management procedures are suppressing regeneration of prickly acacia, has become much more of a problem in undertaken. although suppression of regeneration by the Mitchell Grass Plains of central west- Prickly acacia seedlings and juveniles sheep has been shown in other woody ern Queensland since many properties have lower survival on sites where sheep species (Pressland 1975, Lange and Purdie are present, whether by consumption or trampling of young seedlings, or by Table 3. Percentage of prickly acacia (Acacia nilotica ) juveniles 100 to 300cm height at each of repeated browsing of older juveniles. We the 8 sites. Differences in mean between cattle-grazed and sheep-grazed sites are significant (t = 2.872, df = 6, p (2-tail) = 0.0284). saw no evidence that cattle graze prickly acacia seedlings, in accordance with Site A. nilotica Mean S. D. S.E. Barker (1996) who found no evidence for 100Ð300cm herbivore suppression of recruitment in (%) prickly acacia, though there were some Grazed by Cattle losses due to trampling in heavily used Giru 30.0 areas. The cohort of young seedlings in Bowen 32.8 the sheep paddock completely disappeared Nocoleche 48.6 within the first month, due to a combina- Marathon 43.25 38.662 8.741 4.37 tion of trampling and direct herbivory. Grazed by Sheep The heavily grazed and dwarfed individu- Allaru North 12.82 als which were observed at 2 of the sheep- Allaru South 35.0 Garomna North 7.59 grazed sites indicates that sheep will Garomna South 13.16 17.142 12.175 6.087 browse prickly acacia beyond the seedling

386 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 rain and flooding followed by several successive years of high aggregate rainfall which provide follow-up rains for establishment. Similarly high desiccation rates of seedlings of Acacia ligulata Cunn. ex Benth. and Casuarina cristata Miq. ssp. pauper F. Muell. (variable, up to 80%) were shown within the first couple of (dry) years after emergence in western New South Wales (Auld 1995). Prickly acacia is not as prone to desiccation as these species, and given the high seed loads, it seems likely that at least some plants establish in most years, but as with other shrubs in the arid zone there are pulses of recruitment during high rainfall years associated with La Niña events (Brown and Carter 1998). The effects of La Niña generated recruitment flushes of prickly acacia in the Mitchell grasslands have probably been amplified because of the replacement of sheep by cattle as the dom- Missing inant herbivores. (Grazed/Trampled)

Dead Control of prickly acacia (Desiccated) We suggest that prickly acacia is more Surviving likely to become a management problem on cattle properties than sheep properties in the Mitchell grasslands. At present in Fig. 4. Percentage losses by desiccation, missing (either trampled or grazed) and survival in these areas it is only at high densities in cohorts of prickly acacia (Acacia nilotica) seedlings at 5 locations in central Queensland. creeklines and boredrains. Densities are Seedling cohorts germinated during the wet season January 1996 rains and their progress was followed until July 1996. lower on upland sites but populations are continuing to regenerate rapidly, suggesting that further increases in density and have been changed from sheep to cattle ficult management problems. Harrington spread are likely. Of prime concern are the enterprises is supported. This also explains (1991) suggested that although competi- prickly acacia infestations under higher why landholders who still run sheep are tion from grasses was important in limit- rainfall regimes such as those on the east much less concerned than others about the ing the survival of woody plant seedlings coast of Queensland where it is able to pest potential of prickly acacia (Brown in most years, climatic conditions were form dense unmanageable thickets on and Carter 1998). Where sheep are still occasionally adequate for mass establish- most landscape types. As a priority, man- present, prickly acacia seedlings have not ment and that post-establishment distur- agement strategies should aim to prevent survived in large numbers since the major bances such as fire would be critical to further spread of prickly acacia from prop- germination event which occurred during managing shrub populations. Mortality erty to property in eastern Queensland and 1973/74, and some landholders even due to desiccation of prickly acacia to prevent introduction of prickly acacia expressed concern that older trees were seedlings may reach 60% within the first into other regions in Queensland, Western dying off and not being replaced rapidly few months post-emergence. Even higher Australia, the Northern Territory and enough to maintain a good source of mortality of seedlings is found in other northern New South Wales where comput- drought fodder and shade for their livestock arid zone shrubs including narrow-leaved er modelling predicts that the climate (B. Fells, pers. comm.) Alternatively, on hopbush (Dodonaea viscosa Jacq. ssp. would support severe infestations properties without sheep, prickly acacia angustissima DC., syn. D. attenuata (Kriticos 1997). The most effective means seedlings have had high survivorship over Cunn.), a native increaser species of south- of preventing spread will be by quaranti- the last 25 years and density has continued ern Australian rangelands. Harrington ning cattle from infested properties before to increase since 1973/74 (Brown and (1991) estimated from watered pot trials transporting them to other properties with- Carter 1998). Landholders on cattle prop- that in only 6 out of 97 years have soil in Queensland or interstate. An appropri- erties were more concerned about the pest moisture levels been sufficient to allow ate quarantine period would be 6 days, the potential of prickly acacia, since its value widespread recruitment in western New time taken for seeds to pass through the as fodder and shade could be negated by South Wales. Callitris columellaris F. digestive tract of cattle (Carter and Cowan the costs of increased difficulty in man- Muell. shows high seedling loss to desic- 1993). Quarantining livestock for a brief agement of stock and possible losses of cation (100% in 18 months) even during a period before moving between paddocks grass fodder by shading and competition. high rainfall season in South Australia should also be effective in preventing fur- The episodic La Niña generated mass (Read 1995), further indicating that pulses ther spread on infested properties. recruitment in prickly acacia and other of regeneration in many native shrubs rely Control techniques which are attuned to woody weeds may present particularly dif- on La Niña episodes of heavy prolonged the ecology of the pest species concerned,

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 387 and to the processes of the ecosystem tices have already been used with some Brown, J.R. and S. Archer 1987. Woody within which it occurs are more likely to success in other species, particularly for plant seed dispersal and gap formation in a be effective. Relatively minor changes in mesquite (Prosopis spp) in North America North American subtropical savanna wood- management such as the use of an alterna- (Jacoby 1985, 1986), and should be con- land: the role of domestic herbivores. Vegetatio 73:73Ð80. tive species of livestock which can browse sidered for the control of leguminous Brown, J.R. and S. Archer 1989. Woody the pest plant more effectively may be a shrubs in other tropical grasslands, such as plant invasion of grasslands: establishment of very economical means of achieving con- prickly acacia in Queensland. After wide- honey mesquite (Prosopis glandulosa var. trol. Sheep may be used in inland low- spread recruitment episodes, fire may be glandulosa) on sites differing in herbaceous rainfall areas, but do not thrive in very used to control shrubs, an alternative tech- biomass and grazing history. Oecologia 80: high rainfall areas. In the low-rainfall nique which has been found useful with 19Ð26. Mitchell Grasslands of central western other woody weed species in northern Brown, J.R. and J. Carter 1998. Spatial and Queensland, sheep grazing may be suffi- Queensland (Grice 1997) and the USA temporal patterns of exotic shrub invasion in cient to control the levels of prickly acacia (Ortmann et al. 1998). Fire is an attractive an Australian tropical grassland. Landscape Ecol. 13:93Ð102. recruitment experienced in most seasons. and cheap treatment considering that fod- Carter, J.L. 1994. The spatiotemporal pattern However, when mass recruitment occurs der availability far exceeds that required of an Acacia nilotica (prickly acacia) inva- associated with prolonged rainfall and for herd use during high rainfall years. sion into the Mitchell grasslands. Honours flooding it is highly unlikely that even The possibilities for cost-effective control Thesis, James Cook Univ. of North with sheep grazing at moderate to high of prickly acacia by controlled burning Queensland. levels, that there would be adequate graz- should be investigated. Some (presum- Carter, J.O. and D.C. Cowan 1993. ing pressure to defoliate all seedlings. ably) native insects were observed to Population dynamics of prickly acacia, Some plants would always establish dur- cause seedling mortality, although only at Acacia nilotica subsp. indica (Mimosaceae). p. 83Ð104 In: E.S. Delfosse (eds), Pests in ing the periodic La Niña phases which low percentages. There may be some pastures: weed, invertebrate and disease pests occur about every 20 years in eastern value in importing and testing insect of Australian sheep pastures. CSIRO Australia. In addition, the increased avail- species which consume either seeds or, Information Services, Melbourne. ability of palatable herbage in high rainfall more particularly, seedlings of prickly Carter, J.O., P. Jones, and D.C. Cowan years may reduce the relative acceptability acacia. A national program to cap free- 1991. Control of woody weeds in western of prickly acacia seedlings at precisely the flowing artesian bores should also reduce Queensland. Rep. to the Australian Wool time when suppression by hervivory the area of key habitat where Acacia nilot- Corp., Queensland Dept. of Primary would be required to control shrub num- ica can rapidly establish, thus providing a Industries. bers. This phenomenon has been observed regular source of seed for cattle to spread Cottam, G. and J.T. Curtis 1956. The use of distance measures in phytosociological sam- with rabbits grazing western myall to upland landscapes. pling. Ecol. 37: 451Ð460. (Acacia papyrocarpa) in enclosures with Crisp, M.D. 1978. Demography and survival and without available herbage (Lange and under grazing of three Australian semi-desert Graham 1983), and may help explain the Literature Cited shrubs. Oikos 30: 520Ð528. widespread establishment of prickly aca- Greig-Smith, P. 1983. Quantitative plant ecol- cia on both sheep and cattle properties ABM 1996. Climatic records. Australian Bur. ogy. Third edition. University of California during 1974/75. During such establish- of Meteorology Telephone Advis. Serv., Press, Berkeley and Los Angeles, Calif. ment periods, the stocking rates of sheep Brisbane. Grice, A.C. 1997. Post-fire regrowth and sur- required to achieve control would most Adamson, D.A. and M.D. Fox 1982. Change vival of the invasive tropical shrubs Cryptostegia grandiflora and Ziziphus mau- likely be deleterious to the survival of in Australasian vegetation since European settlement. p. 109Ð160 In: J.M.B. Smith ritiana. Aust. J. Ecol. 22: 49Ð55. desirable native shrub species, and also (eds), A history of Australasian vegetation. Harper, J.L. 1977. Population biology of cause soil erosion and compaction. So, McGraw-Hill, Sydney. plants. Academic Press, London. although grazing by sheep may prevent Archer, S. 1989. Have southern Texas savan- Harrington, G.N. 1979. The effects of feral increases in population density in most nas been converted to woodlands in recent goats and sheep on the shrub populations in a years, there may still be peaks of regenera- history? Amer. Nat. 134: 545Ð561. semi-arid woodland. Aust. Rangel. J. 1: tion during La Niña wet periods. Archer, S. 1994. Woody plant encroachment 334Ð345. The recovery of the Giru population to into Southwestern grasslands and savannas: Harrington, G.N. 1991. Effects of soil mois- rates, patterns and proximate causes. p. ture on shrub seedling survival in a semi-arid extremely high densities only 15 years 13Ð68 In: M. Lavra, W. Laycock and R. grassland. Ecology 72: 1138Ð1149. after chaining demonstrates the ability of Pieper (eds), Ecological implications of live- Harrington, G.N., M.H. Friedel, K.C. prickly acacia to regenerate following top stock herbivory in the West. Soc. for Range Hodgkinson, and J.C. Noble 1984. removal. These results suggest that chain- Manage., Denver, Colo. Vegetation ecology and management. p. 41Ð ing cannot be recommended as a control Auld, T.D. 1995. The impact of herbivores on 77 In: G.N. Harrington, A.D. Wilson and measure for prickly acacia in high rainfall regeneration in four trees from arid Australia. M.D. Young (eds), Management of areas, unless some form of follow-up Aust. Rangel. J. 17: 213Ð227. Australia’s rangelands. CSIRO, Melbourne. Barker, M. 1996. Literature review: The ecol- Harvey, G.J. 1981. Recovery and viability of treatment is applied. Chaining is very ogy and management of Acacia nilotica expensive and should only be used in situ- prickly acacia (Acacia nilotica ssp. indica ) subsp. indica (Benth) Brenan. p. 38Ð53 In: seed ingested by sheep and cattle. p. 34Ð45 ations and seasons where there is likely to F. Tiver, B. Wilson and W. Forno (eds) Proc. In: B.J. Wilson and J.T. Swarbrick (eds) be a successful outcome, such as at lower Woody Weeds Workshop, 16th and 17th Proc. 6th Australian Weeds Conf., Brisbane. rainfall sites, especially if carried out dur- March 1995, CSIRO Davies Laboratories, Queensland Weed Soc.. Townsville. CSIRO Division of Tropical ing droughts. Hennessy, J.T., R.P. Gibbens, J.M. Tromble, Crops & Pastures. Other combinations of ecologially Blake, S.T. 1938. The plant communities of and M. Cardenas 1983. Vegetation changes attuned control methods may be appropri- Western Queensland and their relationships from 1935 to 1980 in mesquite dunelands ate for prickly acacia. Such control prac- with special reference to the grazing indus- and former grasslands of southern New try. Proc. Roy. Soc. Qld XLIX: 156Ð204. Mexico. J. Range Manage. 36: 370Ð374.

388 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Holmes, P.M. and R.M. Cowling 1997. The Lange, R.T. and R. Purdie 1976. Western Pressland, A.J. 1975. Productivity and man- effects of invasion by Acacia saligna on the myall, (Acacia sowdenii ), its survival agementof mulga in south-western queens- guild structure and regeneration capabilities prospects and management needs. Aust. land in relation to tree structure and density. of South African fynbos shrublands. J. Appl. Rangel. J. 1: 64Ð69. Aust. J. Bot. 23:965Ð976 Ecol. 34: 317Ð332. Miller, E.A. and C.B. Halpern 1998. Effects Read, J. 1995. Recruitment characteristics of Humphries, S.E., R.H. Groves, and D.S. of environment and grazing disturbance on the white cypress pine (Callitris glaucophyl- Mitchell 1991. Plant invasions of Australian tree establishment in meadows of the central la) in arid South Australia. Rangel. J. 17: ecosystems. A status review and manage- Cascade Range, Oregon, USA. J. Appl. Ecol. 228Ð240. ment directions. Australian National Parks 9: 265Ð282. Silvertown, J. and J. Lovett-Doust 1993. and Wildl. Serv., Canberra. Miller, M.F. 1994. Large African herbivores, Introduction to plant population biology. Jacoby, P.W. 1985. Restoring mesquite savan- bruchid beetles and their interactions with Blackwell Scientific Publications, Oxford. na in western Texas, USA, through brush and Acacia seeds. Oecologia 97: 265Ð270. Skarpe, C. 1990. Shrub layer dynamics under cacti management. p. 223Ð228 In: J.C. Milton, S.J. 1994. Growth, flowering and different herbivore densities in an arid savan- Tothill and J.J. Mott (eds), Ecology and man- recruitment of shrubs in grazed and in pro- na, Botswana. J. Appl. Ecol. 27:873Ð885. agement of the world’s savannas. Australian tected rangeland in the arid Karoo, South Tiver, F. and M.H. Andrew 1997. Relative Africa. Vegetatio 111:17Ð27. Acad. of Sci., Canberra. effects of herbivory by sheep, rabbits, goats Moore, C.W.E. 1969. Application of ecology Jacoby, P.W. 1986. Control and management and kangaroos on recruitment and regenera- to the management of pastoral leases in of undesirable woody plants on semi-arid northwestern New South Wales. Proc. Ecol. tion of shrubs and trees in eastern South rangelands. p. 259Ð263 In: P.J. Joss, P.W. Soc. Aust. 4: 39Ð54. Australia. J. Appl. Ecol. 34:903Ð914. Lynch and O.B. Williams (eds) Proc. Second Myster, R.W. and B.C. McCarthy 1989. Weltzin, J.F., S. Archer, and R.K. International Rangeland Congress: Effects of herbivory and competition on sur- Heitschmidt 1997. Small-mammal regula- Rangelands: a resource under seige, vival of Carya tomentosa (Juglandaceae) tion of vegetation structure in a temperate Adelaide, S.A. Australian Acad. of Sci. seedlings. Oikos 56:145Ð148. savanna. Ecology 78:751Ð63. Kent, M. and P. Coker 1992. Vegetation Nicholls, N. 1991. The El Niño/Southern description and analysis: a practical Oscillation and Australian vegetation. approach. CRC Press & Belhaven Press, Vegetatio 91: 23Ð36. Boca Raton, Ann Arbor, Mich. and London, Ortmann, J., J. Stubbendieck, R.A. Masters, England G.H. Pfeiffer,and T.B. Bragg 1998. Kriticos, D.J. (1997). A climatic analysis of Efficacy and costs of controlling eastern red- the potential distribution of prickly acacia in cedar. J. Range Manage. 51:158-163. Australia. A report prepared for Land PNSW 1901. Royal commission to inquire into Protection, Queensland Department of the condition of the crown tenants of the Natural Resources, Brisbane, Queensland Western Division of New South Wales. Part and Cooperative Research Centre for 1. Report and summary of evidence. Votes Tropical Pest Management, Brisbane, and proceedings of the New South Wales Queensland. Legislative Assembly during the session of Lange, R.T. and C.R. Graham 1983. Rabbits 1901, with the various documents connected and the failure of regeneration in Australian therewith. 4:131Ð66. Parliament of New arid zone Acacia. Aust. J. Ecol. 8: 377Ð381. South Wales, Sydney.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 389 J. Range Manage. 54: 390Ð395 July 2001 Endophytic fungi in Canada wild rye in natural grasslands

MARY ANN VINTON, EMILY S. KATHOL, KENNETH P. VOGEL, AND ANDREW A. HOPKINS

Authors are associate professor, Department of Biology and Program for Environmental Science, Creighton University, Omaha, Nebr. 68178; graduate research assistant, Institute for Environmental Studies, University of Wisconsin, Madison, Wis. 53706; research leader, USDA-ARS and adjunct professor, Agronomy Department, University of Nebraska, Lincoln, Nebr. 68583; and research leader, Forage Biotechnology Group, Noble Foundation Inc., Ardmore, Okla. 73401.

Abstract Resumen

Some grasses harbor endophytic fungi living in intercellular Algunos zacates albergan hongos endofiticos que viven en los spaces in the leaves, stems and reproductive organs. The fungi espacios intracelulares de las hojas, tallos y órganos reproduc- can dramatically affect the physiology and ecology of plants. For tivos. Los hongos pueden afectar dramáticamente la fisiología y example, fungi may produce toxins that deter herbivores and ecología de las plantas. Por ejemplo, el hongo puede producir they may alter the water status of the plant to increase drought toxinas que desalientan a los herbívoros y ellos pueden alterar el tolerance. The distribution of fungal infection in natural plant estado hídrico de la planta para incrementar la tolerancia a populations is unknown for many host species. We investigated sequía. La distribución de la infección fungal en poblaciones de the occurrence of endophytic fungi in Elymus canadensis L. plantas naturales es desconocida para muchas de las especies (Canada wild rye) from 13 remnant prairie sites in the midwest hospederas. Investigamos la ocurrencia de hongos endofiticos en and 23 sites in the southern Great Plains. Collections of plant tis- Elymus canadensis L. (Canada wild rye) en 13 sitios de pradera sue came from Nebraska, Kansas, Minnesota, Iowa, Missouri, en el medio oeste y en 23 sitios en las Grandes Planicies del Sur. Illinois, Oklahoma, and Texas. All midwest plants were grown in Colecciones de tejidos de plantas arribaron de Nebraska, a common garden site in eastern Nebraska. Seeds collected from Kansas, Minnesota, Iowa, Missouri, Illinois, Oklahoma, and Oklahoma and Texas accessions were planted in the greenhouse. Texas. Todas las plantas provenientes del medio oeste se culti- At least 3 tillers from 2 plants of each accession were screened varon en un sitio de jardín común en el este de Nebraska. Las for endophytes, using light microscopy. The endophytic fungus semillas colectadas de las entradas de Oklahoma and Texas se was found in seed of all accessions and in plants from all but 4 plantaron en invernadero. Al menos 3 hijuelos de dos plantas de accessions. The functional significance of the fungus is unclear, cada entrada se inspeccionaron mediante luz microscópica para but it may affect plants by enhancing productivity or deterring determinar los endófitos. El hongo endófito se encontró en las herbivores. The widespread occurrence of endophytic fungi in semillas de todas las entradas y en plantas de todas menos 4 natural populations of E. canadensis suggests that the plant-fun- entradas. El significado funcional del hongo no es claro, pero gal association may be long-standing and important in the evolu- puede afectar las plantas aumentando su productividad o tion and success of this native prairie species. desalentando a los herbívoros. La ocurrencia tan amplia y dis- persa de los hongos endofiticos en las poblaciones naturales de E. Canadiensis sugiere que la asociación planta-hongo puede ser Key Words: Elymus canadensis, Epichlo typhina, Neotyphodium, importante en la evolución y éxito de esta especie nativa de las geographical pattern, mutualism, tallgrass prairie pradera

Many grasses are infected by clavicipitaceous fungal endophytes that grow in the intercellular portions of the stems, leaves enhance the growth and productivity of the plant (Belesky and and reproductive organs. The fungi are often asymptomatic and Fedders 1995), especially under drought conditions (Arachevaleta are known to occur in all grass subfamilies and in most of the et al. 1989). Bacon (1995) and Ball et al. (1993) reviewed the his- large grass genera (Clay 1990). Much of the research on fungal tory of the endophyte, Neotyphodium coenophialum, (formerly endophytes concerns the incidence and the effects of the infection known as Acremonium coenophialum) in tall fescue in which the in the important forage and turfgrass genera, Festuca (fescue) and particularly hardy, disease-resistant and (unknown at the time) Lolium (ryegrass). Endophytic fungi in agronomic Festuca and endophyte-infected cultivar, KY 31, was widely adopted through- Lolium decrease the palatability of the grass to insect and mam- out the United States from the 1940’s onward. The existence and malian herbivores and can cause toxicosis in livestock due to fun- role of the fungal endophyte in KY 31 was documented in the gal and possibly, plant, production of alkaloids (Bacon et al. late 1970’s, when reports of livestock disorders began to accumu- 1977, Funk et al. 1983 and Clay et al. 1985). The fungi can also late (Bacon et al. 1977, Hoveland et al. 1980). Recently, efforts to characterize the evolution and ecology of We are grateful to Kimberly Woods, Erin Goergen, Dan Deatsch, Jayme the fungal-plant relationship in natural grass endophytes have Horning and Renae Schmitt for field and lab assistance and to Dr. Nick Hill at the University of Georgia for performing the alkaloid analysis and immunoblot assay. been undertaken—for example, is the association mutualistic and This work was supported by the Clare Boothe Luce endowment at Creighton how might such an arrangement have arisen? White (1988) pre- University and by the NSF Long Term Ecological Research Program (DEB sented some hypotheses about the origin and evolution of some 96328510) at Konza Prairie Research Natural Area. of the known plant-fungal associations. In some grasses, the Manuscript accepted 2 Sept. 2000.

390 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 endophytic fungus forms external fruiting in about 60% of the E. canadensis individ- Materials and Methods structures (stromata) that prevent the grass uals in North America (White 1987). The from flowering—thus the fungus com- fungus is similar to Epichloë typhina pletes its sexual lifecycle at the expense of (Ascomycetes), but because the sexual Collections of E. canadensis germplasm the host plant. Since the host incurs some structures are seldom observed, it has been ranged from Minnesota to Texas, with 8 negative impacts, this type of association placed, along with other related grass states represented (Fig. 1). Sites consisted is pathogenic and White (1988) called this endophytes into the genus Neotyphodium of virgin tallgrass prairie from roadsides, a “Type 1” association. In “Type 3” asso- (Glenn et al. 1996). We screened fresh cemeteries, railroad right of ways or pre- ciations, stromata have never been plant tissue collected from 2 sites in serves, pastures, or farmland which had observed and the fungus appears to spread Nebraska and Kansas for the presence of reverted to rangeland (Table 1). Some of asexually, by growing into the embryo and Neotyphodium. We also screened tissue the tissue was collected from a common dispersing with the seed, and also spread- from a common garden that had been garden site, which harbored plant acces- ing with clonal growth of the grass. In this established from seed from 11 remnant sions from 11 different sites (Sites 1Ð11 in type of association, the fungus appears to tallgrass prairies in Nebraska, Iowa, Table 1) and some of the tissue was col- have positive effects on the plant, by pro- Minnesota, Missouri, and Illinois, and lected directly from the sites. tecting it from herbivores and enhancing from greenhouse grown plants derived The common garden site near Mead, growth. However it should be noted that from seed collected from Oklahoma and Nebr. (41.2¡N, 96.5¡W) was established in the classification of many endophyte infec- Texas. the following way. E. canadensis seed was tions as mutualisms has been heavily influenced by results from a few agronomic species. Recent results from native species have emphasized the variety of negative, neutral and positive plant consequences (other than release from herbivory) that can result from endophyte infection (Saikkonen et al. 1998, 1999). White (1988) further defines a Type 2 association, in which only 1Ð10% of the individual plants within an infected population produce stromata, even though 50Ð75% of the individuals may harbor the fungus. The fungal-plant association in Elymus canadensis is thought to be Type 2 (White 1988) but more field observations are necessary to quantify the frequency and type of fungal infection in this species. The frequency and type of infection of endophytic fungi throughout the range of a potential host are well-known for only a few host species. These species tend to be forage species tested because of the potential for causing livestock toxicity. The distribution of these species has been extensively influenced by human land management and planting. Studies on the extent of the fungal distribution within and between natural populations may shed light on the origin and evolution of the plant-fungus association. In one of the most complete studies to date on a natural grass population and its endophytes, Schulthess and Faeth (1998) found high seasonal and spatial variability in Neotyphodium starrii in the grass Festuca arizonica. Our goal was to describe the extent of endophytic fungal infection in Elymus canadensis in the central grassland region of the United States. E. canadensis is a native, cool-season bunchgrass, abundant in tall and mixed-grass prairies. This species is known to harbor endophytic fungi, and a previous study of herbarium specimens suggested that fungi are present Fig. 1. Location of Elymus canadensis collection sites.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 391 Table 1. Sites where germplasm of Elymus canadensis was collected and screened for the presence of a fungal endophyte. See Figure 1 for numbered site locations. Plant material from sites 1Ð11 and 14Ð35 was propagated in a greenhouse and transplanted into a common garden before endophyte screening took place. Tillers and seeds from sites 12Ð13 were collected directly from the site and screened for endophyte presence.

Site Number Location Nearest Town Longitude/Latitude Endophyte Endophyte In Seed In Plant 1 Loda Cemetery Loda, Ill 88.05W/40.32N + + 2 McLean Right of Way Danvers, Ill 89.10W/40.32N + + 3 Beach Cemetery Rockford, Ill 89.08W/42.08N + + 4 Holt County Mound City, Mo 95.12W/40.08N + + 5 Atchison County Roadside Rockport, Mo 95.29W/40.25N + + 6 Iron Horse Hayfield, Minn 92.50W/43.55N + + 7 Compass Worthington, Minn 95.40W/43.40N + + 8 Willow Township Cemetery Charter Oak, Ia 95.36W/42.04N + + 9 Sioux City Sioux City, Ia 96.20W/42.28N + + 10 Narodni Hrbitior Cemetery Touhy, Nebr 96.52W/41.08N + + 11 Nine Mile Prairie Lincoln, Nebr 96.50W/40.45N + + 12 Vinton Ranch Mullen, Nebr 101.20W/41.70N + + 13 Konza Prairie Manhattan, Kans 96.50W/39.20N + + 14 OKCS-38 Beaver, Okla 100.29W/36.36N + + 15 OKCS-30 Elk City, Okla 99.40W/35.15N + + 16 OKCS-26 Mangum, Okla 99.46W/35.03N + + 17 OKCS-29 Erick, Okla 99.54W/35.05N + + 18 OKCS-23 Snyder, Okla 98.55W/34.48N + + 19 OKCS-20 Snyder, Okla 98.55W/34.48N + + 20 OKCS-16 Waurika, Okla98.05W/34.09N + + 21 OKCS-7 Lone Grove, Okla 97.16W/34.10N + + 22 OKCS-19 Lawton, Okla 98.30W/34.27N + + 23 OKCS-9, OKCS-40 Frederick, Okla 98.52W/34.16N + + 24 TXCS-13 Graham, Tex 98.41W/33.11N + - 25 TXCS-28 Wellington, Tex 100.27W/34.50N + + 26 TXCS-27 Childress, Tex 100.17W/34.43N + + 27 TXCS-17 Paducah, Tex 100.17W/34.15N + + 28 TXCS-20 Guthrie, Tex 100.14W/33.34N + + 29 TXCS-22 Crowell, Tex 99.35W/33.48N + + 30 TXCS-23 Henrietta, Tex 98.01W/33.38N + + 31 TXCS-15 Electra, Tex 98.54W/33.58N + + 32 TXCS-11 Montague, Tex 97.39W/33.39N + + 33 TXCS-30 Montague, Tex 97.37W/33.45N + Ð 34 TXCS-12 Nocona, Tex 97.57W/33.31N + Ð 35 TXCS-24 Dallas, Tex 97.07W/32.56N + Ð collected in 1989 from remnant prairies in emergence, the seedlings were thinned to The plots were evaluated for yield and the central United States (Hopkins et al. 1 seedling per tube. Seedlings of the forage quality in 1991 and 1992. In 1993, 1995). At each site, spikes were collected accessions were transplanted into 3 field seed was harvested on a plot basis from in a haphazard manner from plants located evaluation nurseries in the spring of 1990. the plants at the 3 locations. The seed was throughout the remnant site. Seed from all The evaluation nurseries were located at threshed, cleaned and bulked by accession. the spikes collected at a site were threshed Mead, Nebr., Ames, Iowa (Lat. 42.0¡N, It was possible to maintain the genetic and the seed was bulked. The bulked seed Long. 93.6¡W), and West Lafayette, Ind purity of each accession using this process was given an accession number that iden- (Lat 40.4¡N, Long. 86.9¡W). At each loca- because E. canadensis is a self-pollinated tified both the accession and the collection tion, the seedlings of each accession were species (Jensen et al. 1990). Seed from 11 site. The accessions represent a sample of transplanted into single row evaluation remnant prairie accessions were used to the germplasm from each respective plots. Rows and plants within rows were plant larger nurseries (Table 1, Sites prairie. Seed from each accession was wet spaced 1.1 m apart. There were 10 plants 1Ð11). The accessions that were planted chilled for 3 weeks at 4.5¡C and planted in per plot at Mead and Ames and 7 plants were those that had the most potential for the greenhouse into plastic seedling tubes per plot at West Lafayette. There were 2 use in pasture and prairie renovation based or mini-pots in February 1990. After replications of each plot at the 3 locations. on the agronomic evaluations. Seedlings

392 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 were propagated in the greenhouse using for the presence of stromata, the sexual Results the procedures described above and transform of fungal reproduction. Stromata planted into field nurseries at Mead in the appear on E. canadensis as a white exter- The fungal endophyte appeared in leaf spring of 1993. Each nursery consisted of nal mat of hyphae, 3Ð10 cm long, and sheaths as straight and sometimes wavy 12 rows of 40 plants with rows and plants enveloping the flag leaf and culm (White strands of hyphae that were typically within rows spaced 1.1 m apart. The nurs- and Bultman 1987, White and Morgan- much longer than an individual cell and eries were managed for seed production. Jones 1987). All tillers from one-third of never appeared to invade the cell (Fig. 2). They were cultivated as needed for weed the plants from each accession were manu- In seeds, the hyphae appeared as dense control by roto-tilling between plants and ally checked in July-August 1998 for the mycelial mats. In 36 populations of rows. Herbicides were also applied as presence of stromata. Since E. canadensis Elymus canadensis from 8 states, the needed for weed control. The nurseries in this region typically forms seed heads in endophyte was found in every seed exam- were fertilized with 112 kg/ha N as July and August, the presence of stromata ined, and in at least 1 plant from all but 4 NH4NO3 each spring. Seed of accessions on mature tillers should be most evident accessions (TXCS-12, TXCS-13, TXCS- from Oklahoma and Texas were collected during this time period. 24, TXCS-30). Two accessions (OKCS- in 1997 in the same manner as seed from The identity of the fungus in E. 26, OKCS-40) contained endophyte in the midwestern sites. canadensis was assumed to be similar to only 1 of the 2 plants examined. In tall Three fresh tillers from at least 3 differ- the Neotyphodium endophytes in other C3 fescue, factors such as temperature, mois- ent plants were collected from each of the grasses, such as Festuca, and the same fungi ture, and time influence endophyte viabili- 11 established Elymus canadensis acces- as that previously described in Elymus ty in seed (Williams et al. 1984). It is pos- sions at Mead and from the 2 prairie sites species by White and Morgan-Jones (1987) sible that viability of the endophyte, but (Konza Prairie and Vinton Ranch) in and White and Bultman (1987). To provide not of the seed, was lost during seed stor- Kansas and Nebraska in 1997. Late in the some corroboration of fungal identity, we age in these accessions, resulting in pres- growing season, 3 additional flowering used a commercially available immunoblot ence of endophyte free plants. Despite tillers were collected from each of the 2 assay to Neotyphodium (Agrinostics Ltd. thorough field observations, no evidence prairie sites. Two plants and 3 seeds were Co.; 1501 Hickory Hill Drive; Watkinsville, of stromata were found on the 11 acces- examined for each Oklahoma and Texas Ga. 30677). The immunoblot produced a sions at Mead. accession. The midwestern plants and positive reaction to the E. canadensis seeds were examined in a laboratory at endophyte in a random sample of tillers. Creighton University and the Oklahoma In addition, we plated out the fungi in a Discussion and Texas material was examined at the random sample of seeds and greenhouse- Noble Foundation, using similar proce- grown plants. Seeds and 5 mm sections of Two other studies on the extent of endo- dures. The fresh tillers were taken to the tillers were surface sterilized with 1.25% phyte infections in natural populations of laboratory and kept refrigerated in plastic Clorox (NaOCl) for 15 min. and rinsed Elymus (canadensis and virginicus) have bags until they could be screened for twice in sterile water, as described in been done. White (1987) examined endophyte infection. We followed proce- Bacon and White (1994). Seed and tillers herbarium specimens at the University of dures outlined in Bacon and White (1994) were placed in potato dextrose agar for 5 Texas, Texas A&M, and Sul Ross State to prepare and stain the tissue. Sectioned weeks and observed every 2Ð3 days. Seeds University. He found that 38 of 62 indi- leaf sheath tissue from mature plants was tended to be more contaminated with bac- viduals (61%) of E. canadensis and 21 out placed within a 10% potassium hydroxide teria and other fungi than tillers; a more of 45 individuals (47%) of E. virginicus (KOH) solution overnight to soften and thorough decontamination protocol (e.g. were infected. He suggested that 1Ð10% of clear the tissue. Leaf sheath tissue from Marshall et al. 1999) may be necessary for these individuals bears the stromata stage younger plants was not treated with KOH. seeds. Two weeks after the initial plating, for potential sexual reproduction, while in An epidermal peel of the tissue was made endophytic fungal hyphae grew out the the remaining infected individuals, the and aniline blue stain was placed onto the ends of the tiller sections so that the entire fungus reproduces asexually by growing tissue. The tissue was warmed for 1 mass was dumbbell-shaped. A swab of the into the seed (White and Bultman, 1987). minute and a light microscope was used to endophytic fungus was placed on a fresh Clay and Leuchtmann (1989) performed detect fungal hyphae, visible at 100x plate and in 2Ð3 weeks the fungal mass the second study on the extent of endo- power and confirmed at 400x. To screen was 2Ð3 cm in diameter, white and cot- phyte infection in Elymus. They examined seeds for the presence of the fungi, we tony on the top and brown when viewed over 150 seed collections from E. virgini- placed seeds within a 1N sodium hydrox- from the bottom of the plate. Samples of cus and found that 72% of the seeds were ide (NaOH) solution to soften overnight. the fungi were examined via light endophyte infected. The seed was collect- Then seeds were deglumed and placed microscopy and we noted the appearance ed from the vicinity of Indiana University within a warm aniline blue stain for one of solitary phialides which appeared to in south central Indiana. In these samples, and a half minutes. The individual seed have basal septa. Conidia were produced both the Epichloë (stromata present on was then squashed for microscopic exami- after 2Ð3 weeks of growth. These plating culm) and Neotyphodium (no stromata nation. Infection was detected through observations match those of White and development) types of fungal endophyte endophytic hyphae found within the aleu- Morgan-Jones (1987), and provide evi- were detected. rone layer of the seed. Seeds and tillers of dence that the E. candensis fungal endo- No evidence of stromata was present in Oklahoma and Texas accessions were phyte should be placed in the our field populations (Mead only). examined at the Noble Foundation in 1998 Neotyphodium group described by Glenn Stromata are most obvious when plants using the same procedures given above. et al. (1996). are fairly mature and the flowering culms We also checked each accession at Mead are elongating to produce seed heads, a

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 393 We found higher incidence of infection than did either White (1987) or Clay and Leuchtmann (1989), as our infection rate approached 100%. Leuchtmann (1992) documented endophyte infection rates of 58 to 80% in native populations of Lolium perenne, L. multiflorum, Festuca arundinacea and F. pratensis in natural habitats in Europe. A number of studies have shown increases in the frequency of fungal endophytes in plant populations through time (e.g. Thompson et al. 1989, Shelby and Dalrymple, 1993). These increases are likely due to either 1) contagious spread of the fungus or 2) increased growth and fitness of the endophyte-infected plants due to greater herbivore resistance and competitive ability. Our results suggest that contagious spread is unlikely, since we observed no external, spore-producing stromata. Furthermore, our collections came primarily from relatively old habitats (e.g. virgin tallgrass prairie). The Oklahoma and Texas collections came from more disturbed sites than the midwestern accessions, but essentially no commercial varieties of E. canadensis are available in this region, so even the tissue from disturbed areas probably represents indigenous plants. Therefore, it seems possible that the fungal endophyte in Elymus canadensis increases plant fitness, through enhanced growth or herbivore resistance. Preliminary tests of a few E. canadensis tillers suggest that ergot alkaloid levels are substantially less than the levels in endophyte-infected tall fescue (N. S. Hill, personal communication). The ergot alkaloids are one of the means by which mammalian herbivores are deterred in tall fescue, but at least 3 other alkaloidal compounds may be involved in herbivore deterrence in Neotyphodium-infected tissue (Siegel and Bush 1994, 1997) . Other means by which the endophytic fungus could have positive effects on the plant are through increasing the growth and ability of the plant to cope with drought stress, as has been found in tall fescue (Arachevaleta et al. 1989). Fig. 2. Slides of endophytic fungal hyphae (arrows) in seed (A) and sheath tissue (B) from However, the possibility exists that Elymus canadensis. Slides were cleared and stained with aniline blue solution. Neotyphodium infection in E. canadensis, despite its widespread occurrence, does not confer drought tolerance or herbivore stage that occurred in JulyÐAugust at the ta development remain unclear. However, resistance on plants. Saikkonen et al. Mead common garden site. In other studies these results do clearly demonstrate that (1999) found no evidence that endophytes of stromata occurrence, plants growing in fungal transmission in E. canadensis, as in confer grazing resistance in native Arizona wet areas were more likely to have stroma- tall fescue and ryegrasses, occurs primarily fescue populations and suggest endo- ta than plants in dry uplands (White, per- via seed. Since the plant materials evaluat- phytes in natural populations may be sonal communication). Our common gar- ed at Mead were 2 seed generations important in increasing pathogen resis- den plants were generally large and vigor- removed from the original plants in the tance and competitive ability of adult ous, as they were maintained in cultivated remnant prairies, the presence of the endo- plants rather than in mediating interactions plots with minimal competition. Thus, it is phyte in the plants demonstrates that in E. with herbivores (Saikkonen et al. 1998). unlikely that these plants were lacking in canadensis the endophyte is transmitted More experiments on the alkaloid levels, resources, so the factors promoting stroma- across generations via seed.

394 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 herbivore preference, pathogen resistance Funk, C.R., P.M. Halisky, M.C. Johnson, Schulthess, F.M. and S.H. Faeth. 1998. and drought response of endophyte-infect- M.R. Siegel, A.V. Steward, S. Ahmad, Distribution, abundances, and associations of ed and uninfected plants of E. canadensis R.H. Hurley, and I.C. Harvey. 1983. An the endophytic fungal community of Arizona are necessary to elucidate the ecological endophytic fungus and resistance to sod web- fescue (Festuca arizonica). Mycologia significance of this widespread plant-fun- worms: association in Lolium perenne L. 90:569Ð578. Biotechnology 1:189Ð191. Shelby, R.A. and L.W. Dalrymple. 1993. gal association. Glenn, A.E., C.W. Bacon, R. Price, R.T. Long-term changes of endophyte infection in Hanlin. 1996. Molecular phylogeny of tall fescue stands. Grass and Forage Sci. 48: Acremonium and its taxonomic implications. 356Ð361. Literature Cited Mycologia 88:369Ð383. Siegel, M.R. and L.P. Bush. 1994. Importance Hopkins, A.A., K.P. Vogel, K.J. Moore, K.D. of endophytes in forage grasses, a statement Johnson, and I.T. Carlson. 1995. of problems and selection of endophytes. p. Arachevaleta, M., C.W. Bacon, C.S. Genotypic variability and genotype x envi- 135Ð150. In: C.W. Bacon and J.F. White Hoveland, and D. E. Radcliffe. 1989. Effect ronment interactions among switchgrass (eds.), Biotechnology of endophytic fungi of of tall fescue endophyte on plant response to accessions from the midwestern USA. Crop grasses. CRC Press, Boca Raton, Fla., USA. environmental stress. Agron. J. 81: 83Ð90. Sci. 35:565Ð571. Siegel, M.R. and L.P. Bush. 1997. Toxin pro- Bacon, C.W. 1995. Toxic endophyte-infected Hoveland, C.S., S.P. Schmidt, C.C. King Jr., duction in grass/endophyte associations. p. tall fescue and range grasses: historic per- J.W. Odom, E.M. Clark, J.A. McGuire, 185Ð208. In: G.C. Carroll and P. Tudzynski spectives. J. Anim. Sci. 73:861Ð870. L.A. Smith, H.W. Grimes, and J.L. (eds.), The Mycota. V. Plant Relationships, Bacon, C.W. and J.F. White. 1994. Stains, Holliman. 1980. Association of Epichloë Part B. Springer-Verlag, Berlin. media and procedures for analyzing endo- typhina fungus and steer performance on tall Thompson, R.W., H.A. Freiborg, and B.B. phytes, p. 47Ð56. In C.W. Bacon and J.F. fescue pasture. Agron. J. 72:1064Ð1065 Redick. 1989. Sampling intensity and timing White (eds.), Biotechnology of endophytic Jensen, K.B., Y.F. Zhang, and D.R. Dewey. for detecting Acremonium coenophialum fungi of grasses. CRC Press, Boca Raton, 1990. Mode of pollination of perennial incidence in tall fescue pastures. Agron. J. Fla., USA. species of the tribe Triticeae in relation to 81:966Ð971. Bacon, C.W., J.K. Porter, J.D. Robbins, and genomically defined genera. Can. J. Plant White, J.F., Jr. 1987. Widespread distribution E.S. Luttrell. 1977. Epichloë typhina from Sci. 70:215Ð225. of endophytes in the Poaceae. Plant Disease toxic tall fescue grasses. Appl. and Environ. Leuchtmann, A. 1992. Systematics, distribu- 71:340Ð342. Microbiol. 34:576Ð581. tion, and host specificity of grass endophytes. White, J.F., Jr. 1988. Endophyte-Host associa- Ball, D.M., J.F. Pedersen, and G.D. Natur. Toxins 1:150Ð162. tions in forage grasses. XI. A proposal con- Lacefield. 1993. The tall-fescue endophyte. Marshall, D., B. Tunali, and L.R. Nelson. cerning origin and evolution. Mycologia 80: Amer. Sci. 81:370Ð380. 1999. Occurrence of fungal endophytes in 442Ð446. Belesky, D.P. and J.M. Fedders. 1995. Tall species of wild Triticum. Crop Sci. White, J.F., Jr. and T.L. Bultman. 1987. fescue development in response to 39:1507Ð1512. Endophyte-host associations in forage grass- Acremonium coenophialum and soil acidity. Saikkonen, K., S.H. Faeth, M. Helander, and es. VIII. Heterothallism in Epichloë typhina. Crop Sci. 35: 529Ð533. T.J. Sullivan. 1998. Fungal endophytes: A Amer. J. of Bot. 74:1716Ð1721. Clay, K. 1990. Fungal endophytes of grasses. continuum of interactions with host plants. White, J.F., Jr. and G. Morgan-Jones. 1987. Annu. Rev. of Ecol. and Systematics 21: Annu. Rev. Ecol. Syst. 29:319Ð343. Endophyte-host associations in forage grass- 275Ð297 Saikkonen, K., M. Helander, S.H. Faeth, F. es. IX. Concerning Acremonium typhinum, Clay, K. and A. Leuchtmann. 1989. Infection Schulthess, and D. Wilson. 1999. the anamorph of Epichloë typhina. of woodland grasses by fungal endophytes. Endophyte-grass-herbivore interactions: the Mycotaxon. 29:489Ð500. Mycologia 81:805Ð811. case of Neotyphodium endophytes in Williams, M.J., P.A. Backman, E.M. Clark, Clay, K., T.N. Hardy, and A.M. Hammond Arizona fescue populations. Oecologia 121: and J.F.White, Jr. 1984. Seed treatments Jr. 1985. Fungal endophytes of grasses and 411Ð420. for control of the tall fescue endophyte their effects on an insect herbivore. Acremonium coenophialum. Plant Disease Oecologia 66:1Ð6. 68:49Ð52.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 395 J. Range Manage. 54: 396Ð399 July 2001 ‘Immigrant’ forage kochia seed viability as impacted by storage methods

ALISON STEWART, VAL JO ANDERSON, AND STANLEY G. KITCHEN

Authors are adjunct faculty, Life Science Department, Palomar College, San Marcos, Calif. 92069; professor, Botany and Range Science Department, Brigham Young University, Provo, Ut. 84602; and botanist, Shrub Sciences Laboratory, Rocky Mountain Research Station, USDA Forest Service, Provo, Ut. 84606.

Abstract Resumen

‘Immigrant’ forage kochia (Kochia prostrata (L.) Schrad.) is a La Kochia forrajera (Kochia postrata (L) Schrad) ‘Inmigrant’ valuable introduced subshrub, often used in reclamation plant- es un valioso subarbusto introducido que a menudo es utilizado ings and seedings on western rangelands. Seedling establishment en plantaciones y siembras para restaurar los pastizales del is best from fresh seed; however, many users plant stored seed oeste. El establecimiento de plántulas es mejor a partir de semil- and experience poor seeding success. One cause for failure is loss la nueva, sin embargo, muchos usuarios plantan semilla almace- of seed viability in storage. Forage kochia seed was harvested on nada y obtienen un pobre establecimiento de plántulas. Una de 4 dates in fall 1996 from 2 sites (wildland and irrigated) and test- las causas del fracaso es la perdida de viabilidad de la semilla ed for viability when fresh and after storage treatments. Storage durante el almacenaje. Se cosecho semilla de Kochia forrajera en treatments included low and high seed water contents (2Ð6% and 4 fechas de otoño de 1996 y en 2 sitios (con riego y natural) y se 12-16%), cold and warm storage temperatures (2¡ and 25¡ C), probaron para determinar su viabilidad cuando estaban recién and duration of storage (4, 8, and 12 months). Mature, highly cosechadas y después de tratamientos de almacenamiento. Los viable forage kochia seed remains viable in storage longer than tratamientos de almacenamiento incluyeron bajos y altos con- seed harvested prematurely. Low seed water content (2Ð6%) is tenidos de agua de la semilla (2Ð6% y 12Ð16%), temperaturas de essential to preserving maximum seed viability. Storing seed at a almacenamiento frías y calientes (2° y 25°C) y duración de alma- cold temperature (2¡ C) is also helpful in maintaining viability. cenamiento (4, 8 y 12 meses). La semilla madura de alta viabilidad permanece viable mas tiempo bajo almacenamiento que la semilla cosechada prematuramente. Un bajo contenido de agua Key Words: Kochia prostrata, revegetation, seed care, greenstripping (2-6%) en la semilla es esencial para conservar la máxima viabilidad de la semilla. Almacenado la semilla a temperaturas frías Forage kochia (Kochia prostrata (l.) Schrad.) was first intro- (2°C) también es útil para mantener la viabilidad. duced to the United States from the Soviet Union during the early 1960’s (Keller and Bleak 1974). It is a semi-evergreen subshrub native to arid and semiarid regions of central Eurasia where it is planted year-old seed and experienced low seeding success. A valuable forage (Balyan 1972). Many assessions of forage kochia probable cause of this problem is low seed viability due to short have been tested as possible forage and reclamation plants for shelf-life of the seed between the time of viability testing and the semi-arid locations since its introduction (Keller and Bleak 1974, time of purchase, which creates the potential for undetected loss- Stevens et al. 1985, McArthur et al. 1996). The variety es in viability (Moghaddam 1978, Stevens and Jorgensen 1994). ‘Immigrant’ was released in 1985 for forage and erosion control To maximize seeding success and financial return, it is beneficial on greasewood-shadscale (Sarcobatus vermiculatus (Hook.) Torr. to understand how viability changes over time in response to stor- -Atriplex confertifolia ( Torr. & Frem.) Wats.), sagebrush-grass age conditions (Stevens and Jorgensen 1994). (Artemisia spp.-grass), and pinyon-juniper (Pinus spp.-Juniperus This research examined the effects of storage conditions, har- spp.) rangelands of the Intermountain West (Stevens et al. 1985). vest date (an index of seed maturity), and maternal growth envi- Immigrant forage kochia has been used successfully as a revege- ronment on viability of Immigrant forage kochia seed. These fac- tation species on harsh sites (Blauer et al. 1993, Frischknecht and tors undoubtedly influence seeding success on western rangelands. Ferguson 1984, McArthur et al. 1974, Monsen and Turnipseed 1990) and is used extensively for seeding after fires on cheatgrass (Bromus tectorum (L.) dominated rangelands (Horton et al. 1994, Methods McArthur et al. 1990). It has the valuable characteristic of sprout- ing after fires on these sites (McArthur et al. 1990). Fruits (hereafter referred to as seed) were collected from 2 Seed demand for Immigrant is generally high because of its sites. The first was a USDI Bureau of Land Management seeded range of uses and adaptability. For best establishment, fresh seed (Immigrant) site, located 11 km north of Dugway, Tooele should be planted in late fall or early winter (Haferkamp et al. County, Ut. (40¡ 20' N., 112¡ 44' 36" W.) where several hundred 1990, Monsen and Kitchen 1994). Many users, however, have mature forage kochia plants were present. The Natural Resources Conservation Service has classified the soil as a very deep, well- drained Tooele fine, sandy loam (Coarse-loamy, mixed, superac- Manuscript accepted 10 Oct. 00.

396 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 tive, calcareous, mesic Typic Torriorthent) 25¡ C) x 3 levels of seed water contents Germinated seed plus dormant seed which receives an average of 17 cm of during storage (fresh seed with no storage, equaled total viable seed for each dish. annual precipitation (Trickler, et al. 2000). low seed water content at 2-6%, and high Percent viability was calculated for each The second site was an irrigated field oper- seed water content at 12-16%) x 4 storage replication and was arcsin transformed ated by Stevenson Intermountain Seed near lengths (0, 4, 8, and 12 months)]. Seed before analysis to normalize the data. A Manti, Sanpete County, Ut. (39¡ 16' 30"N., was then further air-dried or rehydrated factorial analysis of variance appropriate to 111¡ 38' 8" W.) where certified Immigrant until the desired seed water content levels the completely randomized experimental forage kochia seed is grown for commer- were achieved. Each of the sublots was design was used to determine significance cial use. The crop is irrigated as needed to weighed and stored in a plastic vial, with of treatments and interactions (SAS 1998). maximize production, and the soil is a each group of vials sealed in a plastic bag Sigurd gravely loam (Loamy-skeletal, car- and placed in a cardboard box. bonatic, mesic Xeric Torrifluvent) (Soil Percent seed viability was assessed for Results and Discussion Conservation Service 1981). each seed lot, when fresh and after each Seed was harvested from both sites in storage period. Each test included 4 repli- Maternal Growth Environment 1996 on 4 October, 18 October, 1 cations of 25 seeds from each seedlot. Maternal growth environment of the November, and 15 November. Twenty Seed was placed in 100 mm X 15 mm seed may affect ripening rate or other fac- plants were selected at each site to repre- plastic petri dishes on two 1-mm thick tors of importance to seed quality (Balyan sent the population’s variability. Seed was blotters (Anchor Paper, St. Paul, Minn.) 1972). Effects of seed maturity, growth handstripped from each of these plants on saturated with tap water. Dishes were ran- environment, and storage conditions on each collection date and the phenological domized, stacked, and placed in plastic seed viability of Immigrant forage kochia stage of seed maturity was recorded to bags in order to retain moisture. To ensure seed were highly significant (p < 0.01). allow application of this data to subse- even light treatment for all dishes, a blank Seed from the wildland site was more quent years and multiple sites. The seeds dish with 2 dampened blotters was placed viable (75%) when fresh compared to seed were then air-dried for 3 to 10 days. on the top of each stack. Blotters were from the irrigated site (65%). Viability Empty and immature fruits, fruit frag- resaturated as needed throughout the ger- after storage was lower for seed from both ments, leaves, and small stems were mination test. Stacks were randomly sites, with the relative difference being removed using 1.0mm, 1.8 mm, and arranged in a germination chamber and similar to that of their original viability, as 4.8mm rounds (Seedburo Equipment rearranged after weekly counts. wildland seed was 45% and irrigated seed Company, Chicago, Ill.) Seed was incubated in a controlled envi- was 38% viable overall, after 12-months A subsample (3 to 20 g) of each seed lot ronment chamber with a 12-hour diurnal storage. Causes of these differences would was dried to 0% moisture in a drying oven photoperiod at 10/20¡ C. Every 7 days, the be highly speculative at this point, as fur- at 125¡ C. This sublot was used as a refer- germinated seed in each dish were counted ther studies over time or involving more ence in calculating seed water content for and removed. Germination was defined as sites would be warranted. Thus, in all fol- the levels desired in storage. The remain- 5+ mm radicle emergence (Young et al. lowing discussion, tables, and figures, data ing fresh seed was then divided evenly 1981). After 28 days, firmness of unger- shown are means from both sites. into 32 sublots for a complete factorial minated seed in each dish was determined arrangement of the storage treatments [4 using a cut test to examine embryonic tis- harvest dates x 2 growth environments sue (Association of Official Seed Analysts Harvest Date (wildland and irrigated sites) x 3 storage 1988). Dormant seed was defined as firm An important consideration concerning temperatures (fresh seed with no storage, but ungerminated after 28 days. low seed viability of forage kochia is early cold storage at 2¡ C, and warm storage at harvest. Seed growers may feel compelled

Table 1. Means (standard errors) of percent viability for ‘Immigrant’ forage kochia seed incubated for 28 days in a 12-hour diurnal photoperiod at 10/20¡ C. Seed was harvested from an irrigated site and a wildland site in central Utah in fall 1996 and tested for viability when fresh and after storage treatments. High seed water content was 12-16% and low was 2Ð6%. Storage at a cold temperature was 2¡ C, and the warm temperature was 25¡ C. For all means, N = 8.

STORAGE LENGTH 4 months 8 months 12 months Harvest Water Fresh STORAGE TEMPERATURE Date Content Seed Cold Warm Cold Warm Cold Warm ------(%) ------4 Oct. High 43 (4) 0 (0) 23 (4) 1 (0) 17 (5) 0 (0) Low 11 (3) 15 (4) 9 (2) 13 (4) 15 (3) 11 (3) 17 (5) 18 Oct. High 75 (3) 14 (4) 54 (5) 16 (5) 43 (6) 4 (1) Low 77 (5) 78 (4) 66 (4) 75 (3) 72 (4) 64 (4) 85 (2) 1 Nov. High 81 (2) 0 (0) 65 (3) 1 (0) 41 (4) 0 (0) Low 89 (2) 87 (2) 87 (3) 88 (4) 83 (4) 82 (4) 92 (2) 15 Nov. High 86 (4) 1 (0) 82 (5) 4 (3) 69 (7) 0 (0) Low 82 (4) 92 (1) 85 (4) 81 (6) 85 (4) 84 (4) 87 (3)

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 397 Fig. 1. Percent viability of ‘Immigrant’ forage kochia seed Fig. 2. Percent viability of ‘Immigrant’ forage kochia seed from both growth from all collection dates and both growth environments environments, meaned across all storage lengths, stored with 2 seed water stored with 2 seed water content levels (low at 2Ð6% and content levels (low at 2Ð6% and high at 12Ð16%) and at 2 temperatures (cold high at 12Ð16%) and at 2 temperatures (cold at 2¡ C and at 2¡ C and warm at 25¡ C) shown over successive harvest dates (4 October, warm at 25¡ C) shown over increasing length of storage 18 October, 1 November, and 15 November). This 3-way interaction was sig- (0, 4, 8, and 12 months). This 3-way interaction was significant at p < 0.01. For means of fresh seed N = 8, and for all other means N nificant at p < 0.01. For all means N = 32. = 24. to harvest before the seed ripens fully in easily hand-stripped. By the fourth har- trolled warehouse storage conditions October or November to prevent losses vest, seed at the wildland site was still (Balyan 1972, Jorgensen and Davis 1984, associated with fall storms (Moghaddam very ripe and mostly still on the stalk. At Keller and Bleak 1974). Not stored prop- 1978). However, immature seed may not be the commercial site, large amounts of seed erly, seed can lose 80 to 90% viability in capable of surviving storage and/or produc- had already shattered and dropped, signi- less than a year (Moghaddam 1978, ing viable seedlings (Waller et al. 1983). fying it had reached full maturity. Stevens et al. 1985). Seed collected from both sites on the When fresh seed was tested, viability was The interaction among seed water con- first harvest date (4 October) were imma- low (17%) for seed from the first harvest, as tent, storage temperature, and length of ture. The seed and stems were still very expected from its appearance. Viability was storage was highly significant (p < 0.01). green, moist, and not easily stripped from high for fresh seed from the second, third, Figure 1 illustrates the effects of seed the inflorescence. Seed maturity, or the and fourth harvests (88% collectively) water content and storage temperature developmental stage for optimum germi- because all or most of the seed was mature over time on seed viability. Seed stored nation, is judged in the field stage when by then. Seed from the last 3 harvests also with a high seed water content at a warm seed can be easily stripped by hand from retained viability over time (Table 1). Seed temperature lost 94% viability, while seed the inflorescences, after the stems have viability from the first harvest varied but stored at a cold temperature with a high changed to a reddish color and dry up was typically lower with storage. seed water content lost only 20% viability. (Balyan 1972, Waller et al. 1983). By 18 Storing seed with low water content, October, approximately half of the seed at Storage Conditions whether in a cold or warm storage temper- the collection sites had started to mature ature, preserved seed viability for the and turn red. By 1 November, the seed Forage kochia seed is known to have a short shelf-life, especially under uncon- majority of seed, with only 9% viability was fully ripe, as it was very red, dry, and lost overall. It is imperative to store forage

398 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 kochia seed with a low water content to Literature Cited to Interagency Agreement No. ID910 between ensure preservation of viability. USDI, Idaho Bureau of Land Management Differences among the effects of seed and USDA, Forest Service, Intermoun. Res. Association of Official Seed Analysts. 1988. Sta. USDA, Forest Serv., Intermoun. Res. water content, storage temperature, and Rules for testing seeds. Stone Printing Sta., Shrub Sci. Lab., Provo, Ut. seed maturity level also led to a highly Company, Lansing, Mich. Vol. 6, No. 2. Monsen, S. B. and D. Turnipseed. 1990. significant interaction (p < 0.01). Seed Balyan, G. A. 1972. Prostrate summer cypress Seeding forage kochia into cheatgrass infest- stored with low water content at a cold or and its culture in Kirghizia. (Translated from ed areas. p. 66Ð71. In: E. D. McArthur, E. M. warm temperature was able to retain most Russian) Al Ahram Cen. Science. Transl., Romney, S. D. Smith, and P. T. Tueller Nat. Tech. Information Ser. TT77-59026. of the seed viability after storage (Fig. 2). (compilers). Proc. symposium on cheatgrass Blauer, A. C., E. D. McArthur, R. Stevens, invasion, shrub dieoff, and other aspects of This was especially true for the most and S. D. Nelson. 1993. Evaluation of road- shrub biology and management. USDA mature seed from the latest harvest. They side stabilization and beautification plantings Forest Serv. Gen. Tech. Rep. INT-276. remained 85% viable after 12 months in in south-central Utah. USDA Forest Serv. Odgen, Ut. storage, compared to 87% viable when Res. Paper INT-462. Ogden, Ut. SAS. 1998. SAS user’s guide. SAS Institute, fresh. Mature seed appeared to be most Frischknecht, N. C. and R. B. Ferguson. Cary, N. C. 1984. Performance of Chenopodiaceae resilient to adverse storage conditions. Soil Conservation Service. 1981. Soil survey species on processed oil shale, p. 293Ð297. of Sanpete Valley Area, Utah. USDA, Soil Figure 2 also depicts the dramatic loss of In: A. R. Tiedemann, E. D. McArthur, H. C. Cons. Serv., Washington, D. C. viability in seed from all harvest dates Stutz, R. Stevens, and K. L. Johnson (com- Stevens, R. and K. R. Jorgensen. 1994. which were stored with a high seed water pilers). Proc. symposium on the biology of Rangeland species germination through 25 content at a warm temperature. Seed Atriplex and related chenopods. USDA and up to 40 years of warehouse storage. p. Forest Serv. Gen. Tech. Report INT-172. stored with a high seed water content in a 257Ð265. In: S. B. Monsen and S. G. Kitchen Odgen, Ut. (compilers). Proc. ecology and management cold temperature retained much more via- Haferkamp, M. R., D. C. Ganskopp, K. L. of annual rangelands. USDA Forest Serv. bility than those stored with the same seed Marietta, and B. W. Knapp. 1990. Gen. Tech. Report INT-GTR-313. Ogden, water content at a warm temperature. Environmental influences on germination of Ut. Storing forage kochia seed at a cold tem- utricles and seedling establishment of Stevens R., K. R. Jorgensen, E. D. perature aids in retaining seed viability; ‘Immigrant’ forage kochia. J. Range Manage. McArthur, and J. N. Davis. 1985. 23:518Ð522. however, storage with a low seed water ‘Immigrant’ forage kochia. Rangelands Horton, H. H., S. B. Monsen, R. L. Newhall, 7:22Ð23. content is most effective. Stewart et al. and R. Stevens. 1994. Forage kochia holds Stewart, A., V. J. Anderson, and S. G. (1999) found that these storage conditions ground against cheatgrass, erosion. Utah Sci. Kitchen. 1999. ‘Immigrant’ forage kochia also preserved maximum dormancy and 55:10Ð11. (Kochia prostrata) seed germination as maintained the most delayed and desyn- Jorgensen, K. R. and J. N. Davis. 1984. A affected by storage conditions. p. 274Ð279. technique for retaining seed viability in chronized germination rate for forage In: E. D. McArthur, W. K. Ostler, C. L. Kochia prostrata (L.) Schrad. p. 166Ð167. Wambolt (compilers). Proc. shrubland eco- kochia seed. In: A. R. Tiedemann, E. D. McArthur, H. C. tones. USDA Forest Serv., Rocky Mountain Stutz, R. Stevens, and K. L. Johnson (com- Res. Station Proc. RMRS-P-11. Ogden, Ut. pilers). Proc. symposium on the biology of Trickler, D., C. D. Franks, and D. Hall. 2000. Conclusions Atriplex and related chenopods. USDA Soil survey of Tooele County, Utah, Parts of Forest Serv. Gen. Tech. Report INT-172. Box Elder County, Utah, Davis County, Odgen, Ut. Recommendations to obtain higher seed Utah, Millard County, Utah, Salt Lake Keller, W. and A. T. Bleak. 1974. Kochia County, Utah, White Pine County, Nevada. viability from stored Immigrant forage prostrata: a shrub for western ranges?. Utah USDA Nat. Resources Conserv. Serv. kochia seed include delaying harvest until Sci. 35:24-25. Washington, D. C. seed is mature, when seed is red and easily McArthur, E. D., B. C. Guinta, and A. P. Waller, S. S., C. M. Britton, D. K. Schmidt, hand-stripped from the inflorescence. This Plummer. 1974. Shrubs for restoration of J. Stubbendieck, and F. A. Sneva. 1983. is typically sometime from October to depleted ranges and disturbed areas. Utah Germination characteristics of two varieties November (Balyan 1972). Early collection Sci. 34:28Ð33. of Kochia prostrata (L.) Schrad. J. Range yields mostly nonviable seed, while later McArthur, E. D., A. C. Blauer, and R. Manage. 36:242-245. collection yields highly viable seed which Stevens. 1990. Forage kochia competition Young, J. A., R. A. Evans, R. Stevens, and R. with cheatgrass in central Utah. p. 56Ð65. In: are also longer-lived in storage. L. Everett. 1981. Germination of Kochia E. D. McArthur, E. M. Romney, S. D. Smith, prostrata seed. Agron. J. 73:957Ð961. To maintain high seed viability in stor- and P. T. Tueller (compilers). Proc. sympo- age, first priority should be given to dry- sium on cheatgrass invasion, shrub dieoff, ing fresh seed to a low seed water content and other aspects of shrub biology and man- (2Ð6%) and maintaining that level through agement. USDA Forest Serv. Gen. Tech. the term of storage. A second priority Report INT-276. Odgen, Ut. should be to store the low-water content McArthur, E. D., S. C. Sanderson, and J. N. seed at a cold temperature (2¡ C). As the Davis. 1996. Adaptation of forage kochia use of forage kochia increases on western accessions across an environmental gradient rangelands, these recommendations will in Rush Valley, Utah. Arid Soil Research and Rehabilitation 10:125Ð138. aid in obtaining and maintaining the high- Moghaddam, M. R. 1978. Kochia prostrata— est possible viability when Immigrant for- a plant material for range improvement in age kochia seed is stored and planted. arid and semiarid regions. Rangeman’s J. 5:153Ð154. Monsen, S. B. and S. G. Kitchen. 1994. Annual Report—summary report of progress related

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 399 J. Range Manage. 54: 400Ð408 July 2001 Carbon and nitrogen dynamics in elk winter ranges

ROMULO S.C. MENEZES, EDWARD T. ELLIOTT, DAVID W. VALENTINE, AND STEPHEN A. WILLIAMS

Author Menezes was a research fellow of the Brazilian CNPq at the time of this study, Elliott is an associate professor, and Williams is a research associate at the Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, Colo., 80523; Valentine is a professor at the Department of Forest Sciences, University of Alaska, Fairbanks, Alaska, 99775-7200.

Abstract Resumen

Recent increases in elk (Cervus elaphus L.) herbivory and El reciente incremento en la herbivoría del alce (Cervus ela- changes in hydrology towards drier conditions have contributed phus L.) y los cambios en la hidrología hacia condiciones mas to declines in willow (Salix spp. L.) communities in the winter secas han contribuido a la disminución de las comunidades de ranges for elk in Rocky Mountain National Park. In 1994, we “Willow” (Salix spp. L) en los pastizales de invierno para alces constructed 12 large elk exclosures in 2 watersheds of the winter del Parque Nacional de las Montañas Rocallosas. En 1994 con- range for elk in the park, and conducted field experiments from struimos 12 grandes exclusiones contra alce en 2 cuencas 1995 to 1999 to investigate the effects of herbivory and proximity hidrológicas de pastizales de invierno para alce del parque y de to surface water on the dynamics of C and N. Litterfall biomass 1995 a 1999 condujimos experimentos de campo para investigar averaged 65.6 and 33.0 g m-2 inside and outside the exclosures, los efectos de la herbivoría y proximidad de la superficie de agua respectively. Elk herbivory increased (P < 0.05) N concentration en las dinámicas de C y N. La biomasa de mantillo promedió of willow litter from 1.25 to 1.49%, but there were no differences 65.6 y 33.0 g m-2 dentro y fuera de las exclusiones respectiva- in losses of C and N from litterbags placed in grazed and mente. La herbivoría del alce aumentó (P < 0.05) la concen- ungrazed plots in any of the growing seasons. Carbon losses from tración de N del mantillo de “Willow” de 1.25 a 1.49%, pero no litterbags were higher in lower landscape positions (P = 0.001), in hubo diferencias en las pérdidas de C y N de bolsas con mantillo comparison to upper landscape positions. Shoot biomass of wil- colocadas en parcelas con y sin pastoreo en ninguna de las esta- low plants fertilized with N averaged 27.3 g and was higher (P < ciones de crecimiento. Las pérdidas de carbón de las bolsas con 0.05) than that of unfertilized plants, which averaged 20.2 g, indi- mantillo fueron mayores en las posiciones de terrenos bajos (P = cating that N availability limits plant growth in our study sites. 0.001), en comparación con las posiciones de terrenos altos. La Elk herbivory had no effect on soil inorganic N availability, even biomasa de tallos de plantas de “Willow” fertilizadas con N though we estimated that the return of N to the soil in grazed promedió 27.3 g y fue mayor (P < 0.05) que la de las plantas sin plots could be as much as 265% of the N return in exclosed plots. fertilizar, la cual promedió 20.2 g, indicando que la disponibili- In the long-term, greater return of N to the soil combined with dad de N limita el crecimiento de las plantas en nuestros sitios de increased litter quality in the grazed plots could contribute to estudio. La herbivoría del alce no tuvo efecto en la disponibilidad increases in N cycling rates and availability, and these changes del N inorgánico del suelo, a pesar de que estimamos que el could affect ecosystem structure and function in the winter range retorno de N al suelo en las parcelas con pastoreo pudiera ser for elk in Rocky Mountain National Park. tanto como el 265% del N retornado en las parcelas excluídas. A largo plazo, el mayor retorno de N al suelo, combinado con un aumento en la calidad del mantillo de las parcelas con pastoreo contribuir a incrementar las tasas de reciclaje de N y su disponi- Key Words: Willow, Salix, Carex, litterfall, litter decomposition, bilidad, y estos cambios podrían afectar la estructura y función nitrogen availability. del ecosistema en los pastizales de invierno para alce del parque Nacional de la Montañas Rocallosas. Since 1968, elk (Cervus elaphus L.) numbers in Rocky Mountain National Park, Color. have been managed under a policy of natural regulation, which rests on the assumption that density-dependent mechanisms would result in an equilibrium between 3,300 animals, and park managers are concerned about the effects large ungulate herbivores and plant resources. During this period, of these increases on the soils and vegetation of the elk winter elk numbers have increased from approximately 1,000 to about range within the park (Singer et al. 1998b). Willow (Salix spp. L.) communities have reportedly been declining in elk winter ranges of the park during the last few The authors wish to thank J. Gensen, L. Hoogenstein, M. Kaye, R. Rochelle, M. decades (Hess 1993, Singer et al. 1998b), and several studies are Schrijvers, L. Schroeder, L. Zeigenfuss, J. Williams, and T. Wotan for assistance currently being conducted to investigate the extent of these with field and laboratory work. We also thank F. Singer and D. Binkley for help- changes (R. Peinetti, pers. comm., 1999). Similarly, declines in ing with the design and data analysis of some of the experiments. Helpful comments to the manuscript were provided by Therese Johnson, Ryan Monello, Gary willow populations have also been reported for Yellowstone Frasier and two anonymous reviewers. This study was primarily funded by the National Park (Chadde and Kay 1991, Kay and Wagner 1994, Biological Resources Division of the U.S. Geological Survey and also by the Singer et al. 1998a). In addition to increased elk herbivory, 2 National Park Service. other factors have been proposed to explain these apparent Manuscript accepted 10 Oct. 00.

400 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 declines in willow communities of Rocky surface water on the dynamics of C and N plots were chosen and marked off as Mountain National Park: (1) climates are in the winter ranges of elk in Rocky paired plots open to grazing (grazed plots). warmer and drier this century, possibly Mountain National Park. This information The area within each exclosure was sub- resulting in lowered stream flows and less is necessary for helping park managers for- divided into 15 m x 23 m sub-plots and 2 water availability to plants (Singer et al. mulate policies that will maintain herbi- treatments were imposed throughout the 1998b); and (2) beaver populations have vore populations at levels that are adequate period of the study: (1) 75% current annu- declined on the eastern slope of the park for preserving the natural functioning of al growth removal (clipped plots), and (2) (Stevens and Christianson 1980), which these ecosystems. Therefore, the objective no clipping at all (ungrazed plots). The may further contribute towards the drying of this study was to perform experimental 75% current annual growth removal treat- of these ecosystems. field manipulations to investigate the ment was applied between January and Large herbivores can significantly influ- effects of elk herbivory and proximity to April of 1995, 1996, 1997, and 1998, and ence plant community structure and bio- surface water on the C and N cycles in the consisted of clipping all forage shrubs and geochemical cycles within the soil-plant winter ranges of elk in the park. herbaceous plants in each sub-plot. All system (Frank et al. 1994, Frank and clipped plant biomass was removed from Groffman 1998, Hamilton et al. 1998, the exclosures. Therefore, each site con- Schuman et al. 1999, Wijnen et al. 1999). Methods sisted of: (1) grazed plot (outside the Herbivores can influence nutrient cycling exclosure); (2) ungrazed plot; and (3) by removing plant biomass and returning Study Sites clipped plot (both inside the exclosure). more readily available nutrients to the soil The winter range for elk in Rocky Eight sites (4 in Moraine Park and 4 in (McNaughton et al. 1988, Frank et al. Mountain National Park encompasses Horseshoe Park) were placed in areas with 1994, Hamilton et al. 1998), increasing about 10,000 ha, which includes land with- little or no beaver activity, and contained soil N mineralization rates and plant N in the eastern side of the park and private heavily browsed willow plants, which had uptake (Frank and Groffman 1998, Wijnen and national forest lands outside the park their height suppressed by elk browsing et al. 1999), spatially redistributing nutri- in the town of Estes Park and Estes Valley, (short willow). The other 4 sites (2 in each ents within the landscape (McNaughton Colo. (Singer et al. 1998b). Our study sites park) were located in nearby (about 1 to 2 1985, Afzal and Adams 1992, Russelle were located in 2 riparian ecosystems on km) wetter areas, generally containing 1992), or decreasing the amount of litter- the northeastern side of Rocky Mountain taller willow plants subjected to less fall and nutrient return to the soil in litter National Park: 1) Moraine Park, along the browsing by elk (tall willow). The differ- (Pastor et al. 1993). Big Thompson River watershed, at an ence between the willow plants in the 2 Beaver (Castor canadensis Kuhl) can elevation of 2,481 m and 2) Horseshoe areas (tall willow and short willow) was also influence plant communities and bio- Park, along the Fall River watershed, at an strictly morphological since the willow geochemical cycles of ecosystems. By elevation of 2,598 m. The latitude and lon- species composition of the communities in building dams, beavers contribute to the gitude of the area of the watersheds are the 2 areas was the same. In half of the entrapment of sediment and organic matter 105¡ 36' N and 40¡ 22' W. The 2 water- short willow sites (2 in each park), hydro- and modify water availability, nutrient sheds are within 5 km of each other and manipulation treatments were imposed by cycling, and the dynamics of organic mat- have perennial alpine snowfields at their placing sheet metal check dams on ter decomposition (Naiman et al. 1986, headwaters. Mean annual precipitation for ephemeral stream channels both inside the Naiman and Melillo 1984). It has been the sites is 41 cm (Singer et al. 1998b) and exclosures and in the grazed plots. We suggested that the observed declines in peak stream flow usually occurs in early to expected these check dams to catch beaver populations in the eastern slope of mid-June (USDA 1995, 1996, 1997). The snowmelt and rain runoff through the Rocky Mountain National Park have con- 30-year average temperature for the adja- spring and raise the water table at the sites. tributed to a decrease in the surface area of cent Estes Valley ranges from 9 to 17¡C Twenty-five dams were installed in April water (ponds and streams) within the win- during the 5-month growing season of May and May 1995 and were relatively suc- ter range of elk since the beginning of this through September (Alstad et al. 1999). cessful in holding additional water at these century, therefore decreasing water avail- The study area consists of wet meadows sites. The dams were intended to add ability for willows. These reductions in dominated by willow (mainly Salix monti- water, but in no way was the treatment water availability could further reduce the cola L., S. geyeriana Anderss., and S. plan- able to simulate water additions in the ability of willow to respond to elk her- ifolia Pursh), other shrubs such as birch amounts accomplished by beaver dams on bivory (Singer et al. 1998b) and could also (Betula spp. L.), sedges (Carex spp. L.), larger, permanent streams (Singer et al. alter the biogeochemical cycles of those rushes (Juncus balticus Willd.), and grasses 1997). In each exclosure and associated ecosystems. However, the extent of the (Phleum spp. L., Calamagrostis spp. grazed plot, an average of 5 shallow (0.5 influences of these changes over the elk Adans., Bromus spp. L., Poa spp. L.). The to 2 m) wells were installed in the spring winter ranges of the park is unknown. elk population of Estes Valley numbers of 1995 for the purpose of monitoring Plant-available N is usually a limiting about 3,300 animals, of which about one groundwater levels. During early 1996 and element for plant growth in terrestrial third generally spends the winter within the 1997, 3 beaver dams were constructed ecosystems (Power 1977, Kiehl et al. park (Larkins 1997, Singer et al. 1998b). near 2 sites within the wetter area of 1997, Wijnen et al. 1999) and the cycling Moraine Park, but these dams were of N in these systems is linked to the C Experimental Treatments washed out during the spring flood of cycle by interactions between decom- In the wet meadows of both parks, 12 1996 and 1997. posers, plants, and herbivores (Aber and exclosures (30 m x 46 m each) were erect- Melillo 1991, Pastor and Naiman 1992). ed within willow communities along the There is no available information about the rivers between August and November of Litterfall Litter was collected in each experimen- effects of elk herbivory or the reduction in 1994. Next to each exclosure, 30 m x 46 m tal plot during the fall of 1995, 1996, and

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 401 1997, through the use of 15 greenhouse least 10 m away from a stream or a pond diameter and combined in a paper bag. trays (totaling ~ 2.3 m2) arranged in a 5 x and 0.5 m higher in the landscape than After collection, the samples were taken to 3 regularly spaced grid (9.1 m x 15.9 m). lower landscape positions. Bags of both the laboratory, air-dried, and passed through The grids were established randomly with- willow and Carex litter were placed under a 2 mm sieve. Soil particle distribution was in each sub-plot before willow senescence the canopies of the selected shrubs (‘wil- measured in each sample using the hydrom- began, and each tray was anchored to the low canopies’) and in open grass areas eter method (Gee and Bauder 1986). Sub- ground using 2 or more large spikes. Litter (‘Carex plots’) located within 2 m of the samples (10 g) of each sample were ground was collected weekly from early shrubs. Two bags of each litter type were to a fine powder with a ball mill. The sand September to late October until litterfall placed within each treatment replicate and fraction (> 53 µm) of each sample was was complete. The litter was then compos- their results pooled in order to reduce ground to a fine powder with a ball mill, for ited within each experimental replication, microsite variability. determination of particulate organic matter sorted by genus and litter type, air dried, In all experiments, the litterbags were (POM) C and N (Cambardella and Elliott and weighed. Oven-dry corrections were placed on the soil surface and left in the 1992). Total C and N in the total soil and applied within each category by drying a field during the entire length of the grow- sand fraction were determined with a LECO subsample at 60¡C. Litterfall biomass was ing season (from late May until mid- CHN-1000 analyzer. calculated as oven dry mass per unit area. September). At the end of the season, they In addition, during the summer of 1996 Total N and C content of litter was deter- were collected, air-dried, weighed, ground we collected soil samples (0 to 20 cm) mined using a LECO CHN-1000 analyzer. to a fine powder to pass a 40 mesh sieve, under willow trees and in associated open and stored until analysis. Carbon and N in grass areas next (within 2 m) to the trees. Litter Decomposition the decomposed litter were analyzed using A total of 33 pairs of samples (shrub During September and October of 1994, a LECO CHN-1000 analyzer, and C and N canopy plus open grass) were taken from before the establishment of the exclosures, losses were calculated in an ash-free dry the 12 ungrazed plots within the exclo- we collected litter material throughout the weight basis by subtracting the amounts in sures of Moraine Park and Horseshoe study area to generate a standard litter that the post-decomposition from the pre- Park. The samples were air-dried and was used in the decomposition experi- decomposition litter. sieved through a 2 mm screen. Sub-sam- ments. Willow leaf litter was obtained by ples (10 g) of each sample were ground to locating greenhouse trays directly under Elk Dung Quantification a fine powder with a ball mill, and total willow canopies throughout the study area We estimated the amount of C and N soil C and N were determined using a (dominated by S. monticola, S. geyeriana, returned to the soil in elk dung by count- LECO CHN-1000 analyzer. and S. planifolia) and collecting the leaves ing the number of scat piles along 30 m Soil moisture (0 to 14 cm) measure- periodically. Carex litter was collected by transects within our experimental grazed ments were performed weekly in 8 sites in clipping and collecting standing dead bio- plots, and measuring the concentrations of Moraine Park and Horseshoe Park (4 in mass. We dried all litter in a 35¡C forced C and N in the dung. The survey was con- each watershed) by Time Domain air oven, and subsamples (2 g) from the 2 ducted after the elk herds left the winter Reflectometry (TDR) (Ledieu et al. 1986) standard litter types (willow leaves and range for the summer range during late with a Trase System model 6050x1 during Carex tissue) were enclosed in 1 mm spring 1997. We selected 8 grazed plots (4 the growing season of 1997. The TDR nylon mesh bags. These bags containing in each park) and established 4 randomly rods were vertically placed in each mea- the standard litter were used in litter placed transects per plot. In each transect, surement position and left there for the decomposition experiments to investigate we measured the distance from the scat whole season. Within each site and graz- the effects of herbivory, landscape posi- piles to the transect, and calculated the ing treatment, soil moisture was measured tion, and plant cover on the decomposition density of piles per area. Only scat piles under willow canopies and in associated rates of willow and Carex litter during the that were visually identified as from the Carex plots next to the willow shrubs in growing seasons of 1995, 1996, and 1997. previous fall and winter were counted. To both upper and lower landscape positions. During the growing season of 1995, we estimate dry matter and C and N content Within 3 ungrazed plots in each park, soil investigated the effect of herbivory on lit- in each dung pile we obtained 51 samples temperature was measured using HOBO¨ ter decomposition by randomly placing 4 (26 from Horseshoe Park and 25 from temperature data loggers during the grow- bags of each litter type (willow leaves and Moraine Park) by collecting all dung from ing season of 1997. The loggers were Carex tissue) in the ungrazed plots within fresh piles during late Fall of 1997. After wrapped with a thin plastic film to avoid the exclosures and in the grazed plots out- collection, the samples were oven-dried at damage by soil moisture, and were buried side the exclosures (no bags were placed 50¡C, weighed, ground to a fine powder, in a vertical position from 1 to 6 cm of in the clipped plots) for all of the 12 sites. and sub-sampled for determination of depth. In each of the sites, we performed The results from the 4 bags of each litter moisture (oven-dried at 105¡C) and ash comparisons of soil temperature between type within each treatment replicate were content (500 ¡C). The concentrations of C (1) willow canopies and Carex plots and combined to reduce microsite variability and N in the dung were determined using (2) streamside and upper landscape posi- within each of the 12 treatment replicates. a LECO CHN-1000 analyzer and tions. The temperature measurements were In 1996 and 1997, we investigated the expressed on an ash-free dry weight basis. performed every 15 minutes for periods of effect of herbivory, landscape position, 7 to 14 days. and plant cover on litter decomposition. Soil Characteristics and N Availability In 1995, 1996, and 1998 in situ soil N For this, we selected, in each of the Soil samples (0Ð15 cm) were collected in availability in the experimental plots was ungrazed and grazed plots within the 12 July 1997 from the grazed, ungrazed, and assessed using ion-exchange resin bags. sites, 2 willow shrubs located at 2 differ- clipped plots. Within each treatment replica- Paired cation and anion resin bags made ent landscape positions: (1) lower land- tion, a total of 25 to 30 cores were randomly from nylon stockings and containing about scape positions, next to a stream or a 3 collected with a soil core sampler 2 cm in 15 cm of exchange resins were placed 5 pond, and (2) upper landscape positions, at

402 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 cm beneath the soil surface (Binkley 1984). Table 1. Litterfall biomass in ungrazed, clipped, and grazed plots of Moraine Park and Horseshoe In 1995 and 1996, fifteen pairs of resin Park during 1995, 1996, and 1997. Values represent means (n = 12) with standard errors in bags were placed in a regularly spaced grid parentheses. Means within the same group followed by different letters are significantly different at P < 0.05. (9.1 x 15.9 m) within each treatment (grazed, ungrazed, clipped) in the 12 sites. Willow (Salix Other shrub Herbs2 Wood Unidentified All To analyze the temporal variability of N Treatment spp.) leaves leaves1 material litter availability, 2 sets of bags were placed in ------(g m-2) ------each of the 3 treatments during each of the 1995 growing seasons of 1995 and 1996. The Ungrazed 32.9 (9.8) a 5.9 (2.7) ab 10.1 (2.4) 3.0 (1.0) 0.6 (0.2) 52.5 (10.2) a first set was left in place from mid-June to Clipped 34.1 (8.5) a 13.2 (6.3) a 8.0 (1.0) 4.4 (1.4) 0.3 (0.1) 60.0 (8.9) a mid-July, and the second set from mid-July Grazed 19.1 (7.1) b 1.7 (0.6) b 6.4 (0.9) 3.1 (1.4) 0.5 (0.2) 30.9 (8.5) b to mid-August. A different experimental 1996 procedure was utilized in 1998, in which 6 Ungrazed 55.0 (13.6) a 9.1 (3.9) ab 3.1 (0.6) 3.1 (1.1) 1.4 (0.4) 71.6 (12.6) a pairs of resin bags were randomly placed Clipped 47.1 (10.6) ab 18.3 (8.6) a 2.6 90.5) 1.6 (0.4) 0.8 (0.2) 70.2 (9.7) a within each of the 12 ungrazed and grazed Grazed 26.6 (8.1) b 3.7 (0.8) b 3.4 (0.5) 5.1 (2.2) 0.7 (0.3) 39.4 (9.1) b plots (no bags were placed in the clipped 1997 plots), and left in the field from May to Ungrazed 45.3 (12.3) a 8.7 (4.0) ab 14.3 (3.3) 3.1 (1.0) - 71.5 (11.1) a October. For all 3 years, after removal of Clipped 41.6 (10.4) a 15.5 (6.3) a 7.2 (0.7) 2.2 (0.7) - 66.4 (10.1) a the bags, the N adsorbed in the resins was Grazed 15.9 (6.0) b 3.0 (0.9) b 7.5 (1.0) 2.4 (1.1) - 28.8 (7.1) b extracted with 50 ml of 2 M KCl, and the 1 Mostly birch (Betula spp.) leaves. extracts were frozen until analysis for 2Litter material from forbs and Carex spp. combined. Ð + NO3 -N and NH4 -N on an Alpkem automated spectrometer. higher elevations, willow shoots (current -2 In 1997 and 1998, in situ measurements m inside and outside the exclosures, year growth) were collected from the of net N mineralization were performed by respectively. On average, willow leaves plants inside the subplots, dried at 60¡C, conducting field soil incubations as accounted for 58% of the litterfall biomass weighed, and ground to a fine powder to followed by herbs (20%), other shrub described in Kolberg et al. (1997) using pass a 40 mesh sieve. Concentrations of C leaves (16%), wood (5%), and unidenti- aluminum cores 15 cm long and 5 cm in and N in shoots were determined using a fied material (1%). However, the use of diameter. During the 1997 growing season, LECO CHN-1000 analyzer. trays for collecting litterfall may underes- cores were placed in upper and lower land- timate the amount of grass litterfall, since scape positions within the 12 ungrazed and a significant portion of the senescent grazed plots of the 2 watersheds. Within Statistical Analyses tillers still remain attached to the plant and each landscape position and grazing treat- Statistical analyses were performed were not collected and counted as litter. ment, cores were placed under willow using the SAS Statistical Package (SAS, Willow leaf litterfall in the ungrazed and shrubs and in associated Carex patches Version 6.12, SAS Institute Inc., Cary, clipped plots was greater than in the within 2 m of the willow plants. Four cores N.C., 1995). The data on litterfall, litter nutrient content, litter decomposition, soil grazed plots during the 1995 and 1997 were placed inside each treatment replicate seasons, but in 1996 there were no signifi- to reduce micro-site variability. Cation and characteristics, N availability, and N fertilization were analyzed using a split-plot cant differences between clipped and anion resin bags were placed in the bottom grazed plots (Table 1). Leaf litter from of each core to capture the inorganic N factorial design where watershed was considered a random effect. Watersheds and other shrubs, mostly birch (Betula spp.), leached from the core. During the 1998 was significantly lower in the grazed plots growing season, 6 open-top field soil incu- height of willow plants were not significantly different (P < 0.05) for any of the when compared to the clipping treatment bation cores were placed within the inside the exclosures, but there were no ungrazed and grazed plots in 3 different 6- variables analyzed, therefore the data values from tall and short willow sites in both differences between grazed and ungrazed week incubation periods (June to July, July plots. No treatment differences were to August, and August to October). Net Moraine Park and Horseshoe Park were pooled (12 replications) in the analyses to observed for the amounts of herb or wood soil N mineralized during the incubation litter during the three growing seasons. periods was calculated by subtracting the determine the effect of browsing on litterfall and N availability, and the effects of Inside the exclosures, even the removal initial amount of inorganic N in the soil of 75% of current annual growth in the from the final amount of inorganic N after browsing, proximity to surface water, and canopy position on litter decomposition. clipped plots did not result in significant the incubations, and the results were differences between the ungrazed and expressed in g N m-2. The data on soil nutrient content between willow canopies and open grass areas was clipped plots during the growing seasons. analyzed using paired t-tests. We suggest this lack of difference Nitrogen Fertilization between clipped and ungrazed plots In each ungrazed and grazed plot in the occurred in part because the artificial clip- 12 sites, we placed 2 paired circular sub- Results and Discussion ping of willow did not satisfactorily simu- plots (each with 2 m radius) around willow late elk browsing. Other studies have plants at the end of the growing season of demonstrated the limitations of clipping 1998. Within each pair of circular subplots, Litterfall experiments to reflect accurately the natur- we applied 2 fertilization treatments: (1) no Litterfall biomass in the ungrazed and al patterns of herbivory (Paige 1999). fertilization, and (2) 10 g N m-2 as ammo- clipped plots was greater than in the Visual observations in our field plots sug- nium nitrate. During late July 1999, before grazed plots for the 3 growing seasons gested that clipped plants inside the exclo- the elk returned from the summer range at (Table 1). Across all growing seasons, lit- sures were morphologically similar to the terfall biomass averaged 65.6 and 33.0 g

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 403 Table 2. Nitrogen content and carbon to nitrogen ratio of different litter types in ungrazed, important factor contributing to decompo- clipped, and grazed plots of Moraine Park and Horseshoe Park in 1997. Values represent means sition and, in general, litter decomposition (n = 12) with standard errors in parentheses. Means within the same group followed by different increases with increasing soil moisture in letters are significantly different at P < 0.05. semi-arid ecosystems (Schlesinger 1997). Higher C losses observed in streamside Willow (Salix Other shrub positions in our study are likely due to high- Treatment spp.) leaves leaves1 Carex Forbs Nitrogen (%) Ungrazed 1.25 (0.10) b 1.23 (0.15) 1.40 (0.11) 1.79 (0.13) Table 4. Carbon and nitrogen losses from litter Clipped 1.27 (0.09) b 1.11 (0.13) 1.22 (0.08) 1.71 (0.15) bags placed in upper and lower landscape Grazed 1.49 (0.08) a 1.09 (0.11) 1.23 (0.09) 1.82 (0.12) positions of Moraine Park and Horseshoe Park during the growing seasons of 1996 and Carbon to nitrogen ratio 1997. Values represent means (n = 12) with Ungrazed 45.8 (3.2) a 48.5 (12.0) 37.2 (2.9) 31.0 (3.0) standard errors in parentheses. Clipped 43.0 (4.2) a 53.4 (11.6) 42.1 (2.8) 32.6 (2.9) Grazed 37.7 (3.1) b 49.9 (14.3) 43.5 (3.1) 31.4 (2.6) Landscape position C loss N loss (%) (%) plants in the ungrazed treatment, regarding to N ratios in litter may lead to faster litter 1996 height and canopy structure, while the decomposition and greater nutrient avail- Streamside 31.7 (2.3) 5.7 (6.1) grazed plants were apparently more sup- ability (Ritchie et al. 1998, Irons et al. Upper landscape 20.3 (1.9) 12.8 (6.0) P-value 0.001 N.S.1 pressed and shorter than the plants in the 2 1991). In our study site, the effects of elk treatments inside the exclosures. These herbivory on willow litter N concentration 1997 patterns probably result from the addition- could lead to increases in the rate of litter Streamside 18.1 (1.9) 6.5 (4.2) al damage to willow leaders caused by elk decomposition and nutrient cycling, which Upper landscape 20.4 (1.3) 12.9 (2.7) could lead to changes in species composi- P-value N.S N.S. when striping off leaves from the plants, 1 as compared to artificial clipping. On tion and ecosystem functioning (Aber and Not significantly different at P < 0.05. average, elk may browse on more than Melillo 1991, Holland et al. 1992, Ritchie et al. 1998, Stohlgren et al. 1999). 70% of the leaders in each plant in our study sites, and may remove nearly 40% er soil water availability (Fig. 1), suggesting of the length of each leader (Singer et al. Litter Decomposition that eventual reductions in surface water 1998b). Additional field observations from Losses of C and N from willow and may lead to reductions in litter decomposi- our experiments demonstrate that an aver- Carex litter bags was not affected by graz- tion rates in our sites. However, no signifi- age of 20% of the length of browsed wil- ing treatments in any of our experiments. cant differences in willow or Carex litter low leaders may die after elk browsing However, in the 3 growing seasons, C decomposition were observed between due to bark damage, while only 2% of the losses from willow litter bags were higher streamside and upper landscape positions length of the leader may die in the case of than from Carex litter bags and, interest- around the 2 beaver ponds in 1996. Average C and N losses from litter bags of the 2 litter artificially clipped plants (R. Peinetti, ingly, N losses from willow litter were lower than from Carex litter (Table 3). types placed in streamside and upper land- pers. comm., 1999). We suggest that the In 1996, C losses from litter bags were scape positions around the ponds were 36.4 differences in litterfall observed between higher in streamside positions than in and 2.9%, respectively. grazed and clipped treatments in our study upper landscape positions, but no signifi- Litter bags placed under willow may result from: (1) greater leader damage cant differences were observed for N loss- canopies lost significantly more C and N during elk browsing, in comparison to arti- es during 1996 or C and N losses during than bags placed in Carex plots (Table 5), ficial clipping, and/or (2) greater increases 1997 (Table 4). Soil moisture is usually an even though soil moisture levels were in plant height in clipped plants, in com- slightly lower under willow canopies, parison to grazed plants, due to differences Table 3. Carbon and nitrogen losses from wil- compared to Carex plots, especially in in the patterns of tissue removal during elk low (Salix spp.) and Carex leaf litter bags in Horseshoe park (Fig. 1). Average maxi- browsing or artificial clipping, which may Moraine Park and Horseshoe Park during influence canopy architecture. the growing seasons of 1995, 1996, and 1997. Table 5. Carbon and nitrogen losses from litter Willow leaf litter in the ungrazed and Values represent means (n = 12) with stan- bags placed under willow (Salix spp.) clipped plots had lower N content and dard errors in parentheses. canopies and in Carex spp. plots in Moraine higher C to N ratio than willow leaf litter Park and Horseshoe Park during the grow- in the grazed plots, but no significant Litter type C loss N loss ing seasons of 1996 and 1997. Values repre- treatment differences were found in litter sent means (n = 8) with standard errors in (%) (%) parentheses. from other shrubs, Carex, or forbs (Table 1995 2). Similar to our findings, Alstad et al. Willow 30.2 (2.7) 6.3 (2.0) (1999) reported that early season willow Carex 22.9 (2.6) 10.3 (2.1) Position C loss N loss tissue N concentration in plants under elk P-value N.S. 1 0.026 (%) (%) herbivory in our sites was significantly 1996 1996 higher than in plants protected from her- Willow 29.0 (1.9) 3.4 (5.1) Willow canopies 35.7 (1.7) 24.2 (1.8) bivory. Often, grazing leads to increases in Carex 22.9 (2.4) 15.2 (4.7) Carex plots 7.7 (2.9) -1.6 (2.4) plant tissue N (McNaughton 1985, P-value 0.046 0.005 P-value 0.001 0.022 Holland and Dettling 1990, Coughenour 1997 1997 1991, Hamilton et al. 1998) due to faster Willow 22.1 (1.4) 2.7 (2.4) Willow canopies 23.1 (1.5) 15.5 (1.7) nutrient cycling and uptake by plants or a Carex 16.4 (1.8) 16.7 (4.3) Carex plots 16.0 (3.5) 3.4 (3.5) P-value 0.013 0.005 reduction in tissue biomass for allocation P-value 0.001 0.012 of N. Higher N concentration and lower C 1Not significantly different at P < 0.05.

404 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 decomposition and/or (2) Carex plants may have held litter bags off the soil, which may have let them dry out more and decompose less than bags placed under willow canopies.

Return of N to the Soil Based on the biomass and N content of aboveground litter in our sites (Tables 2 and 3), we calculated that the N return to the soil in aboveground litter during the 1997 growing season was greater in the ungrazed and clipped plots (0.83 and 0.82 g N m-2, respectively) than in the grazed plots (0.42 g N m-2), excluding the contribution of N in wood litter in all treatments. Litter from willow, other shrubs, and herbs contributed to 62, 17, and 21% of the N returned to the soil in litter inside the exclosures, and 51, 16, and 33 % of the N returned to the soil in litter within the grazed plots, respectively. Elk dung biomass deposited on the soil during the 1997-98 season averaged 42.2 ± 6.2 g m-2 across all sites. This value is similar to those reported by Frank and McNaughton (1992), who found that average herbivore dung deposition during the 5 month season in the winter range of Yellowstone National Park was 76.9 ± 30.1 g m-2. In our sites, average elk dung N concentration in the samples collected in late fall of 1997 was 2.0 %. Based on our results, we estimated that approximately 0.87 ± 0.12 g N m-2 returned to the soil in elk dung during the 1997Ð98 winter season in our study site. Therefore, the amount of N returned to the soil as elk dung plus aboveground plant litter averaged 1.3 g m-2 Fig. 1. Soil moisture (0 to 14 cm) under willow canopies and in Carex plots in upper and in the grazed plots. The estimated amount lower landscape positions of Horseshoe Park and Moraine Park from early June to late August of 1997. Error bars represent standard errors of the means (n = 8). of N returned to the soil in elk urine in our sites, based on the diet and specific characteristics of the herd, could be approxi- mum soil temperatures from 1 to 6 cm in contributing to reductions in soil tempera- mately 98% of the N returned to the soil in depth during the 1997 growing season ture and soil moisture. We suggest that the dung (K. Schoenecker, pers. comm., were significantly lower under willow rate of nutrient loss from litter bags was 1999). Based on these estimates, after canopies than in Carex plots in both higher under willow canopies because: (1) Moraine and Horseshoe parks (Fig. 2). shading by willow canopies may decrease including the potential N inputs from These results indicate that the presence of soil temperature and help preserve mois- urine, the total amount of N returned to the soil in the grazed plots could be as high as willow shrubs has a significant influence ture at the top few centimeters of the litter -2 on microclimatic conditions in our sites, layer and soil, and this may enhance litter 2.2 g N m , which corresponds to 265%

Table 6. Soil characteristics (0Ð15 cm) of ungrazed, clipped, and grazed plots of Moraine Park and Horseshoe Park in July 1997. Values represent means (n = 12) with standard errors within parentheses.

Treatment Total C Total N POM1 C POM N Sand Silt Clay pH2 ------(g kg soil-1) ------

Ungrazed 50.3 (9.0) 3.38 (0.63) 15.9 (3.5) 0.81 (0.19) 523 (59) 209 (40) 152 (19) 4.64 (0.10)

Clipped 47.7 (7.1) 3.27 (0.54) 13.3 (2.0) 0.63 (0.09) 494 (55) 235 (47) 161 (25) 4.67 (0.12)

Grazed 42.7 (6.2) 2.82 (0.44) 11.3 (2.0) 0.53 (0.12) 549 (37) 234 (29) 118 (19) 4.60 (0.11) 1Particulate Organic Matter 2Measured in water (2:1, water:soil)

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 405 N (0 to 30 cm) between soil samples taken in Carex plots or under willow canopies. Total soil C and N averaged 62 and 4.4 g kg-1 in Carex plots and 58 and 4.0 g kg-1 under willow canopies, respectively. In all experiments with both ion- exchange resin bags and field soil core incubations, there were no significant differences in soil N availability between grazing treatments during the years of the study. Several studies have reported increases in the rates of soil N mineralization with herbivory (McNaughton et al. 1988, Holland and Detling 1990, Frank and Evans 1997). Frank and Groffman (1998), reported that N availability in plots grazed by elk was 100% higher than exclosed plots. It is possible that the short time (4 years) since the establishment of the exclosures in our study did not allow for the development of detectable differences in soil N mineralization and availability between grazing treatments. Alternatively, since the explanations for the influences of herbivores on N availability are not quite well understood, other mechanisms may have contributed to the lack of differences in N availability between grazing treatments. The assessment of N availability with ion-exchange resin bags during 1995 and 1996 indicated that, in general, both + Ð NH4 -N and NO3 -N availability were higher during early to mid-season and declined afterwards (Table 7). In 1998, there was only 1 resin bag incubation period, and the total amount of N adsorbed to the bags was slightly higher than the sum Fig. 2. Soil temperature (1 to 6 cm) under willow canopies and in Carex plots in Horseshoe of both periods of either 1995 or 1996, Park and Moraine Park during July 1997. Vertical lines represent the range of the 95% probably because the incubation period in confidence interval for the means of maximum temperatures (n = 3). 1998 was a few weeks longer. On average, + the amount of NH4 -N adsorbed to the resin bags was 137 to 412% higher than of the N returned as aboveground litter in Yellowstone National Park. In addition, Ð the exclosed plots. Our results are consis- we found no differences in total soil C and NO3 -N during the 3 growing seasons. tent with the findings of Frank and McNaughton (1992), who found that elk Table 7. Inorganic nitrogen adsorbed to ion exchange resin bags during different incubation peri- and bison populations in Yellowstone ods during 1995 and 1996, and from 1 incubation period during 1998. Values represent means (n National Park excreted 0.81 to 4.60 g N m-2 = 12) with standard errors within parentheses. year-1, an amount that corresponded to Ð + Ð + roughly 4 times the amount of N returned Incubation period NO3 -N NH4 -N NO3 -N + NH4 -N in litterfall in their study site. ------(mg bag Ð1) ------1995 June to July 1.08 (0.23) 4.45 (0.63) 5.53 (1.45) Soil Characteristics and N Availability July to August 0.64 (0.32) 2.12 (0.44) 2.78 (1.29) There were no significant differences in P-value 0.0151 0.001 0.001 total soil C and N, POM C and N, soil tex- 1996 ture, and soil pH between grazing treat- June to July 0.95 (0.52) 3.39 (0.81) 4.34 (1.14) ments in our sites 4 years after the estab- July to August 1.05 (0.55) 1.44 (0.53) 2.49 (0.87) lishment of the exclosures (Table 6). P-value N.S.2 0.001 0.001 Similar to our findings, Frank and 1998 Groffman (1998) found no differences in July to October 3.01 (0.55) in soil total C and N between grazed plots 7.29 (1.98) 10.30 (2.43) 1P-value of comparisons between means of incubation periods. and exclosed plots that had been protected 2 from herbivory for 33 to 37 years in Not significantly different at P < 0.05.

406 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 8. Inorganic nitrogen mineralized during field soil incubations (0 to 15 cm) using aluminum return of N to the soil. Stohlgren et al. cores during 1997 and 1998. Values represent means for all treatments (n = 12) with standard (1999) reported that exotic species were errors within parentheses. more likely to invade landscape patches 1 Ð + Ð + higher soil N and moisture, which could Incubation period NO3 -N NH4 -N NO3 -N + NH4 -N lead to a decline in native plant species and ------(g N mÐ2) ------ecosystem diversity (Billings 1990, 1997 D’Antonio and Vitousek 1992). Therefore, June to July 0.11 (0.04) 0.55 (0.15) 0.66 (0.16) eventual increases in N availability in our 1998 sites due to elk herbivory could lead to June to July 0.71 (0.44) 0.81 (0.80) 1.51 (0.77) changes in plant species composition and July to August 1.13 (0.38) 1.33 (0.95) 2.46 (1.17) August to October 0.51 (0.23) 0.34 (0.52) 0.85 (0.59) alter ecosystem functioning, because of 1 shifts in the competitive interactions Length of incubation period: 1997 = 4 weeks; 1998 = 6 weeks each period. between plant species (Tilman 1982, 1988, Holland et al. 1992, Sterner 1994, Ritchie + during early to mid-season when plant et al. 1998). The higher proportions of soil NH4 -N could benefit plant productivity in our growth and nutrient requirements are sites, since plants with an evolutionary probably greater, the higher availability of history of grazing show elevated growth nutrients during that period may contribute responses to ammonium relative to other to the synchronization of nutrient supply Literature Cited and demand and enhance primary production and nutrient retention within the sys- Table 9. Inorganic nitrogen adsorbed to ion tem (Myers et al. 1994). Aber, J.D. and J.M. Melillo. 1991. Terrestrial ecosystems. Saunders Coll. Publ. Philadelphia, exchange resin bags under willow (Salix Interestingly, the presence of willow had spp.) canopies and in Carex spp. plots dur- Penn. ing different incubation periods of the 1995 a significant effect on N availability in our Afzal, M. and W.A. Adams. 1992. and 1996 growing seasons. Values represent experiments with ion-exchange resin bags. Heterogeneity of soil mineral nitrogen in pas- means (n = 12) with standard errors within During both incubation periods of 1996, ture grazed by cattle. Soil Sci. 56:1160Ð1166. parentheses. the amounts of inorganic N adsorbed to Alstad, K.P., J.M. Welker, S. Williams, and resin bags located under willow canopies M.J. Trlica. 1999. Carbon and water rela- Position June to July July to August was higher (P < 0.05) than in bags placed tions of Salix monticola in response to winter Ð2 browsing and changes in surface water 1995 ------(g N m ) ------in Carex plots (Table 9), but no significant hydrology: an isotopic study using δ13C and Willow canopies 5.69 (2.13) 2.87 (1.20) differences were observed during 1995. δ180. Oecologia, 120:375Ð385. Carex plots 5.80 (1.92) 2.87 (1.11) 1 The higher N availability may be a conse- Billings, W.D. 1990. Bromus tectorum, a biotic P-value N.S. N.S. quence of higher amounts of litter N cause of ecosystem impoverishment in the 1996 inputs and higher rates of N loss from lit- Great Basin. p. 301Ð322. In: G.M. Woodwell Willow canopies 4.98 (0.77) 3.07 (0.55) ter under willow canopies, as indicated by (ed.), The earth in transition: patterns and Carex plots 4.01 (0.68) 2.42 (0.37) our findings in 1996. processes of biotic impoverishment. P-value 0.018 N.S. Cambridge Univ. Press, Cambridge, UK. The data from the N fertilization experi- 1Not significantly different at P < 0.05. Binkley, D. 1984. Ion exchange bags: factors ment demonstrated that willow growth in affecting estimates of nitrogen availability. the winter ranges for elk is limited by N Soil Sci. Soc. Amer. J. 48:1181Ð1184. availability, independently of grazing Cambardella, C.A. and E.T. Elliott. 1992. inorganic forms of N, particularly when treatment. Both inside and outside the Particulate soil organic-matter changes across a grassland cultivation sequence. Soil subject to defoliation (Ruess 1984, Ruess exclosures, N fertilizer additions increased willow shoot length, shoot biomass, and Sci. Soc. Amer. J. 56:777Ð783. and McNaughton 1987, Hobbs 1996). Chadde, S.W. and C.E. Kay. 1991. Tall wil- Similarly to the results from the experi- the amount of N in the shoots (Table 10). low communities in Yellowstone’s northern ments with ion-exchange resin bags, the Based on our findings, we conclude that range: a test of the “natural regulation” para- + proximity to surface water had little effect digm. p. 231Ð261. In: R.B. Keiter and M.S. amounts of net NH4 -N mineralized in the soil cores were usually higher than on the dynamics of C and N in the winter Boyce (eds.), The greater Yellowstone NO Ð-N (Table 8). In addition, total inor- ranges for elk during the period of our ecosystem: redefining America’s Wilderness 3 Heritage. Yale University Press, New York, ganic N in the soil was higher during early studies. In addition, we suggest that elk herbivory could lead to long-term increas- N.Y. to mid-season during the 1998 growing Coughenour, M.B. 1991. Biomass and nitro- season (Table 8). If plant uptake is higher es in N availability in our sites, because of gen responses to grazing of upland steppe on induced increases in both litter quality and Yellowstone northern winter range. J. Appl. Ecol. 28:71Ð82. Table 10. Effects of nitrogen fertilization on willow (Salix spp.) growth and N assimilation during D’Antonio, C.M. and P.M. Vitousek. 1992. the growing season of 1999. Values represent means (n = 12) followed by standard errors Biological invasions by exotic grasses, the between parentheses. grass/fire cycle, and global change. Annu. Rev. of Ecol. and Syst. 23:63-87. Shoot Shoot Amount of N Frank, D.A. and P.M. Groffman. 1998. Treatment Shoot length biomass concentration per shoot Ungulate vs. landscape control of soil C and (cm) (g) (%) (g) N processes in grasslands of Yellowstone N fertilizer (10 g N m-2) 28.6 (1.4) a1 27.3 (2.5) a 2.25 (0.05) 0.62 (0.06) a National Park. Ecol. 79: 2229Ð2241. Frank, D.A. and R.D. Evans. 1997. Effects of No fertilization 22.5 (1.1) b 20.2 (2.4) b 2.14 (0.06) 0.43 (0.05) b native grazers on grassland N cycling in 1 Means followed by different letters are significantly different at P < 0.05. Yellowstone National Park. Ecol. 78: 2238Ð2248.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 407 Frank, D.A. and S.J. McNaughton. 1992. The Myers, R.J.K., C.A. Palm, E. Cuevas, I.U.N. Singer, F.J., E.T. Elliott, M.B. Coughenour, ecology of plants, large mammalian herbi- Gunatilleke, and M. Brossard. 1994. The J.M. Welker, D.W. Valentine, S.A. vores, and drought in Yellowstone National synchronization of nutrient mineralization Williams, L.C. Zeigenfuss, K.P. Alstad, Park. Ecol. 73:2043Ð2058. and plant nutrient demand. p. 81Ð116 In: and R.S.C. Menezes. 1997. Large mam- Frank, D.A., R.S. Inouye, N. Huntly, G.W. P.L. Woomer and M.J. Swift (eds.), The bio- malian herbivores, plant interactions and Minshall, and J.E. Anderson. 1994. The logical management of tropical soil fertility. ecosystem processes in five national parks. biogeochemistry of a north-temperate grass- TSBF and Sayce Publishing, UK. Second Ann. Rept. to Biol. Res. Div., USGS, land with native ungulates: nitrogen dynam- Naiman, R.J., and J.M. Melillo. 1984. 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Modification of ecosystems forests of Isle Royale Nat. Park. Ecol. 74: community structure. Princeton Univ. Press, by ungulates. J. Wildl. Manage. 60:695Ð713. 467Ð480. Princeton, N.J. Holland E.A. and J.K. Detling. 1990. Plant Power, J.F. 1977. Nitrogen transformations in Tilman, D. 1988. Plant strategies and the response to herbivory and belowground the grassland ecosystem. pp. 195Ð204. In: dynamics and structure of plant communities. nitrogen cycling. Ecol. 71:1040Ð1049. J.K. Marshall (ed.), The belowground Princeton University Press, Princeton, N.J. Holland, E.A., W.J. Parton, J.K. Detling, ecosystem: a synthesis of plant-associated U.S.D.A. Snow Survey Office (1995, 1996, and L. Coppock. 1992. Physiological processes. Range Sci. Dept., Sci. Series No. and 1997). Snowpack data for Rocky responses of plant populations to herbivory 26, Colorado State Univ., Fort Collins, Colo. Mountain National Park. Nat. Resources and their consequences for ecosystem nutri- Ritchie, M.E., D. 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National Park Serv., Tech. Report 93. Grazing and the dynamics of nutrient and Kiehl, K, P. Esselink, and J.P. Baker. 1997. energy regulated microbial processes in the Nutrient limitation and plant-species compo- Serengeti grasslands. Oikos 49:101Ð110. sition in temperate salt marshes. Oecologia SAS Institute. 1995. SAS User’s Guide. 111:325Ð330. Release 6.12. SAS Institute Inc., Cary, N.C. Kolberg, R.L., B. Rouppet, D.G. Westfall, Schlesinger, W.H. 1997. Biogeochemistry: An and G.A. Peterson. 1997. Evaluation of an analysis of global change. Academic Press, in situ net soil nitrogen mineralization San Diego, Calif. method in dryland agroecosystems. Soil Sci. Schuman, G.E., J.D. Reeder, J.T. Manley, Soc. Amer. J. 61:504Ð508. R.H. Hart, and W.A. Manley. 1999. Impact Larkins, K.F. 1997. Patterns of elk movement of grazing management on the carbon and and distribution in and adjacent to the eastern nitrogen balance of a mixed-grass rangeland. boundary of Rocky Mountain National Park. 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408 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 J. Range Manage. 54: 409Ð412 July 2001 Anti-quality components in forage: Overview, significance, and economic impact1

VIVIEN GORE ALLEN AND EDUARDO SEGARRA

Authors are Thornton Distinguished Chair, Department of Plant and Soil Science, and professor, Department of Agricultural and Applied Economics, Texas Tech University, Lubbock. Tex. 79409-2122.

Resumen Abstract Although recognized in importance from the dawn of history, Aunque su importancia se reconoce desde las épocas tem- forages have too often been underestimated and undervalued pranas de la historia, los forrajes también frecuentemente han perhaps in part because animal performance has frequently sido subestimados y subvaluados, en parte porque a menudo el failed to reflect apparent forage quality. Anti-quality compo- comportamiento productivo del animal ha fallado en reflejar la nents, diverse impediments to quality, have evolved as structural calidad aparente del forraje. Los compuestos anti-calidad, components and as secondary metabolites. They include mineral obstáculos variados de la calidad, han evolucionado como com- imbalances or can be related to the presence of insects and dis- ponentes estructurales y metabolitos secundarios. Ellos incluyen eases. Animal behavior and adaptation are increasingly recog- desbalances minerales o pueden ser relacionados a la presencia nized as important aspects of anti-quality factors. An anti-quality de insectos o enfermedades. El comportamiento animal y la component may reduce dry matter intake, dry matter digestibili- adaptación se reconocen mas y mas como aspectos importantes ty, or result in nutritional imbalances in animals. They can act as de los factores anti-calidad. Un componentes anti-calidad puede a direct poison compromising vital systems, result in abnormal reducir el consumo de materia seca, la digestibilidad de la mate- reproduction, endocrine function, and genetic aberrations, trig- ria seca o producir en los animales desbalances nutricionales. ger undesirable behavior responses, or suppress immune func- Ellos pueden actuar directamente como veneno dañando sis- tion leading to increased morbidity and mortality. The economic temas vitales, producir una reproducción anormal, problemas impact of anti-quality factors on individual herds can be devas- endocrinológicos, aberraciones genéticas desencadenar respues- tating but definable. Broadscale economic impacts of anti-quality tas de comportamiento indeseable o suprimir la función inmune factors are far more difficult to estimate. A loss of 0.22 kg/day in incrementando la morbilidad y mortalidad. El impacto económi- potential gain of stocker cattle due to antiquality factors during a co de los factores anti-calidad en los hatos individuales puede ser 166-day grazing season translates into a loss of about $55/steer at devastador pero definible. Los impactos a amplia escala de los $1.45/kg or over $2 billion annually when applied to the U.S factores anti-calidad son mas difíciles de estimar. Una perdida de stocker cattle. Economic losses to tall fescue (Festuca arundi- 0.22 kg/día de la ganancia potencial del ganadero debido a fac- nacea Schreb.) toxicosis in the U.S. beef industry are probably tores anti-calidad durante una época de apacentamiento de 166 underestimated at $600 million annually. Reproductive and días se traduce en una perdida de aproximadamente $55 dolares/ death losses of livestock due to poisonous plants have been esti- novillo, a un precio de $ 1.45/kg, o de mas de 2 billones anuales si mated at $340 million in the 17 western states alone. These exam- se aplica al total de la ganadería de E.U.A. Las perdidas ples of economic losses due to anti-quality factors may be upper económicas de la industria del ganado de carne de los E.U.A. por bounds of actual losses but even if a small proportion of the la toxicosis del Alta fescue (Festuca arundinacea Schreb.) son expected losses were eliminated through research, the potential probablemente subestimadas en $600 millones anuales. Solo en payoff would be extremely high. los 17 estados del oeste, las perdidas por muerte y reproducción del ganado debido a plantas tóxicas han sido estimadas en $ 340 millones. Estos ejemplos de perdidas económicas debido a los Key Words: nutrition, animal health, performance, forage quali- factores anti-calidad pueden ser los limites superiores de las per- ty, toxins didas actuales, pero aun si una pequeña proporción de las perdidas esperadas fuera eliminada a través de investigación, el pago por estas perdidas sería extremadamente alto.

1Appreciation is expressed to Karen Launchbaugh, Univ. of Idaho and the Overview and Significance Society for Range Management and Rosa Muchovej, Univ. of Florida and American Forage and Grassland Council who organized this symposium and co- chaired this event. Appreciation is also express to Richard Joost who has served as The importance of forages has echoed through the ages. The the senior editor for the publications resulting from this symposium. The USDA- Natural Resource Conservation Service (NRCS) provided financial support for this value of forages was recognized from the early dawn of history as symposium and for the resulting publications. Without the support of the NRCS, animals became domesticated and were moved from place to this symposium would not have been possible. place in search of forage (Combs 1936). Alfalfa is thought to Manuscript accepted 14 Jan. 01. have been cultivated before the development of the written lan-

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 409 guage (Bolton et al. 1972). During the set- There has always been concern that anti- review of ‘Milestones in Forage tlement years in the U.S., the value of for- quality components in forages have the Research,’ Reid (1994) concluded that forages went largely unrecognized with for- potential to compromise food safety and age quality was definable as “some prod- ages frequently relegated to lands of mar- human health. Ergotism in humans con- uct of digestibility and intake of the diet.” ginal arable value (Edwards 1948). Often, suming wheat (Triticum aestivum L.), rye Mott and Moore (1969) described forage there was little recognition of differences (Secale cereale L.), pearlmillet [Pennisetum quality as composed of both ‘forage nutri- in value among forage species. This senti- americanum (L.) Leeke], and other small tive value’ (chemical composition, ment began to change as P. V. Cardon grains contaminated with Claviceps species digestibility, and nature of digested prod- stated in the 1948 Yearbook of has been documented both historically and ucts) and ‘forage consumed’ (acceptability, Agriculture, “..., in the wake of war and in during modern times (Krishnamachari and rate of passage, and availability). Raymond the glow of our unprecedented production, Bhat 1976, Lewis 1977) Humans can (1968) suggested that quality is defined by this country looks to the future and consid- potentially be exposed to several mycotox- the equation ‘Nutrient intake = intake of ers again the land and its management - feed dry matter x digestibility of feed dry ins by direct consumption of grains conta- this time, as never before, in terms of matter x efficiency of utilization of digest- minated with products of fungal growth grass.” (Cardon 1948). In his preface to ed nutrients’. More general definitions of although strict control of food quality on Forages: Resouces for the Future, Burton forage quality include “Characteristics that (1986) states “Forages, particularly the the U.S. market makes this unlikely to make forage valuable to animals as a grasses, are the most important plants on occur (CAST 1989, Wood 1992). source of nutrients; the combination of the face of the earth”. Occupying more However, possible long-term exposure to chemical and biocharacteristics of forage than half the land area in the U.S. and low levels of mycotoxins in the food sup- that determines its potential to produce world wide, forages provide about three ply is of potential concern. Human con- meat, milk, wool, or work” (Barnes and fourths of the energy and more than half sumption of animal products affected by Beard 1992, Barnes et al. 1995). Ball et al. of the protein in human diets (Burton anti-quality factors is also of concern. (1991) suggest that forage quality is best 1986). Because ruminants and equine Ammoniation of hay has been related to defined in terms of animal performance obtain 60 to 100% of their feed nutrients hyperexcitability in cattle (i.e. Crazy Cow and that it is ultimately the animal rather from forages and because of the economic Syndrome) and high death losses of calves than the human that determines forage importance of forage consuming livestock either at birth or within a few days of birth quality. and wildlife, the value of forage rivals that (Essig et al. 1986). A case study in Although each of these definitions proof the most important field crops. For too Mississippi suggested that milk from a vides useful mathematical and philosophi- long the nutritional and economic value of cow fed ammoniated hay could produce cal concepts regarding forage quality, each forages has been underestimated and symptoms of hyperexcitability in a non- one appears to fall short of a succinct defi- under-recognized. related calf fed the milk (Essig et al. 1986) nition. Dictionary definitions of ‘quality’ As the human population increases, land raising concerns about milk safety for generally refer to the ‘degree of excel- areas suitable for intensive crop produc- humans. In the U.S., it is unlikely that lac- lence’. Thus, we propose that forage quali- tion decrease, and issues of renewable tating dairy cows would be fed ammoniat- ty is best described as the degree to which resource conservation become more com- ed hay but this could occur in other parts a forage meets the nutritional require- pelling. As Cardon (1948) stated over a of the world. ments of a specific kind and class of ani- half century ago, “... around grass, farmers The subject of anti-quality factors is far mal. An ‘anti-quality component’ would, can organize general crop production so as reaching and includes pastures and har- therefore, be defined as any factor that to promote efficient practices that lead to vested forages as well as rangelands and diminishes the degree to which a forage permanency in agriculture.” grazeable forestlands. The following meets the nutritional requirements of a Quality of forage is paramount in obtain- papers in this volume were part of a sym- specific kind and class of animal. The ing optimum animal performance. Any fac- posium held in 1999 on ‘Anti-quality word ‘animal’ is necessary in these definitions to include both ‘livestock’ and tor or ‘anti-quality component’ that pre- Components in Forages’ at the joint meet- ‘wildlife’. Furthermore, it is necessary to vents forage from contributing its nutrition- ing of the Society for Range Management specify the kind and class of animal al potential takes on added importance with and the American Forage and Grassland Council. It is hoped that this symposium because animal nutritional needs and increased recognition of forage as a feed detoxification abilities vary. A forage that resource. During recent years, much helped to synthesize the current state of knowledge and to present the information meets the nutritional needs for dry cows progress has been made in several areas would, thus, be a high quality dry cow perhaps most dramatically in elucidating in written format that will serve as a reference for the industry. The subject of anti- feed, but may not meet the requirements the etiology of tall fescue (Festuca arundi- for finishing steers and would, therefore, nacea Schreb.) toxicosis and its relation- quality factors will continue to evolve as new information is generated and this is be a low quality finishing diet. Likewise, a ship to the endophyte fungus indeed a topic that will need to be revisit- chemical toxin or a physical inhibitor to Neotyphodium coenphialum [(Morgan- ed in the future. intake for 1 species or class of animal may Jones and Gams) Glenn, Bacon, and not affect another species or class of ani- Hanlin; Glenn et al. 1996]. Advances have mal in a similar manner. Animal behavior also been made in identifying specific tox- What is Forage Quality and and adaptation are increasingly being rec- ins, and physical and chemical factors that ognized as important aspects of anti-quali- affect intake and digestibility. The role of Anti-quality ? ty factors. For example, ability of the pre- animal behavior in avoidance of anti-quali- gastric fermentor to detoxify many of the ty factors has great potential and is the sub- It is necessary to clearly understand potentially harmful plant metabolites has ject of a paper presented in this symposium. what forage quality is before we can begin long been recognized. Palatability, rate of to address its’ antithesis, antiquality. In his

410 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 passage, digestibility, nutrient density and potential performance. The economic es. However, this strategy would result into balance, and intake are all factors deter- impact of anti-quality components on ani- higher associated cost of production. If the mining the degree to which the forage is mal health and production are often diffi- impediments to quality or anti-quality fac- able to meet the nutritional demands of the cult to estimate. Nevertheless, broadscale tors were identified and eliminated, it animal. Therefore, as suggested by Mott estimates are needed to provide perspec- might be more cost effective. and Moore (1969), quality of the forage is tive and to help focus research efforts into The economic impact of mineral imbal- going to be driven by the combination of areas of high potential economic improve- ances in forages is often poorly under- chemical and physical characteristics that ment. Estimates of the impact of dimin- stood. However, hypomagnesic grass determine ‘forage nutritive value’ and ished forage quality with lowered potential tetany has been widely researched. This ‘intake’ and these are terms that should be for gain highlight the magnitude of eco- metabolic deficiency of Mg has been esti- defined as a subset under the definition of nomic impact. An example of this can be mated to result in the loss of 1 to 3% of forage quality. derived from calculations using the current the beef cows in the U.S. annually. If the beef cattle herd in the U.S. and estimates loss is 1% of the 42.6 million cows and of expected daily gains based on National heifers that had calved by 1 January 1999 Classes and Kinds of Anti-qual- Research Council data (NRC 1984). (Agricultural Statistics 1999), the estimat- ity Components As of 29 January 1999, there were 16.8 ed financial loss to producers would be million steers and 19.6 million heifers about $150 million assuming a 500 kg weighing 227 kg or more in the U.S. cow worth about $0.77/kg. Fortunately, Anti-quality components encompass a (Agricultural Statistics 1999). The stocker Mg supplementation strategies are avail- diverse array of unrelated causative phase of cattle production into which these able that can largely prevent grass tetany agents. These may have evolved as struc- cattle could be placed, can make efficient but represent an increase in the cost of tural components of the plant or as sec- use of forage for economical gains. Ball et production both in terms of added inputs ondary metabolites resulting in plant al. (1991) summerized beef steer perfor- and labor requirements. defense mechanisms. Anti-quality compo- mance on 15 forage systems or specific Tall fescue (Festuca arundinacea nents can be revealed as mineral deficien- forages in the Southern U.S. and found that Schreb.) is one of the most important cool- cies, toxicities, and nutritional imbalances. daily gains ranged from 0.43 to 1.08 season grasses grown in the U.S. occupy- The origin of anti-quality attributes can be kg/day during an average 146-day grazing ing over 14 million ha (Sleper and phytochemicals in plant tissues or structur- season. Stocker systems in Virginia Buckner 1995). Widely adapted, this long- al inhibitors in leaf and stem arrangement. demonstrated that steers gained 0.90 Specific chemical inhibitors of quality can lived perennial forms the basis of many kg/day during a 166-day grazing season forage-livestock systems. However, much result from plant metabolism or from from April to October in an all forage sys- microbial origin. Anti-quality factors in of this fescue is infected with the endo- tem (Allen et al. 1994). Estimates based on phyte-fungus Neotyphodium coenophialum forages can furthermore be related to the NRC (1984) requirements for a 227 kg presence of insects and diseases. (Shelby and Dalrymple 1987). Presence of steer fed to gain 0.90 kg/day indicate that a the fungus confers stress tolerance to the An anti-quality component may simply dry matter intake (DMI) of 6.26 kg/day at act as a reducer of dry matter intake plant (see review by Latch 1997) but pro- a given nutritive value is required. If nutri- duction of alkaloids by both the plant and (DMI), may reduce dry matter digestibili- tive value is diminished and related DMI ty, or result in nutritional imbalances. The the fungus result in a myrid of animal dis- declines to 6.08 kg/day, a decline in intake orders (Steudemann and Hoveland 1988). anti-quality factor may act as a direct toxin of 0.18 kg/day, daily gains would be It has been estimated that the endophyte in that shuts down vital systems in animals, it expected to drop to 0.68 kg/day. This tall fescue results in loss of over $600 mil- may result in abnormal reproduction, dis- translates into over 8 million kg/day loss of lion annually to the beef cattle industry turb endocrine or neurological function, potential gain. If a value of $1.54/kg is alone (Fribourg et al. 1991). Recent evi- cause genetic aberrations, or may suppress assumed, this results in an approximate immune function leading to increased mor- cost of $12.33 million per day for all dence suggests that this may be an under- bidity and mortality. Because of the many stocker cattle in the U.S. or $0.34/stocker estimate. It has been widely accepted that and disrelated syndromes and yet the per day. This level of loss of potential gain, removal of livestock from infected tall fes- potential for many interactions and subtle represents a total economic loss for the cue pastures resulted in a fairly rapid dissi- interrelationships, the field of anti-quality 166-day period of over $2 billion. pation of symptoms of tall fescue toxicosis factors is both complex and compelling. Calculated another way, and again using but this now appears not to be the case. the Virginia example for steer perfor- Research has shown that one effect of the mance, over the 166-day grazing period, toxicity is a decline in specific immune Economic Impact of steers gained 151 kg vs 113 kg that were function (Saker et al. 1998) during the Anti-quality Components gained under the lower quality diet. The 38 grazing period. It has now been demon- kg difference would be worth about strated that this loss in immune function is The economic impact of anti-quality $55/steer at $1.45/kg. These levels of eco- long-lasting, and was measurable through- factors on individual flocks and herds can nomic losses due to the degradation of for- out the stress of cross country transporta- be devastating when the result is a large age quality could be considered to be an tion and a following 150-day feedlot fin- loss in production, reproduction, morbidi- upper bound of the actual level of loss. ishing period (Saker et al. 2001; Allen et ty, or mortality. Economic consequences That is, it would be expected that if stocker al. 2001). The lowered immunity is likely can also be severe if the loss is but a single producers were to be aware of the potential to contribute to added costs of medications animal with high economic value. The weight gain losses due to the lower quality and labor in treating animals that are less- economic effect is much less obvious of the diet, they might internalize this into tolerant to stress and disease (Purdy et al. when the result is a subtle decrease in their operations to minimize potential loss- 1989).

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 411 Poisonous plants occur in all types of Literature Cited Krishnamachari, K.A.V.R. and R.V. Bhat. grazing lands including both range and 1976. Poisoning of ergoty bajra (pearl millet) intensively managed pastureland and are in man. Indian J. Med. Res. 64:1624Ð1628. one of the most important economic Allen, V.G., J.P. Fontenot, and A. Brock. Latch, G.C.M. 1997. An overview of neoty- 1994. Forage systems for stocker cattle, p. impediments to profitable livestock pro- phodium-grass interactions, p. 1Ð11. In: 156Ð158. Anim. and Poultry Sci. Res. Rep. C.W. Bacon and N.S. Hill (ed.), duction (James et al. 1992). Based on an No. 11. Virginia Polytechnic Institute and Neotyphodium/Grass Interactions. Plenum estimated 1% death loss in cattle, a 3.5% State University, Blacksburg, Va. Press, New York, N.Y. death loss in sheep, and a 1% decrease in Allen, V.G., K.R. Pond, K.E. Saker, J.P. Lewis, W.H. (ed.). 1977. Medical botany, p. calf and lamb crops due to poisonous Fontenot, C.P. Bagley, R.L. Ivy, R. Evans, 416Ð418. John Wiley & Sons, New York, plants, the economic impact within the 17 C.P. Brown, T.M. Dettle, M.F. Miller, and N.Y. western states was estimated at $340 mil- J. Montgomery. 2001. Tasco-Forage: III. Mott, G.O., and J.E. Moore. 1969. Forage lion annually (Nielsen and James 1991, Influence of a seaweed extract on perfor- evaluation techniques in perspective. p. L-1 James et al. 1992). In their review of the mance, monocyte immune cell response, and to L-7. In: R.F Barnes, D.C. Clanton, C.H. impact of poisonous plants on the livestock carcass characteristics in feedlot-finished Gordon, T.J. Klopfenstein, and D.R. Waldo steers. J. Anim. Sci. 79:1032Ð1040. (ed.), Proc. Natl. Conf. Forage Quality industry, James et al. (1992) divide eco- Agricultural Statistics. 1999. USDA-NASS, nomic losses into direct and indirect losses. Evaluation and Utilization. Nebraska Center U.S. Gov. Printing Office, Washington, D.C. Cont. Educ. Lincoln, Neb. Direct losses were described to include Ball, D.M., C.S. Hoveland, and G.D. Nielsen, D.B. and L.F. James. 1991. death, emaciation, slow growth, decreased Lacefield. 1991. Southern forages. Potash & Poisonous plants - Proc. 3rd Int. Symp., Iowa reproductive efficiency, abortion, and birth Phosphate Inst. and Foundation Agron. Res. State Univ. Press, Ames. defects. Indirect losses included costs Atlanta, Ga. NRC. 1984. Nutrient requirements of beef cat- incurred to prevent losses or poisoning, Barnes, R.F and J.B. Beard (ed.). 1992. A tle (7th ed.). National Academy Press, medical costs incident to poisoning, losses glossary of crop science terms. Crop Sci. Washington, D.C. of forage quality due to need to alter har- Soc. Amer. Madison, Wis. Purdy, C.W., N.A. Cole, and J.A. vesting schedules, stress effects on man- Barnes, R.F, D.A. Miller, and C.J. Nelson Stuedemann. 1989. The effect of fescue tox- agement, risk, and effects on land values (ed.). 1995. Forages: an introduction to icosis on classical complement in yearling grassland agriculture. Vol. I. Iowa State and grazing permits. In addition to their feedlot steers. J. Vet. Diagn. Invest. 1:87-89. Univ. Press, Ames, Iowa. Raymond, W.F. 1968. Components in the application to poisonous plants, these types Bolton, J.L., B.P. Goplen, and H. Baenziger. nutritive value of forages, p. 47-62. In: C.M. of losses should be accounted for in 1972. World distribution and historical Harrison, M. Stelly, and S.A. Breth (ed.), accessing economic consequences of many developments, p.1Ð34. In: C.H. Hanson (ed.), Forage economics-quality. Amer. Soc. types of anti-quality factors. Alfalfa Science and Technology. No. 15. Agron., Madison, Wis. The potential economic losses discussed Amer. Soc. Agron. Madison, Wis. Reid, R.L. 1994. Milestones in forage research above, represent only a few of the Burton, G.W. 1986. Preface. In: Forages: (1969Ð1994), p. 1-58. In: G.C. Fahey, Jr. areas/issues on which anti-quality compo- Resources for the future. Counc. Agr. Sci. (ed.), Forage quality, evaluation, and utiliza- nents have an impact. Even if these areas Tech. Rep. 108. Ames, Iowa. tion. Amer. Soc. Agron., Madison, Wis. were to be the only ones affected by anti- Cardon, P.V. 1948. A permanent agriculture, p Saker, K.E., V.G. Allen, J. Kalnitsky, C.D. 1Ð5. In: A. Stefferud (ed.),. Grass. The year- Thatcher, W.S. Swecker Jr., and J.P. quality components in forage, the potential book of agriculture. USDA, U.S. Gov. associated total economic damage would Fontenot. 1998. Monocyte immune cell Printing Office, Washington, D.C. response and copper status in beef steers that be over $3 billion. At the same time, how- CAST. 1989. Mycotoxins: economic and grazed endophyte-infected tall fescue. J. ever, this level of damage provides an esti- health risks. Counc. Agr. Sci. Tech. Rep. Anim. Sci. 76:2694Ð2700. mate of the potential payoff of research 116. Ames, Iowa. Saker, K.E., V.G. Allen, J.P. Fontenot, P. addressing the anti-quality components in Combs, J.F. 1936. Growing pastures in the Bagley, R. Ivy, and R. Evans. 2001. Tasco- forage issue. Even if a very small propor- south, p. 2. Univ. North Carolina Press, Forage: II. Monocyte immune cell response tion of the expected losses were to be Chapel Hill, N.C. and performance of beef steers grazing tall eliminated through research dedicated to Edwards, E.E. 1948. The settlement of grass- fescue treated with a seaweed extract. J. minimize the negative impacts of anti- lands, p. 16Ð25. In: A. Stefferud (ed.), Grass. Anim. Sci. 79:1022Ð1031. quality components in forage, a relatively The yearbook of agriculture. USDA, U.S. Shelby, R.A. and L.W. Dalrymple. 1987. Gov. Printing Office, Washington, D.C. Incidence and distribuion of the tall fescue large research program could be afforded. Essig, H.W., E.G. Morrison, H.D. That is, the potential payoff, i.e. benefit- endophyte in the United States. Plant Disease Palmertree, R.R. Evans, D.H. Laughlin, 71:783Ð786. cost ratio, of such a research program C.E. Cantrell, R. White, R.L. Ivy, and R. Sleper, D.A. and R.C. Buckner. 1995. The would be extremely high. It is hoped that Gebhart. 1986. Ammoniated hay for cow fescues, p. 345-356. In: R.F Barnes, D.A. the information presented in this sympo- wintering diets. Bull. 949. Mississippi Agr. Miller, and C.J. Nelson (ed.), Forages: an sium will highlight the need and provide Forest. Exp. Sta. Mississippi State, Miss. introduction to grassland agriculture. Vol. I. the impetus for further research and the Glenn, A.E., C.W. Bacon, R. Price, and R.T. Iowa State Univ. Press, Ames, Iowa. dedication of funding sources to support Hanlin. 1996. Molecular phylogeny of Steudemann, J.A., and C.S. Hoveland. 1988. this research for forages are the key to Acremonium and its taxonomic implications. Fescue endophyte history and impact on ani- economical production of ruminants and Mycologia 88:369Ð383. mal agriculture. J. Prod. Agr. 1:39Ð44. Fribourg, H.A., K.D. Gwinn, A.B. Chestnut, Wood, G.E. 1992. Mycotoxins in foods and equine and are central to the protection of J.W. Oliver, J.C. Waller, J.H. Reynolds, our natural resources. Forages ARE the feeds in the United States. J. Anim. Sci. and B.V. Conger. 1991. Tall fescue and the 70:3941Ð3949. most important plants on earth and imped- fungal endophyte. Tennessee Farm Home iments to their potential as a feed source Sci. 160:10Ð29. take on parallel importance. James, L.F., D.B. Nielsen, and K.E. Panter. 1992. Impact of poisonous plants on the livestock industry. J. Range Manage. 45:3Ð8.

412 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 J. Range Manage. 54: 413Ð419 Structural anti-quality characteristics of range and pasture plants

EMILIO A. LACA, LISA A. SHIPLEY, AND EDWARD D. REID

Authors are assistant professor, Department of Agronomy and Range Science, University of California, Davis, assistant professor, Department of Natural Resource Sciences, Washington State University, Pullman, Wash., and research assistant, Department of Range Ecology and Management, University of Idaho, Moscow, Ida.

Abstract Resumen

Structural anti-quality characteristics are physical plant traits Las características estructurales anti-calidad son característi- that reduce the performance and productivity of herbivores and cas físicas que reducen el comportamiento productivo de los her- quality of their agricultural products. Most structural anti-quali- bívoros y la calidad de sus productos agropecuarios. La mayoría ty characteristics of plants affect the rate at which herbivores de las características estructurales anti-calidad afectan la tasa a gather and ingest forages, reducing the total amount of food la cual los herbívoros recolectan e ingieren el forraje, reduciendo obtained or increasing the time necessary to obtain food. la cantidad de alimento obtenido o incrementando el tiempo Structural anti-quality can substantially influence searching time necesario para obtener el alimento. Las características estruc- (e.g., plant crypticity, distribution), cropping time (e.g., plant turales anti-calidad pueden influir substancialmente el tiempo de fibrousness, tensile and shear strength ), and bite size (e.g., plant búsqueda (por ejemplo, plantas encriptadas y su distribución), canopy structure, spinescence). Plant structural characteristics tiempo de cosecha (por ejemplo, la fibrocidad de la planta, y la can also reduce digestion (e.g., silica), cause injury (e.g., spines, resistencia tensil y de corte) y el tamaño de la mordida (por awns, burrs, calluses), or reduce the quality of animal products, ejemplo, estructura de la copa de la planta, cantidad de espinas). such as wool (e.g., propagules). The effects of structural anti- Las características estructurales de la planta también pueden quality characteristics depend on the morphology of the herbi- reducir la digestión (por ejemplo, sílice), causar daño (por ejem- vore, especially its size, the morphology of the focal plant, and plo, espinas, aristas, callos, pelos) o reducir la calidad de los pro- their context within the habitat. Integrated grazing management ductos animal, tales como la lana (por ejemplo propágulos). Los plans should consider options to reduce the negative effects of efectos de las características estructurales anti-calidad dependen structural anti-quality. Carefully selecting appropriate livestock de la morfología del herbívoro, especialmente su tamaño, la mor- species with previous experience, and the appropriate season of fología de la planta focal y su contexto dentro del hábitat. Los grazing can minimize anti-quality on rangelands. Because struc- planes de manejo integral del apacentamiento deben considerar tural anti-quality may actually promote sustainability of grazing opciones para reducir los efectos negativos de las características systems by preventing severe defoliation, or by providing refuges estructurales anti-calidad. Seleccionando cuidadosamente la for highly desirable forages, it may not be desirable to completely especie animal apropiada, basados en experiencias previas, y la counteract their effects. estación de apacentamiento apropiada se puede minimizar la anti-calidad en los pastizales. Debido a que las características estructurales anti-calidad puede promover la sustentabilidad de los sistemas de apacentamiento al evitar la defoliación severa o Key Words: bite size, chewing, canopy structure, intake rate, preveer refugios para las plantas forrajeras altamente deseables, physical plant defenses, spines puede ser no del todo deseable contraatacar sus efectos

The performance and production of wild and domestic herbivores depends on receiving adequate quality and quantity of for- traits such as canopy architecture, growth form, and mechanical age over many time scales. Biochemical and physical characteris- deterrents to grazing, as well as spatial and temporal characteristics of plants that reduce the performance of herbivores feeding tics of groups of plants that potentially reduce the value of a plant on them compared to a similar plant without the trait are defined as food. Here we review the modes of action and effects on herbi- as ‘anti-quality’. Structural anti-quality characteristics include all vores of different structural anti-quality characteristics of plants, physical plant traits that cause grazing avoidance that do not including crypticity and spatial distribution, canopy structure, directly depend on the chemical composition of plant tissues plant fibrousness and resistance to chewing, tensile and shearing (Briske 1996). Plants may have individual structural anti-quality strength, stems and pseudostems, spinescence, awns, burrs, and calluses, and silica. In addition, we offer suggestions for manage- We would like to thank K. Launchbaugh for suggestions on the manuscript. ment techniques that will reduce the negative affects of structural This work is partially based on research supported by grant IS-2331-93C from US- characteristics in herbaceous and woody range and pasture plants Israel Binational Fund for Agricultural Research and Development, and award 970133 from NRI Competitive Grants Program/USDA to E. Laca. that will yield improved animal productivity and wool or hide Manuscript accepted 25 Nov. 00. quality.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 413 Modes of Action and Effects of properties, field context in which the trait without cues (Bazely and Ensor 1989, Structural Anti-quality is most detrimental to animals, body size Edwards et al. 1997, Howery et al. Characteristics of Plants of most susceptible herbivores, and char- 1999a,1999b, Kidunda and Rittenhouse acteristics of the target plant (Table 1). For 1992, Ortega and Laca 1997, Renken et al. example, short plants are more detrimental 1998). A simple model of grazing behav- Overview to large animals when forage availability ior showed that when herbivores can Structural anti-quality traits of both is low and grazing time is limited (Table detect desirable plants or patches from a herbaceous and woody range plants pri- 1). Short plants may be used more effi- distance, harvesting is greater than when marily serve to reduce the rate at which ciently by small ruminants with low plants are cryptic (Demment and Laca herbivores can gather and ingest (harvest) requirements than by larger animals 1993). Crypticity reduces an animal’s har- forages (Fig. 1). Herbivores invest up to (females vs. males, sheep vs. cattle, Illius vesting rate the most when bites are small half of their day harvesting food (Bunnell and Gordon 1987, 1991). This knowledge and little forage is available. Model pre- and Gillingham 1985, Belovsky and Slade can be used by scientists and managers to dictions were qualitatively corroborated in 1986, Owen-Smith 1988). Therefore, foresee and reduce the negative effects of experiments with cattle in artificial forag- structural characteristics of plants that each of the following plant anti-quality ing arenas where food patches were increase the time needed to find, crop, characteristics. marked using flags or other visual cues and/or chew food of sufficient quality and (Laca and Ortega 1996). Cattle exhibited quantity reduce the time available for Crypticity and spatial distribution greater foraging efficiency (intake/dis- other life requisites (e.g., parental care, Cryptic plants are difficult to find and tance walked) when feed pellets were thermoregulation, rumination, and rest) thus reduce foraging efficiency of herbi- marked with flags, a visual cue immedi- and thus reduce production and survival. vores (Feeny 1976). Apparent plants allow ately recognized by cattle. Likewise, Therefore, forage intake has the potential animals to walk directly from one preferred Howery et al. (1999a) found that steers to limit herbivore production in most plant to the next, whereas a cryptic plant searching for fixed or variable forage loca- rangeland and pasture ecosystems. In fact, requires that foragers search blindly until tions in a 0.64 ha arena with artificial visu- the effects of structural anti-quality may plants are randomly encountered. Foraging al cues spent more time feeding and less exceed that of the more well-known bio- efficiency and intake rate are affected by time in non-foraging activities than with- chemical anti-quality characteristics of the time it takes herbivores to find desirable out cues. Animals exposed to fixed and plants (Shipley et al. 1999, Van der wal et forages. In any given rangeland, intake rate variable forage arrangements with cues al. 2000). Structural plant characteristics declines and energy expenditure for loco- also located feed more efficiently and had such as spines, burrs, calluses, and awns motion increases as animals become more higher intakes than without cues. can also injure animals, affecting their sur- selective in their food choices (Murray Like crypticity, certain spatial distribu- vival (Cooper and Owen-Smith 1986, 1991, Laca and Demment 1996). These tions of forage plants may serve as an anti- Crampton 1974), reduce the quality of effects are more pronounced when desir- quality trait by affecting herbivore prefer- products such as hides and wool able plants are cryptic. ence and efficiency (Vivås and Sæther (Stubbendieck et al. 1992), or reduce Quantitative experimental information 1987, Danell et al. 1991). When a pre- digestibility of forage (e.g., silica, Van about the effects of crypticity and spatial ferred food is distributed randomly or uni- Soest 1982, Fig. 1). Many aspects of plant distribution of forages on herbivore nutri- formly, herbivores have lower intake rates structure have multiple negative effects on tion is scarce. Models and experiments in than when distributions are patchy (Laca the ingestion-digestion process and animal controlled conditions clearly indicate that and Ortega 1996). Cattle had a higher performance. Therefore, for each structur- intake rate increases when desirable for- intake rate on feed pellets with flags than al plant characteristic, it is important to ages are easy to detect and encounter. those without flags only when spatial dis- understand its main mode of action, level Animals learn to associate forages with tribution was uniform or random, but not of experimental support for its anti-quality visual cues forage more efficiently than when feed was patchy (Laca and Ortega 1996). The fact that intake rate in patchy distributions is less affected by crypticity indicates that cattle use mechanisms other than visual cues to detect patches of desirable forage. Cattle and sheep can overcome the effects of crypticity when food locations are predictable based on spatial memory (Edwards et al. 1997, Laca 1998). However, spatial memory is expected to be effective only in selecting feeding sites or larger areas (Bailey et al. 1996). Whether plant dispersion and patchiness serves an anti-quality function depends on the spatial scale considered. Foraging intensity per shrub, tree, small patch, or feeding station increases with decreasing patch density (Vivås and Sæther 1987, Danell et al. 1991, Shipley and Spalinger 1995). More specifically, herbivores take Fig. 1. The modes of action by which structural antiquality characteristics of plants influence larger bites and more bites per stem in animal fitness and production.

414 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 1. Structural antiquality characteristics of plants, including their effects on animal performance, the level of experimental proof

AntiÐquality trait Effects Proof Context Animal Plant Crypticity Lower bite and intake rate Limited Low herbage mass Large Rare Random distribution Lower bite and intake rate Limited Low herbage mass Large Low density Short stature Reduced bite mass and intake Plenty Low herbage mass Large Low bulk density

Low bulk density Reduced bite mass and intake rate Some Low herbage mass Large Short Pseudostems Reduced bite mass and intake rate Some Low herbage mass Large and small Short Stems, (hedging, wolf plant) Reduced bite mass, bite rate and Good Early stages of Medium Bunchgrass, intake rate; barrier; injury bunchgrass Shrub Tensile and shearing strength Reduced bite area, bite mass and Limited Late phenological stages; Small Grass bite rate, fatigue tropical grasses Fibrousness, resistance to Reduced bite and intake rate; Plenty High herbage mass; All C4, mature or chewing lower passage rate tropical pastures dormant plants Twig thickness Restricted relation between bite mass Good Small, Medium Dormant shrubs and quality; reduced bite rate Spinescence Reduced bite mass and rate; injury; Plenty Low primary productivity Medium Woody plants disease; Awns, calluses, burs Reduce bite and intake rate injury; Good All, particularly Mature; Stipa, disease; damage product sheep, goats Bromus, Hordeum Silica Injury; promotes tooth wear; Good High primary productivity Grazers Grass urinary calculi patches that contain fewer stems and are In grasslands, bite mass is often con- may serve to deter herbivory by separating scattered further apart, presumably to strained by the structure, especially height bites (Myers and Bazely 1991, Vivås et al. maximize intake rate at the expense of for- and bulk density, of the canopy of grasses 1991). In some plant species, herbivory age quality. The proportion of a small and forbs (Black and Kenney 1984). In an increases branching and produces a hedge patch (i.e., feeding station) removed by a experiment using controlled canopy struc- effect that reduces bite size and accessibil- herbivore increases with decreasing densi- tures, bite mass of cattle was 0.26 g in 8- ity. However, in other plant species such ty. Therefore animals may have a higher cm tall swards, but only 0.12 g in 4-cm as birch (Betula spp), moose browsing harvesting rate at the patch when patches swards, despite a constant forage mass increased length, diameter and leaf size of are further apart. However, this trend is kept at 500 kg/ha by varying bulk density re-grown stems, which were in turn used reversed at the scale of a large patch or (Ungar et al. 1991). Moreover, livestock more heavily than unbrowsed trees habitat (i.e., large groups of shrubs/trees). seem to select patches that yield greater (Danell et al. 1985). More animals spend more time in habitats intake rate (Arnold 1987, Laca et al. Canopy structure and its effect on intake that provide more food, and thus relatively 1993). Thus, sward structure has a pro- rate changes with plant phenology and more biomass is removed and daily intake nounced effect on selective defoliation plant fibrousness. Because nutritional is increased in more productive habitat patterns of vegetation. Herbaceous plants quality is often inversely related to bite patches (Vivås and Sæther 1987, Danell et that yield small bites tend to be avoided, mass, bite mass is a trade-off between har- al. 1991, Edenius 1991). and plants that offer large bites of good vesting rate and nutritional quality quality forage tend to be preferred. (Shipley et al. 1999, Vivås et al. 1991). For example, as grasses mature from vege- Canopy structure Depending on the relative and absolute abundance of tall and short plants in the tative to reproductive stages, overall nutri- Canopy structure determines the size tional value declines (Van Soest 1982, and arrangement of bites of vegetation in grassland, short plants may become unprofitable to the herbivore (Laca et al. Nelson and Moser 1994). During the vege- space. Bite mass is one of the main deter- tative stage of grass phenology, the nutri- minants of short-term intake rate by herbi- 1994a). Similarly, browsing herbivores tend to tional quality differs little among plant vores (Black and Kenney 1984, Spalinger parts. As grasses mature, the proportion of and Hobbs 1992, Gross et al. 1993). The prefer woody plant species and portions of plants that provide larger leaves and thick- more fibrous stems and older leaves mechanisms of cropping (i.e., severing or increases, resulting in large variation in er and longer annual growth twigs (Danell prehending a bite) and chewing are such nutritional quality within a plant or sward et al. 1994, Shipley et al. 1998). The that, for a wide range of bite mass, intake (Hacker and Minson 1981). To compen- arrangement of leaves and stems on some rate increases up to 10 fold with increasing sate for the decline in quality as grasses bite mass (Gross et al. 1993, Shipley et al. plants, such as willow (Salix spp.), allow mature, herbivores select higher quality 1994). This range certainly brackets bite herbivores to strip many leaves in 1 bite, parts. However, increased selectivity mass values that normally can be obtained which substantially increases intake reduces harvesting rates by slowing crop- by livestock and wildlife in rangelands (Stapley 1998). Larger herbivores can ping rate and reducing bite size to the and most pastures. Thus, under most obtain a larger bite when branching archi- point that adjacent plants that allow higher rangeland conditions, herbivores are at tecture allows them to take multiple stems intake become preferred. How well herbi- least partially limited by bite mass they in one bite (Vivås et al. 1991). However, vores can compensate for changes in nutri- can obtain. small, thin stems branching at wide angles tional quality depends upon the animal’s

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 415 size and mouth morphology. Because of bite area that may be cropped (Demment vores spend more time foraging, but often large mouth parts, larger herbivores are et al. 1992). Bite area declined more not enough to compensate completely generally less able to select small, more steeply with increasing bulk density in (Cooper and Owen-Smith 1986). Spines nutritious parts of plants than smaller her- dallisgrass (Paspalum dilatatum Poir.) influence harvesting rate by reducing bite bivores. Likewise in woody range plants, than in wild oats (Avena fatua L.). This mass and/or decreasing cropping rate the amount of lignin and cell wall general- difference was attributed to the greater (Belovsky et al. 1991). ly increases with twig diameter (Vivås and tensile strength of dallisgrass, with leaf Spines reduce bite mass by impeding Sæther 1987), but intake rate also increas- blades 14% lighter (4.3 vs. 4.9 mg) and stripping motions and separating leaves, es. Because large herbivores require a 89% stronger (11.5 vs. 6.1 Newtons/blade) which forces animals to crop leaves indi- greater intake rate than do smaller herbi- than wild oats (Demment et al. 1992). At vidually (Milewski et al. 1991, Pellew vores to meet their nutritional require- equal bulk density, dallisgrass foliage was 1984, Stapley 1998). Large herbivores that ments, plants with smaller leaves and expected to be 2.2 times stronger than oat require large bites, such as kudus twigs are less profitable and provide a foliage. Although tensile strength is not an (Tragelaphus strepsiceros)and giraffes greater defense against large herbivores absolute limitation to biting (Hughes et al. (Giraffa camelopardalis), may be particu- (Spalinger and Hobbs 1992). 1991), it may reduce intake rate by impos- larly affected by spinescence. Thorns and ing a cost in terms of effort, energy, and spines also reduce the fraction of a twig Plant fibrousness and resistance to time. When grazing swards of high tensile that may be pruned and the diameter at strength, steers sometimes failed to sever chewing which the twig is clipped (Cooper and the bites of grass apprehended, and had to Owen-Smith 1986). Therefore, small Resistance to ingestive chewing, mea- release some of the forage before being sured as the number of chews per unit leaves combined with thorns have the able to complete the biting motion (E. A. greatest anti-quality effects on medium to mass of particles comminuted to pass a Laca, University of California, Davis, per- 1.18 mm sieve, is positively related to large herbivores (Belovsky et al. 1991, sonal observation). Gowda 1996, Milewski et al. 1991) fiber content (McLeod et al. 1990, Balch Bite mass on woody plants is also con- 1971). Therefore, intake rate can decline because their bite size is more severely trolled by the force required to sever for- with increasing fiber content in forages restricted. because of the associated increase in age. Obtaining a larger bite usually Spines also slow cropping rate by chewing time necessary to adequately requires that the animal “prune” a thicker requiring herbivores to carefully manipu- process the forage. In herbaceous plants, twig or multiple twigs (Vivås et al. 1991). late plants in their mouths to avoid pain resistance to ingestive chewing can be Because the force required to crop a twig and injury (Belovsky et al. 1991, Cooper considerably greater for stems than for increases curvilinearly with twig diameter and Owen-Smith 1986, Dunham 1980). leaves (McLeod et al. 1990). Stems also (Shipley et al. 1999), thick or multiple Hooked thorns especially catch on lips, are more resistant than leaves to chewing twigs may restrict bite mass or at least tongues, and ears (Cooper and Owen- during rumination. Chewing during inges- slow cropping rate, particularly for small Smith 1986). The influence of thorns on tion accounts for much of the variation in browsing herbivores. As twig diameter ingestion depends on the size of the forag- intake rate within feeding stations, and increases, herbivores must switch from ing animal. Smaller animals can maneuver thus fibrousness directly reduces intake using incisors to molars to crop bites, mouthparts more easily among thorns to rate (Laca et al. 1994b). For example, which slows intake (Cooper and Owen- pluck small leaves, and therefore, thorns short-term intake rate of moose (Alces Smith 1986). alces), deer (Odocoileus virginianus), and may be less effective in reducing cropping snowshoe hares (Lepus americanus) was rates. Pointed muzzles and mobile lips on lower on red maple stems (Acer rubrum, Stems and pseudostems larger animals may be adaptations for 64% neutral detergent fiber, NDF) than on Cured reproductive stems can effective- feeding on thorny vegetation (Myers and red maple leaves (32% NDF) for a wide ly deter grazing by cattle, particularly Bazely 1991). However, large animals range of bite sizes (Shipley and Spalinger when plants are in an early phenological with larger mouths, like giraffes and rhi- 1992). Likewise, intake rate of cattle was stage (Ganskopp 1993, Ganskopp et al. nos (Diceros bicornis), often can bite off greater for the less fibrous legume-leaf 1992). Plants with stems were less likely and chew thorns that impede smaller ani- fractions than for grass leaf and stem frac- to be grazed and severely defoliated than mals (Owen-Smith 1988, Pellew 1984). In tions (McLeod and Smith 1989). Sheep those without stems. In experiments with fact, spines may also reduce harvesting eating perennial ryegrass (Lolium perenne hand-constructed swards, Flores et al., rates of very small herbivores, such as L.) with high shear strength had a signifi- (1993) found that a bottom layer of dallis- plains woodrats (Neotoma micropus), by cantly lower intake rate (6.5 g/min) than grass stems acted as a barrier to grazing, physically impeding or injuring them as did those eating ryegrass with low leaf but pseudostems had no detrimental effect. they climb up to harvest berries, seeds, shear strength (7.6 g/min; MacKinnon et The effects of the layer of stems were evi- and foliage (Cooper and Ginnett 1998). al. 1988). Although ryegrass progenies dent only if the stems were higher than the Spinescence also can injure and physi- that differed in shearing strength by 50% biting depth animals would select in a sim- cally block animals from feeding on the differed in harvesting rate, there was no ilar sward made only of leaf laminae. plant or cause so much pain that the ani- discernible difference in their digestion mal refuses to feed on it. For example, rate or potential degradability. Thus, effects of fibrousness on eating rate are Spinescence prickles on species such as blackberry beyond the effects of fiber on forage Herbivores generally have lower intake (Rubus idaeus) can interlock, holding digestibility and retention time. rates on plants with spines, thorns, prick- stems together and making the patch diffi- les, and hairs than the same plants with cult or impossible to penetrate (Myers and these structures removed (Cooper and Bazely 1991). Some injuries from spines Tensile and shearing strength Owen-Smith 1986, Dunham 1980, Gowda cause chronic, rather than immediate pain Increasing tensile strength of foliage 1996). When intake rate is reduced, herbi- and injury. Scratches and scar tissue can tends to reduce bite size by reducing the

416 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 be found in the digestive tract of kudus ly have more rigid and sharper edges that (Flores et al. 1989a, 1989b, Ortega-Reyes and domestic goats inhabiting Acacia spp. can affect harvesting rates by reducing rel- and Provenza 1993a, 1993b). Therefore, woodlands, suggesting that thorns may ative bite mass (Reid 2000). For example, grazing experience can be used by man- injure and scar buccal or esophageal sheep presented with similar sized plants agers to reduce the effects of structural mucosa, and may make these animals of indiangrass (Sorghastrum nutans (L.) anti-quality of plants on herbivores. more susceptible to disease (Cooper and Nash) and big bluestem (Andropogon ger- This review of structural anti-quality Owen-Smith 1986). ardii Vitman) strongly prefer big bluestem factors leads to the following conclusions: Because spinescence slows harvesting despite no noticeable differences in nutri- 1. Structural anti-quality can have multiple rate of herbivores, the anti-quality effects tional quality between the grasses. modes of action, from reducing short- of spines varies with habitat productivity, Indiangrass, which has higher silica con- term intake rate by increasing search accessibility, proportion of the landscape tent than big bluestem, has stiffer and and locomotion costs, to lowering pas- covered, nutrient concentration and sea- sharper-edged blades, which limited bite sage rate by increasing resistance to sonal dynamics in relation to its neighbors mass (Reid 2000). Small herbivores, such chewing, to directly injuring herbivores. (Grubb 1992). The consequences of as voles (Microtus ochrogaster), also pre- 2. Reduction of intake rate by limitation of reduced intake rate to a herbivore are more fer grasses with lower silica content (Gali- bite mass and bite rate is widespread. pronounced where intake rate is more lim- Muhtasib et al. 1992). However, the effects These limitations are more severe for iting, such as in arid environments that of silica on preference do not seem to be large herbivores with high physiologi- have a low primary productivity, where, universal. Shewmaker et al. (1989) found cal demand in environments with low not surprisingly, spines are more common no relationship between silicon content and primary productivity. (Belovsky and Schmitz 1991). forage preference in sheep. 3. Effects of anti-quality factors depend on High silica content of plant tissues can herbivore characteristics, notably body Awns, burrs and calluses also be detrimental to herbivores by pro- size, characteristics of the focal plant, Many plant species have evolved mech- moting rapid tooth wear (Baker et al. and its context within the habitat. The anisms of propagule dispersal that are 1959, Riet-Correa et al. 1986). The pro- influence of a given anti-quality trait detrimental to herbivores. Awns, calluses ductive life span of cattle, particularly depends on the characteristics of other and spikelets such as in Avena, Stipa, reproductive beef and dairy cows, can plants available to the herbivore. Thus, Bromus, Sitanion and Hordeum spp., are extend beyond 7-8 years. Yet, where for- because quality, diversity and quantity noxious to livestock because they are ages have high silica content, and when of potential forages vary with season bristly or scabrous, bearing stiff hairs animals are chronically forced to graze and successional stage, so does the arranged like harpoons, or sharp calluses. close to the soil in excessively short effects of a particular anti-quality factor. These structures can bury into soft tissues swards, tooth wear may cause culling of 4. Structural and chemical anti-quality fac- (eyes, mouth, nostrils, and ears), causing otherwise productive animals because they tors are interdependent. Forage fibrous- distress and infections (Crampton 1974). cannot bite and chew enough forage to ness, spines, and stems are structural bar- Sheep and other fiber-producing livestock realize their production potential. Silicon riers based on lignin and cellulose, which are also susceptible to injury in any area of content in forages may further reduce ani- are quantitative chemical defenses. the skin, because their hide is more deli- mal health by causing urolithiasis (Baker As a direct consequence of the fact that cate than that of bovines (American Sheep et al. 1961a,1961b, Bailey 1976). structural anti-quality factors tend to limit Industry Association 1996). Such lesions forage intake over the long term by con- cause distress, reduce productivity, conta- straining ingestion constraints, manage- minate the carcass, and reduce the quality Conclusions and Management ment recommendations follow general of the hides. Fruiting structures with Implications grazing management guidelines to ensure thorns and hooks, such as those produced that herbivores achieve sufficient quality and quantity of intake. The following by burr clover (Medicago polymorpha L.), Any plant trait that affects herbivore diet as well as propagules from several grasses, management recommendations should be choice serves an anti-quality function considered in the context of a general contaminate and reduce the value of the (Belovsky and Schmitz 1991). Therefore, fleece (American Sheep Industry grazing management plan developed for the efficacy of any structural anti-quality the enterprise as a whole. Association 1996, Stubbendieck et al. characteristic of plants depends on the 1992). 1. Carefully select livestock species and characteristics of other plants in the envi- type to match the forage characteristics ronment, the nutritional status of the herbi- of specific zones and paddocks. Silica vore, and herbivore species. Because of 2. Ensure pastures have forage that opti- Several studies have examined how sili- the relationship between body size and a mizes grazing efficiency for specific ca affects herbivores, most notably its variety of morphological and physiologi- herbivores. For example, small rumi- effect on digestion (Van Soest 1982), cal characteristics of ruminants (Demment nants are better suited for grasses with tooth wear (Riet-Correa et al. 1986), and and Van Soest 1985, Illius and Gordon shorter swards. as a cause of urinary calculi (Emerick 1987, Shipley et al. 1994), body size has 3. Periodically “clean” grasslands to 1987, 1988). Silica is an indigestible struc- an overriding influence on the effects of remove old stems and standing dead tural component of most grasses (Van any particular anti-quality trait (Table 1). forage by grazing with very high animal Soest and Jones 1968). Silica in grasses A number of anti-quality traits affect densities for short times or by mowing. herbivores by making it hard for them to reduced in vitro digestibility 3 units per When using animals as the cleaning bite, handle, and chew forages. However, unit of silica (Van Soest and Jones 1968). tool, use animals with low physiologi- the ability of herbivores to deal with dif- Furthermore, silica may affect intake rates cal demands and good teeth, like hors- ferent canopy structures, stems, and spines in a similar fashion as other structural comes, wethers and mature dry cows. pounds. Grasses with higher silica general- improves with experience and learning

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 417 4. Determine the abundance of plants with Baker, G., L. H. P. Jones, and I. D. Demment, M. W., and P. J. Van Soest. 1985. high silica in different paddocks and Wardrop. 1959. Cause of wear in sheep’s A nutritional explanation for body-size pat- assess their impact on tooth wear. teeth. Nature 184:1583Ð1584. terns of ruminant and nonruminant herbi- Those paddocks should be used by live- Baker, G., L. H. P. Jones, and I. D. vores. Am. Nat. 125:641Ð672. Wardrop. 1961b. Opal phytoliths and min- stock with good teeth whose longevity Demment, M. W., E. A. Laca, N. G. eral particles in the rumen of the sheep. Aust. Seligman, and E. D. Ungar. 1992. in the herd is not an issue. J. Agric. Res. 12:473Ð482. Integrating sward structure and ingestive 5. Determine which paddocks and seasons Bazely, D. R. and C. V. Ensor. 1989. behavior to determine intake rate in cattle. have an abundance of plants with awns, Discrimination learning in sheep with cues Univ. of California Volcani Center, Davis, calluses, burs and other structures that varying in brightness and hue. Appl. Anim. Calif. cause injuries and reduce the quality of Beh. Sci. 23:293Ð299. Dunham, K. M. 1980. The feeding behaviour fiber, hides, and carcasses. Plan grazing Belovsky, G. E. and O. J. Schmitz. 1991. of a tame impala Aepyros melampus. Afr. J. management such that susceptible live- Mammalian herbivore optimal foraging and Ecol. 18:253Ð257. the role of plant defenses, pp. 1-28. In: R. T. Edenius, L. 1991. The effect of resource deple- stock are not in these paddocks when Palo and C. T. Robbins (eds.), Plant defenses noxious plant structures are abundant. tion on the feeding behaviour of a browser: against mammalian herbivory. CRC Press winter foraging by moose on Scots pine. J. 6. In areas with challenging forage struc- Inc., Boca Raton, Fla. Appl. Ecol. 28:318Ð328. ture, use animals that have experience Belovsky, G. E. and J. B. Slade. 1986. Time Edwards, G. R., J. A. Newman, A. J. with the forages, or gradually introduce budgets of grassland herbivores: body size Parsons, and J. R. Krebs. 1997. Use of cues livestock to the new forages. This is similarities. Oecologia 70:53Ð62. by grazing animals to locate food patches: best accomplished by placing naïve ani- Belovsky, G. E., O. J. Schmitz, J. B. Slade, An example with sheep. Appl. Anim. Beh. mals with experienced ones at times and T. J. Dawson. 1991. Effects of spines Sci. 51:59Ð68. when their productivity and survival and thorns on Australian arid zone herbivores Emerick, R. J. 1987. Answer to silica stones. of different body masses. Oecologia South Dakota Farm Home Res. 38:10Ð12. does not depend on structurally defend- 88:521Ð528. Emerick, R. J. 1988. Urinary calculi, pp. ed forages. Black, J. L. and P. A. Kenney. 1984. Factors 523Ð531. In: D. C. Church (ed.), The rumi- These management guidelines are pro- affecting diet selection by sheep: II. Height and density of pasture. Aust. J. Agr.. Res. nant animal. Digestive physiology and nutri- posed to prepare herbivores for the struc- tion. Prentice Hall, Englewood Cliffs, N. J. tural challenges presented by forage 35:551Ð563. Briske, D. D. 1996. Strategies of Plant Survival Feeny, P. 1976. Plant apparency and chemical plants. It is, however, important to defense. Rec. Adv. Phytochem. 10:1Ð40. acknowledge positive aspects of anti-qual- in Grazed Systems: a Functional Interpretation, pp. 37Ð67. In: J. G. Hodgson Flores, E. R., F. D. Provenza, and D. F. ity factors on grazed ecosystems. By pre- and A. W. Illius (eds.), The ecology and Balph. 1989a. The effect of experience on venting complete defoliation, or by pro- management of grazing. 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JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 419 J. Range Manage. 54: 420Ð430 July 2001

Lignin and fiber digestion

KENNETH J. MOORE AND HANS-JOACHIM G. JUNG

Authors are professor, Department of Agronomy, Iowa State University, Ames, Iowa 50011; and research dairy scientist, USDA, Agricultural Research Service, Plant Science Research Unit and U.S. Dairy Forage Research Center Cluster, St. Paul, Minn. 55108.

Abstract Resumen

Lignin is a polymer formed from monolignols derived from the La lignina es un polímero formado de monolignoles derivados phenylpropanoid pathway in vascular plants. It is deposited in de la vía fenilpropanoide de las plantas vasculares. Se deposita the cell walls of plants as part of the process of cell maturation. en las paredes celulares de las plantas como parte del proceso de Lignin is considered an anti-quality component in forages maduración de la célula. En los forrajes, la lignina se considera because of its negative impact on the nutritional availability of como un componente anti-calidad por su impacto negativo en la plant fiber. Lignin interferes with the digestion of cell-wall poly- disponibilidad nutricional de la fibra de la planta. La lignina saccharides by acting as a physical barrier to microbial enzymes. interfiere con la digestión de los polisacáridos de la pared celular Lignification therefore has a direct and often important impact al actuar como barrera física para las enzimas microbianas. Por on the digestible energy (DE) value of the forage. There are a lo tanto, la lignificación tiene un impacto directo, y a menudo number of plant-related factors that affect lignification in indi- importante, en el valor de la energía digestible (ED) del forraje. vidual plants and plant communities. Lignification is under Hay un número de factores relacionados con la planta que genetic control and there are considerable differences in lignin afectan la lignificación de las plantas individuales y de las comu- concentration and composition among species and even geno- nidades vegetales. La lignificación esta bajo control genético y types within species. Genetic differences in lignification are first hay considerables diferencias entre especies, y aun entre genoti- expressed at the cellular level and are affected by biochemical pos de la misma especie, respecto a la concentración y composi- and physiological activities of the cell. As cells differentiate, dif- ción de la lignina. Las diferencias genéticas de lignificación se ferences in lignification occur depending on the tissues and expresan primeramente a nivel celular y son afectadas por las organs being developed. Lignification tends to be most intense in actividades bioquímicas y fisiológicas de la célula. Conforme la structural tissues such as xylem and sclerenchyma. Plant organs célula se diferencia ocurren diferencias en la lignificación, containing high concentrations of these tissues, such as stems, are dependiendo de los tejidos y orgános que se estén desarrollando. less digestible than those containing lower concentrations. The La lignificación tiende a ser mas intensa en tejidos estructurales relative proportion of lignified tissues and organs typically como el xilema y esclerénquima. Los órganos de la planta que increases as plants mature so there is often a negative relation- contienen altas proporciones de estos tejidos, tales como los tal- ship between digestibility and maturity. All of these plant los, son menos digestibles que aquellos que contienen bajas con- processes respond to environmental factors that can affect the centraciones. La proporción de tejidos y órganos lignificados extent and impact of lignification. Temperature, soil moisture, típicamente aumenta conforme la planta madura, por lo que a light, and soil fertility can have either direct or indirect effects on menudo hay una relación negativa entre la digestibilidad y lignification. The most useful management practices for minimiz- madurez. Todos estos procesos de la planta responden a factores ing the negative effects of lignification are manipulation of the ambientales que pueden afectar la cantidad e impacto de la lig- plant community such that it contains more desirable species and nificación. La temperatura, humedad del suelo, luz y fertilidad harvest management to maintain plants in a vegetative stage of del suelo pueden tener también efectos directos o indirectos en la development. lignificación. Las practicas de manejo mas útiles para minimizar los efectos negativos de la lignificación son la manipulación de las comunidades vegetales para que contengan mas especies Key Words: Anti-quality, digestibility, forage quality, forage uti- deseables y el manejo de la cosecha para mantener las plantas en lization estado vegetativo.

Lignin is considered an anti-quality component in forages because of its negative impact on the nutritional availability of plant fiber. It differs from most other classes of antiquality com- secondary metabolite. Its evolution in plants is primarily related ponents in forages in that it is a structural compound rather than a to plant structure and function and not as a defense mechanism against other organisms. As a component of the cell wall, lignin plays an important role in morphogenesis. Cell walls form the Journal Paper N. J-18367 of the Iowa Agriculture and Home Economics Experiment Station, Ames, Iowa, Project No. 2899, and supported by Hatch Act structural framework of the plant architecture that provides and State of Iowa.. mechanical support for plant organs (Varner and Lin 1989). Cell Manuscript accepted 27 Nov. 00. walls also are involved in water balance, ion exchange, cell

420 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 recognition, and protection from biotic Lignin Biochemistry converts 5-hydroxyferulic acid to sinapic stresses (Boudet 1998, Varner and Lin acid is reduced in activity. As more lignin 1989, Vian 1982). mutants and transgenic plants involving Lignin is an integral component of plant While lignin has been recognized as a the lignin pathway have been character- cell walls. It is the last major biopolymer distinct chemical entity of plant cell walls ized, it has become apparent that this path- to have evolved within the plant kingdom for over 100 years (Sjostrom 1981), there way is actually more of a web than linear and is generally regarded as the second is still considerable scientific argument (Sewalt et al. 1997b). Because of this web most abundant compound, after cellulose, concerning its structure, biosynthesis, and structure and the ability of plants to incor- in the biosphere (Boudet 1998, Monties measurement. These uncertainties arise porate non-typical phenylpropanoid pre- 1991). The most important function of from the complexity of lignin synthesis cursor molecules, the results of biotechno- lignin in plants is as a structural compo- and the resultant complexity of lignin mol- logical manipulation of the pathway have nent to lend strength and rigidity to the ecules. While generalized structures for yielded unexpected results and unique cell wall. It is also important in limiting lignin have been drawn, it is not yet possi- lignin structures (Boudet 1998, Ralph et water loss by reducing permeability of the ble to definitely determine the complete al. 1998). Apparently lignin plays such an cell wall, and in impeding disease organ- structure of any isolated lignin molecule, important role in plant development that isms (Dean and Eriksson 1992, Zeikus let alone the structure of lignin in the plant alternative routes and precursors can be 1980). All of these attributes are desirable cell wall. Because there is no standard used to provide the amount of lignin nec- from the perspective of plant function and lignin structure for reference, measure- essary for normal development. When survival, but limit the nutritional value of ment of lignin concentration is empirical lignin concentration has been significantly the plant for herbivores. and very dependent on methodology. All reduced through biotechnology, non- Fiber is a nutritional entity which is of these ambiguities have made it very dif- viable plants result (Jung and Ni 1998). defined as much by its biological proper- ficult to clarify the roles of lignin in plant Deposition of lignin in the cell wall of ties as its chemical composition (Van growth and development, and the mecha- grasses appears to involve ferulate esters Soest et al. 1991). With regard to forages, nism by which lignin limits cell wall of arabinoxylans as nucleation sites. In it has been traditionally defined as the digestibility. annual ryegrass (Lolium multiflorum complex of dietary nutrients that are rela- Lignin can be characterized as a polymer Lam.), lignin cross-links to ferulates con- tively resistant to digestion and are slowly formed from monolignols derived from the sisted only of structures that would form if and only partially degraded by herbivores phenylpropanoid pathway in vascular monolignols reacted with the ferulates (Chesson and Forsberg 1988, Van Soest plants. Recent reviews provide excellent directly rather than polymeric lignin react- 1982). By this definition, fiber is com- coverage of the process and biochemistry ing with ferulate esters (Ralph et al. 1995). posed of structural polysaccharides, wall of lignification (Baucher et al. 1998, This ferulate mediated cross-linking struc- proteins, and lignin. The main antiquality Boudet 1998). Lignin is deposited in the ture is illustrated in Fig. 2. Unlike ferulic role of lignin in forages is in limiting cell walls of plants as part of the process of acid, p-coumarate (the other major cell- digestion of the structural polysaccharides cell maturation after cell elongation has wall hydroxycinnamic acid) in grasses cellulose and hemicellulose (Hatfield et al. ceased. Based on difficulty of lignin does not have a lignin/polysaccharide 1999, Moore and Hatfield 1994). extraction from the cell wall, it has been cross-linking function and most p- Lignification controls the amount of fiber concluded that lignin is chemically linked coumarate is esterified to lignin rather that can be digested and, therefore, has a to carbohydrates and possibly proteins in than polysaccharide (Ralph et al. 1994). direct and often important impact on the the cell wall to form large macromole- Because of complex lignin structure and digestible energy (DE) value of the forage cules. The only cross-linking structure of linkage to other cell-wall polymers, analy- (Jung and Allen 1995). Lignification also lignin to other cell-wall components that sis of lignin concentration in forages is influences the amount of dry matter that has been definitively characterized is the difficult. The standard method used in ani- can be consumed by an animal (Mertens linkage of lignin to arabinoxylans in grass- mal and agronomic sciences is the acid 1994). The undigested portion of the forage es via ferulic acid molecules (Ralph et al. detergent lignin (ADL) method, of which 1995), although chemical extraction data passes slowly through the digestive system ∝ there are sulfuric acid hydrolysis and per- and contributes to the fill effect of the diet. does point toward -ether linkages of manganate oxidation versions of the The greater the concentration of undegrad- lignin directly to polysaccharides method (Van Soest 1967, Goering and able fiber in the diet the less dry matter an (Watanabe 1989). Undoubtedly there are Van Soest 1970). The traditional lignin animal can consume. Therefore, lignifica- other lignin cross-linking structures involv- method used in wood chemistry, Klason tion impacts forage nutritive value by both ing both polysaccharides and proteins. lignin, was long believed to give inaccu- decreasing DE concentration and limiting The basic pathway of lignin biosynthe- rate results with forages because of per- dry matter intake (Moore et al. 1993). sis in plants is illustrated in Fig. 1. ceived contamination (Van Soest 1967, In this paper we discuss the biochem- Guaiacyl-type lignin typically comprises Lai and Sarkanen 1971). It has now been istry of lignin and how it affects the 95+% of the lignin found in gym- shown that the Klason lignin method does digestibility of forage fiber. We also con- nosperms, whereas angiosperms generally not suffer from contamination when sider factors that affect lignification and deposit significant amounts of both guaia- applied to forages and that the ADL therefore the quality of forages. Finally, cyl- and syringyl-type lignins. Small method under-estimates lignin concentra- we discuss management implications of amounts of p-hydroxyphenol lignin are tion (Kondo et al. 1987, Hatfield et al. lignin and suggest strategies for improving present in most plants. The 5-hydroxygua- 1994, Lowry et al. 1994). This under-esti- forage quality. iacyl-type lignin is only known to accu- mation is especially severe for grasses. mulate in the bm3 (brown midrib) mutant The problem with the ADL method of corn (Zea mays L.) (Lapierre et al. appears to be solubilization of lignin at the 1988). This particular lignin product accu- acid detergent fiber step of the procedure mulates in bm3 corn because the gene that

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 421 for cell-wall digestion as lignin does not directly impact digestibility of plant cell solubles. The reason DM digestibility is negatively correlated with lignin concentration is because the concentration of lignin always increases as cell-wall concentration rises, and forage cell walls are always less digestible than cell solubles. The negative relationship of lignin concentration and cell-wall digestibility is true regardless of the method of lignin analysis employed and has been observed with in vivo and in vitro measures of digestibility (Jung et al. 1997). Generally, the slope of this negative relationship is less for legumes than grasses, suggesting that lignin is more inhibitory of digestion in grasses (Van Soest 1964, Buxton and Russell 1988). This conclusion has been drawn primarily from research where lignin was measured as ADL and it should be considered suspect because the ADL method under-estimates lignin concentration more severely in grasses than legumes. The opposite conclusion may in fact be true. Microscopic studies suggest that lignin may be more inhibitory in legumes than grasses because lignified legume tissues are virtually indigestible whereas thick-walled, lignified grass tissues can be digested to leave only thin- walled indigestible residues (Engels 1989, Engels and Jung 1998). Several mechanisms have been suggested for how lignin may inhibit cell-wall digestion, however, it is now generally Fig. 1. A schematic representation of the lignin biosynthetic pathway starting from phenylalanine (Phe). Tyrosine is the second precursor to this pathway via tyrosine ammonia agreed that lignin simply acts as a physical lyase to form p-coumaric acid. The enzymes involved in lignin synthesis include: PAL, barrier to the microbial enzymes reaching phenylalanine ammonia lyase; C4H, cinnamate 4-hydroxylase; C3H, 4-coumaroyl hydrox- their target polysaccharides (Chesson ylase; OMT, O-methyltransferase; F5H, ferulate 5-hydroxylase; 4CL, 4-coumarate-CoA 1993, Jung and Deetz 1993). Previous ligase; CCoA3H, 4-coumaroyl-CoA hydroxylase; CoAOMT, caffeoyl-CoA O-methyltrans- hypotheses concerning toxicity, exclusion ferase; CCR, cinnamoyl-CoA reductase; CAD, cinnamyl alcohol dehydrogenase, and per- of water-soluble enzymes due to oxidase. hydrophobicity, etc. can probably be discounted. Questions still remain as to how (Kondo et al. 1987, Lowry et al. 1994). tion the hydroxycinnamic acids into their lignin structure, cross-linkage to other Recent work indicates that Klason lignin 2 linkage forms. Ether-linked hydroxycin- cell-wall polymers, and deposition and is a much more accurate method for deter- namic acids can also be measured by diox- distribution in the wall may modify the mining lignin concentration of forages ane-HCl hydrolysis (Scalbert et al. 1985). impact of lignin as a physical barrier to than ADL (Jung et al. 1999). However, Unfortunately, the other 5 cross-linking cell-wall digestion. This is perhaps best lignin concentration estimates from these structures of ferulic acid in lignin/polysac- illustrated by the fact that while the nega- 2 methods are positively correlated. charide bridges cannot currently be quanti- tive relationship of lignin concentration is Analysis of the hydroxycinnamic acids fied (Ralph et al. 1992). always observed when examined across in cell walls and their cross-linking to forage samples of different maturities, lignin involves 2 steps because these com- when plant maturity is similar (i.e. - for- pounds are present in more than 1 structur- Lignin and Forage Quality ages from breeding studies, corn silage, al form in the cell wall. Ferulates and p- etc.) large differences in lignin concentra- coumarates that are only ester-linked to It is a well established fact that lignin tion and cell-wall digestibility are polysaccharide or lignin are extracted with concentration of forages is negatively cor- observed but lignin and digestibility are alkali at room temperature (Hartley 1972, related with digestibility (Jung and Deetz often not correlated (Jung and Vogel 1992, Jung and Shalita-Jones 1990). Extraction 1993). While this relationship has been Jung and Buxton 1994, Jung et al. 1994). with stronger alkali at 170¡C cleaves both reported for both dry matter (DM) and Obviously there must be modifying factors ester- and ether-linked hydroxycinnamic cell-wall digestibility (Van Soest 1964, which influence the inhibitory effect of acids (Iiyama et al. 1990). A combination Smith et al. 1972), it only has significance lignin on cell-wall digestion. of these extractions can be used to parti-

422 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 appears likely that ferulate cross-linking of lignin to polysaccharide does influence cell-wall digestibility.

Factors Affecting Lignification

Within the greater context of forage quality there are a large number of factors that can influence the nutritive value of forage. These can be arranged into a hierarchy that indicates the relative dependence of the various levels involved (Fig. 3). It should be realized that all of these processes are dynamic and that there are feedback mechanisms functioning from Fig. 2. Illustration of the cross-linking structure in grasses where ferulate esters of arabi- higher to lower levels. Consequently, there noxylan form bridges to lignin. The linkage shown between lignin and ferulic acid is the are a large number of interactions that can 4-O-§ structure. The peroxidase/H2O2 reaction which catalyzes the cross-links also yields occur which may confound attempts to 8-O-4, 5-§, 8-5, 5-5, and 8-§ structures. The 4-O-§ linkage accounts for only about one sort out the effects of various factors on quarter of the cross-links between feruloylarabinoxylan and lignin, but it is the only one forage nutritive value. The effects of that can be quantified because it yields intact ferulic acid after high-temperature alkaline lignin on forage quality can be altered and, hydrolysis (Ralph et al. 1992). therefore, manipulated at any level in the hierarchy of factors affecting nutritive It was proposed by Jung and Deetz Vitman), and corn (Jung and Vogel 1992, value. (1993) that lignin composition, as mea- Jung and Buxton 1994). This may be sured by the syringyl-to-guaiacyl lignin because ferulate cross-links form early in Ecosystem ratio, would alter the inhibitory impact of grass development and subsequent deposi- The ecosystem level factors that we are lignin on cell-wall digestion because bm tion of lignin and cell-wall polysaccha- concerned with in regard to forage quality mutants have more digestible cell walls rides dilute cross-link concentrations are the edaphic, climatic, and biotic fac- and a reduced syringyl-type lignin con- (Morrison et al. 1998). However, using a tors associated with a given environment tent. However, because bm mutants also corn cell culture model system Grabber et that determine the potential plant commu- have less total lignin and generally slight- al. (1998) have demonstrated that reduced nities that can be grown. The ecosystems ly lower cell-wall concentrations (Cherney ferulate cross-linking will increase cell- in which forages are grown vary from the 1990), the bm mutants are not suited to wall degradability. Recently Casler and very simple to the highly complex and test the validity of the lignin composition Jung (1999) found that smooth bromegrass diverse. At one end of this spectrum are hypothesis. Results from 2 transgenic (Bromus inermis Leyss) genotypes select- highly uniform and inherently productive tobacco (Nicotiana tabacum L.) experi- ed for reduced ferulate cross-linking environments. These can be easily manip- ments where O-methyltransferase and cin- exhibited improved cell-wall digestibility ulated through management of soil fertili- namyl alcohol dehydrogenase activities compared to genotypes with high concen- ty, water, and pests such that the environ- were down-regulated showed improved trations of ferulate ether cross-links. It ment can be modified to a large extent to cell-wall digestibility when the syringyl- to-guaiacyl lignin ratio was reduced but lignin concentration was not altered (Bernard Vailhe et al. 1996, 1998). However, no change in cell-wall digestibility was observed in an Arabidopsis thaliana [(L.) Heynh] mutant that deposits only guaiacyl-type lignin rather than the normal mixture of syringyl- and guaiacyl-type lignins (Jung et al. 1999). Obviously the impact of lignin composition on digestibility is still unresolved. Jung and Deetz (1993) also proposed that ferulate cross-linking of lignin to polysaccharide in grasses was crucial for lignin to impede cell-wall digestion. Attempts to show negative correlations of ferulate cross-linking (measured as ether- linked ferulic acid) have met with limited success in switchgrass (Panicum virgatum L.), big bluestem (Andropogon gerardii Fig. 3. Hierarchy of factors affecting forage quality.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 423 suit the needs of a specific and generally introduced plant community. In contrast are extremely diverse and inherently less productive environments. These environments are not easily manipulated and consequently have limited potential for modification through management. Forage production within these environments generally involves extensive management of native plant communities. Management of forage quality in these environments is generally accomplished through grazing management and to a lesser extent, other forms of vegetation management.

Plant Species As described earlier, plant communities utilized for forage vary from simple monocultures of cultivated species to complex and diverse native plant communities. The concentration and composition of lignin varies greatly among genera, species, and, to some extent, within species comprising forage plant communities. Fig. 4. Relationship between lignin concentration of fiber and fiber digestibility in legumes Nearly all important cultivated and and grasses (Adapted from Smith et al. 1972). many native forages belong to either the grass family (Poaceae) or the legume family (Fabaceae), which are of the subclasses digestible energy when making compar- improvement in forage quality through Monocotyledonae and Dicotyledonae, isons between grasses and legumes. either direct or indirect modification of respectively. There are large differences in Other dicotyledonous forbs have lignins lignin by breeding. Selection for decreased lignification between grasses and legumes that are more similar to those of legumes lignin in alfalfa (Medicago sativa L.) on a and also differences in the impact of lignin than of grasses (Higuchi 1990). Most whole-plant basis resulted in changes in per se on their forage quality (Fig. 4). dicotyledonous shrubs and trees have rela- both fiber concentration and plant mor- Lignin concentration of legumes often tively high lignin concentrations and con- phology (Kephart et al. 1989, 1990). appears comparable to that of grasses comitantly low fiber digestibility. This is Alfalfa lines selected for low lignin had when expressed as a proportion of dry reflection of the fact that they contain shorter stems, higher leaf to stem ratios matter. However, when expressed as a more heavily lignified tissues than do and higher concentrations of fiber in stem proportion of fiber, legumes demonstrate a herbaceous species. The foliage of some bases than high lignin lines. This selection wider range of lignin concentrations that browse species, however, can often be for lower acid detergent lignin in alfalfa are generally higher than those of grasses quite digestible (Chriyaa et al. 1997). resulted in variable and inconsistent (Buxton and Brasche 1991, Buxton and Cool-season and warm-season grasses effects with respect to improving fiber Russell 1988). As indicated earlier, this have similar lignin and fiber composition digestibility (Jung et al. 1994). difference may be a result of analytical (Jung and Vogel 1986, 1992). The primary Improvements made by selection for problems regarding lignin measurement. distinction between cool- and warm-season high dry matter digestibility in grasses The range in fiber digestibility is similar grasses is that warm-season species gener- have been related to changes in lignifica- between legumes and grasses indicating ally have higher fiber and, therefore, higher tion in some cases. In smooth bromegrass, that there are qualitative differences lignin concentrations at comparable growth selection for improved dry matter between the 2 families in the way lignin stages. Anatomical differences between digestibility was correlated with changes interacts with other fiber components cool- and warm-season grasses appear to in lignification (Casler and Carpenter (Buxton et al. 1987, Buxton 1989). account for most of the difference in fiber 1989, Jung and Casler 1990) and it was The most important difference between composition between the 2 types of grasses concluded that there may be some poten- grasses and legumes is in the concentra- (Akin 1989). Warm-season grasses parti- tial for improving digestibility by selection tion of fiber. Grasses have much higher tion more dry matter into lignified tissues for low lignin. However, in switchgrass, fiber concentrations than legumes and with thickened secondary walls. substantial improvements in dry matter conversely a lower concentration of readi- Even within a single species or cultivar digestibility have been made without ly digestible cell contents (Buxton and there may be significant genotypic differ- changing either the concentration of fiber Russell 1988). So even though lignin has a ences in lignification since many forage or lignin (Moore et al. 1993). Selection for negative impact on the fiber digestibility cultivars are synthetic populations (Casler high digestibility has resulted in changes of legumes, the fact that they contain and Vogel 1999, Vogel and Pedersen in fiber digestibility independent of lignin much less fiber than grasses lessens its 1993). These differences provide the concentration, but may be related to how impact on overall digestible energy con- genetic variability necessary to make lignin interacts with the cell-wall polysac- centration. For these reasons, lignin con- improvements in the forage quality of charides (Gabrielson et al. 1990). centration is not a good indicator of these species through traditional breeding Ploidy level has been demonstrated to approaches. There are several examples of have an impact on lignin concentration of

424 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 forage grasses. In Brachiaria, lignin con- Molecular geneticists have recently Moisture deficit generally decreases lig- centration was higher in tetraploid than in altered lignin biochemistry of tobacco and nification, although this effect occurs diploid accessions (do Valle et al. 1988). alfalfa using anti-sense gene modification largely as a function of changes in plant However, there were no differences in techniques (Halpin et al. 1994, Sewalt et development and morphology (Buxton fiber digestibility among the ploidy levels. al. 1997b, Sewalt and Dixon 1997). Down and Casler 1993). In alfalfa, total-cell wall In Napiergrass (Pennisetum purpureum regulating the activities of phenylalanine concentration increased with increasing Schumach.), differences in morphology ammonia-lyase and cinnamate 4-hydroxy- irrigation levels, but cell-wall composition were observed among triploid, tetraploid, lase reduced lignin concentration and was unaffected (Halim et al. 1989). and hexaploid lines, but the chemical com- resulted in improved fiber digestibility in Differences in forage digestibility between positions of various morphological struc- transgenic tobacco (Sewalt et al. 1997a). stressed and non-stressed plants were tures were similar (Schank and In alfalfa, reducing the activities of the attributed to delayed plant maturity caused Chynoweth 1993). methylating enzymes COMT and caf- by water stress. Excess moisture can also feoyl-CoA O-methlytransferase resulted in reduce whole-plant lignin concentration. Biochemistry and Physiology only modest changes in lignin concentra- Growing alfalfa under conditions of Genotypic differences among forages tion and fiber digestibility (Sewalt and excess moisture stunted plant development are initially expressed at the biochemical Dixon 1997). Molecular approaches such which resulted in lower concentrations of level in response to environmental stimuli. as these offer great promise for developing lignin and other fiber components The biosynthesis of lignin as described forage cultivars with improved quality (Buscaglia et al. 1994). earlier is a complex process involving a characteristics (Dixon et al. 1996). Light intensity and quality also can number of enzyme-mediated reactions However, it is unlikely that transgenic for- affect lignification of forages. Low light (Boudet 1998). Lignin concentration and age cultivars will be available to producers decreases lignification on a whole-plant composition is regulated by these enzymes any time in the near future. basis (Buxton and Fales 1994). As with and can be altered by attenuating their Physiological responses to several envi- most other environmental responses, this activities (Dixon et al. 1996). ronmental factors may affect the extent of decrease is generally related to delayed A well-known example of biochemical- lignification that occurs within a forage development of the plant rather than ly altered lignin is the bm mutation. The plant community. Temperature, soil mois- changes in lignification at the cellular bm mutation is characterized by darkened ture, light, and soil fertility can have either level (Buxton and Casler 1993). Shaded coloration of the leaf mid vein and usually direct or indirect effects on lignification plants tend to be less lignified (Buxton is related to lowered concentrations and (Buxton and Casler 1993, Nelson and 1996). However, the effects of light inten- altered composition of lignin (Cherney et Moser 1994). sity on lignification and fiber digestion are al. 1991). It occurs naturally in corn and Lignification tends to increase in plants not always consistent. Henderson and has been induced through mutagenesis in grown under warmer temperatures. This Robinson (1982) reported that increasing sorghum (Sorghum bicolor (L.) Moench.) appears to be related mostly to increased light intensity had variable effects on lig- (Fritz et al. 1981, Porter et al. 1978) and activities of lignin synthetic enzymes at nification and fiber digestibility of sub- pearlmillet (Pennisetum americanum (L.) higher temperatures (Buxton and Fales tropical grass species. Kephart and Buxton Leeke)(Cherney et al. 1988). The pheno- 1994), but may also be related in some (1993) similarly reported that the effects typic effects of bm mutations have been instances to increased partitioning of plant of shading on lignification of a number of well characterized (Fritz et al. 1990, dry matter to more lignified tissues (Cone temperate and warm-season grasses was Gerhardt et al. 1994, Moore et al. 1989) and Engels 1990, da Silva et al. 1987). inconsistent, however, in their study shad- and have been related to altered enzyme Wilson et al. (1991) reported that growing ing consistently resulted in improved dry activities (Bucholtz et al. 1980, Grand et al. a number of tropical and temperate forage matter digestibility. 1985). The bm trait is of particular interest species under a higher temperature regime Light quality apparently does not impact in forages because it is usually associated did not alter the proportion of various tis- lignification, but may influence fiber with relatively significant increases in fiber sues, but rather appeared to increase the digestibility independent of lignification. digestibility (Akin et al. 1986, Cherney et intensity of lignification. Similar results Jung and Russelle (1991) grew orchard- al. 1991, Wedig et al. 1987). Commercial were reported for tall fescue (Festuca grass (Dactylis glomerata L.) and birds- varieties of bm corn and sorghum have arundinacea Schreb.) grown under 4 tem- foot trefoil (Lotus corniculatus L.) under been developed and have been demonstrat- perature regimes (Akin et al. 1987). low pressure sodium or flourescent-incan- Increasing temperature did not affect leaf ed to result in improved animal perfor- descent lights in a study designed to evalu- anatomy, but negatively affected the pro- mance (Grant et al. 1995, Lusk et al. 1984, ate the effects of light quality on fiber portion of tissues degraded. Fales (1986) Weller and Phipps 1986). composition and digestion independent of found that growing tall fescue under Only recently, however, have the genet- plant age. They found that fiber digestibil- increasing temperatures did not affect lig- ic mechanisms involved in bm mutations ity of orchardgrass decreased under sodi- nification, but increased indigestible fiber been studied. In the bm mutant of corn, um lamps. The effect on birdsfoot trefoil 3 concentration. Henderson and Robinson the trait has been linked to changes in the fiber digestibility was the opposite. In both (1982) reported that increasing growth structure of the O-methyl transeferase cases, changes in fiber digestion were not temperatures of subtropical grass species (COMT) gene (Vignols et al. 1995). This related to changes in lignification. gene codes for the enzyme that catalyzes resulted in increased lignification and decreased fiber digestibility. Despite the Soil nutrients can have both direct and the methylation of 5-hydroxyferulate indirect effects on lignification. Deficiencies (Boudet 1998). The mutation lowers the apparent inconsistencies of the effects of temperature on lignification, the negative of many plant nutrients impede growth and activity of the resulting enzyme and development in a manner similar to other results in a lower lignin concentration and effect of increasing temperature on fiber digestibility appears to be consistent (Akin plant stresses (Miller and Reetz 1995). an altered lignin composition (Vignols et Therefore, lignification is generally reduced al. 1995). and Chesson 1989, Ford et al. 1979).

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 425 in plants growing under conditions of low ondary thickening the actual quantity of Morphology soil fertility. However, there is little evi- lignin may be higher in secondary walls Lignification increases as plants mature dence to suggest that fertilization affects lig- due to their large volume (Terashima et (Brink and Fairbrother 1994, Cherney et al. nification when nutrient levels are adequate al.1993, Wilson 1993). 1993, Cuomo et al. 1996, Hockensmith et to support normal plant growth or that The process of lignification occurs rela- al. 1997). This is largely a function of manipulating soil fertility would be a useful tively rapidly in growing tissues. In changes in the morphology of the plant, management tool for altering lignification. sorghum leaf blades, lignin was present in and to a lesser degree, the aging of plant Nitrogen fertilization has variable effects very low concentrations in the leaf inter- tissues (Anderson 1985). Changes in plant on lignification depending on plant species calary meristem, but increased dramatical- morphology are related to ontogeny and the environment in which it is grown. ly to near maximum in cells adjacent to (Nelson and Moser 1994). In grasses, Nitrogen fertilization had little or no the meristem less than 1 day old (Volenec developmental morphology is character- impact on lignin concentration of pearlmil- et al. 1986). Lignification in developing ized by 4 primary growth stages: 1) vege- let stover (Powell and Fussell 1993). In stems is somewhat slower. In elongating tative, 2) elongation, 3) reproductive, and alfalfa, lignin concentration was unaffected corn internodes, lignification was initiated 4) seed ripening (Moore et al. 1991, Moore by increasing inorganic nitrogen available within 2 days after elongation began and and Moser 1995). During vegetative devel- for plant growth (Cherney et al. 1994). by 4 days had proceeded into all elongated opment, the stems remain near the crown Plant responses to nitrogen may be affect- tissues (Morrison and Buxton 1993). and the above ground portion of the plant ed by other environmental factors. Collins Lignin concentration varies greatly from consists primarily of leaves. During elon- et al. (1990) observed an increase in fiber one cell type to another. Consequently, gation stem internodes lengthen, increasing concentration of oat (Avena sativa L.) for- degradability of plant tissues is variable the proportion of stem tissue in the canopy age with increasing nitrogen fertilizer in 1 and related to lignin concentration. relative to leaves. During the later 2 environment, but small decreases occurred Tissues with high lignin concentrations growth stages, inflorescences develop, fer- in response to nitrogen fertilizer in 3 other include the epidermis (grasses), xylem, tilization occurs, and seeds develop. environments. However, lignin concentra- and sclerenchyma (Akin et al. 1990, Development of legumes and other herba- tion was unaffected by fertilization. Buxton and Redfearn 1997, Chesson et al. ceous dicots also occurs in vegetative and Sanderson et al. (1995) reported a signifi- 1986, Twidwell et al. 1991). These tissues reproductive stages (Kalu and Fick 1981). cant interaction between plant density and are relatively undegradable by rumen During vegetative development, stem nitrogen fertilization. In their experiment, microbes (Grabber el al. 1992) and com- growth occurs simultaneously with leaf lignin concentration increased with prise a large proportion of the indigestible development. Continued cambial growth in increasing plant density in corn fertilized fraction of forages (Buxton and Redfearn dicot stems results in accumulation of indi- with nitrogen. However, lignin concentra- 1997, Twidwell et al. 1991, Akin and gestible xylem tissues. In determinate tion was unaffected by plant density in Chesson 1989). Other tissues such as mes- species, stem growth ceases with the onset unfertilized corn. ophyll and other types of parenchyma are of reproductive growth, while in indetermi- Sulfur fertilization has been reported to not lignified, contain a large proportion of nate species, reproductive and vegetative decrease lignification and improve fiber metabolites, and are highly degradable. growth may occur simultaneously. digestibility in sorghum (Ahmad et al. Between these extremes are tissues with As plants mature, the ratio of leaves to 1995), but did not affect either lignin con- intermediate and variable degradability stems decreases (Albrecht et al. 1987, centration or fiber digestibility in tall fes- such as phloem and collenchyma (Akin Nordkvist and Åman 1986, Martiniello et cue or orchardgrass (Chestnut et al. 1986). 1989, Wilson 1993). al. 1997). Because stems contain more lig- It has been suggested that fiber concentra- The digestibility of a forage represents the nified structural tissues and less metaboli- tion in tall fescue may be related to the relative contributions of various plant tissues cally active tissues than leaves, the ratio of nitrogen to sulfur levels available to total herbage dry matter (Magai et al. digestibility of stems is generally much for plant growth (Sweeney and Moyer 1994). The higher the proportion of structur- less than that of leaves (Akin 1989, 1997). However, no such relationship al and other lignified tissues, the lower the Twidwell et al. 1988). Using a lignin stain occurred in corn fertilized with varying digestibility of the forage (Akin 1989). and image analysis, Twidwell et al. (1991) rates of nitrogen and sulfur (O’Leary and A significant proportion of the differ- characterized the anatomy of switchgrass Rehm 1990). ences among species in lignin concentra- leaves and stems. They reported that stems tion and fiber digestion reflect differential contained a greater proportion of structural partitioning among various tissues. Warm- Plant Anatomy and other lignified tissues than leaves and season grasses for example, tend to have a that these tissues were more resistant to Lignification occurs during the process higher proportion of lignified tissues than degradation when incubated in buffered of cell differentiation and is generally cool-season grasses (Akin 1989). Differences rumen fluid for 24 and 48 hours. Bruckner coincident to secondary wall formation in fiber digestibility of warm-season and and Hanna (1990) reported similar find- (Iiyama et al. 1993). Lignin deposition is cool-season grasses have been related to ings in a study on the anatomy and initiated in the corners of the cell adjacent anatomical characteristics. Warm-season digestibility of leaves and stems of small to the middle lamella and proceeds inward grasses generally have a higher proportion of grain species. into the primary and secondary walls. structural and other indigestible tissues than Lignin concentration increases with Lignification is always preceded by depo- cool-season grasses (Wilson and Hattersley maturity in grasses (Cherney et al. 1993, sition of structural carbohydrates and lags 1989, Wilson and Kennedy 1996). Foster et al. 1996, McBee and Miller behind development of the currently 1993, Titgemeyer et al. 1996) and legumes developing cell wall layer. Because of (Bidlack and Buxton 1992, Kratchunov this, lignin concentration is usually higher and Naydenov 1995). Quantitatively, the in the primary than the secondary wall. changes in lignification that occur as However, in cells with pronounced sec-

426 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 plants mature have the largest impact on (Hirschfeld et al. 1996, Norton et al. 1997). Akin, D.E., W.W. Hanna, and L.L. Rigsby. forage quality of the factors that can be Again, decisions with regard to defoliation 1986. Normal-12 and brown midrib-12 modified by forage management. In grass- management need to be weighed against sorghum: variations in tissue digestibility. Agron. J. 78:827Ð832. es, lignin concentrations more than double other factors such as yield and effects on Akin, D.E., S.L. Fales, L.L. Rigsby, and M.E. as plants develop from vegetative to repro- plant persistence. In addition to defoliation, Snook. 1987. Temperature effects on leaf ductive stages of growth while in legumes, maturation of forages can be controlled by anatomy, phenolic acids, and tissue digestibility the increase is somewhat less dramatic burning, clipping, and application of plant in tall fescue. Agron. J. 79:271Ð275. (Albrecht et al. 1987, Bidlack and Buxton growth regulators (Mitchell et al. 1996, Akin, D.E., N. Ames-Gottfred, R.D. Harley, 1992, Brink and Fairbrother 1994). Roberts and Moore 1990). However, none R.G. Fulcher, and L.L. Rigsby. 1990. Microspectrophotmetry of phenolic compounds of these other treatments has the impact of in Bermudagrass cell walls in relation to rumen Management Implications properly timed defoliation. microbial digestion. Crop Sci. 30:396Ð401. The goal of managing forage quality is There are a number of postharvest treat- Albrecht., K.A., W.F. Wedin, and D.R. Buxton. not necessarily to minimize lignin concen- ments that can be used to improve the 1987. Cell-wall composition and digestibility of alfalfa stems and leaves. Crop Sci. 27:737Ð741. tration, but rather to minimize its impacts digestibility of fiber in highly lignified forages. These have been reviewed in some Anderson, B. 1985. The influence of aging on for- on fiber digestion and intake. To some age quality of individual switchgrass leaves and extent, management can be used to manip- detail by Fahey et al. (1993). There are 4 stems. p.946-949. In Proceedings of the XV ulate lignification and its impact on fiber basic strategies employed in postharvest Intl. Grassl. Congr. digestion at each of the levels discussed in treatments that have been developed to Anderson, B., J.K. Ward, K.P. Vogel, M.G. the previous section (Fig. 3). However, lessen the impact of lignin on fiber diges- Ward, H.J. Gorz, and F.A. Haskins. 1988. Forage quality and performance of yearlings from a practical perspective, the most use- tion. These include alkaline hydrolysis, enzymatic hydrolysis, oxidation, and micro- grazing switchgrass strains selected for differing ful management practices for this purpose digestibility. J. Anim. Sci. 66:2239Ð2244. are manipulation of the plant community bial treatments. Of these, alkaline hydrolysis Baucher, M., B. Monties, M. Van Montagu, and such that it contains more desirable (less is by far the most common and practical. W. Boerjan. 1998. Biosynthesis and genetic lignified and more digestible) plants, har- Alkaline treatments have been demon- engineering of lignin. Crit. Rev. Plant Sci. vest management to maintain plants in a strated to improve the digestibility of 17:125Ð197. grasses, but not legumes. The reagents Bernard Vailhe, M.A., J.M. Besle, M.P. Maillot, vegetative state of development, and when A. Cornu, C. Halpin, and M. Knight. 1998. necessary, postharvest treatments to most commonly used for this purpose are ammonia and various hydroxides (Fahey Effect of down-regulation of cinnamyl alcohol improve the digestibility of low quality dehydrogenase on cell wall composition and on harvested forages. et al. 1993). Ammoniation of forages can degradability of tobacco stems. J. Sci. Food Species and variety selection are extreme- be accomplished using anhydrous ammo- Agr. 76:505Ð514. nia applied in gaseous form or by incorpo- ly useful tools for managing forage quality Bernard Vailhe, M.A., C. Migne, A. Cornu, rating urea with the forage (Fritz et al. M.P. Maillot, E. Grenet, and J.M. Besle. within the constraints of an ecosystem. 1991, Moore et al. 1985, Sewalt et al. 1996. Effect of modification of the O-methyl- Obviously, other factors such as yield, sea- 1996). Ammoniation increases fiber transferase activity on cell wall composition, sonal growth distribution, and establishment ultrastructure and degradability of transgenic digestibility and crude protein concentra- and production costs may be as or more tobacco. J. Sci. Food Agr. 72:385Ð391. tion whereas treatment with sodium Bidlack, J.E. and D.R. Buxton. 1992. Content important than forage quality. However, hydroxide only increases fiber digestion, altering species composition, either by seed- and deposition rates of cellulose, hemicellulose, however, sodium hydroxide treatment and lignin during regrowth of forage grasses ing or vegetation manipulation, can greatly generally results in greater increases in and legumes. Can. J. Plant Sci. 72:809Ð818. enhance the yield of available nutrients and fiber digestibility than ammoniation. Of Boudet, A. M. 1998. A new view of lignification. productivity of the system. The goal is to the alkaline treatments used to improve Trends in Plant Sci. 3:67Ð71. develop a plant community with inherently Brink, G.E. and T.E. Fairbrother. 1994. Cell forage digestibility, ammoniation is the wall composition of diverse clovers during pri- high quality characteristics. easiest to use. In all cases, chemical treat- Establishment of improved cultivars of mary spring growth. Crop Sci. 34:1666Ð1671. ments used to enhance fiber digestion Bruckner, P.L. and W.W. Hanna. 1990. In vitro adapted species can enhance productivity result in greater improvements when digestibility of fresh leaves and stems of small- of forage-livestock systems and increase applied to poor quality roughages such as grain species and genotypes. Crop Sci. economic returns. Studies have demon- mature grasses and cereal crop residues 30:196Ð202. strated substantial improvements in the than when applied to higher quality for- Bucholtz, D.L., R.P. Cantrell, J.D. Axtell, and performance of beef cattle grazing pas- ages (Klopfenstein 1978). V.L. Lechtenberg. 1980. Lignin biochemistry tures with improved forage quality charac- of normal and brown midrib mutant sorghum. J. Agr. Food Chem. 28:1239Ð1241. teristics (Anderson et al. 1988, Moore et Buscaglia, H.J., H.M. Van Es, L.D. Geohring, al. 1995). Estimates in the value of Literature Cited H.C.A.M. Vermeulen, G.W. Fick, and R.F. increased production realized from Lucey. 1994. Alfalfa yield and quality are improvements in forage quality range affected by soil hydrologic conditions. Agron. J. Ahmad, M.R., V.G. Allen, J.P. Fontenot, and 86:535Ð542. from $50 to $85 per hectare per year G.W. Hawkins. 1995. Effect of sulfur fertiliza- (Vogel and Sleper 1994). Buxton, D.R. 1989. In vitro digestion kinetics of tion on chemical composition, ensiling charac- temperate perennial forage legume and grass Defoliation management is probably the teristics, and utilization by lambs of sorghum stems. Crop Sci. 29:213Ð219. most powerful tool available to producers silage. J. Anim. Sci. 73:1803-1810. Buxton, D.R. 1996. Quality-related characteristics for managing forage quality. Timing of Akin, D.E. 1989. Histological and physical factors of forages as influenced by plant environment harvest and grazing events such that for- affecting digestibility at forages. Agron. J. and agronomic factors. Anim. Feed Sci. Tech. 81:17Ð25. 59:37-49. ages are maintained in a vegetative state is Akin, D.E. and A. Chesson. 1989. Lignification as the most effective and straightforward Buxton, D.R. and M.R. Brasche. 1991. the major factor limiting forage feeding value Digestibility of structural carbohydrates in cool- approach to managing the decline in forage especially in warm conditions. XVI International season grass and legume forages. Crop Sci. quality associated with plant maturity Grassland Congress, Nice, France. p. 1753Ð1760. 31:1338Ð1345.

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430 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 J. Range Manage. 54: 431Ð440 July 2001 Herbivore response to anti-quality factors in forages

K.L. LAUNCHBAUGH, F.D. PROVENZA, AND J.A. PFISTER

Authors are assistant professor, Rangeland Ecology and Management Dept., University of Idaho, Moscow, Ida. 83844; professor, Rangeland Resources Dept., Utah State University, Logan, Utah. 84322; and, research scientist, USDA-ARS Poisonous Plants Research Laboratory, Logan, Utah 84341.

Abstract Resumen

Plants possess a wide variety of compounds and growth forms Las plantas poseen una amplia variedad de compuestos y for- that are termed “anti-quality” factors because they reduce forage mas de crecimiento que son llamadas factores "anti-calidad" value and deter grazing. Anti-quality attributes can reduce a porque reducen el valor del forraje y desalienta el apacentamien- plant’s digestible nutrients and energy or yield toxic effects. to de ellas. Los atributos anti-calidad pueden reducir los nutri- Herbivores possess several adaptive mechanisms to lessen the entes y energía digestibles de la planta o producir efectos tóxicos. impacts of anti-quality factors. First, herbivores graze selectively Los herbívoros poseen varios mecanismos adaptativos para to limit consumption of potentially harmful plant compounds. aminorar los impactos de los factores anti-calidad. Primero, los Grazing animals rely on a sophisticated system to detect plant herbívoro apacientan selectivamente para limitar el consumo de nutritional value or toxicity by relating the flavor of a plant to its compuestos vegetales potencialmente dañinos. Los animales en positive or negative digestive consequences. Diet selection skills apacentamiento dependen de un sistema sofisticado para detec- are enhanced by adaptive intake patterns that limit the deleteri- tar el valor nutricional o la toxicidad de las plantas relacionando ous effects of plant allelochemicals; these include cautious sam- el sabor de la planta con sus consecuencias digestivas positivas o pling of sample new foods, consuming a varied diet, and eating negativas. Las habilidades para seleccionar la dieta aumentan plants in a cyclic, intermittent, or carefully regulated fashion. por los patrones adaptativos de consumo que limitan los efectos Second, grazing animals possess internal systems that detoxify or perjudiciales de los aleloquímicos de la planta, estos incluyen la tolerate ingested phytotoxins. Animals may eject toxic plant precaución de probar nuevos alimentos, consumiendo una dieta material quickly after ingestion, secrete substances in the mouth variada y comiendo plantas de una manera cíclica, intermitente or gut to render allelochemicals inert, rely on rumen microbes to o cuidadosamente regulada. Segundo, los animales en apacen- detoxify allelochemicals, absorb phytochemicals from the gut and tamiento poseen sistemas internos para detoxificar o tolerar la detoxified them in body tissues, or develop a tolerance to the ingestion de fitotoxinas. Los animales pueden expulsar rápida- toxic effects of plant allelochemicals. Understanding the behav- mente el material vegetal toxico después de la ingestión, segre- ioral and metabolic abilities of herbivores suggests several live- gan substancias en la boca o el intestino para hacer inertes a los stock management practices to help animals contend with plant aleloquímicos, dependen de los microbios ruminales para detoxi- anti-quality characteristics. These practices include offering ani- ficar los aleloquímicos, absorber los fitoquímicos del intestino y mals proper early life experiences, selecting the appropriate live- detoxificarlos en los tejidos corporales o desarrollar una toleran- stock species and individuals, breeding animals with desired cia a los efectos tóxicos de los aleloquimicos de la planta. El attributes, and offering nutritional or pharmaceutical products entendimiento de las habilidades de comportamiento y metabóli- to aid in digestion and detoxification. cas de los herbívoros sugiere varias prácticas de manejo del ganado para ayudar a los animales a contender con las carac- terísticas anti-calidad de las plantas. Estas prácticas incluyen el Key Words: anti-quality, conditioned aversions, detoxification, ofrecer a los animales experiencias apropiadas durante las diet selection, forage quality, foraging, grazing behavior, toxic primeras etapas de su vida., seleccionar las especies e individuos plants de ganado mas apropiados, criar animales con los atributos deseados y ofrecer productos nutricionales o farmacéuticos que Forage “quality” is the collective assessment of a plant’s ability auxilian en la digestión y detoxificación. to contribute to growth and production of grazing animals. Rangeland forages usually also contain compounds that limit or adversely affect animal production. These attributes are termed dietary and metabolic mechanisms to exploit plant nutrients and “anti-quality” because they restrict “quality” in some way. overcome the negative effects of anti-quality attributes. Implicit in this delineation is the idea that quality and anti-quality Successful livestock management on rangelands requires an parameters are measured by animal response. The grazing value understanding of plant nutritional content and potential effects of of a specific forage cannot be determined by a few simple labora- anti-quality attributes. However, managers must also be cog- tory procedures because grazing animals possess a variety of nizant of the skills herbivores possess to harvest nutrients and avoid toxins. In this paper, we will examine how anti-quality The publication was made possible by the Grazing Lands Technology Institute plant attributes affect diet selection and intake. We will also of the Natural Resources Conservation Service, Fort Worth, Texas 76115 examine the behavioral and digestive strategies that animals Manuscript accepted 27 Nov. 00.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 431 employ to overcome the anti-quality aspects and gain access to the nutrient and energy resources of plants. Finally, we will suggest management approaches to help animals contend with anti-quality attributes in forages.

Anti-quality Attributes Affect Diet Selection Through Digestive Consequences

Grazing animals are unquestionably sensitive to the quality and anti-quality Fig. 2. When an animal eat a plant it receives digestive feedback in the form of energy, nutri- attributes of plants. For example, animals ents, illness, or toxicosis. If the feedback is positive, preferences are formed to the plant select diets of higher quality than the aver- and if the feedback is negative, aversions are formed. The strength of the preference or age forage available (Arnold 1981, aversion is determined by the magnitude, nature, and timing of digestive feedback. Provenza 1995). Animals also limit their consumption of toxins by selecting plants be eaten in future encounters. The key to distasteful (Fig. 2). This is known as a and plant parts of relatively low toxin con- how animals respond to anti-quality fac- hedonic shift. This “evaluation” system is centration (Provenza 1995, Pfister 1999). tors in plants is therefore centered on the based on processes occurring at a sub-con- How animals sense the quality or toxicity consequences of consumption (Fig. 1). scious level that selectively relate gastro- of forages has been an active area of When a grazing animal smells and tastes intestinal feedback with the flavor, rather research for more than 3 decades. It is a plant, the flavor is either pleasing or dis- than the sight or texture, of a food (Garcia now clear that animals ascribe forage tasteful depending on the animal’s previ- 1989, Provenza 1995). These flavor-con- value by relating plant flavor to positive or ous grazing experiences. If the plant is sequence relationships form the basis for negative digestive consequences new to the animal, its initial hedonic value dietary likes and dislikes. (Provenza 1995, 1996). Grazing decisions depends on its similarity to familiar plants. Once the hedonic value of a plant is are based on a series of interrelated and Grazing animals tend to consume new established, the animal uses its senses of cumulative consequences of consumption. foods that are similar to preferred foods smell and sight to differentiate between A plant’s chemical and structural attrib- and avoid new foods that are similar to plants and seek foods with high hedonic utes dictate its digestive consequences foods they dislike (Launchbaugh and value and avoid aversive foods. Searching because they set the potential digestible Provenza 1993, Provenza et al. 1999). and selective grazing are cognitive process- energy, nutrient yield, or toxicity of the When a plant is eaten, it provides feed- es that can be further reinforced by interac- plants. The digestion and detoxification back during digestion and metabolism. tions with other animals (Thorhallsdottir et abilities of grazing animals, and their The flavor (i.e., taste and odor) of a plant al. 1990a, 1990b). The resulting behavior microbial symbionts, determine the actual becomes more or less pleasing to the ani- patterns lead to increased consumption of yield of nutrients, energy, or toxins. The mal depending on digestive consequences. foods that are likely to yield nutritional results of these plant and animal interac- If consumption of a plant improves the benefit and limited consumption of toxic or tions determine a forage’s palatability or nutrient or energy status of the animal, the low quality plants. hedonic value (i.e., pleasurable and dis- plant flavor becomes more desirable or Grazing preference also depends on the agreeable sensations experienced through pleasing to the animal. If consumption of animal’s nutritional state (Provenza 1995, taste and smell). Palatability, in turn, the plant yields illness or digestive Provenza et al. 1998). When need for a affects the probability that the plant will malaise, the flavor becomes aversive and nutrient is high, preferences for foods containing the nutrient are high. When needs are met, preference declines. For example, lambs fed diets of inadequate sodium, energy, or protein show a strong preference for foods high in sodium, energy, or protein, respectively (Villalba and Provenza 1996, 1999). Thus, an animal’s nutritional state influences its incentive to seek and eat particular plants.

How Plant Anti-quality Attributes Drive Diet Selection and Intake Fig. 1. Digestive consequences are at the center of how animals respond to anti-quality factors in forages. The actual digestive feedback animals receive is determined by plant forage quality and animal digestive and detoxification abilities. The consequences of consumption, Plants possess a wide variety of chemi- in turn, affect diet selection and intake and the nutrients and energy available for animal cal and physical properties that reduce for- growth and maintenance. age value and serve as grazing deterrents.

432 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 From the animal’s perspective, the effects infusions of energy (Villalba et al. 1999, to learn to avoid a nutritious food that of anti-quality attributes can be expressed Smith et al. 1999). A high content of yields toxic effects several days or weeks along a continuum from those that reduce structural carbohydrates, such as cellulose after consumption. There are several exam- the forage nutrient or energy yield to those or hemicellulose, in plants may have little ples in nature where animals prefer less producing toxic or ill effects. How strong- effect on the extent of digestion and yet toxic or nontoxic plants apparently because ly a plant attributes affects diet selection reduce preference and intake by delaying they produce less negative gastro-intestinal or intake therefore depends on the magni- the digestive gain of plant material. consequences upon consumption than tude, timing, or nature of digestive feed- alternatives (Provenza 1995, Pfister 1999). back (Fig. 2). Create Toxic Effects and Food Aversions can also be formed to foods Aversions that are not commonly considered “toxic”. Soluble carbohydrates or nitrogen content Reduce Digestive Benefits Many allelochemicals in rangeland and of some feeds or forages can be so dense Herbivores can quite effectively distin- pastureland plants cause a variety of dele- as to cause gastro-intestinal malaise when guish between plants that differ in terious neurological, metabolic, and ter- eaten in excessive amounts. For example, digestible energy or nutrients (Villalba and ratogenic effects and are therefore termed ruminants often form aversions to fruits Provenza 1996, 1997a, 1997b). Lambs toxic. For discussions on the toxic effects and grains because excessive energy con- formed strong preferences for flavored of plant compounds refer to other papers sumption can cause illness (Provenza straw when consumption was followed by in this volume or a recent review by 1995). Aversions have been demonstrated ruminal infusions of starch (Villalba and Cheeke (1998). These toxic effects can when high doses of energy supplements, Provenza 1997a, Smith et al. 1999), cause severe production losses and yet not such as propionate, were administered to volatile fatty acids (Villalba and Provenza alter diet selection or intake. Strong flavor sheep during a meal (Ralphs and Cheney 1996, 1997b), or protein sources (Villalba aversions are observed only when a phyto- 1993, Villalba and Provenza 1996). and Provenza 1997c). Preference for most toxin stimulates the emetic centers of the Ruminants eating foods high in rumen- rangeland forages is positively correlated midbrain and brainstem that control nau- degradable protein can also experience with digestive benefits (Arnold and Hill sea and vomiting (Grant 1987, Garcia high levels of ruminal ammonia, suffer 1972, Arnold 1981). Phytochemicals that 1989, Provenza et al. 1992, 1994a, malaise, and decrease intake (Prins and reduce the potential digestive yield of a Provenza 1995). Herbivores can readily Beekman 1989, Villalba and Provenza plant can therefore be viewed as anti-qual- form aversions to feeds that stimulate the 1997c). ity factors. For example, lignin (Van Soest emetic system, however they may not be 1994), tannins (Reese 1979), and resinous able to avoid feeds that do not cause nau- compounds (Meyer and Karasov 1991) sea (e.g., cause allergies, bloating, or can reduce forage digestibility by forming lower intestinal discomfort; Garcia 1989, How Animals Contend with insoluble complexes with nutrients. High Provenza et al. 1992). Further evidence to Anti-quality Factors content of indigestible compounds, such the important role of the emetic system is as silica and waxes, can dilute the diges- that anti-emetic drugs can attenuate lithi- To live a healthy life on rangeland, her- tive gain of a plant and reduce preference um chloride-(Provenza et al. 1994a) and bivores must consume nutritious plants (Herms and Mattson 1992). Plant alkaloid-induced (Aldrich et al. 1993) and avoid toxic or low quality plants. digestibility can also be reduced by allelo- aversions in sheep. Foraging animals face the challenge of chemicals that inactivate digestive Aversive post-ingestive feedback causes obtaining nutritious diets in environments enzymes or harm gut microbes. For exam- cattle, sheep, and goats to decrease intake where nutritional value and toxicity vary ple, a wide variety of plants including, of foods containing toxins such as alka- greatly from plant to plant, place to place, potatoes (Solanum tuberosum L.), soy- loids in larkspur (Delphinium spp.; Pfister and time to time. To meet this challenge, beans (Glycine max [L.] Merr.) , cotton- et al. 1997) and tall fescue (Festuca arun- herbivores possess several adaptive behav- seeds (Gossypium L.) , and tomatoes dinaceae Schreb.; Aldrich et al. 1993), ioral mechanisms that limit toxins and (Solanum lycopersicum L.) contain trypsin condensed tannins in blackbrush increase nutrients ingested, and internal systems that detoxify or tolerate ingested and chymotrypsin inhibitors that can inter- (Coleogyne ramossisma Torr.; Provenza et phytotoxins. fere with protein digestion, particularly in al. 1990), essential oils in big sagebrush monogastric animals (Reese 1979, Slansky (Artemisia tridentata Nutt.; Fraker 1999) 1992). Compounds that precipitate pro- and juniper (Juniperus spp.; Pritz et al. Selective Grazing teins, like gossypol (Slansky 1992) and 1997), and allelochemicals in mesquite Selective grazing is the herbivore’s first tannins (Reese 1979, Robbins et al. 1991), (Prosopis glandulosa Torr.; Baptista and line of defense against the negative effects can also decrease digestibility by binding Launchbaugh 2001). Conditioned aver- of plants with toxins or anti-quality attrib- and inactivating digestive enzymes. sions may be mild (i.e., temporary) or utes (Launchbaugh 1996). To make wise Allelochemicals also have anti-microbial strong (i.e., permanent) depending on the grazing decisions, animals must either be effects that inhibit rumen or cecal/colon toxin dose and when and how the toxin born knowing what to eat or avoid, learn microbes thereby reducing digestibility affects the gut and brain. Doses of allelo- appropriate dietary habits from peers, or (Allison 1978). chemicals that make animals intensely ill learn from individual experiences. Diet The magnitude of digestive feedback form stronger aversions than weak emetic selection strategies employed by herbi- can strongly affect intake and preference; stimulants (Ralphs and Cheney 1993, vores have been reviewed in several publications (Provenza et al. 1992, 1998, however, the rate at which nutrients or Launchbaugh and Provenza 1994). To Launchbaugh 1996, Provenza 1995, 1996, energy are liberated may also be impor- form lasting aversions, consequences must tant. Sheep prefer foods paired with rumi- Pfister 1999, Foley et al. 1999). The fol- be experienced within 8 hours of con- lowing discussion provides an overview nal energy infusions immediately after sumption (Burritt and Provenza 1991). It consumption to those paired with delayed with reference to animal responses to anti- is difficult, if not impossible, for animals quality factors in plants.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 433 Instinctive Avoidance larkspur with their mothers, sharply cur- resource and may seldom encounter truly Some researchers contend that animals tailed consumption a few days later novel plants. This allows greater opportu- are instinctively attracted to sweet flavors (Pfister and Gardner 1999), perhaps nity to ‘sort out’ feedback from individual and repelled by bitter flavors (Rhoades because of adverse feedback (Pfister et al. or similar groups of plant species. 1979, Owen 1992). Many plant toxins 1997). Nonetheless, social facilitation can Collectively, these mechanisms enable supposedly taste bitter (e.g., saponins and play a significant role in ameliorating herbivores to discriminate among foods cyanogenic glycosides), have offensive aversions. Ewes and lambs averted to a within a meal. odors (e.g., terpenes), or provoke an pelleted ration ingested more of the ration astringent sensation when eaten (e.g., tan- when feeding with non-averted peers than Adaptive Intake Patterns nins); however, these attributes are not when feeding alone (Thorhallsdottir et al. Sorting out the quality and anti-quality universally repellent (Glendinning 1994). 1990a). Cattle also consumed more of a attributes of forages requires keen diet Sheep (Arnold and Hill 1972) and cattle toxic plant they had been conditioned to selection skills by the herbivore. (Pfister et al. 1996) do not necessarily avoid when feeding with non-averted Successfully navigating the temporal and avoid bitter tastes nor do sheep form peers (Lane et al. 1990). Likewise, lambs spatial variation of forage quality in graz- stronger aversions to bitter than to sweet form stronger aversions to a palatable ing environments can be accomplished by flavors (Launchbaugh et al. 1993). shrub when exposed to the shrub with knowing how much to eat, when to eat, Furthermore, animals acquire preferences other lambs that avoid the shrub than and what else to eat. for bitter and sour flavors when consump- when eating with peers that consumed the tion is followed by calorie enhancement shrub (Provenza and Burritt 1991). Selecting a Varied Diet even when these flavors were not initially Grazing animals have a strong natural preferred (Sclafani 1991). There is consid- Individual Learning about Plant propensity to select diets composed of erable evidence questioning the existence Allelochemicals several plant species and sample available of an innate recognition system for plant Conditioned aversions are powerful plants on a regular basis. This behavior nutritional or toxic qualities based on fla- mechanisms by which animals learn to may increase the likelihood of ingesting vor or any other plant quality. identify and avoid toxic plants (Garcia necessary nutrients (Westoby 1978) and 1989, Provenza et al. 1992). Many range- reduce the potential of overingesting tox- Learning from Mother and Peers land plants contain compounds that pro- ins (Freeland and Janzen 1974). Plants Livestock live in multi-generational duce aversions if eaten in sufficient quan- contain an immense array of allelochemi- groups in which dietary information can tities, as discussed above. Aversions can cals, most of which are toxic if consumed be easily passed from experienced to inex- be easily demonstrated by offering an ani- in substantial quantities (Cheek 1998). perienced animals. Young livestock there- mal a single novel food and inducing gas- However, plants with toxins also contain fore do not require perfect and complete tro-intestinal illness immediately follow- varying kinds and amounts of nutrients. dietary information at birth. Learning from ing ingestion; however, generalist herbi- Thus, diet selection among toxic plants is mother may even begin before young her- vores rarely eat 1 plant per feeding bout a tradeoff between nutrient gain and bivores, take their first bites. Flavors in (Westoby 1978). Several mechanisms potential toxicity (Freeland 1991, uterine fluid can influence food aversions enable herbivores to attribute digestive Provenza 1996). Mammalian herbivores (Smotherman 1982). Mother’s milk is also effects to specific plants rather than to all possess many metabolic pathways to a source of information for young live- the plants in a meal. One way herbivores detoxify phytotoxins, but each pathway is stock. Nolte and Provenza (1992) found apparently accomplish this task is by generally specific to a single or a group of that orphan lambs raised on onion-fla- regarding unfamiliar plants with caution. phytotoxins. Some scientists have suggest- vored milk preferred onion-flavored feed When consuming mixed meals of familiar ed that by eating a variety of plants, ani- later in life. Lambs quickly lean to avoid and novel foods, herbivores preferentially mals spread the ingestion of toxins over harmful novel foods their mother was form aversions (Burritt and Provenza several detoxification pathways (Freeland trained to avoid, and to consume novel 1989, 1991) or preferences (Provenza et and Janzen 1974, Freeland 1991). Varied alternatives consmed by mother (Mirza al. 1999, Villalba and Provenza 2000) to diets may also increase the amounts of and Provenza 1990, 1994). Nursing calves novel dietary items. For example, when some toxic foods that can be eaten because began to eat substantial quantities of lambs experience toxicosis after eating a of interactions between allelochemicals locoweed (Oxytropis spp.; Pfister, unpub- meal of 4 familiar and 1 novel food they that reduce toxicity (Freeland et al. 1985, lished observations) and low larkspur subsequently avoided only the novel food Launchbaugh 1996). (Delphinium nuttallianum Pritz.; Pfister (Burritt and Provenza 1991). When forag- and Gardner 1999) on the same day as ing bouts include several novel plants, Cyclic and Intermittent Intake their grazing mothers; suggesting that plants that dominate the diet are probably The toxic effects of a plant are deter- calves mimicked their mother’s diet. ‘weighted’ more than less consumed mined largely by the amount eaten; but, Young livestock can also learn appropriate plants, even if the minor foods were the ingestion rate may also be important. food choices from other adult animals and responsible for more positive or negative Grazing animals can avoid toxicoses by peers (Thorhallsdottir et al. 1990a, 1990b). feedback (Provenza et al. 1994b). limiting their consumption of a specific Animals are, however, more influenced Furthermore, digestive feedback begins toxic plant each day to allow sufficient by their own dietary experiences than by quickly after consumption and flavor- time for detoxification (Foley et al. 1995, mother or other social models. Lambs con- feedback interactions during a feeding 1999). For example, lambs limit intake of sistently avoided a food after experiencing bout could help animals attribute digestive the toxin lithium chloride as a function of toxicosis even if their mothers readily con- benefits or liabilities to specific plants. the amount of lithium chloride infused sumed the food (Provenza et al. 1993, Finally, grazing livestock on rangelands into their rumen before a meal (Wang and Pfister et al. 1993). Calves that initially ate are usually quite familiar with the forage Provenza 1997). Animals might also vary

434 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 toxic plant consumption daily to limit mouth or gut to render allelochemicals is capable of detoxifying some toxins potential cumulative effects of specific inert, rely on rumen microbes to detoxify through induction of the P450 enzyme toxins. Field studies with tall larkspur allelochemicals, or absorb phytochemicals system (Brattsten 1979). The inducible (Delphinium occidentalis S. Wats.) from the gut and then detoxify them in presence of a nasal detoxification system revealed that consumption above 25Ð30% body tissues. Additionally, animals can may facilitate the consumption of some of the diet for 1 or 2 days led to reduced build a tolerance to the toxic effects of noxious-smelling plants, like tansy rag- consumption on subsequent days (Pfister some plant allelochemicals. Much has wort (Senecio jacobaea L. ) consumed by et al. 1988). In pen studies, cattle respond- been written about animal abilities to goats and sheep (Cheeke 1998). ed to larkspur dosing with distinct cycles detoxify plant substances. For more Some plant toxins are bound or of food intake such that 1 to 3 days of detailed reviews, see Freeland and Janzen sequestered by other ingested material that higher consumption were followed by 1 to (1974), Allison (1978), Brattsten (1979), prevent toxic actions (Smith 1992). 3 days of reduced consumption (Pfister et McArthur et al. (1991), Smith (1992), and Geophagy (i.e., eating soil) is common al. 1997). Cattle have a dose-response Cheeke (1998). among ungulates (Jones and Hanson threshold of 14 to 18 mg of toxic alka- 1985). Despite the widespread belief that loid/kg body weight, so periods of reduced Ejection mineral licks are sought by animals for consumption below this threshold proba- Once a toxin is eaten, it is in the animals their sodium content, it is more likely that bly allowed animals to recover from the best interest to quickly get rid of it. This other minerals (e.g., Ca, P, S) are more larkspur-induced illness. can be accomplished through vomition or important (Jakle 1969, Jones and Hanson diarrhea (Kingsbury 1983). Sheep, goats, 1985). Detoxification pathways using sul- Regulating Intake of Plant and cattle can and will vomit in response phur are metabolically expensive and sul- Allelochemicals to eating toxins (Mullenax et al. 1966, phur is usually in short supply (Brattsten Many allelochemicals may impart a dis- Oehme and Barrett 1986). In ruminants, 1979, McArthur et al. 1991). Thus, animals tinct flavor to plants. When plant flavor vomition is problematic because animals might practice geophagy to ingest sulphur. and toxicity are highly correlated, herbi- can aspirate the gut contents into their Moreover, mineral licks are often high in vores apparently regulate food intake lungs, which can be fatal. Vomiting in various clays (Jones and Hanson 1985) and based on post-ingestive feedback and then ruminants is apparently sensitive to dose, some clays naturally bind to phytotoxins adjust intake based on flavor intensity as some toxic plant doses resulted in vom- (Smith 1992). Geophagy may, therefore, (Launchbaugh et al. 1993). This may iting, whereas higher doses produced deactivate some ingested plant toxins. explain how animals commonly choose severe retching (Mullenax et al. 1966). among plant parts, individuals, or popula- Horses probably do not vomit except when near death, but commonly experi- Degradation by Microbes tions to select bites with lower than aver- Ruminants often have a significant ence diarrhea (Oehme and Barrett 1986). age amounts of phytotoxins. This behav- advantage over nonruminants when deal- Diarrhea aids in rapid elimination of tox- ior, summarized by Pfister (1999), has ing with toxic plants because their large ins from the gut which reduces absorption. been observed to minimize consumption forestomach is well adapted to degrade or In some episodes of diarrhea, there is a of cyanide (in sudangrass, Sorghum bicol- detoxify plant toxins (Oehme and Barrett or [L.] Moench ssp. drummondii [Nees ex decrease in intestinal motility, further 1986, Smith 1992, Pfister 1999). The near- Steud.] de Wet & Harlan; and bracken reducing the absorption of toxins. ly neutral pH of the rumen environment fern, Pteridium aquilinum [L.] Kuhn), tan- may modify a plant toxin or the toxin may nins (in blackbrush), alkaloids (in lupine, Complex Formation be quickly diluted in the large volume Lupinus spp.; reed canarygrass, Phalaris Chemical reactions during ingestion (e.g., 225 to 265 liters for cattle) of the arundinaceae L.; and, tall fescue), and ter- may provide protection against the effects rumen. Of great significance for ingesting penes (in sagebrush, Artemisia spp.). of some plant toxins. Some browsing her- toxic plants is the massive number of Flavor may not, however, always be a bivores secrete proline-rich proteins rumen microbes which transform allelo- good indicator of toxicity. If toxicity (PRPs) in their saliva which bind to chemicals. Generally, for a rumen microbe changes without a change in flavor, herbi- ingested tannins reducing absorption and to degrade a toxic plant compound, utiliza- vores are likely to overingest toxic plants toxic effects (Robbins et al. 1991). tion of the compound must yield energy, because they are not “warned” by a flavor Interestingly, salivary proteins from gener- and the microbial population must inhabit cue. When lambs were offered a feed with alist herbivores, like bear and deer, bind a particular rumen niche that allows it to a constant flavor and variable toxic feed- several tannins whereas proteins from spe- survive when the toxin is not present back, they consumed an amount based on cialist feeders, like moose and beaver, (Weimer 1998). Microbial interactions the maximum, rather than the average, bind only the tannin most commonly with most phytotoxins lead to degradation dose of the toxin (Launchbaugh et al. found in their diets (Hagerman and or detoxification rendering the compounds 1993). This response reduced the risk of Robbins 1993). Cheeke (1998) speculated inert or less detrimental. In some cases, lambs over-ingesting a toxin even when that physical forces during ingestion might however, rumen microbes can convert toxicity changes were not accompanied by allow animals to eat more of some plants innocuous substances into toxic com- flavor changes. containing highly volatile chemicals, such pounds such as the conversion of nitrite as sagebrush. Many terpenes may be lost from the less toxic nitrate and the hydrolysis of cynogenic glycosides to toxic hydro- Detoxification and Tolerance through volatilization during chewing as gen cyanide (Allison 1978). Animals possess several mechanisms to when pygmy rabbits eat sagebrush (White negate or restrict the toxic effects of plant et al. 1982). Increased chewing and rumi- allelochemicals once ingested. Animals nating has also been weakly associated Tissue-level Detoxification may eject toxic plant material quickly with increased sagebrush consumption in Once plant toxins are absorbed from the after ingestion, secrete substances in the sheep (Fraker 1999). Further, nasal tissue gut into the blood, they are often trans-

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 435 ported to the liver (i.e., hepatic tissue). production of proline-rich saliva in Management Practices to Help The liver primarily and secondarily the response to high-tannin diets (Mehansho Animals Contend with Anti- kidney, intestinal mucosa, lungs, and skin et al. 1985, Robbins et al. 1991). quality Attributes contain enzyme systems that metabolize Rumen microbes may also facilitate the (or alter) toxic compounds rendering them ability of animals to adapt to diets high in inert (McArthur et al 1991). This biotrans- phytotoxins. Microbial populations can The most common approaches to reduc- formation involves several enzyme sys- change rapidly depending on the sub- ing losses caused by anti-quality factors in tems that generally yield polar compounds strates available for degradation (Van forage plants are to change the plant com- that can be excreted in urine or feces. For Soest 1994). For example, ruminants that munity or grazing management strategy. more details on detoxification in mam- have dietary experience with oxalate-con- Poisonous plants have been sprayed and mowed; shrublands with low forage value malian tissue see Brattsten (1979), taining plants can tolerate levels of have been treated with herbicides, McArthur et al. (1991), Smith (1992), or oxalates that would be lethal to nonadapt- Launchbaugh (1996). mechanically altered, or burned to remove ed animals (James and Cronin 1974, the shrubs in favor of herbaceous forages; Allison and Cook 1981). This protection and, toxin-free forage varieties (e.g., endo- Tolerance from oxalates is attributed to oxalate- phyte-free fescue) have been developed The last line of defense against the dele- degrading rumen bacteria (Allison and and planted. Grazing periods have also terious effects of plant allelochemicals Cook 1981). Likewise, dietary experience been planned to minimize negative occurs when the tissues vulnerable to with nitrate-containing plants often leads impacts of anti-quality factors. A more damage by an allelochcemial become less to increased tolerance of nitrates attributed contemporary approach is to change the sensitive or shielded in a process called to increased populations of nitrite-degrad- grazing animal, rather than the vegetation, physiological tolerance (Provenza et ing rumen microbes (Smith 1992). to promote or encourage the animal’s nat- al.1992) or target-site insensitivity Exposure to fibrous diets at a young age ural abilities to combat anti-quality attrib- (Slansky 1992). Some herbivore species or has also been shown to improve fiber utes. A first step in creating herds or individuals are more tolerant to specific digestibility later in life (Distel et al. flocks of animals that can overcome anti- toxic plants than others. For example, 1994). These “inducible defenses” could quality attributes is to identify the most sheep can tolerate and detoxify more explain why herbivores often appear less significant challenges that specific forag- pyrrolizidine alkaloids than cattle and it sensitive to toxic or low quality plants ing situations present to herbivores. For therefore takes 5 times more tall larkspur with continued exposure. Nonetheless, example, in sagebrush-dominated commu- to poison sheep compared to cattle (Olsen adaptation does not develop to all toxins. nities, selecting or shaping animals with a 1978). The superior tolerance of larkspur The effects of many toxins are cumulative significant ability to digest and detoxify by sheep was thought to result from differ- and animals get progressively more poi- monoterpene essential oils could greatly ences in ruminal metabolism; however, soned as they continue to ingest plant increase the amount of available forage. recent studies indicate that nicotinic material containing these toxins. Once a foraging challenge is identified, acetylcholine (nAch) receptors of sheep management plans can be drafted to help animals meet this challenge. bind the larkspur toxins much less avidly Influence of Animal Nutritional Status than do cattle nAch receptors (Stegelmeier on Detoxification Offer Animals Proper Early Life et al. 1999). Detoxification of plant allelochemicals is a metabolically costly endeavor requir- Experiences Attempts to fashion animals with specif- Influence of Previous Dietary ing nutrients and energy to alter toxins and maintain an acid-base equilibrium (Jessop ic dietary attributes could begin at birth Experience on Degradation, and Illius 1997, Foley et al. 1999). because early life experiences can strongly Detoxification, and Tolerance Improving the nutritional state of the ani- affect dietary habits later in life. Previous The ability of a compound to restrict mal can often lead to increased rates of dietary experiences can influence the fla- plant quality or cause toxicosis depends detoxification or decreased toxic effects vor preferences of animals (Nolte and partly on the dietary experience of the her- (Freeland and Janzen 1974, Boyd and Provenza 1992) and their ability to digest bivore. With continued consumption of a Campbell 1983), which can lead to (Distel et al. 1994), detoxify (Distel and plant containing a specific allelochemical, increased intake of foods that contain tox- Provenza 1991, Robbins et al. 1991), and the animal may gain an ability to over- ins (Wang and Provenza 1996). Nutrient harvest (Ortega-Reyes and Provenza come its negative effects (Freeland and and energy availability can influence plant 1993) specific plants. Furthermore, experi- Janzen 1974). It is well known that toxicity by altering rates of gastro-intesti- ences early in life often have a more last- enzyme systems in animal tissue can nal absorption and enzymatic detoxifica- ing effect on consumption patterns than increase their detoxification capacity and tion, availability of co-substrates for experiences later in life (Distel et al. efficiency in the repeated presence of a detoxification, environmental conditions 1994). Exposing animals to potentially troublesome plants in their youth may toxic substrate (Freeland and Janzen 1974, in the gastro-intestinal tract or body fluids, improve their ability to harvest, digest, Brattsten 1979). In the case of tansy rag- and capacity for tolerance (Boyd and and detoxify the plants when they mature. wort alkaloids, pretreatment of animals Campbell 1983, Slansky 1992, Cheeke with the alkaloid jacobine results in ele- 1998). Dietary nutrients and energy are vated alkaloid detoxification activity also required to maintain healthy rumen (Miranda et al. 1980). Enhanced secretion microbial populations (Van Soest 1994) and activity of chemical complexing sub- important for detoxification of many plant stances has also been observed with the allelochemicals (Allison 1978).

436 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Select Appropriate Livestock abilities of animals are heritable character- impact animal production. In several Species and Individuals istics (Winder et al. 1995, Launchbaugh et cases, these examinations led to the devel- It is well known that animal species dif- al. 1999, Snowder et al. 2001). These opment of “antidotes” that help herbivores fer in diet selection and intake. For exam- inherited characteristics could influence disarm specific allelochemicals or survive ple, when juniper consumption was com- diet selection and intake in several ways. their biological assaults. For example, pared for several rangeland herbivores in Animals that have superior abilities to understanding the specific action of fescue Texas, a clear pattern emerged of juniper detoxify specific allelochemicals should be alkaloids lead to the development of a intake as follows: deer>goats>sheep>cattle able to eat plants containing these phyto- compound (i.e., a dopamine antagonist) (Launchbaugh et al. 1997). A simple chemicals and experience less negative that blocks metabolic effects of the alka- approach to making use of low quality or feedback. A genetic basis for the detoxifi- loid (Aldrich et al. 1993). Supple- toxic forages is to select a livestock species cation abilities of animals is evidenced by mentation of calcium can improve survival that naturally makes good use of the target the observation that detoxification of some of sheep grazing halogeton (Halogeton plant. For example, sheep can more safely drugs (e.g., hexobarbitol; Vessell 1968) glomeratus [Bieb.] C.A. May) infested graze larkspur-infested rangeland than cat- and phytotoxins (e.g., flauoroacetates; rangeland because rumen microbes detoxi- tle because they are more able to survive Oliver et al. 1979, Mead et al. 1985) is fy oxalates in halogeton by forming insol- the toxic effects of larkspur (Olsen 1978, strongly inherited. Dietary preferences are uble calcium oxalates that are excreted in Pfister 1999). This simple concept is how- also influenced by inherited characteristics. the feces (James and Cronin 1974). ever often difficult for livestock producers Animals that are able to extract above Increased levels of dietary sulfur (Conn to enact because changing the species average amounts of energy from specific 1979) and vitamin B12 (Brattsten 1979) being raised generally requires substantial plants, because of superior digestive abili- have been shown to decrease the forma- changes in fencing, livestock handling ties, should experience greater positive tion of hydrogen cyanide from cyanogenic equipment, management skills, knowledge, digestive feedback and form stronger and glycoside containing plants. The toxic and philosophy. A more acceptable way to longer lasting preferences for these plants. effects of larkspur alkaloids can be coun- assemble groups of animals with desired The inheritance of enzyme systems teracted by injections of the cholinergic involved in digestion is well documented dietary and digestive attributes might be to drug, physostigmine (Pfister et al. 1994). (Velázquez and Bourges 1984). select an adapted breed within a species. The complexing action of some allelo- Differences in absorption of minerals Research on cattle (Herbel and Nelson chemicals, such as tannins, can be sur- 1966, Winder et al. 1996), sheep (Warren (Green et al. 1989) and nutrients (Beaver et mounted by supplementing animals with et al. 1984), goats (Warren et al. 1984, al. 1989) during digestion have been traced compounds such as polyethylene glycol Pritz et al. 1997), and horses (Mariner and to animal breed and therefore indicate a Alexander 1991) has revealed that breeds genetic basis for digestion. Given the that bind with the ingested phytochemicals differ in dietary characteristics. important role of digestive feedback in before they can bind dietary and microbial Individual variation within a breed may directing diet selection, it is not surprising proteins (McNabb et al. 1993). Simply also create a basis for selecting animals to that several studies have revealed signifi- improving the nutritional state of animals meet specific foraging challenges. Research cant inheritance values for diet patterns. A can often lead to increased rates of detoxi- on the behavioral, metabolic, and production study of 60 young male Spanish goats in fication and decreased toxic effects effects of anti-quality factors have consistent- Texas showed dietary similarities between (Freeland and Janzen 1974, Foley et al. ly revealed that animals vary significantly in sire groups even though all goats were 1995), which can lead to increases in their response to toxic or low quality plants. raised in a similar environment (Warren et intake of foods that contain toxins (Wang Furthermore, dietary differences between al. 1983). A more recent study with and Provenza 1996). animals appear to be relatively consistent Spanish x Boer cross goats revealed that Development of vaccines to inoculate through a grazing season and between years the consumption of juniper by free-ranging animals against specific plant toxins is (Launchbaugh et al. 1997). Most toxic plants goats had a heritability of .28 (C.A. Taylor, becoming a reality. Recent work in with acute neurological effects (e.g., lark- unpublished data). In other words, 28% of Australia (Edgar et al. 1998) and in the spurs; lupines; poison hemlock, Conium the variation in juniper consumption could U.S. (Lee and Stegelmeier, personal com- maculatum L.; broom snakeweed, be attributed to goat sire. Winder et al. munication) indicate that commercial vac- Gutierrezia sarothrae [Pursh.] Britton & (1995) reported significant heritability esti- cines against some plant toxins (e.g., Rusby; pine needles, Pinus spp.) exhibit wide mates for consumption of several range pyrrolizidine alkaloids) are feasible. One variability in dose response when ingested by plants by Brangus cattle in New Mexico. ancillary benefit of developing toxin-pro- livestock (Pfister 1999). In future years, indi- Examination of big sagebrush consumption tein conjugates for vaccines is the concur- vidual animals may be screened for response by more than 400 Rambouillet ewes over 2 rent use of such conjugates for immunoas- to anti-quality factors or susceptibility to tox- years concluded that 25Ð28% of individual says that will be useful for field-based ins. For example, susceptibility to larkspur variation in sage consumption was herita- assessment of toxin concentrations. alkaloids could be tested using a muscle ble (Snowder et al. 2001). These studies biopsy to indicate the binding affinity of the point clearly to the possibility of breeding individual to toxic alkaloids. Using this or animals to overcome the challenges of spe- Conclusions similar approaches, groups of animals may cific anti-quality attributes. be assembled to access nutrients and with- Foraging on rangelands and pasture stand toxins in chemically defended plants. Offer Nutritional or Pharmaceutical poses several significant challenges to the Products to Aid in Digestion and herbivores. Grazing animals must utilize Breed Animals with Desired Detoxification the nutritional value of plants to evade Attributes The examination of anti-quality factors starvation, gain weight, and produce young while avoiding and negating the anti-quali- There is significant and growing evi- in plants often focuses on the biological dence that the digestive and detoxification mechanisms by which phytochemicals ty attributes that are an implicit component

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 437 of almost all forages. Livestock manage- Burritt, E.A. and F.D. Provenza. 1989. Food Grant, V.L. 1987. Do conditioned taste aver- ment in these situations can be significant- aversion learning: Ability of lambs to distin- sions result from activation of emetic mecha- ly challenging. Developing grazing plans guish safe from harmful foods. J. Anim. Sci. nisms? Psychopharmacology. 93:405Ð415. to minimize the impacts of plant anti-quali- 67:1732Ð1739. Green, L.W., J.F. Baker, and P.F. Hardt. ty attributes requires an understanding of Burritt, E.A. and F.D. Provenza. 1991. 1989. Use of animal breeds and breeding to Ability of lambs to learn with a delay overcome the incidence of grass tetany: A the behavioral and metabolic mechanisms between food ingestion and consequences review. J. Anim Sci. 67:3463Ð3469. that herbivores employ to extract nutrients given meals containing novel and familiar Hagerman, A.E. and C.T. 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440 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 J. Range Manage. 54: 441Ð446 July 2001 Animal health problems caused by silicon and other mineral imbalances

HENRY F. MAYLAND AND GLENN E. SHEWMAKER

Authors are research soil scientist, Northwest Irrigation and Soils Research Laboratory, USDA-ARS, 3793N 3600E, Kimberly, Ida 83341-5076; and extension forage specialist, University of Idaho, Twin Falls, Ida 83303-1827. e-mail

Abstract Resumen

Plant growth depends upon C, H, O, and at least 13 mineral El crecimiento vegetal depende del C,H,O y al menos de 13 ele- elements. Six of these (N, K, Ca, Mg, P, and S) macro-elements mentos minerales mas. Seis de estos macroelementos (N, K, Ca, Mg, P y S) normalmente ocurren en las plantas en concentra- normally occur in plants at concentrations greater than 1,000 mg -1 kg-1 level. The remaining micro-elements (B, Cl, Cu, Fe, Mn, Mo, ciones mayores a 1000 mg kg . El resto de los elementos (B, Cl, Cu, Fe, Mn, Mo, y Zn) normalmente se encuentran en las plantas and Zn) normally occur in plants at concentrations less than 50 -1 mg kg-1. Trace amounts of other elements (e.g., Co, Na, Ni, and en concentraciones menores a 50 mg kg . Cantidades traza de Si) may be beneficial for plants. Silicon concentrations may otros elementos (por ejemplo, Co, Na, Ni y Si) pueden ser benéfi- -1 cas para las plantas. En algunos zacates forrajeros las concentra- range upwards to 50,000 mg kg in some forage grasses. Mineral -1 elements required by animals include the macro-elements Ca, Cl, ciones de silicio pueden variar hasta 50,000 mg kg . Los elemen- K, Mg, N, Na, P, and S; the trace or micro-elements Co, Cu, Fe, tos minerales requeridos por los animales incluyen los macroele- I, Mn, Mo, Se, and Zn; and the ultra-trace elements Cr, Li, and mentos Ca, Cl, K, Mg, N, Na, P y S, los elementos traza o Ni. When concentrations of these elements in forages get ‘out of microelementos Co, Cu, Fe, I, Mn, Mo, Se y Zn y los elementos whack’ their bioavailability to animals may be jeopardized. ultra-traza Cr, Li y Ni. Cuando las concentraciones de estos ele- Interactions of K x Mg x Ca, Ca x P, Se x S, and Cu x Mo x S are mentos en los forrajes alcanzan proporciones altas su biodisponi- briefly mentioned here because more detail will be found in the bilidad puede estar en peligro. Las interacciones de K x Mg x Ca, literature. Limited published information is available on Si, so Ca x P, Se x S, y Cu x Mo x S se mencionan brevemente aquí we have provided more detail. Silicon provides physical support porque en la literatura seran encontrados mas detalles. La infor- to plants and may reduce susceptibility to pests. However, Si may mación publicada disponible sobre Si es limitada por lo que have negative effects on digestibility and contribute to urinary nosotros damos mas detalle de ello. El silicio provee un soporte calculi in animals. físico a las plantas y puede reducir la susceptibilidad a las plagas. Sin embargo, el Si puede tener efectos negativos en la digestibilidad y contribuir a formar cálculos urinarios en los animales. Key Words: Forage, mineral interaction, mineral requirements, mineral nutrition, ruminant diets. and subsequent animal health problems. Silicon will be discussed Simple deficiency or excess of dietary mineral elements may in more detail since current coverage is sparse. cause animal health concerns. In addition there are known imbalances among elements that directly or indirectly affect bioavailability of other elements (Grace and Clark 1991, Grace 1994). Silicon Through out the review, reference will be made to ruminant mineral requirements as given in Table 1. Nearly all mineral elements, Silicon receives major emphasis in this review because its role whether essential or nonessential, can adversely affect an animal if in forage and animal nutrition has not been greatly investigated. included in the diet at excessively high levels (Gough et al. 1979, Silicon uptake, and subsequent deposition on leaf cell-wall, and NRC 1980). Forage, concentrates, mineral supplements, and especially on the leaf perimeter provides physical support to drinking water serve as sources of consumed mineral elements. plants. Silicon deposits also reduce susceptibility to insect and Soil ingestion provides yet another source of soluble or extractable fungal attack and may also reduce animal preference or palatabil- mineral elements (Mayland et al. 1975). The connection between ity for certain plants (Jones and Handrek 1967, Shewmaker et al. minerals in the diet and health of animals has been previously cov- 1989). There is unpublished work (Mayland, unpublished) sug- ered by others, including Harris et al. 1989, Kabata-Pendias and gesting a negative relationship between forage Si and digestibility Pendias 1992, Mayland and Cheeke 1995, Nicholas and Egan of forage. In preliminary, unverified experimentation he found 1975, Reid and Horvath 1980, Spears 1994. This paper will gener- that in vitro dry matter digestibility of forage grasses was ally overlook simple cases of deficiency or toxicity. Instead it decreased 4 units for each unit of Si present in the forage. emphasizes mineral interactions leading to mineral imbalances Shewmaker et al. (1989) suggest the following as possible roles of Si on digestibility. Once eaten, Si may reduce digestibility of Manuscript accepted 27 Nov. 00. forage by 1) acting as a varnish on the plant cell wall and reduc-

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 441 Table 1. Nutrient element concentrations normally found in coolÐseason grasses and legumes and ing phenological maturity and are greatest their requirement by sheep and cattle. in leaves, intermediate in inflorescences, and least in stems. Awns contain high con- 1 2 Concentrations in Forages Dietary requirements centrations of Si. Silicon concentrations in Element Grasses Legumes Sheep Cattle leaves of Agropyron, Pseudoroegneria, Ð1 ------(g kg ) ------and Thinopyrum increase at nearly twice Calcium, Ca 3Ð 6 3Ð 14 3Ð4 3Ð4 the rate of those in Critesion, Hordeum, Chlorine, Cl 1Ð 5 1Ð 5 1 2 Magnesium, Mg 1Ð 3 2Ð 5 1 2 Leymus and Psathyrostachys (Fig. 1). Nitrogen, N 10Ð40 10Ð 50 10Ð15 10Ð 5 Elymus leaves contain higher concentra- Phosphorus, P 2Ð 4 3Ð 5 2 2 tions of Si at the vegetative stage than Potassium, K 10Ð 30 20Ð40 3 8 other groups, but the accumulation rate is Silicon, Si3 10Ð 40 0.5Ð1.5 requirement not established 3 intermediate. Sodium, Na 0.1 Ð 3.0 0.1Ð 2 1 2 Silicon is much more soluble in NDF Sulfur, S 1Ð4 2Ð 5 1Ð2 1Ð 2 than ADF extractions (Shewmaker, et ------(mg kgÐ1) ------al.1989). They found that in vegetative Boron, B 3Ð40 30Ð 80 requirement not established grass, about 32% of total leaf Si remains in Copper, Cu 3Ð15 3Ð 30 5Ð6 7 Ð 10 the NDF residue. However, about 76% Fluorine, F3 2Ð20 2Ð 20 1Ð 2 1 Ð 2 Iron, Fe 50Ð250 50Ð 250 40 40 remains in the ADF residue. Some of the Si Manganese, Mn 20Ð100 20Ð 200 25 25 is insoluble in both extracts. These insolu- Molybdenum, Mo 1Ð5 1Ð10 <0.1 <0.1 ble portions of Si increase with aging. Zinc, Zn 10Ð 50 15 Ð 70 25 Ð 40 25 Ð 40 Preference relates to estimated dry matter ------(µg kgÐ1) ------digestibility at boot and anthesis, but is not Cobalt, Co3 50Ð300 200Ð300 100 60 related to fiber or Si measurements. Chromium, Cr3 200Ð1000 200Ð 1000 Trace Trace Leaf Si concentration ranges from 7 g Iodine, I3 40Ð 800 40Ð 800 500 500 kg-1 in Hordeum to 47 g kg-1 in bluebunch Nickel, Ni 200Ð1000 200Ð1000 60Ð70 60Ð70 3 wheatgrass (Pseudorogneria spicata = Selenium, Se 50Ð200 50Ð200 30Ð200 40Ð300 Agropyrum spicatum [Pursh] Scribn. & 1 Herbage data are generalized from Fageria et al. (1991), Gough et al. (1979), Jones and Thomas (1987), Marschner Smith). Indian ricegrass (Oryzopsis (1986), Mayland (unpublished), Mays (1974), and Reid and Jung (1970) 2Animal data are generalized from Grace (1994), Grace and Clark (1991), Jones and Thomas (1987), NRC (1980). F, hymenoides (Roemer & J.A. Schultes) ex -1 while not required by animals is beneficial to bones and teeth. Dietary requirements are for growing sheep and lactating Piper) contains 25 g Si kg in leaves at the cattle. Requirements may be different for other animal classes. 3 anthesis stage. Medusahead (Elymus Required by animals but not grasses or legumes. caput-medusae L.) is very unpalatable and contains up to 113 g Si kg-1, whereas ing accessibility to rumen microflora, 2) rumen microbial accessibility to cell wall cheatgrass (Bromus tectorum L.) contains complexing trace elements like Zn and structure (Smith and Nelson 1975, Harbers 44 g Si kg-1 (Bovey et al. 1961). reducing their availability to rumen et al. 1981), thereby reducing apparent Silicon accumulation in 3 groups of microflora, or 3) complexing enzymes that digestibility of herbage (Van Soest and grasses as a function of growth stage is are integrally involved in rumen metabolism. Jones 1968). Mika (1986) reported that a shown in Figure.1. The wheatgrasses Silicon (Si) is absorbed as monosilicic water-soluble form of Si inhibits activity (group 1) generally reach physiological acid [Si(OH)4] by plant roots, transported of cellulases and other digestive enzymes, maturity quicker than wildryes (with the throughout the plant, and deposited pri- whereas the insoluble form is chemically exception of Russian wildrye) and wild marily in epidermal cells, stoma and tri- inert. Thus, exogenous Si from ingested barleys (group 2). Group 1 plants tend to chomes of leaves (Jarvis 1987). Some of soil or dust adhering to herbage probably have fewer leaves, which on average may this Si remains in soluble forms. Most Si, has little direct effect on digestibility. be chronologically older than leaves of however, is incorporated into or onto the Silicon, in addition to affecting forage group 2 plants. These older leaves of cell wall structure or precipitated with quality, is implicated in animal health group 1 plants may have higher concentra- other elements to form amorphous crys- (Jones and Handreck 1967). In some early tions of Si because passively-transported talline deposits called phytolyths research, urolithiasis in steers was related Si, taken up as a soluble component in the 2 (Blackman and Bailey 1971, Moore 1984). (r = 0.56) to Si concentrations in Montana transpiration stream, accumulates for a [The structure, shape, and color of plant forage grasses (Parker 1957). However, longer time in leaves or because of differ- phytolyths differ among grass genera and Bailey (1976) later reported that frequency ences in active transport (requiring ener- may be used for classification purposes in of urinary calculi encountered in Alberta gy) of Si from roots to leaves. archeological sites.] Silicon uptake is cattle was inversely related to urine vol- largely passive, i.e., taken up with the ume and water intake. This cause and transpiration stream, however, recent evi- effect relationship has not been resolved. Silicon in tall fescue and its relation to dence has demonstrated that some energy Ingestion of certain Si minerals may cattle preference. mediated uptake of Si occurs in grasses increase the rate of tooth wear, thus reduc- In our studies of cattle preferences (Jarvis 1987, Mayland et al. 1991). ing the effective lifetime of grazing ani- among tall fescue cultivars, preference The incorporation of Si into scabrous mals (see also Soil Ingestion). scores were not related to soluble or insol- tissue is perceived as a defense mecha- Shewmaker et al. (1989) determined the uble Si in ADF and NDF residue, nor to nism against some insects (Moore 1984) Si concentration in 31 accessions of C-3 total Si at any phenological stage and possibly against grazing by large her- grasses and the relationship of Si concen- (Mayland, unpublished). Thus, cattle pref- bivores (McNaughton et al. 1985). Silicon tration to sheep preference. Silicon con- erence for these grasses is a function of taken up by forage plants may also reduce centrations in leaves increase with advanc- factors other than Si components. There is

442 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 An alternative to fertilization or direct supplementation is to increase Mg in forage through plant breeding (Sleper et al. 1989). Progress has been made with Italian ryegrass (Lolium multiflorum Lam.) ( Moseley and Baker 1991, Moseley and Griffiths 1984), perennial ryegrass (Lolium perenne L.) (Binnie et al. 1996), and tall fescue (Mayland and Sleper 1993, Crawford et al. 1998). The new cultivars have resulted in reduced values of K/(Mg+Ca) in forage, increased levels of blood plasma Mg in animals, and in high risk situations these high magnesium cultivars have reduced the incidence of grass tetany death losses by grazing animals. Potassium levels of 28 g kg-1 DM in herbage will provide near maximum herbage yield of cool-season grasses. However, increases in solution K concentration reduce uptake of both Ca and Mg by Fig. 1. Leaf silicon (Si) accumulation in CÐ3 grasses as predicted by growth stage. Group 1 plants, even at higher solution K levels genera include Thinopyrum, Agropyron, and Pseudoroegneria, the wheatgrasses. Group 2 resulting in less than maximum forage genera include Critesion, Hordeum, Psathyrostachys, and Leymus, wildÐbarley and wildrye. yield. Smith et al. (1985) reported that Mg Data are adapted from Shewmaker et al. 1989. concentrations level out at 1.9 g kg-1 when herbage contains ≥ 25 g K kg-1; whereas Ca evidence that Si concentration is higher in Magnesium absorption by both plants concentration continues to decrease to a grazed plants than ungrazed plants on the and ruminants is negatively affected by K. low of 6 g kg-1 as forage K increases to 65 g Serengeti (McNaughton and Tarrants That interaction is the basis for the K kg-1. High herbage K levels also depress- 1983) and in western wheatgrass K/(Mg+Ca) ratio in forages that provides a es Mg and Ca absorption by ruminants. (Pascopyrum smithii = Agropyrum smithii risk index. Calcium may counter some of On the other hand, K concentrations in [Rydb.] A. Love) on the northern plains the effects of K on Mg absorption. The dry-mature or winter grass (standing or (Brizuela et al. 1986). Brizuela also risk of grass tetany increases exponentially harvested) may be inadequate for cattle reports that hand-defoliated little bluestem when the herbage K/(Ca+Mg) increases requirements. This may occur because of (Schizachyrium scoparium [Michx.] Nash) above 2.2 (expressed as moles of charge weathering and leaching of K from the contains lower Si concentrations than non- basis). Other factors that reduce Mg avail- curing forage. Minimum critical levels for defoliated plants. The different Si concen- ability to ruminants include high concen- cattle are in the range of 5Ð10 g kg-1. trations may be a result of grazing-induced trations of N and low concentrations of During summer, 20 g K kg-1 DM may be ecotypic differentiation (Detling and total soluble carbohydrate. Prudent use of desired to reduce heat stress in cattle. Painter 1983). The theory that Si is a N and K fertilizers is warranted to mini- Prudent applications of fertilizer K are short-term defense against large herbi- mize risk of grass tetany (Mayland and vores is clouded by the interaction with required to meet plant growth require- Wilkinson 1989, Mayland et al. 1990). ments, and not aggravate the risk of low- increased nutritional value of regrowth Aluminum in acid soil solutions may also forage over initial forage. ered Mg and Ca uptake by plants and reduce Ca and Mg uptake by cool season absorption by animals. grasses and increase susceptibility to grass tetany (Rengel and Robinson 1989). Magnesium x Potassium x Restoring available soil P to concentra- Calcium x Phosphorus Calcium tions adequate for good plant growth has also elevated Mg and Ca concentrations in grass leaves (Reinbott and Blevins 1994). Milk fever or parturient paresis, is char- Hypomagnesemic grass tetany is proba- acterized by low blood Ca (<1.0 mmol bly the most important metabolic problem Severity of economic livestock losses -1 can be reduced by delaying early spring liter ). It occurs during late pregnancy and in ruminants caused by mineral imbal- onset of lactation. This situation can occur ances (Mayland 1988). It is characterized use of grass pastures, grazing with stocker -1 and dry cows, and supplementing animals even though herbage contains 4.4 g Ca kg by low blood plasma Mg concentrations DM. Animals must be treated parenterally (<0.4 mmol liter-1) and most assuredly by with soluble Mg. The Mg may be provided in drinking water, licks, salt, or perhaps as a with Ca for several days. Calcium:phos- low urinary Mg concentrations (< 0.8 phorus ratio of 2:1 (wt:wt) is ideal, but 8:1 mmol liter-1). Although 2 g Mg kg-1 DM is dust on the forage. On acid soils; liming with Ca-Mg limestone (dolomite) rather has been tolerated. In extreme situations, adequate to meet Mg requirements in most cattle and sheep may be observed chewing situations, cows and ewes near parturition than calcium limestone (calcite) would increase Mg availability to plants and likely on bones. This behavior may be indicative and continuing into lactation, may need of a P deficiency. Animal nutritional -1 to grazing animals. The method chosen will extra Mg (10 to 30 g Mg cow-day , 2 to 3 guides generally discuss ratios of Ca:P -1 be greatly dependent on local conditions. g Mg ewe-day ). rather than absolute dietary concentrations.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 443 Sulfur x Selenium and acute toxicosis (selenosis) may occur sider growing these animals in other areas when animals ingest excess Se (> 5 mg kg-1) where F intake is much less (Mayland, (Mayland 1994). personal experience). A blind staggers, or more correctly, Animal performance can be good on polioencephalomalacea may occur if rumi- pastures containing 0.3 mg I kg-1 DM, nants ingest excess sulfate sulfur (James et Copper x Molybdenum x however, the northern half of the U.S. and al. 1994, Mayland 1995, O’Toole et al. Sulfur x Iron Canada is generally I-deficient (McDowell 1996). This occurs when ruminant organ- 1992, Miller and Ammerman 1995). Salt isms reduce SO4 to the toxic H2S form. (NaCl) is a common carrier of supplemen- Sulfate in drinking water should be con- Copper deficiencies may occur in graz- tal I for both human and domestic live- sidered suspect in these cases (Mayland ing animals (Baker and Ammerman 1995). stock and will be identified as iodized salt 1995). Interactions of S x Se may occur Reduced bioavailability of Cu occurs in (Miller and Ammerman 1995). Dietary when S fertilization results in forage crop the presence of increased intake and intakes of 1 to 2 mg I kg-1 DM must be yield response. The reduced Se absorption bioavailability of Mo, S, and Fe. The for- considered when animals are eating goitro- by the plant may occur because of a direct mation of thiomolybdates in the gut, genic plants like turnips and other Brassica competition of S reducing the uptake of Se reduces absorption of Cu by animals species (Miller and Ammerman 1995). or may occur by dilution of Se in the plant (Baker and Ammerman 1995). Dietary Cu (Mayland and Robbins 1994, Wu and intake should be decreased in those areas Huang 1991). where herbage Mo levels are extremely Ultra-Trace Elements low. When Mo levels are high as they might be in some meadow soils, then Cu Selenium supplementation should be increased. The elements Al, As, Cr, Ni, V, Sn are Copper requirements for cattle are about presumed essential for ruminants although research data are not available. If required, Selenium is needed for animal health in twice those for sheep. Several incidences of Cu toxicity in grazing sheep have been the dietary concentrations must be extreme- low concentrations but is toxic at high. It ly low. Using the definition of essentiality may occur in high to toxic (to animals) reported on recently manured pastures. These are associated with swine or poultry for plants; one might also add Ba, Br, F, Rb, levels in herbage grown on Cretaceous -1 manures from operations where Cu- and Sr. We have measured <0.5 mg Cd kg geological soils, especially in the Central DM and 0.5 to 6 mg F kg-1 DM in grass Plains of North America. In other areas, anthelmintics are used for control of intestinal parasites (McDowell 1992, herbage. We are currently not aware of any herbage Se concentrations may be inade- factors that might affect the bioavailability quate for animal requirements. Dietary Se Suttle and Price 1976). Copper bioavailability differs among some grasses as of these ultra-trace elements. Several of requirements range from 0.03 to as much these elements, if required by plants and as 1.0 mg Se kg-1 DM. The amount is Stoszek et al. (1986) showed for cattle grazing tall fescue or quackgrass. animals, must be at such low concentra- dependent upon the class of animal and tions in nutrient culture or in diet that it is levels of vitamin E, S, and other factors Nutritionists should be alert to signs of Cu deficiency or toxicity in animals, because difficult to conduct a sufficiently ‘clean present in the diet. The effect of Se is environment’ to test their essentiality. complemented to some extent by that of of the many opportunities for interaction vitamin E. High levels of dietary S will that affect Cu bioavailability. counter the availability of Se to ruminants. Interaction with Immunological Whole blood Se concentrations should be greater than 250 nmol liter-1. Cobalt, Fluorine, Iodine Requirements Selenium is the only mineral whose supplementation of food animals is regulated The Co requirements for sheep are about The mineral element requirement of ani- by the US Food and Drug Administration twice those for cattle (Henry 1995). mals is defined as the amount of bioavail- (FDA 1993). Effective 13 September Lambs are most sensitive to Co deficien- able nutrient in the diet required for 1993, the FDA permitted an increase of cy. Fluorine in concentrations of 1 to 2 mg growth and reproduction and further that 0.1 mg Se kg-1 (as sodium selenite or sodi- F kg-1, while not required by animals, is the element is the only component that can um selenate) in complete feeds for ani- beneficial for high tooth and bone density. meet that animal’s needs. There is increas- mals. The use of Se boluses is not permit- Concentrations of 4 to 8 mg F kg-1 will ing evidence (Mayland et al. 1987) sug- ted. Congress and U.S. President Clinton cause brown staining of tooth enamel and gesting that for some trace elements, a suspended the FDA action until 31 concentrations greater than 8 mg F kg-1 higher concentration of the element may December 1995 (Gloyd 1994). Thus, dur- will reduce tooth and bone density and be needed for maintaining the animal’s ing 1995, animal and fowl feeds could increase tendency for breakage. Drinking immune system than is currently consid- contain 0.3 mg Se kg-1 and the osmotic Se water is the primary source of F. Sprinkle ered as required for good growth and per- bolus for cattle could be used as a source irrigation of forages, using high F water, is formance. Experimental results, however, of Se. These on-again, off-again, changed- another way in which animals may ingest are mixed and possibly animal species again regulations have not satisfactorily excess F (Wallender and Keller 1984). dependent (Ward and Spears 1999). met Se nutrition needs of animals. The High F is often associated with thermal Further experimentation is required to sub- current status is that none of the regula- water and with rock phosphates used for stantiate the role of trace element require- tions adequately consider the level nor supplemental P in rations. The F intake ments and the development of full bioavailability of Se in naturally occurring may not be a problem for adult animals. immunological response levels. feedstuffs. Selenium deficiency causes However, for young growing stock intake white muscle disease, ill thrift, and of excess F will weaken tooth and bone reduced fertility, in animals. Alkali disease formation and livestock men should con-

444 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Soil Contamination of Forage Summary References Soil Intake by Animals Discussions of mineral nutrition of for- Bailey, C.B. 1976. Effects of ammonium chloride Mineral element concentrations of ana- age plants and forbs must include the ele- on formation of siliceous urinary calculi in mental needs of both plant and grazing calves. Can. J. Anim. Sci. 56:359Ð360. lyzed herbage samples may be significant- Baker, D.H. and C.B. Ammerman. 1995. ly biased by the presence of dust or soil animal. Grasses require 6 macronutrients Copper bioavailability. 127Ð157. In: C.B. (N, K, Ca, Mg, P, and S) in concentrations Ammerman, D.H. Baker, and A.J. Lewis. adhering to the material (exogenous com- -1 ponents). Such contamination is reflected exceeding 1,000 mg kg . They also Bioavailability of nutrients for animals. by plant sample Fe concentrations greater require 7 micronutrients (B, Cl, Cu, Fe, Academic Press., N.Y. than 250 mg kg-1 DM (Mayland and Sneva Mn, Mo, and Zn) in concentrations rang- Binnie, R.C., D.T. Hohnston, and D.M.B. ing from 0.1 to 50 mg kg-1. Some ultra- Chestnutt. 1996. The effect of a highÐmagne- 1983). Laboratory personnel in the senior sium perennial ryegrass variety on the magne- author’s lab routinely use a level of 400 as trace elements like Ni, Co, Si, and Na may also be needed by cool-season grasses. sium status of sheep. Grass Forage Sci. a threshold indicator of possible soil cont- 51:456Ð463. Grazing animals require 8 macronutri- amination of plant samples. Soil contami- Blackman, E. and C.B. Bailey. 1971. Dissolution ents. This list includes the same 6 needed nation on herbage may elevate the intake of silica from dried grass in nylon bags placed by plants plus Na and Cl. Animals require of Fe, Mn, Se, Co, and other elements in the rumen of a cow. Can. J. Anim. Sci. some of the same micronutrients as plants 51:327Ð332. above the true elemental composition of (Cu, Fe, Mn, Mo, and Zn) plus Co, I and Bovey, R.W., D. Le Tourneua, and L.C. the herbage. Direct soil ingestion by ani- Se. Animals may also require ultratrace Erikson. 1961. The chemical composition of mals may also affect the intake of some quantities of Cr, Li, and Ni. medusahead and downy brome. Weeds mineral elements (Mayland et al. 1975, 9:307Ð311. Grasses may exhibit macronutrient defi- Brizuela, M.A., J.K. Detling, and M.S. Cid. 1977, Sneva et al. 1983 ). This source of ciencies but seldom suffer from micronu- mineral elements may be important when 1986. Silicon concentration of grasses growing trient deficiencies. However, they may not in sites with different grazing histories. Ecol. studying trace element responses of free provide sufficient macronutrients (N, Ca, 67:1098Ð1101. grazing livestock (Mayland et al. 1980). In Mg, P, and S), micronutrients (Cl, Cu or Crawford, R.J., Jr., M.D. Massie, D.A. Sleper, some situations the eating of soil (a form Zn), or other elements (I, Na or Se) and and H.F. Mayland. 1998. Use of an experi- of geophagia) is an attempt to provide a thus fail to meet the animal’s nutritional mental highÐmagnesium tall fescue to reduce dietary buffer. In horses, it is often a needs. Paddocks of cool-season grasses grass tetany in cattle. J. Prod. Agr., 11:491Ð496 behavioral response to boredom with the Detling, J.K. and E.L. Painter. 1983. Defoliation are often fertilized with N and K. If N-fix- responses of western wheatgrass populations subsequent risk of developing an irritating ing legumes are present then P may be with diverse histories of prairie dog grazing. and sometimes fatal case of sand collic. applied to these paddocks and N fertiliza- Oecologia (Berlin) 57:65Ð71. Ingested soil can have another impact on tion is omitted. Grazing animals are gener- Fageria, N.K., V.C. Baligar, and C.A. Jones. animal health as is seen in the following ally supplemented with NaCl and may 1991. Growth and mineral nutrition of field case. Breeding cattle from one area of the also receive additional amounts of I, Se, crops. Marcel Dekker, N.Y. Great Basin, contrasted to cattle from Zn, and Co trace mineral to supplement Food and Drug Administration (FDA). 1993. Food additives permitted in feed and drinking other areas, are routinely discounted when their forage diets. Ruminants may also water of animals; Selenium. Federal Register sold through the regional livestock auction receive supplementary Mg where there is (13 Sept. 1993) 56 (175): 47962Ð47973. barn. This discounting occurs because of a considerable risk of grass tetany. Gloyd, J.S. 1994. Stay of selenium amendments significantly greater loss or wearing of Often grass and forb diets will contain lifted. J. Amer. Vet. Med. Assoc. 205:1639. teeth. These animals may ingest more soil nutrient levels considered adequate, but Gough, L.P., H.T. Shacklette, and A.A. Case. than others. A check of surface minerals the bioavailability of some minerals may 1979. Element concentrations toxic to plants, animals, and man. U.S. Geol. Surv. Bull. 1466. from those grazing lands indicate a hard- be reduced because of interactions like K x Mg, Mo x Cu x S, and S x Se. Split Grace, N.D. 1994. Managing trace element defi- ness (Moh scale) much greater than tooth ciencies. AgResearch, New Zealand Pastoral enamel and thus minerals in the ingested applications of K fertilizer will minimize Agr. Res. Inst., Publ. Palmerston North, N.Z. soil serve as an abrasion to the enamel. the impact of high K levels on Mg avail- Grace, N.D. and R.G. Clark. 1991. Trace ele- Tooth enamel is apatite with a rating of 5, ability to the plant and subsequent animal. ment requirements, diagnosis and prevention of whereas talc is rated 1 and diamond is Forages in some geographic areas con- deficiencies in sheep and cattle. p. 321Ð345. In: tain sufficient mineral nutrients to main- T. Tsuda, Y. Sasaki, and R. Kawashima. (ed.). rated 10. Soil minerals range several tain herbage growth, but there may be an Physiological aspects of digestion and metabo- points above or below 5. insufficient amount of Cu, Mg, Se (not lism in ruminants. Academic Press, San Diego, Calif. needed by plants), or Zn to meet animal Harbers, L.H., D.J. Raiten, and G.M. Paulsen. Urolithiasis requirements. For example, tall fescue is 1981. The role of plant epidermal silica as a well adapted to many areas of the U.S. structural inhibitor of rumen microbial digestion Soils in these areas contain little plant- in steers. Nutr. Rep. Int. 24:1057Ð1066. Male sheep or cattle are more prone to available Se and plants growing on them Harris, K.B., V.M. Thomas, M.K. Peterson, kidney stones when the dietary Ca:P is may not take up sufficient Se to meet ani- S.D. Kachman, and M.J. McInerney. 1989. less than 2:1 or ingested Si is high and mal requirements (McQuinn et al.1991). Influence of minerals on rate of digestion and Management programs that allow for direct percentage degradable in vitro neutral detergent water intake is limited (Bailey 1976). fiber. Nutr. Rep. Int. 40:219Ð226. Supplementing Ca will reduce the inci- or indirect supplementation of these nutri- Henry, P. 1995. Cobalt bioavailability. p. 119Ð dence of this problem only if the stones ents to the animals should be considered. 1126. In: C.B. Ammerman, D.H. Baker, and are analyzed as containing high concentra- Knowledge of mineral element require- A.J. Lewis. Bioavailability of nutrients for ani- tions of P. Providing adequate and quality ments of forages plants and grazing animals. Academic Press. N.Y. drinking water will reduce the incidence mals is essential to understand the com- James, L.F., W.F. Hartley, K.E. Panter, B.L. of silicosis. plex interactions that one element may Stegelmeier, D. Gould, and H.F. Mayland. have on another. 1994. Selenium poisoning in cattle. P. 416Ð420.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 445 In: S.M. Colegate and P.R. Dorling (eds.) CAB Mayland, H.F., L.W. Greene, D.L. Robinson, Reinbott, T.M. and D.G. Blevins. 1994. International Wallingford, U.K. and S.R. Wilkinson. 1990. Grass Tetany: A Phosphorus and temperature effects on Jarvis, S.C. 1987. The uptake and transport of sil- review of Mg in the soilÐplantÐanimal continu- Magnesium, calcium, and potassium, in wheat icon by perennial ryegrass and wheat. Plant and um. Proc. 25th annual Pacific Northwest Anim. and tall fescue leaves. Agron. J. 86:523Ð429. Soil 97:429Ð437. Nutr. Conf., 6Ð8 Nov. 1990, Vancouver, British Rengel, Z. and D.L. Robinson. 1989. Aluminum Jones, L.H.P. and K.A. Handrek. 1967. Silica in Columbia. effects on growth and macronutrient uptake by soil, plants and animals. Adv. Agron. Mayland, H.F., A.R. Florence, R.C. Rosenau, annual ryegrass. Agron. J. 81:208Ð215. 19:107Ð149. V.A. Lazar, and H.A. Turner. 1975. Soil Shewmaker, G.E., H.F. Mayland, R.C. Jones, D.I.H., and T.A. Thomas. 1987. Minerals ingestion by cattle on semiarid range as reflect- Rosenau, and K.H. Asay. 1989. Silicon in CÐ3 in pastures and supplements. p. 145Ð153. In: ed by titanium analysis of feces. J. Range grasses: Effects on forage quality and sheep R.W. Snaydon (ed.) Managed grasslands. Manage. 28:448Ð452. preference. J. Range Manage. 42:122Ð127. Analytical studies (Ecosystems of the world Mays, D.A. (Ed.) 1974. Forage fertilization. Sleper, D.A., K.P. Vogel, K.H. Asay, and H.F. 17B). Elsevier Sci. Publ., Amsterdam. Amer. Soc. Agron. Madison, Wisc. Mayland. 1989. Using plant breeding and KabataÐPendias, A. and H. Pendias. 1992. McDowell, L.R. 1992. Minerals in animal and genetics to overcome the incidence of grass Trace elements in soils and plants. 2nd ed. CRC human nutrition. P. 203. Academic Press, Inc., tetany. J. Anim. Sci. 67:3456Ð3462. Press. Boca Raton, Fla. N.Y. Smith, G.S. and A.B. Nelson. 1975. Effects of Marschner, H. 1986. Mineral nutrition of higher McNaughton, S.J. and J.L. Tarrants. 1983. sodium silicate added to rumen cultures on for- plants. Academic Press. San Diego, Calif. Grass leaf silicification: natural selection for an age digestion, with interactions of glucose, urea Mayland, H.F. 1988. Grass tetany. p. 511Ð523 inducible defense against herbivores. Proc. Nat. and minerals. J. Anim. Sci. 41:891Ð899. and 530Ð531. In: D.C.Church (ed.) The rumi- Acad. of Sci. (USA) 80:790Ð791. Smith, G.S., I.S. Cornforth, and H.V. nant animal: Its physiology and nutrition. McNaughton, S.J., J.L. Tarrants, M.M. Henderson. 1985. Critical leaf concentrations Prentice-Hall. Englewood Cliffs, NJ, Reissued Mcnaughton, and R.H. Davis. 1985. Silica as for deficiencies of nitrogen, potassium, phos- by Waveland Press, Inc. Prospect Heights, Ill. a defense against herbivore and a growth pro- phorus, sulphur, and magnesium in perennial Mayland, H.F. 1994. Selenium in plant and ani- moter in African grasses. Ecol. 66:528Ð535. ryegrass. New Phytol. 101:393Ð409. mal nutrition. P. 29Ð45. In: W.T. McQuinn, S.D., D.A. Sleper, H.F. Mayland, and Sneva, F.A., H.F. Mayland, and M. Vavra. Frankenberger, Jr. and S. Benson. Selenium in G.F. Karuse. 1991. Genetic variation for sele- 1983. Soil ingestion by ungulates grazing a the Environment. Marcel Dekker, Inc. N.Y. nium content in tall fescue. Crop Sci. sagebrush-bunchgrass range in eastern Oregon: Mayland, H.F. 1995. Absorption of excess seleni- 31:617Ð620 Source of dietary minerals. Oregon Agr. Expt. um and sulfur by plants and animals. P. Mika, V. 1986. The effect of the waterÐsoluble Sta. Special Report #682. p 35Ð39. 362Ð371. Proc. National meeting of the Amer. form of silicon in fodder crops on their Spears, J.W. 1994. Minerals in forages. 281Ð317. Soc. for Surface Mining and Reclam., Gillette, digestibility. Sci. Agr. Bohemoslovaca In: G.C. Fahey (ed.). Forage quality, evaluation, Wyoming, June 5Ð8, 1995. 18:185Ð190. and utilization. ASA, CSSA, SSSA. Madison, Mayland, H.F. and P.R. Cheeke. 1995. Miller, E.R., and C.B. Ammerman. 1995. Iodine Wisc.. ForageÐinduced animal disorders. In: R.F bioavailability. p. 157Ð 167. In: C.B. Stoszek, M.J., P.G. Mika, J.E. Oldfield and Barnes, D.A. Miller, and C.J. Nelson (ed.) Ammerman, D.H. Baker, and A.J. Lewis. P.H. Weswig. 1986. Influence of copper sup- Forages. The science of grassland agriculture. Bioavailability of nutrients for animals. plementation on blood and liver copper in cattle 5th ed. Iowa State University Press, Ames, Academic Press. N.Y. fed tall fescue or quackgrass. J. Anim. Sci. Iowa. Moore, D. 1984. The role of silica in protecting 62:263Ð271. Mayland, H. F. and C.W. Robbins. 1994. Italian ryegrass (Lolium multiflorum) from Suttle, N.F. and J. Price. 1976. The potential tox- Sulfate uptake by salinity-tolerant plant species. attack by dipterous stem-boring larvae icity of copperÐrich animal excreta to sheep. Commun. Soil Sci. Plant Anal. 25:2523Ð2541. (Oscinella frit and other related species). Ann. Anim. Prod. 23:233Ð241. Mayland, H.F. and D.A. Sleper. 1993. Appl. Biol. 104:161Ð166. Van Soest, P.J. and L.H.P. Jones. 1968. Effect Developing a tall fescue for reduced grass Moseley, G. and D.H. Baker. 1991. The efficacy of silica in forages upon digestibility. J. Dairy tetany risk. p. 1095Ð1096. In: J. Hogson (ed.) of a high magnesium grass cultivar in control- Sci. 51:1644Ð1648. Proc. 17th Int. Grassl. Congr., Palmerston ling hypomagnesemia in grazing animals. Grass Wallender, W.W. and J. Keller. 1984. Foliar flu- North, New Zealand. 8Ð21 Feb. Dunmore Press, Forage Sci. 46:375Ð380. oride accumulation under sprinkle irrigation. Palmerston North. Moseley, G. and D.W. Griffiths. 1984. The min- Trans. ASAE. 27:449Ð455. Mayland, H.F. and F.A. Sneva. 1983. Effect of eral metabolism of sheep fed high and low mag- Ward, J.D. and J.W. Spears. 1999. The effects soil contamination on the mineral composition nesium selections of Italian ryegrass. Grass and of lowÐcopper diets with or without supplemen- of forage fertilized with nitrogen. J. Range Forage Sci. 39:195Ð199. tal molybdenum on specific immune responses Manage. 36:286Ð288. National Research Council (NRC). 1980. of stressed cattle. J. Anim. Sci. 77:230Ð237. Mayland, H.F. and S.R. Wilkinson. 1989. Soil Mineral tolerance of domestic animals. National Wu, L. and Z.Z Huang. 1991. Chloride and sul- factors affecting magnesium availability in Academy Press. Washington, D.C. fate salinity effects on selenium accumulation plant-animal systems: a review. J. Anim. Sci. Nicholas, D.J.D. and A.R. Egan. 1975. Trace ele- by tall fescue. Crop Sci. 31:114Ð118. 67:3437Ð3444. ments in soilÐplantÐanimal systems. Academic Mayland, H.F., T.R. Kramer, and W.T. Press, Inc., N.Y. Johnson. 1987. Trace elements in the nutrition O’Toole, D., M. Raisbeck, J.C. Case, and T.D. and immunological response of grazing live- Whitson. 1996. Selenium-induced “Blind stock. pp. 101Ð113. In: Judkins, M. B., Clanton, Staggers” and related myths. A commentary on D. C., Petersen, M. K., and Wallace, J. D. (eds.) the extent of historical livestock losses attrib- Proc. Grazing Livestock Nutrition Conference. uted to selenosis on Western US rangelands. 23Ð24 July, Jackson, Wyo. Vet. Pathol. 33:104Ð116. Mayland, H. F., R.C. Rosenau, and A.R. Parker, K.G. 1957. “Water–belly” (urolithiasis) Florence. 1980. Grazing cow and calf respons- in range steers in relation to some characteris- es to zinc supplementation. J. Anim. Sci. tics of rangeland. J. Range Manage. 51:966Ð974. 10:105Ð111. Mayland, H.F., G.E. Shewmaker, and R.C. Reid, R.L. and D.J. Horvath. 1980. Soil chem- Bull. 1977. Soil ingestion by cattle grazing istry and mineral problems in farm livestock. A crested wheatgrass. J. Range Manage. review. Anim. Feed Sci. Tech. 5:95Ð167. 30:264Ð265. Reid, R.L. and G.A. Jung. 1970. Mineral compo- Mayland, H.F., J.L. Wright, and R.E. Sojka. sition of forages. West Virginia Agr. Exp. Sta. 1991. Silicon accumulation and water uptake by Bull. 589T. wheat. Plant and Soil 137:191Ð199

446 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 J. Range Manage. 54: 447Ð461 July 2001 Alkaloids as anti-quality factors in plants on western U.S. rangelands

JAMES A. PFISTER, KIP E. PANTER, DALE R. GARDNER, BRYAN L. STEGELMEIER, MICHAEL H. RALPHS, RUSSELL J. MOLYNEUX, AND STEPHEN T. LEE

Pfister and Ralphs are rangeland scientists, Panter is a reproductive toxicologist, Gardner and Lee are research chemists, and Stegelmeier is a veterinary pathologist with the USDA-ARS Poisonous Plant Research Laboratory, 1150 E. 1400 N., Logan, Ut. 84341. Molyneux, a research chemist, is with the USDA- ARS Western Regional Research Center, Albany, Calif. 94710.

Abstract Resumen

Alkaloids constitute the largest class of plant secondary com- Los alcaloides constituyen la clase mas grande de compuestos pounds, occurring in 20 to 30% of perennial herbaceous species secundarios de las plantas y ocurren en un 20 a 30% de las in North America. Alkaloid-containing plants are of interest, first especies herbáceas perennes de Norte América. Las plantas que because alkaloids often have pronounced physiological reactions contienen alcaloides son de interés, primero porque cuando el when ingested by livestock, and second because alkaloids have ganado consume alcaloides a menudo producen pronunciadas distinctive taste characteristics. Thus, alkaloids may kill, injure, reacciones fisiológicas y segundo porque tienen caracteristicas or reduce productivity of livestock, and have the potential to distintivas de sabor. Así, los alcaloides pueden matar, dañar o directly or indirectly alter diet selection. We review 7 major cate- reducir la productividad del ganado y tienen el potencial para gories of toxic alkaloids, including pyrrolizidine (e.g., Senecio), alterar directa o indirectamente la selección de la dieta. quinolizidine (e.g., Lupinus), indolizidine (e.g., Astragalus), diter- Revisamos 7 categorías principales de alcaloides tóxicos, penoid (e.g., Delphinium), piperidine (e.g., Conium), pyridine (e.g., incluyendo pirrolizidinae (por ejemplo, Senecio), quinolizidina Nicotiana), and steroidal (Veratrum-type) alkaloids. Clinically, (por ejemplo, Lupinus), indolizidina (por ejemplo, Astragalus), effects on animal production vary from minimal feed refusal to diterpenoide (por ejemplo, Delphinium), piperidina (por ejemp- abortion, birth defects, wasting diseases, agalactia, and death. lo, Conium), pyridina (por ejemplo, Nicotiana), and esteroidal There are marked species differences in reactions to alkaloids. (tipo Veratrum). Clínicamente, los efectos de los alcaloides sobre This has been attributed to rumen metabolism, alkaloid absorp- la producción animal varían desde el rechazo mínimo del ali- tion, metabolism, excretion or directly related to their affinity to mento al aborto, defectos de nacimiento, enfermedades mer- target tissues such as binding at receptor sites. In spite of alka- mantes, agalacia y la muerte. Hay marcadas diferencias entre loids reputed bitter taste to livestock, some alkaloid-containing especies en cuanto a las reacciones a los alcaloides. Esto has sido plant genera (e.g., Delphinium, Veratrum, Astragalus, Oxytropis, atribuido al metabolismo del rumen, la absorción del alcaloide, and Lupinus) are often readily ingested by livestock. Management el metabolismo, la excreción o directamente relacionado a su schemes to prevent losses are usually based on recognizing the afinidad con los tejidos blanco, tal como fijarse en sitios recep- particular toxic plant, knowing the mechanism of toxicity, and tores. A pesar de que los alcaloides tiene reputación de ser de understanding the temporal dynamics of plant alkaloid concen- sabor amargo para el ganado, algunos géneros de plantas que tration and consumption by livestock. Once these aforementioned contienen alcaloides (por ejemplo, Delphinium, Veratrum, aspects are understood, losses may be reduced by maintaining Astragalus, Oxytropis y Lupinus) a menudo son ingeridas por el optimal forage conditions, adjusting grazing pressure and timing ganado. Los esquemas de manejo para prevenir perdidas usual- of grazing, aversive conditioning, strategic supplementation, mente son basados en reconocer una planta tóxica en particular, changing livestock species, and herbicidal control. conociendo el mecanismo de toxicidad y entendiendo las dinámi- cas temporales de la concentración de alcaloides en la planta y su consumo por el ganado. Una vez los aspectos antes mencionados Key Words: poisonous plants, plant toxins, forage quality, diet son entendidos, las perdidas se pueden reducir manteniendo selection, grazing management condiciones forrajeras óptimas, ajustando la presión y tiempo de apacentamiento, induciendo un condicionamiento aversivo, uti- Alkaloids are a chemically-diverse group of plant compounds lizando suplementación estratégica, cambiando las especies de with widely varying biological activities when consumed. ganado y controlando las especies toxicas con herbicidas Although most effects are thought to be detrimental, many alkaloids have been developed into beneficial drugs and pharmaceuti- cals. Range plants that contain alkaloids, poison more livestock worldwide than any other class of toxic compounds. The economic loss to the livestock industry specifically from alkaloid- Invited paper presented at the symposium “Anti-Quality Factors in Rangeland containing plants is not known, but livestock losses in cattle and and Pastureland,” Feb. 23-24, 1999, Omaha, Nebraska. Pfister’s email: sheep in the western states to all toxic plants are estimated to [email protected]. exceed $340 million (Nielsen et al. 1988), not including horses Manuscript accepted 27 Nov. 00.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 447 Table 1. Direct and indirect economic losses from poisonous plants related to production and off Do Alkaloids Alter Diet take from domestic livestock and wildlife. Alkaloid-containing plants are responsible for the majority of livestock losses to poisonous plants worldwide. Selection?

Direct losses Indirect losses Alkaloids are reported to taste bitter Death Added fencing to restrict access (Bate-Smith 1972). Garcia and Hankins Wasting/reduced weight gains Herding costs (1975) argued that animals acquire natural Neurological incapacitation (horses) Supplemental feeding aversions to most alkaloids because bitter Abortions Changes in grazing management taste is often linked with toxicity. Some Weak/small offspring Increased veterinary costs for treatment Reduced fertility Lack of immune response to vaccines forage plants such as reed canarygrass Birth defects Lost opportunity to graze forage (Phalaris arundinaceae L.) and certain Inability to sell/harvest animals Lost nutrients in ungrazed forages lupines (Lupinus spp.) are unpalatable Reduced land values because of high alkaloid concentrations Reduced value of grazing permits (Ralphs and Olsen 1987). Nonetheless, Herbicide costs for suppression Robinson (1979) and Glendinning (1994) Increased risk in overall enterprise concluded that alkaloids are not universally repellent to herbivores. Additionally, and goats. This estimate includes only because specific structural features are Molyneux and Ralphs (1992) suggest that death and reproductive losses (e.g., abor- responsible for the biological activity of some toxic alkaloids are not bitter tasting to tions), but other indirect costs also impact the individual compounds. Some alkaloids livestock. Sheep (Arnold and Hill 1972), the livestock industry (Table 1). Our possess a close structural similarity with cattle (Pfister et al. 1996a, Panter et al. objective is to scrutinize the effects of neurotransmitters such as acetylcholine 1997), and pigs (Panter et al. 1985) do not alkaloid-containing plants on livestock (Ach), dopamine and serotonin. This necessarily avoid bitter tastes, nor do sheep production on western rangelands and out- structural similarity partially explains the form stronger aversions to bitter than to line management solutions. We sequen- toxicity of some alkaloids in the central sweet flavors (Launchbaugh et al. 1993). tially review 7 major categories of toxic nervous system (CNS). As a rule, grazing animals are not deterred alkaloids, including pyrrolizidine, quino- Alkaloids occur in about 20% of all vas- by the supposed bitterness of alkaloid-con- lizidine, indolizidine, diterpenoid, piperi- cular plants, with most found in dicotyle- taining plants. Intake of alkaloid-containing dine, pyridine, and steroidal alkaloids. dons (Hegnauer 1963, 1988, Hazlett and plants is primarily regulated by positive or Sawyer 1998). More than 33% of annual negative postingestive consequences (see herbs in North America contain alkaloids Launchbaugh et al. this volume). Alkaloids—Definition and (Levin 1976). Fortunately for livestock Distribution producers, the only monocotyledon family with significant (> 0.05% of dry weight) Indolizidine alkaloids alkaloid concentration is Liliaceae Alkaloids are difficult to define because (Robinson 1979). Obviously, this state- of their diversity, but the alkaloid chemist Major Plant Species ment ignores alkaloids in monocots pro- The indolizidine alkaloid, swainsonine, S.W. Pelletier (1983) defined alkaloids as duced by fungal endophytes (see “a cyclic organic compound containing is the toxin in locoweeds (Molyneux and Thompson et al. this volume). The major James 1982), found within the Astragalus nitrogen...” The presence of a nitrogen alkaloid-containing plants on western atom usually makes alkaloids basic, as and Oxytropis genera of the Fabaceae. ranges are classified by the type of alka- There are more than 350 species of suggested by their name. Alkaloids are loid they contain (Table 2). classified by their heterocylic ring struc- Astragalus and about 30 species of ture and the location of the nitrogen atom Oxytropis in North America. Of these in the ring. Ring structure is important species, only about 10 Astragalus and 2

Table 2. Major classes of plant alkaloids, livestock species primarily affected, body system(s) affected, and major plant genera containing the alkaloids.

Type of Alkaloid Animal Species Body System(s) Affected Plants Containing Toxin Primarily Affected Common name Scientific name Diterpene Cattle Muscle paralysis larkspur Delphinium species Pyrrolizidine Cattle, horses Liver toxin; photosensitization groundsel Senecio species houndstongue Cynoglossum officinale Steroidal (solanum type) Cattle, sheep, horses CNS1 toxin; digestive tract nightshades Solanum species Steroidal (veratrum type) Sheep Birth defects; lung congestion skunk cabbage Veratrum species death camas Zigadenus species Piperidine Cattle, sheep, horses, pigs CNS toxin; birth defects poison hemlock Conium maculatum lupine Lupinus species tobacco Nicotiana species Quinolizidine Cattle, sheep, horses Respiratory paralysis;birth defects lupine Lupinus species Indolizidine Horses, cattle, sheep Digestive, reproductive & CNS locoweed Astragalus and Oxytropis spp. Pyridine Cattle, horses, pigs, sheep CNS toxin; birth defects tobacco Nicotiana species 1CNS = central nervous system

448 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 3. Major locoweed species containing indolizidine alkaloids, primary distribution in the western U.S., and range of swainsonine concentration (mg/g dry weight).

Range in Scientific name1 Common name Distribution Concentration Astragalus ----(mg/g)---- allochrous rattleweed southern California east to Texas 0.7 to 11.52,3 bisulcatus two-grooved milkvetch southern Canada south to New Mexico 0.0 to 0.42,3 drummondii Drummond milkvetch southern Canada south to northern N.M. 0.603 emoryanus red-stemmed peavine Utah and southwestern states into Texas 0.5 to 14 lentiginosus freckled milkvetch western Canada to California; Rocky 0.05 to 0.43,6,7 Mountains south into Arizona to Texas lonchocarpus great rushy milkvetch Nevada, Utah, Colorado, and southwestern 0.0 to 4.42,3,5 states missouriensis Missouri milkvetch southern Canada south to New Mexico 0.12 to 0.182,3 and Texas mollissimus woolly locoweed Utah and Wyoming south to Mexico 0.02 to 10.32,4,5,6 praelongus stinking milkvetch Utah, Nevada, Colorado and southwestern 0.03 to 0.22,3,5 states east into Texas tephrodes ashen milkvetch Nevada, southwestern Utah and New Mexico, 0.0 to 0.92,3 Arizona, and California Oxytropis lambertii Lambert’s locoweed southern Canada south to Arizona and 0.2 to 1.02,5 New Mexico sericea whitepoint locoweed northwest Canada south to Nevada, New 0.05 to 1.23,5,7 Mexico and Oklahoma 1Many species have one or several varieties, but that level of detail is beyond the scope of this paper 2Smith et al. 1992 3Fox et al. 1998 4Davis et al. 1984 5R.J. Molyneux, personal communication 6D.R. Gardner, personal communication 7Molyneux et al. 1989

Oxytropis species have been found to con- Elbein 1989). These accumulated old result in similar etiology and further tain swainsonine (Table 3). Many of these oligosaccharides damage cells in thyroid, increases in dosage do not increase the toxic species are located around the brain, pancreas, and kidney tissue, charac- severity of intoxication (Stegelmeier et al. Colorado Plateau, the Great Basin, and terized as foamy cytoplasmic vacuolation 1995a); however, this threshold is low and portions of the Great Plains. Some (Van Kampen and James 1970, relatively small doses have been shown to Astragalus species contain nitro-toxins Stegelmeier et al. 1995a). Inhibition of produce both clinical and histologic (e.g., Astragalus miser Dougl. ex Hook; Golgi mannosidase II results in abnormal lesions. For example, sheep were intoxicat- see Majak and Benn, this volume) or sele- glycosylation of proteins, affecting hor- ed with average daily swainsonine doses of nium (e.g., Astragalus bisulcatus (Hook.) mones, membrane receptors, and enzymes 0.21 mg/kg body weight/day (as ingested Gray). Other genera worldwide contain throughout the body. Once a sufficient plant material, Pfister et al. 1996b). swainsonine, including Swainsona spp. number of cells are damaged, signs of Swainsonine is water-soluble, and is (Colegate and Dorling 1997) and Ipomoea poisoning are seen, which may occur with- rapidly excreted (Stegelmeier et al. (Molyneux et al. 1995). Within the U.S., in 3 weeks (Van Kampen and James 1995b). Clearance time (T1/2) for swain- Ipomoea spp. (morning glory) have not 1970). Microscopically, damage in the sonine from most tissues is about 20 been examined for swainsonine, but CNS results from vacuolar degeneration of hours; however, for the liver and kidneys Ipomoea batatas (L.) Lam. (sweet potato) both neurons and glia (Stegelmeier et al. it is much longer and requires about 60 can be toxic to livestock through an unre- 1994). Pathological lesions appear within hours. Swainsonine is distributed through- lated mechanism. 1 week after locoweed feeding begins out all tissues and is present in many ani- (Van Kampen and James 1970), and when mal products. Thus, current recommenda- Mechanism of Intoxication locoweed feeding ceases, the cytoplasmic tions are that animal products not be used, Swainsonine has a chemical structure vacuoles disappear quickly (James and and intoxicated animals withheld from similar to mannose and glucose, and this Van Kampen 1971). Residual CNS lesions slaughter for about 8 days after animals similarity may be the basis of its toxicity may resolve quickly depending on the discontinue locoweed ingestion (T1/2 x (Colegate et al. 1989). Swainsonine extent of intoxication (Pfister et al. 10; Stegelmeier et al. 1998a). Lactating inhibits several intracellular mannosidase 1996b), but once a particular threshold is animals that eat locoweed will excrete enzymes responsible for cleaving sugar exceeded, CNS damage becomes perma- swainsonine into the milk within 30 min molecules from oligosaccharides (Broquist nent (James and Van Kampen 1971), and (Broquist 1986); therefore nursing young 1986). Inhibition of ∝-mannosidase and the animal likely will display long-term may become intoxicated (James and subsequent failure to trim mannose from abnormal behavior (Pfister et al. 1996b). Hartley 1977). oligosaccharides, results in accumulation There appears to be a dose-response of mannose-rich oligosaccharides in lyso- threshold for swainsonine, such that Clinical Signs somes and causes cellular disruption, and incomplete enzyme inhibition occurs at The symptoms of locoweed poisoning eventual cell death (Dorling et al. 1989, lower doses. Doses at or above the thresh- are lethargy, muscular incoordination,

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 449 intention tremors, nervousness, and had seizures that severely disrupted pre- should not over-stock or over-utilize excitability, progressing to emaciation, hension and mastication. The loss of body locoweed-infested ranges, and should man- possible maniacal behavior when stressed, condition may also be a direct result of age for sufficient desirable forage so that and death. Horses may be particularly sus- swainsonine on hormonal and digestive grazing pressure does not impel livestock ceptible to intoxication (James and Van functions (Stegelmeier et al. 1995a). Both to begin eating locoweed. When animals Kampen 1971) and may be dangerous aspects probably operate simultaneously become overtly intoxicated, the most eco- when handled. Abortions and water belly to cause weight loss, because weight loss nomical solution may be to remove them (i.e., hydrops amnii) often occur when is not fully attributable to lower food from pasture, and allow time for recovery pregnant animals eat locoweed (Ralphs et intake (Velastegui et al. 1992). before selling (Torell et al. 1999b). al. 1994b). If the fetus survives in utero Mildly or moderately intoxicated ani- intoxication, the newborn offspring often mals can be salvaged and returned to near Whitepoint locoweed (Oxytropis exhibits abnormal suckling behavior, and normalcy by removing them from may not survive (Pfister et al. 1993). sericea) locoweed, and offering supplements Whitepoint locoweed begins growth in Grazing animals that consume locoweeds (Marsh 1909). This does not ensure that at higher elevations (e.g., > 2200 m) are late winter and early spring on shortgrass such animals will be fully productive and prairie rangelands, and the green leaves increasingly susceptible to congestive normal, but they may regain sufficient right heart failure (James et al. 1983). are often more palatable than are dormant body weight to allow resale (Torell et al. grasses. Livestock readily consume green Locoweed poisoning may be diagnosed 1999b). Notwithstanding, severely intoxi- by determining if animals have been locoweed leaves during the spring when cated animals may not regain lost body cool-season grasses are just beginning exposed to locoweed, and by evaluating weight even with supplemental feeding, clinical and pathological signs; affected growth, and warm-season grasses are dor- and will never be productive no matter mant (Ralphs et al. 1993). Grazing of animals show typical overt signs of poi- how intensive the rehabilitation. soning while living, and have pathological whitepoint locoweed may cease when There are pervasive anecdotal accounts warm season grasses begin active growth lesions upon post-mortem examination. of addiction or of animals “seeking out” With living animals, definitive diagnostic in early summer (Ralphs et al. 1993), or locoweed in preference to other desirable livestock may switch diet selection to tests using serum can verify consumption forage. Marsh (1909) reported that of locoweed (Stegelmeier et al. 1995b). other green locoweeds (Oxytropis lamber- locoweed was addictive to various animals, tii Pursh, Ralphs unpublished data), if Serum tests are not very reliable, however, including mules, pigs and pronghorn ante- if suspected animals have not recently available. On mountain rangelands, cattle lope. Lewin (1931) described livestock prefer immature seed pods of whitepoint (i.e., within 2Ð3 days) been eating addiction to locoweed and to the locoweed, as serum swainsonine quickly locoweed, but may also eat mature pods Australian plant Swainsona, long before it and green leaves later in the summer, par- disappears, and enzyme concentrations was known that Swainsona and locoweed quickly return to normal ranges. Future ticularly if grazing pressure is excessive. contained the same toxin. Recent reports of (Ralphs 1987). In contrast to shortgrass work will determine if other diagnostic toxicity in South America (Peru and assays, such as determining glycosylation prairie rangelands, whitepoint locoweed Brazil) from morning glory vines on high elevation rangelands is grazed of specific proteins, may be better indica- (Ipomoea spp.) indicate that livestock tors of intoxication. during summer even though other forage become addicted or dependent on these is also green and actively growing (Ralphs plants (Molyneux, personal communica- et al. 1986, Ralphs et al. 1987, Ralphs Effects on Livestock Nutrition and tion; Tokarnia et al. 1992). Ralphs et al. 1987). Simple changes in grazing manage- Grazing Behavior (1990) reported that dried, ground white- ment can have profound positive impacts A dominant feature of locoweed poison- point locoweed (Oxytropis sericea Nutt. in on losses to whitepoint locoweed. For ing in livestock is gradual emaciation (i.e., T. & G.) was not addictive, but some ani- example, Ralphs et al. (1984) reported wasting, Marsh 1909), which may not mals habituated or become accustomed to reductions in cattle losses from over 20% cease when animals are removed from eating the plant material. The obsessive to less than 3% annually from a simple locoweed (James et al. 1969). In studies consumption that producers observe may change in grazing management. at our laboratory, rats, sheep, cattle, and result from locoweed being relatively more horses have all shown declines in food palatable than associated forage (Ralphs et intake and body condition while eating al. 1993), or alternatively, locoweed may Specklepod locoweed (Astragalus locoweed, and the wasting continued after have pharmacological properties that are lentiginosus Dougl. ex Hook.) locoweed feeding ceased. Steers lost reinforcing (Pfister 1999). Limited studies with cattle and horses weight while grazing locoweed, and gains (Pfister unpublished data) suggest that, during spring, likelihood of animals eating did not resume for 45Ð60 days after Management and Control locoweed feeding ceased (Ralphs et al. locoweed increases greatly when animals Swainsonine usually occurs at very low begin to search avidly for newly growing 2000). Overtly intoxicated horses, when concentrations (0.01 to 0.3% of dry removed from locoweed-infested pastures, cool-season grasses (i.e., “chasing green”). weight) in locoweeds (Table 3), with much Cattle prefer dormant grasses to speckle- continued to decline in body condition of the toxin found in the seeds. over 4 weeks even though their appetites pod locoweed (var. diphysus) during much Fluctuations in swainsonine concentration of the spring, but once cattle begin eagerly did not diminish (Pfister unpublished as the plants mature have little effect on data). The loss of productive function may selecting green grass, they also begin eat- how much locoweed is eaten (Ralphs and ing still-green, but drying, locoweed. result directly from neurological damage Molyneux 1989). The growth habits of because of impaired ability to prehend and During winter, cattle will even eat toxic locoweed in relation to other available for- black stems from previous growing sea- masticate food (Ralphs et al. 1991b). ages generally determine if and how much Ralphs et al. (1991b) reported that sheep sons (Ralphs et al. 1988). During spring, of the plant is eaten. Livestock producers horses intensely search for green grass,

450 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 4. Characteristics, relative toxicity, and general concentration range of toxic alkaloids of the dominant larkspur species in the western U.S.

Class/Species Typical height Elevation Associated plant Typical Alkaloid at maturity communities risk of losses1 concentration2 --(cm)-- --(m)-- --(mg/g)-- Tall Larkspurs D. glaucum 90Ð200 >2000 aspen, conifers, alpine meadows low 1Ð20 D. barbeyi 90-180 >2200 aspen, conifers, alpine meadow, moderate to severe 1Ð29 mountain brush, alpine tundra D. glaucescens 76Ð90 >2000 mountain meadows, sagebrush low to moderate 1Ð12 D. occidentale 90Ð180 >2000 mountain brush, sagebrush, low to severe 0Ð18 conifer, aspen Low Larkspurs D. nuttallianum 20Ð60 >1200 mountain brush, sagebrush, aspen, low to severe 2Ð4 conifer, mountain and foothill meadows D. bicolor 20Ð40 >800 mountain brush, sagebrush, low to severe — D. andersonii 10Ð60 >1200 desert shrub, mountain brush, low to moderate 1Ð4 sagebrush, pinion-juniper Plains Larkspur D. geyeri 40-80 >1500 desert shrub, mountain brush, low to severe 1-4 sagebrush shortgrass prairie 1The risk of losing cattle to these species is a subjective evaluation based on plant toxicity, numbers of grazing cattle threatened during the growing season, and the geographical distribution of the larkspur species. D. glaucescens is relatively more toxic late in the growing season compared to mature plants of the other species. 2These concentrations are general values, and were determined by examining numerous samples collected over the past 6 years at the Poisonous Plant Research Laboratory. The values for low and plains larkspurs should be considered preliminary because they are based on small sample sizes. Multi-site and year analysis for low and plains larkspurs is ongoing (Gardner, unpublished data). For further references see review by Pfister et al. (1999). For concentrations in Canadian low larkspur, see Majak (1993). and simultaneously select green locoweed. that they will avoid toxic plants, including eat locoweed. Herbicidal control of Once horses begin to eat locoweed, con- locoweed, in future encounters (Ralphs et locoweed (Ralphs and Ueckert 1988, sumption may continue until they become al. 1997a). In this procedure, animals are McDaniel 1999) in some pastures can pro- very intoxicated. given a taste of the plant in a corral, then vide a relatively “loco-free” pasture for dosed via stomach pump with a solution of critical times. Herbicidal treatment for this Woolly locoweed (Astragalus mollis- lithium chloride (LiCl) at 200 mg/kg body specific purpose is often economical, even simus Torr.) weight. The LiCl-induced illness is associ- though general spraying to eliminate Woolly locoweed is not very palatable ated with the taste of the toxic plant, and locoweed on a ranch-wide basis is usually to grazing cattle, and probably is not animals avoid eating the target species not economical (Torell et al. 1999a). selected by livestock unless grazing pres- (Ralphs 1992). Averted animals must not sure is excessive (Ralphs et al. 1993). be allowed to graze with non-averted com- Consumption of woolly locoweed appears panions, as social facilitation can quickly Diterpenoid alkaloids to cease with the growth of warm-season extinguish the aversion (Ralphs 1997). grasses (Ralphs et al. 1993). Major Plant Species Cyclic or “on-off” grazing Toxic C19 and C20 norditerpenoid alka- Social facilitation Livestock can be poisoned by low level loids occur primarily in 2 genera from When some animals begin to eat locoweed doses given for as little as 4 Ranunculaceae: larkspurs (Delphinium locoweed, these ‘locoeaters’ can influ- weeks (Pfister et al. 1996b). Nonetheless, spp.) and monkshood (Aconitum spp.). ence other grazing animals, including considering both swainsonine’s rapid There are over 50 species each of nursing calves, to begin eating locoweed clearance and dose-response threshold, it Delphinium and Aconitum, but only a few through social modeling (Ralphs et al. may be possible to expose animals briefly are known to cause livestock poisoning. 1994a). In most situations, ranchers should to locoweed with a low-risk of intoxica- Monkshoods are highly toxic plants, but remove animals that eat locoweed to elim- tion, if they are then allowed to recover on we believe that most reports of livestock inate social influences, and to prevent pro- locoweed-free ranges. Recent work with losses to monkshood are attributable to gressive intoxication. Some producers in sheep (Stegelmeier unpublished data) larkspur (Knight and Pfister 1997). The 2 New Mexico with locoweed-infested pas- shows that animals repeatedly given plants grow together in wet mountain habi- locoweed for 10 days with a 14-day recov- tures have reduced their locoweed losses tats and are easily confused; furthermore, ery period had no detectable permanent by systematically, over several years, monkshood is not usually grazed by cattle. removing any cow from their herds seen damage. On-off grazing schemes may work, but must be approached with cau- Larkspurs are divided into 3 general cate- eating locoweed, before the animal either gories based primarily on mature plant becomes intoxicated or influences her calf tion as they have not been tested under field situations. height and distribution: low, tall, and or companions to eat locoweed (D. plains (Table 4). Most research has Graham, personal communication). focused on tall larkspurs (Pfister et al. Herbicidal control 1999). Livestock losses in the western Aversive Conditioning Producers should, if possible, provide a United States to all types of larkspurs prob- Grazing animals may be conditioned so locoweed-free pasture for spring or fall ably exceed $10 million dollars annually. grazing when animals are most likely to

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 451 Toxic Alkaloids and Occurrence Dobelis et al. 1999). Animals usually die trembling, but will be able to walk and Larkspurs contain many (> 18) norditer- from respiratory failure (i.e., asphyxiation) graze. Severely-intoxicated animals will penoid alkaloids of which the most toxic when the muscles of the diaphragm are be laterally-recumbent, and will be unable are methyllycaconitine (MLA), 14- paralyzed or the CNS respiratory center is to do more than thrash about. Marsh et al. deacetylnudicauline (DAN), and nudi- depressed. Larkspur alkaloid binding to (1916) reported that bloat seldom occurs cauline (NUD; Manners et al. 1993, nAch receptors appears to be correlated to in intoxicated animals, but our observa- 1995). Both MLA and DAN occur to some toxicity in various tissues (Kukel and tions suggest that bloat can be a significant extent in all classes of larkspurs, whereas Jennings 1994), and may explain sheep component of larkspur fatalities. Bloating NUD has not been found in tall larkspurs. tolerance to larkspur if larkspur toxins may occur as a result of paralysis of the A fourth alkaloid, deltaline, is relatively bind less avidly to nAch receptors in sheep rumen eructation (belching) mechanism. low in toxicity, but is the dominant alka- (Stegelmeier et al. 1998b). Cattle may die from bloat alone or asphyx- loid in most tall larkspurs, comprising ≥ Toxicity, but not lethality of MLA + iation from aspirated rumen contents while 40% of the alkaloid composition, while DAN has been established for cattle by recumbent from larkspur paralysis. Some MLA and DAN together comprise another oral doses of dried tall larkspur (Pfister et success of early remedies for larkspur poi- 20 to 50% of the alkaloid mix in tall lark- al. 1994b, 1997a). Cattle typically show soning (e.g., bacon fat and turpentine spurs. The MLA is the dominant alkaloid clinical signs when given an MLA + DAN given orally, Glover 1906) may have been in low larkspurs (Majak et al. 1987, Majak dose of about 20 mg/kg body weight due to bloat reduction. and Engelsjord 1988, Bai et al. 1994). (Pfister and Cheney 1998). A 450 kg cow The concentration of MLA and DAN is may show clinical signs after rapidly eat- ≈ Diagnosis and Treatment highest in immature larkspurs (Pfister et ing 1.8 kg of tall larkspur ( 7.2 kg wet Diagnosis of larkspur poisoning is usual. 1994a, Ralphs et al. 1997b). In tall weight). Assuming the plant material used ally by association, as dead or sick ani- larkspurs, MLA concentrations may in Olsen’s (1978) LD50 study (vegetative mals are found near larkspur plants. exceed 20 mg/g. In a Canadian study, and early flowering tall larkspur) con- Because larkspur poisoning causes no tis- Majak (1993) reported high concentrations tained 12 mg/g of toxic alkaloid, the LD50 sue lesions, pathological examination can of MLA (up to 8.7 mg/g) in vegetative low of MLA + DAN in cattle would be about only rule out other possible causes of larkspurs, and 2 mg/g in flowering plants. 30 mg/kg. Early studies by Marsh et al. death. Currently, no field test exists to Before shattering, tall larkspur pods are (1916) suggest that the lethal dose is lower determine if animals have been poisoned relatively high in toxicity (MLA + DAN = when tall larkspur is given repeatedly over by larkspur. Blood or rumen fluid may 7 to 12 mg/g). Toxicity declines rapidly in 3 to 4 days. contain larkspur alkaloids (Holstege et al. tall larkspurs once pods begin to shatter 1996); even so, cattle can eat substantial (Gardner and Pfister 2000), whereas con- Clinical Signs quantities of larkspur without ill effect, centrations are relatively stable in low Clinical signs of intoxication include and the presence of alkaloids in body flu- larkspurs after the vegetative stage (Majak muscular weakness and trembling, strad- ids only suggests larkspur intoxication. 1993, Gardner, unpublished data). dled stance, periodic collapse into sternal A variety of remedies have been applied recumbency, respiratory difficulty, and by ranchers (e.g., bleeding by cutting the Mechanism of intoxication finally death while in lateral recumbency. tail), but most are without scientific ratio- The primary result of larkspur toxicosis Moderately-intoxicated animals will peri- nale. Treated animals probably survive in livestock is neuromuscular paralysis, as odically collapse while moving, and be in because they did not eat a lethal dose of nicotinic acetylcholine (nAch) receptors in sternal recumbency for 10 to 30 min; larkspur and did not bloat. Drugs that the muscle and brain are blocked by MLA when the temporary paralysis subsides, increase acetylcholine concentration at the and related alkaloids (Aiyar et al. 1979, affected animals may show muscular neuromuscular junction have potential for

Table 5. Relative pyrrolizidine alkaloid (PA) concentration and toxicity of various PA-containing plant species on western U.S. rangelands.

Scientific name Common name Distribution Concentration1 Lethal Dose2 ---mg/g------mg/g---. Cynoglossum officinale houndstongue widespread weed in North America 0.5 to 213 5 to 604 Senecio longilobus threadleaf groundsel midwest south into Texas and west into 1 to 875 10 to 136 New Mexico and Arizona riddellii Riddell’s groundsel midwest south into west Texas and New Mexico 2 to 1805 15 to 457 jacobaea tansy ragwort weed in northwestern U.S. 0.2 to 95 2 to 38 vulgaris common groundsel weed in western U.S. 2 to 35 Not available 1The concentration of total pyrrolizidine alkaloids (N-oxide and free base) in dry plant material. Concentrations vary greatly depending on growing conditions and plant part. The high value for S. riddellii (180 mg/g) is the highest recorded concentration of any type of alkaloid in any plant yet recorded (Molyneux and Johnson 1984). 2Lethal dose may be acute (short-term) or chronic (long-term) depending on dose, because toxicity from pyrrolizidine alkaloids may be delayed by weeks or months from the time animals ingest the plant. 3Pfister et al. 1992; Van Damm et al. 1994 4Baker et al. 1991; Stegelmeier et al. 1996 5Johnson et al. 1985a; Molyneux and Johnson 1984 6Johnson and Molyneux 1984 7Johnson et al. 1985b; Molyneux et al. 1991 8Johnson and Smart 1983

452 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 reversing larkspur toxicity. The choliner- rapidly, and leaf toxicity is low (Gardner Herbicidal Control gic drug, physostigmine (0.08 mg/kg i.v.), and Pfister 2000). Larkspur losses can be economically has been successfully used under field and reduced if dense larkspur populations are pen conditions to reverse clinical larkspur Low larkspur (D. nuttallianum Pritz.) and controlled by herbicides. Picloram, met- intoxication (Nation et al. 1982, Pfister et Plains larkspur (D. geyeri Greene) sulfuron, and glyphosate have proven to al. 1994c). Our current recommendation is Consumption of low larkspur by cattle be effective in killing tall larkspurs when that ranchers not attempt to move partial- appears to increase once low larkspur has applied at specific growth stages ly-paralyzed or recumbent animals, as flowered, and higher grazing pressure will (Mickelsen et al. 1990, Ralphs et al. stress is detrimental. If intoxicated ani- increase amounts of low larkspur eaten 1991c, 1992). These herbicides do not mals bloat, passing a stomach tube or (Pfister and Gardner 1999). Spring graz- reduce toxic alkaloid concentrations in puncturing the rumen with a knife or tro- ing of low larkspur-infested ranges can be treated larkspur plants, and metsulfuron car will relieve gas pressure. problematic, as there may not be sufficient may increase toxicity (Ralphs et al. 1998). forage growth to graze these ranges before Therefore, sprayed areas should not be Impacts on Animal Nutrition and larkspur flowers, but risk appears to grazed until larkspur has withered and Behavior increase once flowering occurs. decomposed. Larkspur poisoning is acute, rather than Fortunately, in most years low larkspurs chronic, thus, animals that survive show are short-lived, so producers must avoid essentially no long-term detrimental heavily infested areas for about 4 weeks Pyrrolizidine Alkaloids effects. Ingestion of larkspur at sub-acute during peak toxicity. Four years of grazing doses has no negative impact on ruminal studies on plains larkspur-infested ranges Major Plant Species fermentation or digestive function (Pfister have shown few distinct patterns of con- Pyrrolizidine alkaloids (PAs) occur on et al. 1989). Larkspur poisoning probably sumption by lactating cows (Pfister, western U.S. rangelands primarily in has no long-term effect on diet selection or unpublished data). Senecio spp. (Asteraceae), and in grazing behavior, although previously-poi- Cynoglossum officinale L., (hound- soned animals eat less larkspur and other Other Management Options stongue, Boraginaceae). In the southeast- forage for a few days after a toxic episode Aversive Conditioning ern U.S., Crotalaria spp. (Fabaceae) also (Pfister et al. 1997a, Pfister and Cheney Cattle can be trained to avoid eating tall contain pyrrolizidine alkaloids. 1998). Eventually, larkspur consumption larkspur through aversive conditioning Worldwide, PAs are probably the most returns to previous levels, and animals (Ralphs 1997), as previously noted with economically-important plant toxins may be intoxicated again. locoweed. Social facilitation, whereby one impacting human health, as PAs contami- animal influences another to eat a particu- nate grain for poultry, ruminant, and non- Grazing Management lar plant, will quickly extinguish the aver- ruminant livestock, and human consumption, as well as herbal teas (Huxtable Tall larkspur (D. barbeyi Huth and D. sion, thus, averted cattle must be grazed 1989). About 3% of the flowering plants occidentale (Wats.) Wats.) separately from non-averted cattle (Lane in the world (> 6000 species) contain PAs Cattle eat little or no tall larkspur before et al. 1990, Ralphs 1997). Animals experi- (Smith and Culvenor 1981), and there are the plant has elongated flowering racemes enced in eating larkspur may also be suc- currently nearly 300 individual known (Pfister et al. 1988a, 1997b). Cattle gener- cessfully averted, although the aversion is PAs (Roitman and Panter 1995). The alka- ally begin consuming tall larkspur after initially more difficult to induce and may loid concentrations in range plants and flowering racemes are elongated, and con- be more fragile and less persistent than for subsequent toxicity vary widely (Table 5). sumption increases as larkspur matures. naive animals (Ralphs 1997). Consumption usually peaks during the pod stage of growth in late summer, when cat- Grazing Sheep Before Cattle Mechanism of intoxication tle may eat large quantities (25 to 60% of Marsh et al. (1916) recommended that The PAs occur in either the free-base or diet, Pfister et al. 1988b). ranchers graze sheep before cattle to take N-oxide form in plants, but neither of The period of greatest risk on tall lark- advantage of the low toxicity to sheep, and these forms is toxic to animals per se spur ranges extends from the flower stage Aldous (1917) noted that sheep grazing on (Winter and Segall 1989). The toxicity of into the pod stage. Many ranchers typical- immature D. occidentale in Nevada had PAs is due to the formation of toxic ly defer grazing on tall larkspur-infested reduced the poisoning risk to cattle. On metabolites in the liver termed pyrroles. ranges until the flower stage to avoid tall larkspur-infested ranges where lark- Pyrroles are formed as a detoxification death losses. This approach wastes much spur grows as discrete patches, sheep can intermediate through the action of liver valuable forage, and often places cattle be herded into or bedded on the patches to enzyme systems, primarily mixed function into larkspur-infested pastures when risk reduce larkspur availability or acceptabili- oxidases (MFOs), but the exact mecha- of losses is high. An additional 4 to 6 ty to cattle (Ralphs et al. 1991a, Ralphs and nism is not clear (Winter and Segall weeks of grazing may be obtained by Olsen 1992). In those areas where larkspur 1989). Pyrroles form adducts within the grazing these ranges early, before larkspur is uniformly spaced over a pasture, sheep liver with hepatic proteins and nucleic elongates flowering racemes (Pfister et al. must eat immature larkspur and leave suffi- acids, and damage liver cells, causing 1997b). The risk of losing cattle is low cient feed for cattle. This can be problemat- enlarged hepatocytes, abnormal bile secre- when grazing before flowering even ic, because early growth tall larkspur may tion, and fibrosis (Stegelmeier et al. 1996). though larkspur is very toxic, because not be palatable to sheep (Ralphs et al. A dysfunctional liver leads to other syn- larkspur consumption is very low. Once 1991a). Sheep grazing has successfully dromes such as chronic wasting disease pods are mature and begin to shatter, lark- reduced cattle losses on ranges with D. and photosensitization. The PAs can also spur ranges can usually be grazed with glaucescens in southwestern Montana (J. cause lesions in the lungs and brain. impunity because pod toxicity declines Helle, personal communication).

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 453 Clinical Signs and Diagnosis behavior directly. For example, horses tongue when other forage was adequate Poisoning from PAs may be either acute may show typical “head pressing” behav- (Pfister unpublished observations). When (high-dose and short-term) or chronic ior as a result of ammonia toxicity from houndstongue contaminates hay, it is read- (lower-dose and long-term). Acute intoxi- liver damage (Cheeke 1989). Intoxicated ily eaten by cattle and horses, and is quite cation is less common, as most animals animals may become intractable and diffi- toxic (Baker et al. 1989). poisoned by PAs develop clinical signs cult to handle as the disease progresses; in slowly over many weeks or months the final stages of poisoning animals may (Cheeke 1989). Acute intoxication can stagger greatly. Liver damage can lead to Quinolizidine Alkaloids kill animals within 1 day if sufficient plant secondary photosensitization, and as material is ingested (Baker et al. 1991). affected animals are sensitive to sunlight, Major Plant Species Chronic intoxication usually results from they become solitary and spend excessive The most problematic plant genera with ingestion of the PA-containing plant for amounts of time seeking shade instead of quinolizidine alkaloids is Lupinus several weeks (Baker et al. 1991, grazing. Severe sunburn may occur espe- (Fabaceae). Although lupine is cultivated Stegelmeier et al. 1996). Typical clinical cially on exposed areas such as the nose, in some parts of the world as forage or signs include depression and lethargy, vulva, udder, etc. Photosensitized, lactat- grain (so-called sweet lupine), in the west- anorexia, and ascites (fluid accumulation ing cows will often develop very inflamed ern U.S. many wild lupine species are in abdomen). None of these signs are spe- and sensitive udders, especially light-pig- toxic to livestock because of high alkaloid cific for PAÐinduced toxicity, thus, the mented animals, and will prematurely concentrations (Keeler 1989). Wink et al. diagnosis is usually made from a liver wean their nursing young. (1995) recently reported on the alkaloid biopsy and associated histopathology. concentration of 36 lupine species from Enlarged liver cells were the dominant Management and Control North America; most contain quinolizidine lesion seen in horses 6 months after they Senecio species alkaloids, but a few also contain piperidine were dosed with a low dose of alkaloids. Managing rangelands so that plant com- alkaloids or both types of alkaloids. Serum chemistry changes may be dramat- munities are in good condition and ade- ic, as many liver enzymes are altered, but quate forage is available is crucial to these changes are also not specific for PA- Mechanisms of Intoxication reducing losses to Senecio spp. (Merrill Quinolizidine alkaloids are both toxic poisoning. Wasting disease (i.e., severe and Schuster 1978). Generally, senecios emaciation) as a result of liver damage is and teratogenic (i.e., causing birth defects) are not very palatable, and are avoided by to livestock (Panter and James 1995). commonly noted, as is “hard, yellow grazing livestock if other forage is avail- liver” disease; all these conditions may be Lupines cause respiratory failure in sheep able. Drought stress and overgrazing can (Kingsbury 1964), but the mechanism is related to PA-induced damage to the liver, increase populations of threadlleaf ground- but can be caused by other toxic plants unknown. Lupine alkaloids bind differen- sel, as the plant is an aggressive invader tially to both nicotinic and muscarinic Ach and diseases (Stegelmeier et al. 1996). (Sharrow et al. 1988). Drought is an espe- Younger animals are more susceptible receptors (Schmeller et al. 1994), and cially dangerous time because other forage affect Na+ and K+ ion channels (Wink et to PA-induced toxicosis because the higher may be lacking and the toxic alkaloid con- metabolic activity of growing liver tissue al. 1995), but a specific relationship to centration in senecio plants increases dur- toxicity has not been developed. Birth encourages pyrrole formation and results ing drought (Molyneux and Johnson in more extensive liver damage (Cheeke defects are apparently caused by the 1984), so grazing animals may ingest high- effects of 2 different, but related, alka- 1989). The PAs are transferred in milk to er quantities of more toxic forage. Senecio nursing young, and there is a danger of loids, anagyrine (a quinolizidine alkaloid, species are also most toxic when plants are Table 6) and ammodendrine (a piperidine human consumption via milk (Molyneux reproducing, thus avoiding pastures when and James 1990). There are marked alkaloid; Panter et al. 1992). For unknown these plants are in bud, flower, or seed is reasons, cattle are uniquely sensitive to the species differences in tolerance for PAs, as prudent. Proper grazing management must goats and sheep are relatively more resis- effects of anagyrine, and ingestion of alka- consider stocking rates, as improper stock- loid-rich lupine causes the condition tant to PA-poisoning than cattle and horses ing may increase the amount of toxic plant (Cheeke and Huan 1995). Detoxification of “crooked calf disease” in bovine offspring consumed when alternative forages (Table 6, Keeler 1989, Panter et al. 1994). PAs occurs to a limited extent in the rumen become limited. Excessive stocking may (Wachenheim et al. 1992), but the liver Crooked calf disease has been associated lead to degradation of the desirable plant with Lupinus laxiflorus Douglas ex Lindl., appears to be the major site of detoxifica- community allowing Senecio species to tion (Cheeke 1994). L. caudatus Kellogg, and L. sericea Pursh increase. Herbicidal control may alleviate (Panter et al. 1992). Crooked calf disease some problems if incorporated into an is caused by reductions in fetal movement Impacts on Animal Nutrition and overall management program (Sharrow et during a susceptible period in gestation Behavior al. 1988). (Panter et al. 1988a). This reduction in Poisoning by PAs clearly has a great fetal movement at the critical time is likely impact on the nutrition of grazing and pen- Houndstongue (Cynoglossum officinale) to interfer with bone, muscle and ligament fed animals. Animals with compromised Houndstongue is not only a toxic plant, development, resulting in mild to lethal liver function will generally show slow but also a noxious weed that is increasing skeletal malformations and cleft palate in weight loss over a long period of time in North America. The plant spreads from calves (Panter et al. 1990, 1988a). Even (perhaps years). Further, PA-intoxication bur-like seeds that cling to animals and though many calves are born alive, most may interfere with mineral and vitamin humans alike, and invades disturbed areas. of these deformities make them virtually nutrition to further degrade animal perfor- Houndstongue is generally unpalatable worthless, and most deformed calves are mance (Cheeke 1989). when growing on rangelands, but we have destroyed shortly after birth. Intoxication by PAs can affect animal observed lactating cows eat green hounds-

454 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 6. Potentially teratogenic Lupinus species nutritional properties and to reduce their Washington, Oregon, Idaho, and Montana, 1 on western U.S. rangelands . Ingestion by alkaloid content for both livestock and causing severe losses. For example, pro- pregnant cattle of Lupinus species with ter- human consumption (Aniszewski 1993). ducers in Adams County, Washington lost atogenic alkaloids (quinolizidine or piperidine) from gestation day 40Ð100 may cause Lupines, being legumes, may contain > over 30% of their calves (> 4000 calves) severe deformities in calves (i.e., crooked calf 20% crude protein (Panter et al. 1999). from lupine-caused birth defects (Panter et disease). So-called “sweet” lupines are relatively al. 1999). low in alkaloid concentrations, and are an Scientific name Common name excellent source of protein for livestock Lupinus (Stanford et al. 1996). Range-grown Piperidine Alkaloids albicaulis pine lupine lupines, particularly the seed pods, are a albifrons white face lupine good source of nutrition if they are low alpestris mountain silvery lupine Major Plant Species enough in alkaloids that toxicity problems Piperidine alkaloids are broadly distrib- andersonii Anderson’s lupine do not develop (Panter et al. 1999). argentous silvery lupine uted in nature, but only a few range plants arbustus2 spur lupine have sufficient amounts to cause toxicity bakeri2 Management and Control problems for domestic livestock. Several burkei Burke’s lupine Losses of livestock from lupine poison- Lupinus species (Fabaceae) contain piperi- caudatus tailcup lupine dine alkaloids (Table 6), in addition to densiflorus ing can largely be prevented by under- elatus standing 2 interrelated aspects. First, the quinolizidine alkaloids (Roitman and Panter elagans highest concentrations of toxic alkaloids 1995). The suspected toxic piperidine alka- excubitus tend to occur in immature lupine plants loids in Lupinus are ammondendrine and N- erectus tall silvery lupine and seed pods. Anagyrine concentrations methyl hystrine (Panter and James 1995). evermannii Everman’s lupine 2 are highest (> 5 mg/g) in early growth, Recently, 8 yearling steers died after eating formosus Lunara lupine Lupinus argenteus Pursh containing high holosericeus and decline to less than 0.5 mg/g after humicola lowland lupine seed shatter, except that concentrations levels of ammondendrine and N-methyl latifolius broadleaf lupine increase when lupine seeds ripen (Keeler ammodendrine (Panter, personal communi- laxiflorus looseflower lupine 1976). Second, pregnant cattle are suscep- cation). These cattle began grazing L. leucophyllus velvet lupine tible to the teratogenic effects of alkaloids argenteus after grasses were depleted. longifolius during a window from days 40 to 70 of The most prominent species containing montigenus Mt. Rose lupine piperidine alkaloids is poison hemlock nootkatensis Nootka lupine (Alaska) gestation, occasionally extending to 100 polyphyllus Washington lupine days (Panter et al. 1997). Birth defects in (Conium maculatum L., Apiaceae). Only 1 rivularis stream lupine cattle can be prevented by using breeding species of Conium grows in North ruber red lupine or grazing programs that avoid placing America, and should not be confused with sericeus silky lupine pregnant cattle in lupine-dominated pas- water hemlock (Cicuta maculata L.). sulphureus yellow lupine tures in the first trimester of gestation Poison hemlock grows in disturbed areas, 1 Adapted from Davis (1982), Davis and Stout (1986) and (Keeler et al. 1977, Panter et al. 1992, waste land, and along waterways, invad- Wink et al. (1995). Species were listed if they contain any of the quinolizidine alkaloid, anagyrine. 1999). Alternatively, risk can be reduced ing perennial hayfields and pastures. The 2These species contain piperidine alkaloids (e.g., ammon- by allowing only short-term access to first alkaloid ever characterized (coniine) dendrine) that are also teratogenic when eaten by cattle lupines by pregnant cattle in some form of was isolated from poison hemlock in 1827 (Panter et al. 1998b). rotational grazing scheme (Panter et al. (Panter and Keeler 1989). In addition to 1999). Herbicidal control of lupines is fea- coniine, poison hemlock contains 4 other Clinical signs sible (Ralphs et al. 1991d), but chemical alkaloids, of which the most toxic alkaloid Lupine toxicity is seen clinically as a control is usually more expensive than is ϒ-coniceine, the biogenic precursor for neurologic disease that progresses from altering a grazing management program. the other Conium alkaloids (Panter and depression and lethargy to muscular weak- Acute toxicity problems are less com- Keeler 1989). The ϒ-coniceine is about 8 ness, collapse, respiratory failure and mon now, but large sheep losses occurred times more toxic than coniine (Bowman death (Panter et al. 1999). Animals that frequently 100 years ago (Chesnut and and Sanghvi 1963, Panter et al. 1998a), survive for 1 or 2 days may recover com- Wilcox 1901). Deaths losses usually occur and this difference has important manage- pletely (Panter et al. 1999), or they may when livestock, usually sheep, ingest a ment implications. succumb several days later (Kingsbury large amount of seed pods in a short peri- 1964). Pregnant cows that eat small od of time (James et al. 1968). This can Alkaloid Occurrence amounts of lupine may not show clinical occur from contaminated hay or from hun- The alkaloid concentration and distribu- signs of intoxication, but give birth to gry animals gaining access to lupine-dom- tion of alkaloids in poison hemlock are deformed offspring (e.g., cleft palate, inated forage, and can be prevented by affected by many factors, including envi- Panter et al. 1994). While sheep, goats, using lupine-free hay and avoiding lupine- ronmental changes and plant maturity and cattle may show signs of acute lupine dominated ranges when other forage is (Cromwell 1956, Leete and Olson 1972). toxicity such as depression and death, the scarce. During some years, lupine popula- Drought stress increases total alkaloid anygyrine-containing lupines cause birth tions will temporarily expand on range- concentrations (Fairbairn and Challen defects in cattle only (Panter et al. 1998b). lands not normally problematic. Livestock 1959). Immature poison hemlock often producers need to be aware of lupine pop- has a high concentration of ϒ-coniceine, ulations and be sufficiently alert to alter which may then be converted predomi- Impacts on Animal Nutrition grazing or breeding programs when these Many lupines are not toxic to livestock, nately into coniine during active growth. eruptions occur. Lupine populations and plant breeders have conducted exten- During flowering, concentrations of ϒ-con- increased dramatically during 1997 in sive breeding programs to enhance lupines iceine also shift to coniine. Thus, coniine is

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 455 the major alkaloid in mature plants and toxicity is made from a knowledge of (Keeler 1979). Anabasine causes fetal seed, whereas ϒ-coniceine dominates the exposure to the plant, and from clinical malformations virtually indistinguishable alkaloid mix in early growth and fall signs. Additionally, many reports suggest from those caused by Lupinus and Conium regrowth. Leaves from young or regrowing that affected animals have a “mousy” odor (Panter and James 1995). plants contain 3 to 6 mg/g of toxic alka- on their breath or urine. Alkaloid screen- loids, whereas immature and mature fruit ing can detect the presence of poison hem- may contain > 10 mg/g (Cromwell 1956). lock alkaloids in body fluids, providing Steroidal (Veratrum-type) confirmation that animals were ingesting Alkaloids Mechanism of Intoxication the plant (Galey et al. 1992). Poison hemlock alkaloids act on both Major Plant Species smooth and striated muscle; the effect on Management and Control The steroidal veratrum-type alkaloids skeletal muscle is a curare-like neuromus- The most critical time of the year to are found primarily in Veratrum species cular blockage, similar to larkspurs. avoid poison hemlock is spring because (false hellebore) and Zigadenus species Unlike larkspur alkaloids, blockage occurs the plant often appears before other forage (death camas, Liliaceae). Western false- only after initial muscular stimulation has emerged. Green seed pods may be hellebore (Veratrum californicum Durand) (Bowman and Sanghvi 1963). When the eaten in mid-to-late summer (Panter and is the dominant species in the western dose is sufficient, the blockage causes Keeler 1989). Furthermore, poison hem- U.S., and occurs in moist mountain mead- muscular paralysis, resulting in depressed lock may regrow in fall after seed shatter. ows, and along slopes and stream banks. respiration. The specific site of blockage Ingestion during fall may coincide with Death camas grows on plains, prairies, and at the neuromuscular junction is not fetotoxicity in pregnant cattle, if they are foothill ranges throughout the western known, nor is the exact mechanism in the first trimester (days 30Ð75, Panter et U.S. There are several species of death (Panter and Keeler 1989). Poison hem- al. 1988b). If poison hemlock has invaded camas, and all should be considered toxic lock alkaloids are also potent teratogens, hay fields, the contaminated hay can poi- even though toxicity can vary within and and ingestion during pregnancy induces son livestock. Even though toxicity among species (Panter and James 1989). skeletal malformations that are virtually decreases upon drying, sufficient toxin indistinguishable from those caused by may be retained to poison livestock (Galey lupines (Panter et al. 1988b). The mecha- et al. 1992). Cattle appear to be particular- Alkaloids and Mechanism of nism of fetotoxicity is thought to be the ly susceptible because of their acceptance Intoxication same, namely reductions in fetal move- of the plant and their sensitivity to the ter- Veratrum species ment during critical phases of gestation atogenic alkaloids. Poison hemlock can be False hellebore has long been recog- (Panter et al. 1988a). easily controlled with phenoxy herbicides nized as a toxic plant for livestock (Hall (Panter et al. 1988b). and Yates 1915), although false-hellebore- Clinical Signs and Diagnosis induced fetotoxicity in sheep was not Poison hemlock causes initial CNS Impacts on Grazing Behavior reported until 1962 (Binns et al. 1962). stimulation with frequent urination and Poison hemlock is reported to be habituat- The primary teratogen is cyclopamine; the defecation, dilated pupils, increased heart ing or even addictive (Kingsbury 1964, closely-related alkaloid veratramine is rate, muscular weakness and trembling Panter and Keeler 1989). Goats (Copithorne very toxic but does not produce abnormal- and ataxia. This initial stage is followed 1937), cows (Penny 1953), and pigs (Panter ities (Keeler 1983). Ingestion of false by depression with further muscular weak- et al. 1985) readily eat fresh hemlock, even hellebore by pregnant sheep on gestation ness, collapse, and death due to respiratory when intoxicated. Panter (1983) reported day 14 results in “monkey-faced” or paralysis (Panter et al. 1988b). Although that intoxicated pigs “relished” the plant, cyclopian lambs with potentially severe animals exhibit tremors, muscular weak- and seemingly developed a craving for craniofacial defects (Binns et al. 1962). ness and collapse, they do not have true poison hemlock. The facial defects result from the toxic seizures and may recover quickly if a sub- insult to the neural tube such that the lethal dose was eaten. Although poison embryonic forebrain fails to divide nor- hemlock is fetotoxic to pregnant animals Related Pyridine Alkaloids mally. Veratrum alkaloids have a structur- as are lupines, Conium is more universally Tree and wild tobacco (Nicotiana spp., al resemblance to cholesterol. Recent teratogenic, affecting cattle, sheep, goats, Solanaceae) are the primary toxic plants in work suggests that a disruption in choles- and pigs (Panter and Keeler 1989). Most the U.S. that contain pyridine alkaloids, terol transport within cells prevents brain pregnant animals that later develop terata closely related to piperidine alkaloids cells from recognizing signals to divide after ingesting poison hemlock also show (Roitman and Panter 1995). Several properly (Incardona et al. 1998). Other initial signs of acute toxicity, and many species of Nicotiana poison livestock in work suggests that cyclopamine may act are fatally intoxicated, unlike the teratoge- the western U.S. (Kingsbury 1964), by competitive binding at Ach receptors nesis from lupine alkaloids. The severity of including N. tabacum (Burley tobacco), N. (Keeler 1988). Other defects and fetal death birth defects varies according to the dose glauca (tree tobacco), N. trigonophylla are possible at later stages of gestation up and the animal species. Sheep are less sen- (wild tobacco) and N. attenuata (wild to 33 days (Keeler et al. 1986). Sheep are sitive than are cattle, goats, and pigs tobacco). Tree and wild tobacco plants are primarily affected because of their propen- (Panter et al. 1988b). Similar birth defects generally not palatable to livestock graz- sity to eat false hellebore but cattle and can be caused by genetic, traumatic, or ing on rangelands (Panter et al. 1992). goats are also susceptible. A single dose of other environmental toxins and the clinical These plants contain nicotine, a well- 1.5 g of purified alkaloid will cause defor- signs and lesions are nonspecific. Because known toxin, and more importantly, the mities in sheep (Keeler 1983). there are no definitive pathological teratogenic piperidine alkaloid, anabasine lesions, the diagnosis of poison hemlock

456 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Death camas fore no special management is needed. For Literature Cited Zygadenine was the first steroidal alka- sheep, false hellebore is quite palatable, and herders must keep bred sheep from loid found in death camas, but the toxicity Aiyar, V.N., Benn, M.H., Hanna, T., Jacyno, has been attributed to zygacine, an acetyl ingesting false hellebore for about 1 J., Roth, S.H., and Wilkens, J. 1979. The ester of zygadenine (Majak et al. 1992, month after the rams are removed (Panter principal toxin of Delphinium brownii Rydb., Makeiff et al. 1997). Zygacine concentra- et al. 1992). This is not difficult to accom- and its mode of action. Experientia 35, tions range from 2 to 4 mg/g, and are plish because false hellebore is limited in 1367Ð1368. highest in vegetative tissue and pods distribution to moist mountain habitats Aldous, A.E. 1917. Eradicating tall larkspur on (Majak et al. 1992). Majak et al. (1992) and grows in easy to identify dense patch- cattle ranges in the National Forests. USDA also reported that 2 related forms of es. Although effective herbicidal control is Farmers Bull. 826. zygadenine were not detected in vegeta- available (Williams and Cronin 1981), it Aniszewski, T. 1993. Nutritive quality of the may not be practical given the location of alkaloidÐpoor Washington lupine (Lupinus tive plants, but concentrations of these polyphyllus Lindl var SF/TA) as a potential alkaloids increased dramatically in pods. the major populations in National Forests protein crop. J. Sci. Food Ag. 61:409Ð421. The mechanism of action is not known. and the ease with which the problem can Arnold, G.W. and J.L. Hill. 1972. Chemical Zygadenine and numerous related alka- be solved by grazing management. factors affecting selection of food plants by loids were found in death camas (Lang ruminants, p. 71Ð101. In: J.B. Harborne and Smith 1998) collected at the site (ed.), Phytochem. Ecol.. Academic Press, Death camas London. where 23 cows died in Nebraska (Collett Death camas is one of the first plants to et al. 1996). Bai, Y., F. Sun, M. Benn, M., and W. Majak. grow during spring, and animals may 1994. Diterpenoid and norditerpenoid alka- graze the plant if other forage is lacking. loids from Delphinium nuttallianum. Clinical Signs and Diagnosis Generally, recognizing the presence of Phytochem. 37: 1717Ð1724. Veratrum species death camas and understanding the acutely Baker, D.C., J.A. Pfister, R.J. Molyneux, Clinical signs of acute false hellebore toxic nature of the plant will aid in avoid- and P. Kechele. 1991. Cynoglossum offici- poisoning, relatively rare in livestock, ing problems. Panter et al. (1987) identi- nale toxicity in calves. J. Comp. Path. 104: fied 3 contributing circumstances that 403Ð410. include salivation, recumbency, reduced Baker, D.C., R.A. Smart, M.H. Ralphs, and heart rate, and dyspnea (Kingsbury 1964). resulted in loss of over 250 sheep in one R.J. Molyneux. 1989. Hound’s–tongue The fetotoxic effects of false hellebore are band. First, hungry ewes with lambs were (Cynoglossum officinale) poisoning in a calf. not generally overt for the dam. If fetal driven through the death camas-infested J. Am. Vet. Med. Assoc 194:929Ð930. deformities are severe, the hormonal sig- pasture. Second, sheep were bedded near BateÐSmith, E.C. 1972. Attractants and repel- nals inducing parturition are disrupted and the death camas, so the plant was readily lants in higher animals. p. 45Ð56. In: J.B. the dead and deformed fetus will be carried available for grazing. Third, the herder Harborne (ed.), Phytochem. Ecol. Academic well beyond term. These ewes will eventu- stressed the sheep by rapidly driving them Press, London. ally show clinical signs from the extended from the area, thus increasing the death Binns, W., L.F. James, J.L. Schupe, and E.J. Thacker. 1962. CyclopianÐtype malforma- gestation and usually die (James 1999). loss (Panter et al. 1987). Death camas can tion in lambs. Arch. Environ. Health be controlled by phenoxy herbicides 5:106Ð108. Death camas (Ralphs et al. 1991d). Bowman, W.C. and I.S. Sanghvi. 1963. Death camas toxicity is characterized by Pharmacological actions of hemlock (Conium maculatum) alkaloids. J. Pharm. excessive salivation, frothing around the Conclusions Pharmacol. 15:1Ð25. mouth, nausea and sometimes vomition Broquist, H.P. 1986. Livestock toxicosis, slob- (Kingsbury 1964, Panter et al. 1987). If bers, locoism, and the indolizidine alkaloids. the dose is sufficient, muscular weakness Alkaloid-containing plants exact a Nutr. Rev. 44:317Ð323. is followed by ataxia, recumbency, and heavy economic toll on livestock produc- Cheeke, P.R. 1989. Pyrrolizidine alkaloid toxi- death. Affected animals have a rapid, tion in rangelands of western North city and metabolism in laboratory animals weak heartbeat, and respiratory distress. America. Losses to these plants can be and livestock. p. 1Ð22. In: P.R. Cheeke (ed.), Death is from heart failure (Panter et al. reduced or eliminated by recognizing the Toxicants of Plant Origin. Vol. 1, Alkaloids. 1987). Diagnosis is made by recognizing toxic plant responsible for specific losses, CRC Press, Boca Raton, Fla. understanding when livestock graze the Cheeke, P.R. 1994. A review of the functional the clinical signs of poisoning, association and evolutionary roles of the liver in the of affected animals with populations of plant and how the toxin affects animals, detoxification of poisonous plants, with spe- grazed plants, and pathological examina- altering management schemes or animal cial reference to pyrrolizidine alkaloids. Vet. tion of tissues from dead animals (Panter species to reduce the risk of losses, or Human Tox. 36:240Ð247. and James 1989). using herbicidal control. Management of Cheeke, P.R. and J. Huan. 1995. Metabolism each toxic plant species is based on and toxicity of pyrrolizidine alkaloids. p. knowledge of the temporal and spatial 155Ð164 In: D.L. Gustine and H.E. Flores Management and Control dynamics of alkaloid concentration and (eds.), Phytochemicals and Health. Amer. Veratrum species consumption by livestock. Losses may be Soc. Plant Physiol. Ser., Vol. 15. Rockville, Livestock management to avoid losses reduced by ensuring that livestock are not Maryland. Chesnut, V.K. and E.V. Wilcox. 1901. The to false hellebore are relatively simple. exposed or have reduced exposure either First, since the window of fetotoxicity is stockÐpoisoning plants of Montana. USDA during periods of greatest risk (e.g., high- Bull. 26. relatively narrow (i.e., 14 to 33 days gesta- est toxin concentrations), or when they are tion), pregnant animals (particularly Colegate, S.M. and P.R. Dorling. 1997. most likely to eat the plant in amounts suf- Bioactive indolizidine alkaloids. p. 1Ð18. In: sheep) should not be allowed access to ficient to cause toxicity. J.P. F. D’Mello (ed.), Handbook of Plant and veratrum-infested pastures during this Fungal Toxicants. CRC Press, Boca Raton, period. Cattle rarely eat the plant, there- Fla.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 457 Colegate, S.M., P.R. Dorling, and C.R. Glendinning, J.I. 1994. Is the bitter rejection Johnson, A.E., R.J. Molyneux, and L.D. Huxtable. 1989. Structural elucidation of response always adaptive? Physiol. Behav. Stuart. 1985b. Toxicity of Riddell’s ground- swainsonine: relationship of structure to 56:1217Ð1227. sel (Senecio riddellii) to cattle. Amer. J. Vet. activity. p. 91Ð99. In: L.F. James, A.D. Glover, G.H. 1906. Larkspur and other poiso- Res. 46:577Ð582. Elbein, R.J. Molyneux, and C.D. Warren nous plants. Colo. Ag. Expt. Sta. Bull. 113. Keeler, R.F. 1976. Lupin alkaloids from ter- (eds.), Swainsonine and Related Glycosides Hall, H.M. and H.S. Yates. 1915. Stock atogenic and nonteratogenic lupins: III. Inhibitors. Iowa State Univ. Press, Ames, Ia. Poisoning Plants of California. Calif. Ag. Identification of anagyrine as the probable Collett, S., D. Grotelueschen, R.A. Smith, Expt. Sta. Bull. 249. teratogen by feeding trials. J. Tox. 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Identification of the glycosides inhibitors fetal and neonatal development: a review. J. Majak, W., R.E. McDiarmid, W. Cristofoli, Range Manage. 45:52Ð62. swainsonine and calystegine B2 in Weir vine F. Sun, and M. Benn. 1992. Content of (Ipomoea sp. Q6 [aff calobra]) and correla- Panter, K.E., M.H. Ralphs, R.A. Smart, and zygacine in Zygadenus venenosus at different tion with toxicity. J. Nat. Prod. 58:878Ð886. B. Duelke. 1987. Death camas poisoning in stages of growth. Phytochem. 31:3417Ð3418. sheep: a case report. Vet. Hum. Toxicol. Nation P.N., M.H. Benn, S.H. Roth, and J.L. Makeiff, D., W. Majak, R.W. McDiarmid, B. 29:45Ð48. Wilkens. 1982. Clinical signs and studies of Reaney, and M.H. Benn. 1997. Panter, K.E., T.D. Bunch, R.F. Keeler, D.V. Determination of zygacine in Zygadenus the site of action of purified larkspur alka- Sisson, and R.J. Callan. 1990. Multiple venenosus (death camas) by image analysis loid, methyllycaconitine, administered par- congenital contractures (MCC) and cleft on thin layer chromatography. J. Agr. Food enterally to calves. Can. Vet. J. 23: 264Ð266. palate induced in goats by ingestion of Chem. 45:1209Ð1211. Nielsen, D.B., N.R. Rimbey, and L.F. James. piperidine alkaloidÐcontaining plants: reduc- Manners, G.D., K.E. Panter, and S.W. 1988. Economic considerations of poisonous tion in fetal movement as the probable cause. Pelletier. 1995. StructureÐactivity relation- plants on livestock. p. 5Ð16. In: L.F. James, Clin. Toxicol. 28:69Ð83. ships of norditerpenoid alkaloids occurring in M.H. Ralphs, and D.B. Nielsen (eds.), The Panter, K.E., D.R. Gardner, R.E. Shea, R.J. toxic larkspur (Delphinium) species. J. Nat. Ecology and Economic Impact of Poisonous Molyneux, and L.F. James. 1998a. Toxic Prod. 58: 863Ð869. Plants on Livestock Production. Westview and teratogenic piperidine alkaloids from Manners, G.D., K.E. Panter, M.H. Ralphs, Press, Boulder, Colo. Lupinus, Conium, and Nicotiana species. p. J.A. Pfister, and J.D. Olsen. 1993. The Olsen, J.D. 1978. Tall larkspur poisoning in 345Ð350. In: T. Garland and A.C. Barr occurrence and toxic evaluation of norditer- cattle and sheep. J. Amer. Vet. Med. Assoc. (eds.), Toxic Plants and Other Natural penoid alkaloids in the tall larkspurs 173:762Ð765. Toxicants. CAB Intern., Oxon, U.K. (Delphinium sp.). J. Agr. Food Chem. 41: Panter, K.E. 1983. Toxicity and Teratogenicity Panter, K.E., D.R. Gardner, C.C. Gay, L.F. 96Ð100. of Conium maculatum in swine and hamsters. James, R. Mills, J.M. Gay, and T.J. Marsh, C.D. 1909. The locoÐweed disease of Ph.D. Diss., Univ. Illinois, Urbana, Ill. Baldwin. 1997. Observations of Lupinus sul- the plains. USDA Bull. 112. Panter, K.E. and L.F. James. 1989. Death phureus–induced “crooked calf disease”. J. Marsh, C.D., A.B. Clawson, and H. Marsh. camasÐearly grazing can be hazardous. Range Manage. 50:587Ð592. 1916. Larkspur poisoning of livestock. Rangelands 11:147Ð149. Pelletier, S.W. 1983. The nature and definition USDA Bur. of Anim. Indust. Bull. 365. Panter, K.E. and L.F. James. 1995. Alkaloid of an alkaloid. p. 1Ð31. In: S.W. Pelletier Merrill, L.B. and J.L. Schuster. 1978. toxicants and teratogens of plant origin. p. (ed.), AlkaloidsÐ Chemical and Biological Grazing management practices affect live- 145Ð154. In: D.L. Gustine and H.E. Flores Perspectives. Vol. 1. John Wiley and Sons, stock losses from poisonous plants. J. Range New York, N.Y.. (eds.), Phytochemicals and Health. Amer. Manage. 31:351Ð354. Penny, R.H.C. 1953. Hemlock poisoning in Soc. Plant Physiol. Ser., Vol. 15. Rockville, McDaniel, K. 1999. Controlling locoweed with cattle. Vet. Rec. 65:669Ð670. herbicides. p. 52Ð54. In: T.M. Sterling and Maryland. Pfister, J.A. 1999. Behavioral strategies for D.C. Thompson (eds.), Locoweed Research: Panter, K.E. and R.F. Keeler. 1989. coping with poisonous plants. p. 45Ð59. In: Update and Highlights. New Mexico Agr. Piperidine alkaloids of poison hemlock K. Launchbaugh, K. Saunders, and J. Expt. Sta. Res. Rep. 730, Las Cruces, N.M. (Conium maculatum). p. 109Ð132. In: P.R. Mosley, (eds.), Grazing Behavior of Mickelsen, L.V., M.H. Ralphs, D.L. Turner, Cheeke (ed.), Toxicants of Plant Origin. Vol. Livestock and Wildlife. Univ. Idaho For. J.O. Evans, and S.A. Dewey. 1990. 1, Alkaloids. CRC Press, Boca Raton, Fla. Expt. Sta. Tech. Bull. Herbicidal control of duncecap larkspur Panter, K.E., D.R. Gardner, and R.J. Pfister, J.A. and C.D. Cheney. 1998. Operant (Delphinium occidentale). Weed Sci. 38: Molyneux. 1994. Comparison of toxic and behavioral analysis of acute tall larkspur 153Ð157. teratogenic effects of Lupinus formosus, L. (Delphinium barbeyi) intoxication in cattle. Molyneux, R.J. and L.F. James. 1982. Loco arbustus, and L. caudatus in goats. J. Nat. Behav. 4:43Ð56. intoxication: indolizidine alkaloids of spotted Toxins 3:83Ð93. Pfister, J.A. and D.R. Gardner. 1999. locoweed (Astragalus lentiginosus). Sci. Panter, K.E., D.R. Gardner, and R.J. Consumption of low larkspur (Delphinium 216:190Ð191. Molyneux. 1998b. Teratogenic and fetotoxic nuttallianum) by cattle. J. Range Manage. Molyneux, R.J. and L.F. James. 1990. effects of two piperidine alkaloidÐcontaining 52:378Ð383. Pyrrolizidine alkaloids in milk: thresholds for lupines (L. formosus and L. arbustus) in Pfister, J.A., R.J. Molyneux, and D.C. intoxication. Vet. Hum. Tox. 32:94Ð103. cows. J. Nat. Toxins 7:131Ð140. Baker. 1992. Pyrrolizidine alkaloid content Molyneux, R.J. and A.E. Johnson. 1984. Panter, K.E., L.F. James, and D.R. Gardner. of houndstongue (Cynoglossum officinale). J. Extraordinary levels of production of 1999. Lupines, poisonÐhemlock and Range Manage. 45:254Ð256. pyrrolizidine alkaloids in Senecio riddellii. J. Nicotiana spp: toxicity and teratogenicity in Pfister, J.A., K.E. Panter, and G.D. Nat. Prod. 47:1030Ð1032. livestock. J. Nat. Toxins 8:117Ð134. Manners. 1994b. Effective dose in cattle of Molyneux, R.J. and M.H. Ralphs. 1992. Plant Panter, K.E., R.F. Keeler, and D.C. Baker. toxic alkaloids from tall larkspur toxins and palatability to herbivores. J. (Delphinium barbeyi). Vet. Human Toxicol. 1988b. Toxicoses in livestock from the hem- Range Manage. 45:13Ð18. 36:10Ð11. locks (Conium and Cicuta spp.). J. Anim. Molyneux, R.J., L.F. James, K.E. Panter, Pfister, J.A., M.H. Ralphs, and G.D. Sci. 66:2407Ð2413. and M.H. Ralphs. 1989. The occurrence and Manners. 1988b. Cattle grazing tall larkspur Panter, K.E., R.F. Keeler, and W.B. Buck. detection of swainsonine in locoweeds. p. on Utah mountain rangelands. J. Range 1985. Congenital skeletal malformations 100Ð117. In: L.F. James, A.D. Elbein, R.J. Manage. 41: 118Ð122. induced by maternal ingestion of Conium Molyneux, and C.D. Warren (eds.) Pfister, J.A., J.B. Astorga, K.E. Panter, and Swainsonine and Related Glycosides maculatum (poison hemlock) in newborn R.J. Molyneux. 1993. Maternal locoweed Inhibitors. Iowa State Univ. Press, Ames, Ia. pigs. Amer. J. Vet. Res. 46:2064Ð2066. exposure in utero and as a neonate does not disrupt taste aversion learning in lambs. Appl. Anim. Behav. Sci. 36:159Ð167.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 459 Pfister, J.A., G.D. Manners, D.R. Gardner, Ralphs, M.H. and D.N. Ueckert. 1988. Robinson, T. 1979. The evolutionary ecology and M..H. Ralphs. 1994a. Toxic alkaloid Herbicide control of locoweeds: a review. of alkaloids. p. 413Ð448. In: G.A. Rosenthal levels in tall larkspur (Delphinium barbeyi) Weed Tech. 2:460Ð465. and D.H. Janzen. (eds.), Herbivores: Their in western Colorado. J. Range Manage. 47: Ralphs, M.H., J.E. Bowns, and G.D. Interaction with Secondary Plant Metabolites. 355Ð358. Manners. 1991a. Utilization of larkspur by Academic Press, New York, N.Y. Pfister, J.A., K.E. Panter, G.D. Manners, sheep. J. Range Manage. 44: 619Ð622. Roitman, J.N. and K.E. Panter. 1995. and C.D. Cheney. 1994c. Reversal of tall Ralphs, M.H., J.O. Evans, and S.A. Dewey. Livestock poisoning caused by plant alka- larkspur (Delphinium barbeyi) toxicity with 1992. Timing of herbicide applications for loids. p. 53Ð124. In: M. Blum (ed.), The physostigmine. Vet. Human Toxicol. 36: control of larkspurs. Weed Sci. 40: 264Ð269. Toxic Action of Marine and Terrestrial 511Ð514. Ralphs, M.H., D. Graham, and L.F. James. Alkaloids. Alaken, Inc., Ft. Collins, Colo. Pfister, J.A., D.C. Adams, M.J. Arambel, 1994a. Social facilitation influences cattle to Schmeller, T., M. Sauerwein, F. Sporer, M. J.D. Olsen, and L.F. James. 1989. Sublethal graze locoweed. J. Range Manage. Wink, and W.E. Muller. 1994. Binding of levels of toxic larkspur: effects on intake and 47:123Ð126. quinolizidine alkaloids to nicotinic and mus- rumen dynamics in cattle. Nutr. Rep. Intern. Ralphs, M.H, L.F. James, and J.A. Pfister. carinic acetylcholine receptors. J. Nat. Prod. 40:629Ð636. 1986. Utilization of white locoweed 57:1316Ð1319. Pfister, J.A., G.D. Manners, D.R. Gardner, (Oxytropis sericea Nutt.) by range cattle. J. Sharrow, S.H., D.N. Ueckert, and A.E. K.W. Price, and M.H. Ralphs. 1996a. Range Manage. 39:344Ð347. Johnson. 1988. Ecology and toxicology of Influence of alkaloid concentration on Ralphs, M.H., G.D. Manners, and D.R. Senecio species with special reference to acceptability of tall larkspur (Delphinium Gardner. 1998. Toxic alkaloid response to Senecio jacobaea and Senecio longilobus. p. spp.) to cattle and sheep. J. Chem. Ecol. herbicides used to control tall larkspur. Weed 181Ð196. In: L.F. James, M.H. Ralphs, and 22:1147Ð1168. Sci. 46:116Ð119. D.B. Nielsen (eds.), The Ecology and Pfister, J.A., G.D. Manners, M.H. Ralphs, Ralphs, M.H., L.V. Mickelsen, and D.L. Economic Impact of Poisonous Plants on Z.X. Hong, and M.A.Lane. 1988a. Effects Turner. 1987. Cattle grazing white Livestock Production. Westview Press, of phenology, site and rumen fill on tall lark- locoweed: diet selection patterns of native Boulder, Colo. spur consumption by cattle. J. Range and introduced cattle. J. Range Manage. Smith, G.S., K.W. Allred, and D.E. Kiehl. Manage. 41: 509Ð514. 40:333Ð335. 1992. Swainsonine content of New Mexico Pfister, J.A., F.D. Provenza, G.D. Manners, Ralphs, M.H., K.E. Panter, and L.F. James. locoweeds. Proc. West. Sec. Amer. Soc. D.R. Gardner, and M.H. Ralphs. 1997a. 1990. Feed preferences and habituation of Anim. Sci. 43:405Ð407. Tall larkspur ingestion: can cattle regulate sheep poisoned by locoweed. J. Anim. Sci. Smith, L.W., and C.C.J. Culvenor. 1981. intake below toxic levels? J. Chem. Ecol. 68:1354Ð1362. Plant sources of hepatotoxic pyrrolizidine 23:759Ð777. Ralphs, M.H, K.E. Panter, and L.F. James. alkaloids. J. Nat. Prod. 44:129Ð152. Pfister, J.A., B.L. Stegelmeier, C.D. Cheney, 1991b. Grazing behavior and forage prefer- Stanford, K. T.A. McAllister, B.M. Lees, and L.F. James, and R.J. Molyneux. 1996b. ence of sheep with chronic locoweed toxico- K.J. Cheng. 1996. Comparison of sweet Operant analysis of chronic locoweed intoxi- sis suggest no addiction. J. Range Manage. white lupin seed, canola meal, and soybean cation in sheep. J. Anim. Sci. 74:2622Ð2632. 44:208Ð209. meal as protein supplements for lambs. Can. Pfister, J.A., M.H. Ralphs, G.D. Manners, Ralphs, M.H., T.D. Whitson, and D.N. J. Anim. Sci. 76:215Ð219. D.R. Gardner, K.W. Price, and L.F. Ueckert. 1991d. Herbicide control of poiso- Stegelmeier, B.L., D.R. Gardner, L.F. James, James. 1997b. Early season grazing by cattle nous plants. Rangelands 13:73Ð77. and R.J. Molyneux. 1996. Pyrrole detection of tall larkspurÐ (Delphinium spp.) infested Ralphs, M.H., D. Graham, M.L. Galyean, and the pathologic progression of rangeland. J. Range Manage. 50: 391Ð398. and L.F. James. 1997a. Creating aversions Cynoglossum officinale (houndstongue) poi- Pfister, J.A., D.R. Gardner, K.E. Panter, to locoweed in naive and familiar cattle. J. soning in horses. J. Vet. Diagn. Invest. G.D. Manners, M.H. Ralphs, B.L. Range Manage. 50:361Ð366. 8:81Ð90. Stegelmeier, and T.K. Schoch. 1999. Ralphs, M.H., D. Graham, L.F. James, and Stegelmeier, B.L., L.F. James, K.E. Panter, Larkspur (Delphinium spp.) poisoning in K.E. Panter. 1994b. Locoweed effects on a and R.J. Molyneux. 1995b. Serum swainso- livestock. J. Nat. Tox. 81Ð94. calf crop. Rangelands 16:35Ð37 nine concentration and ∝Ðmannosidase activ- Ralphs, M.H. 1987. Cattle grazing white Ralphs, M.H., D. Graham, R.J. Molyneux, ity in cattle and sheep ingesting Oxytropis locoweed: influence of grazing pressure and and L.F. James. 1993. Seasonal grazing of sericea and Astragalus lentiginosus palatability associated with phenological locoweeds by cattle in northeastern New (locoweeds). Amer. J. Vet. Res. 56:149Ð154. growth stage. J. Range Manage. 40:330Ð332. Mexico. J. Range Manage. 46:416Ð420. Stegelmeier, B.L., R.J. Molyneux, A.D. Ralphs, M.H. 1992. Conditioned food aver- Ralphs, M.H., L.F. James, D.B. Nielsen, and Elbein, and L.F. James. 1995a. The lesions sion: training livestock to avoid eating poiso- K.E. Panter. 1984. Management practices of locoweed (Astragalus mollissimus), nous plants. J. Range Manage. 45:46Ð51. reduce cattle loss to locoweed on high moun- swainsonine, and castanospermine in rats. Ralphs, M.H. 1997. Persistence of aversions to tain range. Rangelands 6(4):175Ð177. Vet. Path. 32:289Ð298. larkspur in naive and experienced cattle. J. Ralphs, M.H., J.D. Graham, G. Duff, B.L. Stegelmeier, B.L., M.H. Ralphs, D.R. Range Manage. 50: 367Ð370. Stegelmeier, and L.F. James. 2000. Impact Gardner, R.J. Molyneux, and L.F. James. Ralphs, M.H. and R.J. Molyneux. 1989. of locoweed poisoning on steer weight gains. 1994. Serum ∝Ðmannosidase activity and the Livestock grazing locoweed and the influ- J. Range Manage. 53:86Ð90. clinicopathologic alterations of locoweed ence of swainsonine on locoweed palatability Ralphs, M.H., L.F. James, D.B. Nielsen, D.C. (Astragalus mollissimus) intoxication in and habituation, p.39Ð49. In: L.F. James, Baker, and R.J. Molyneux. 1988. Cattle range cattle. J. Vet. Diagn. Invest. A.D. Elbein, R.J. Molyneux, and C.D. grazing Wahweap milkvetch in southeastern 6:473Ð479. Warren (eds.) Swainsonine and Related Utah. J. Anim. Sci. 66:3124Ð3130. Stegelmeier, B.L., L.F. James, K.E. Panter, Glycosides Inhibitors. Iowa State Univ. Ralphs, M.H., G.D. Manners, J.A. Pfister, D.R. Gardner, M.H. Ralphs, and J.A. Press, Ames, Ia. D.R.Gardner, and L.F. James. 1997b. Pfister. 1998a. Tissue swainsonine clearance Ralphs, M.H. and J.D. Olsen. 1987. Alkaloids Toxic alkaloid concentration in tall larkspur in sheep chronically poisoned with locoweed and palatability of poisonous plants. p. species in the western United States. J. (Oxytropis sericea). J. Anim. Sci. 78Ð83. In: USDA Forest Service Tech. Rep. Range Manage. 50: 497Ð502. 76:1140Ð1144. Ralphs, M.H. and J.D. Olsen. 1992. Prior Ralphs, M.H., D.L. Turner, L.V. Mickelsen, Stegelmeier, B.L., K.E. Panter, J.A. Pfister, grazing by sheep reduces waxy larkspur con- J.O. Evans, and S.A. Dewey. 1991c. L.F. James, G.D. Manners, D.R. Gardner, sumption by cattle. J. Range Manage. 45: Herbicides for control of tall larkspur M.H. Ralphs, and J.D. Olsen. 1998b. 136Ð139. (Delphinium barbeyi). Weed Sci. 38: Experimental modification of larkspur 573Ð577. (Delphinium spp.) toxicity. p. 205Ð210. In:

460 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 T. Garland and A.C. Barr (eds.), Toxic Plants Van Damm, N.M., R. Verpoorte, and E. Van Williams, M.C. and E.H. Cronin. 1981. and Other Natural Toxicants. CAB Intern., der Meijden. 1994. Extreme differences in TenÐyear control of western false hellebore Oxon, U.K. pyrrolizidine alkaloid levels between leaves (Veratrum californicum). Weed Sci. Tokarnia, C.H., J. Dobereiner, and P.V. of Cynoglossum officinale. Phytochem. 29:22Ð23. Peixoto. 1992. Poisonous plants of Brazil. p. 37:1013Ð1016. Wink, M., C. Meisner, and L. Witte. 1995. 63Ð70. In: L.F. James, R.F. Keeler, E.M. Van Kampen, K.R. and L.F. James. 1970. Patterns of quinolizidine alkaloids in 56 Bailey, Jr., P.R. Cheeke, and M.P. Hegarty Pathology of locoweed (Astragalus lentingi- species of the genus Lupinus. Phytochem. (eds.), Poisonous Plants. Iowa State Univ. nosus) poisoning in sheep: sequential devel- 38:139Ð153. Press, Ames, Ia. opment of cytoplasmic vacuolation in tissues. Winter, C.K. and H.J. Segall. 1989. Torell, L.A., L.P. Owen, and J.D. Graham. Path. Vet. 7:503Ð508. Metabolism of pyrrolizidine alkaloids. p. 1999b. Healing locoweedÐpoisoned cattle Velastegui, W., G.S. Smith, T.S. Edrington, 23Ð40. In: P.R. Cheeke (ed.), Toxicants of M. Stavanja, D.E. Kiehl, and G.M. before sale decreases economic losses. p. Plant Origin. Vol. 1, Alkaloids. CRC Press, Southward. 1992. Swainsonine content and 80Ð81. In: T.M. Sterling and D.C. Thompson Boca Raton, Fla. comparative toxicity of seedpods, leaves, and (eds.), Locoweed Research: Update and stems from halfmoon locoweed Astragalus Highlights. New Mexico Agr. Expt. Sta. Res. allochrous. Proc. West. Sec. Amer. Soc. Rep. 730, Las Cruces, N.M. Anim. Sci. 43:403Ð404. Torell, L.A., K. McDaniel, L.P. Owen, and Wachenheim, D.E., L.L. Blythe, and A.M. J.D. Graham. 1999a. The economic value of Craig. 1992. Characterization of rumen bac- having a locoweedÐfree area. p. 82Ð83. In: terial pyrrolizidine alkaloid biotransforma- T.M. Sterling and D.C. Thompson (eds.), tion in ruminants of various species. Vet. Locoweed Research: Update and Highlights. New Mexico Agr. Exp. Sta. Res. Rep. 730, Hum. Tox. 34:513Ð517. Las Cruces, N.M.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 461 J. Range Manage. 54: 462Ð465 July 2001 Anti-quality effects of insects feeding on rangeland plants: A review

JOHN B. CAMPBELL

Author is professor, Department of Entomology, University of Nebraska, West Central Research and Extension Center, Route 4ÐBox 46A, North Platte, Nebr. 69101-9495.

Abstract Resumen

The anti-quality effects of the major groups of insects that uti- Se discuten los efectos anti-calidad de los principales grupos de lize rangeland plants for food is discussed. The biology, ecology, insectos que utilizan las plantas del pastizal como alimento. geographical distribution and economic thresholds of grasshop- También se revisó la biología, ecología, distribución geográfica y pers, crickets, Western harvester ants, ranch caterpillars, big- umbrales económicos de chapulines, grillos, hormigas cosechado- eyed or black grass bugs, and white grubs are reviewed. Also dis- ras del oeste, orugas de rancho y pulgas ojonas o chibches negras cussed are practical pest management strategies if they exist. de zacate y gusanos blancos. También se discuten las estrategias Most of these rely on the integration of good range management practicas del manejo de plagas, si ellas existen. Muchas de ellas practices and the control strategy. se basan en la integración de buenas practicas de manejo del pastizal y la estrategia de control.

Key Words: Grasshoppers, harvester ants, range caterpillar, big eyed bugs, rangeland insects. or more species present at a certain type of range, only 8 or 9 species are really causing economic losses. Some species are con- In the United States, over 1,500 species of insects have been sidered beneficial in that they fed only on plants that are consid- noted as being in association with the range ecosystem (Kumer et ered detrimental to the range. For example, Hypochlora alba al. 1976, Thomas and Werner 1981). Fortunately, most of these (Dodge) feeds primarily on Louisiana sagewort, Artemsia ludovi- are not economic in terms of detrimental effects on range plants. ciana Nutt., and secondarily on Western ragweed, Ambrosia The best known damaging species belong to the insect order of psilostacka D.C. The genus Hesperottix feeds mainly on Western Orthoptera—grasshoppers, Hymenoptera—ants and termites, ragweed and Missouri goldenrod, Solidago missouriensis Nutt., Lepidoptera—caterpillars, Coleoptera—beetles, and Homoptera— (Campbell et al. 1974). leafhoppers. Insects are a significant factor in energy flow, nutri- Grasshoppers are classified as grass feeders, mixed feeders or ent cycling, water utilization and vegetative changes in a range forb feeders based on the mandibular type. Generally, the out- ecosystem. break populations belong to the mixed feeder group. Another Many entomology textbooks refer briefly to range insects, but classification is slant-face, to which most of the grassfeeders the 2 major publications that deal specifically and exclusively belong, and the spur throat to which most of the mixed feeders with the subject are Haws et al. (1982) “An Introduction to belong, and band-wings, which are mostly large grasshoppers Rangeland Insects of the Western United States” and Watts et al. that may be either mixed or forb feeders. (1989) “Rangeland Entomology”. This latter publication has been There are 3 life stages in the grasshopper life cycle—egg, noted as the world’s most authoritative treatment on the impor- nymph and adult. Eggs are deposited in soil and a frothy, sticky tant role of insects in rangeland ecosystems. Another publication material is secreted with egg deposition which forms an insulated of note is Pfadt (1994) “Field Guide to Common Western pod composed of soil particles. The number of pods and eggs per Grasshoppers”. This publication contains colored plates of adult pod varies with species. Some species deposit eggs in soil sur- and nymphs of the major rangeland grasshoppers, and the text rounded by roots of grasses; other species select open areas with details the biology habitat and feeding choices for each species. accumulations of surface debris. This publication by itself is a Wyoming Experiment Station Most grasshopper species overwinter in the egg stage, but a few Bulletin, but it is included in the USDA—APHIS Technical overwinter as nymphs. Hatching time is influenced by tempera- Bulletin 1809 “Grasshoppers Integrated Pest Management User ture and can be correlated with soil temperature. In the Northern Handbook”. This latter publication contains material by numer- Plains states, cool-season grasses such as needlegrasses (Stipa ous authors on range management considerations to reduce dam- spp.), wheatgrasses (Agropyron spp.) and bluegrasses (Poa spp.) age from grasshoppers and/or to reduce grasshopper numbers begin growth before grasshoppers become very active. By the based on range management techniques (Anonymous 1996). time grasshoppers begin to defoliate plants, these grasses have Grasshoppers are the most serious of the insect groups that con- completed growth and have enough energy reserves needed for tribute to the anti-quality of range plants. While there may be 50 spring growth the following year. The warm-season grasses such as the bluestems (Agropogan spp.), grama grasses (Bouteloua spp.) and buffalograss Buchloe doctyloides (Nutt.) Engelm., do Manuscript accepted 13 Sept. 00. not begin growth until May and grow most rapidly when temper-

462 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 atures reach 85Ð95¡F, which coincides with foot high and 30 feet in diameter. The area tion around the mouth and nose of live- the greatest grasshopper feeding activity. around the mound is denuded of all vege- stock. The larvae may tie several grass Grass responses to defoliation includes tation. Not only is the vegetation stems together with the cast skin. stoppage of root growth and nutrient destroyed, but wind erosion increases in Livestock tend to avoid grazing in these uptake for several days if more than half the denuded areas. The ants also collect areas because of the spines. of the green herbage is removed. “Shut- seeds that may affect plant production, As the populations become larger, food down” or “slow-down” periods in roots particularly with annual plants. Colonies consumption is heavy. They may destroy increase as severity and frequency of defo- survive for 15Ð20 years, and one mound all of the green grass down to and including liation increase. Removing more than 65% may consist of as many as 60 chambers. some of the crown. If drought conditions of the green herbage one time during the Winged reproductive ants may appear in exist, there is little regrowth, and the roots growing season can reduce total root May after a rain, but some also appear in are unable to store nutrients for the winter, length by 30% or more. If this occurs over the summer and fall. New colonies are and there is no reseeding of annual plants. several years, plants become weak and die formed by mated queens usually in later As they search for food, caterpillars gath- (Campbell et al. 1998). summer. After mating, the queen sheds er in bands a meter or more wide and sever- Damage caused by grasshoppers is more her wings and digs a burrow several inch- al kilometers in length. Ranchers refer to than actual consumption of forage. They cut es deep in the soil. The first brood is com- the feeding of these bands as “windrow- stems and blades while eating only part of posed mostly of female workers. This ing”. The range caterpillar feeds on 40 or them. They eat closer to the ground than brood forages, enlarges the colony, cares more species of grass (Wildermuth and livestock and may kill growing tips of for the young and protects the mound. The Caffrey 1916, Capinera 1978). Huddleston grasses. They cut off seed stocks, reducing workers move the eggs of the second et al. (1976) established the economic seed production, and soil erosion may result brood to newly-constructed chambers threshold as 2 large larvae/m2. Similar val- from denudation by heavy populations. which have been stocked with seeds and ues were derived by laboratory and model Personnel from the Bureau of insect parts as a food source. studies (Bellows et al. 1983, Capinera et al. Entomology and Plant Quarantine kept Most of the mound expansion is in the 1983, Riley et al. 1984). seasonal grasshopper density records for spring, but there is no regrowth in the The adult range caterpillar is a buff to western ranges from 1932—1952. They denuded area later in the season. Lavigne brown moth with a wing span of 50Ð70 estimated that the average number of 1.2 and Fisser (1966) estimated that a single mm. The female mates and deposits eggs grasshoppers/m2 would eat or destroy acre of rangeland supported as many as 15 and dies within about 3 days. Eggs are 14.65 million tons of forage on the 262 colonies. Worker ants from this number of deposited in cylinder-shaped clusters on million acres of western rangeland. This colonies stripped vegetation from as much plants. Larvae undergo six molts before would have provided feed for another 4.9 as one-seventh of an acre. As is true for pupating. This takes 12Ð14 weeks if hatch million animal units (unpublished data grasshoppers, overgrazed range suffers the occurs in the spring but only 7 or 8 if the Cowan and Bell 1973). most damage from the red harvester ant. hatch occurs in the summer. Crickets are close relatives of grasshop- Grazing management will serve to slow the The range caterpillar has in the past pers and have had sporadic outbreaks for increase of new mounds. Insecticides can be been considered cyclic which is probably over a century. In outbreak years, they used to treat the mounds, but this is labor true in the sense of large populations in increase in number and form great migra- intensive and should be approached from an extensive areas. In recent years, some tory bands (Watts et al. 1982). During area-wide control effort to be successful. extensive damage has occurred in local- these outbreaks, they may denude the ized areas virtually every year. rangeland of practically all plants. They Rangeland CaterpillarÐHemilenca Control has changed from massive aerial have been reported to feed on 250 species oliviae Cockerill spray programs over large areas to smaller of range plants (Cowan and Shipman The range caterpillar has 3 discontinu- mist applications of pyrethroids to local- 1947). They seem to have a preference for ous populations, one in Mexico, one in ized areas. If the infestation is early and flower and seed parts reducing the reseed- southcentral New Mexico and the third in appropriate timing of insecticide applica- ing potential of the plants, and if denuding northeastern New Mexico, Colorado, tions occurs in a year with at least some occurs later in the year, the plant wouldn’t Oklahoma and Texas. Dubach et al. moisture, grassy vegetation may recover. be able to store nutrients in the roots for (1988) and Shaw et al. (1987) believe overwintering. The Morman cricket has a these were once a continuous population. White Grubs similar life cycle to grasshoppers except Currently the distribution of the 3 popula- Beetles from the family Scarabaeidae that they are wingless. All crickets in the tions are separated by brush-infested areas are among the most numerous on range. migratory band move in the same direc- which may have been devoid of brush in Those beetles that have grubs as the tion, and the movement is about 0.8 km earlier times. The caterpillar distribution is immature stage are the most damaging. In per day or 40 km (25 miles) in a season generally in blue grama-dominated range- most species, plant damage occurs from (Ueckert 1970). land at elevations between 1,350 and the grubs feeding on roots which kills the 2,400 meters. The northern distribution grass; however, adults of a few species Western Harvester Ants into Colorado is probably limited by also cause plant damage. Kumer et al. The genus Pogonomyrinex is the prima- decreasing late summer precipitation. (1976) collected 37 species from short- ry group of harvester ants in North Caterpillars consume grass, often down grass prairie in northeastern Colorado. America. Cole (1968) has described 22 to the crown, waste unconsumed portions Only 9 species of the group were associat- species. This group ranks next to of leaves as do grasshoppers, and in addi- ed with root feeding, most of the rest were grasshoppers in terms of rangeland dam- tion, discourage grazing because of urtri- dung beetles. The Phyllophaga spp. com- age. Lavigne and Fisser (1966) indicate cation spines from both the larvae and plex are the best known plant damaging the mounds created by the ants may be a their shed skins. These spines cause irrita- group (Anonymous 1971a, 1971b).

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 463 The white grubs (MayÐJune beetles) are Labops have vestigial hind wings, but grasshopper egg pods. This larval stage is creamy white with a shiny brown head, Irbisia have well-developed wings. termed triungulin. Within a month, the lar- have 6 prominent legs and are generally Adult females of the big-eyed bugs vae pass through three more stages with shaped like a “C”. Much of the damage on deposit eggs into grass stems in the fall. each becoming more sedentary. Finally, rangeland probably goes unnoticed if it is The nymphs hatch in the spring in the they change to the pseudopupae which is of moderate intensity. It is generally diag- warmer lower areas and later in the cooler the overwintering stage. As temperature nosed as plant stress as a result of drought. upland areas. and moisture increase in the spring, they Heavy damage may occur only in spots The black grass bugs were first noted as enter the final immature pupal stage from ranging from 10—100 meters in diameter. pests around 1950 when range improve- which adults emerge. There is 1 genera- In some areas such as the Nebraska ment programs were replacing native grass- tion per year. Sandhills, damage may occur only in wet es with introduced grasses especially The interest in the blister beetles is not meadows that are a valuable hay or graz- wheatgrasses. The large areas of a single from the standpoint of damage to range ing source. In addition to destruction of species of grass provided an excellent niche plants but because of the injury to horses the grass, other problems may occur. for the black grass bugs (Higgins et al. or other livestock. They may actually Annual weeds often invade and dominate 1977). A density of 156/m2 reduced seed ingest a blister beetle. The bodies of the the area for a number of years (Randolph head production in intermediate wheatgrass blister beetles contain a vesicant substance and Garner 1961). Drake (1964) suggests by 56% (Malechek et al. 1977). Ansley and called cantharidan. This substance causes that feeding by white grubs creates a mode McKell (1982) showed the black grass bug blisters on skin tissue upon contact. It is of entry for bacterial and fungal diseases feeding reduced leaf length, seedhead usually ingested with the consumption of that kill the weakened plant. height and carbohydrate reserves in root alfalfa hay. Horses are very susceptible to Skunks and other rodents may cause fur- crowns in crested wheatgrass. blister beetle poisoning. Portions or all of ther damage to plants by digging up grubs Control strategies include application of the horse digestive tract can be severely as a food source. This occurs in Nebraska insecticides, (Hagen 1975, Dickerson irritated bringing about secondary infec- in the wet meadow areas. Although there 1978) or heavy grazing in the spring, tions and bleeding (Bauernfeind and are certain cultural or chemical control (Kamm and Fuxa 1977, Hagen 1975). Breeden 1984). Cantharadin is absorbed measures that reduce grub numbers, they Insect resistant varieties have also been and excreted through the kidneys, thus would only be economical to employ evaluated. Hewitt (1980) reported that tall, irritation of the kidney, ureter, urinary where a crop such as wheat is concerned. slender, intermediate and pubescent bladder and urethra could be followed by There is no practical economic method for wheatgrasses were somewhat tolerant to secondary infections and bleeding. The control of white grubs on rangeland. feeding by the black grass bugs. substance also lowers calcium levels and The life cycle of the white grub may take There are many other insect species that causes damage to heart muscle tissue. 3Ð4 years dependent on the species and cli- may sporadically cause severe damage to Capinera et al. (1985) conducted can- mate. Most of the damage is done in the rangeland in some limited areas. Termites, tharadin analysis on several species of second year. The beetles deposit eggs in armyworms, army/cutworms, leafhoppers, blister beetles commonly found in late spring or early summer. Some feeding plant hoppers, spittle bugs, wireworms, bill- Colorado. There were differences in occurs the first season. Grubs move below bugs and numerous others feed on range amounts found between species and sexes. the frost line until spring, then move close plants, but generally are not numerous enough Males apparently produce cantharadin and to the surface to feed on roots. The same to warrant expensive control techniques. pass it to females at mating. The minimum procedure occurs each year in the cycle. One other group of insects I was lethal dose of catharadin is about 1 When the larval cycle has been completed, requested to mention are blister beetles. mg/Kg. Thus a few beetles with a high an earthen cell is prepared and pupation Blister beetles are generally considered catharadin level would kill a small horse, occurs within the cell. The adults remain in beneficial in that the larvae of several but quite a few with a low level would be the cell until spring when they emerge and species are predacious on grasshopper required to kill a large horse. start another generation. eggs. Others are predaceous in the cells of Extension entomologists field quite a few ground-dwelling species of bees. questions yearly from either horse owners Miridae (Plant bugs) Adult blister beetles tend to be gregari- or alfalfa producers on how to avoid buying Many species of this family are associat- ous, and several may be noted feeding on or selling alfalfa hay that contains blister ed with range plants. They have piercing the same flowering alfalfa plant. They also beetles. Generally, blister beetles are pre- sucking mouth parts with which they suck feed on soybeans and blooming goldenrod sent at the second and third cuttings, but juices from plants. and probably other plant species found in probably will not be in the first or fourth The black grass bugs are the best known a range plant complex. cuttings; however, in 1998 in Nebraska, of this group of insects. They are also called Adult blister beetles vary in size and blister beetles were still present at the time big-eye bugs because their eyes appear to be color, but are easily recognized by the of the fourth cutting. Inspection of bales is bulging from the side of their heads. There elongated, narrow, cylindrical and soft not practical because the gregarious behav- are 34 species from 2 genera; Labops and bodies. When viewed from above, they ior of the beetles might cause one bale to Irbisia in this group (Kelton 1980). have a constriction at the back of the head have a large number of beetles, and the Insects such as black grass bugs that where it attaches to the narrowed anterior next bale might not have any. For the same feed by sucking fluids from the cell have end of the thorax (Bauernfeind and reason, chemical control is probably not considerable impact on range plant quali- Breeden 1984). The life cycle of blister practical either unless hay for horses was ty, quantity and plant survival (Haws et al. beetles is complex with several different bringing a premium price. Dead beetles are 1982). The adults of this group are about 6 immature forms. Clusters of eggs are still toxic. Killing the beetles doesn’t mm long and are blackish grey, with buff deposited in the ground. Newly-hatched reduce the toxicity. margins around the edges of the wing. larvae move through the soil feeding on

464 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Literature Cited Haws, B.A., J.F. Werner, D.B. Thomas, J.L. Watts, J.G., E.W. Huddleston, and J.C. Capinera, R.W. Lauderdale, J.B. Knight, Owens. 1982. Rangeland entomology. Ann. E.W. Huddleston, W. Smith, W.C. Rev. Entomol. 27:283Ð311. Anonymous. 1971a. White grubs Ð Nebraska. Campbell, J.D. Evans, A.F. Glover, B.E. Watts, J. Gordon, G.B. Hewitt, E.W. USDA Coop. Econ. Insect Rept. 21:373 Norton, and E. Arlo Richardson. 1982. Huddleston, H. Grant Kinzer, R.J. Anonymous. 1971b. White grubs—Colorado. Rangeland Insects of the Western United Lavigne and D.N. Ueckert. 1989. USDA Coop. Econ. Insect Rept. 21:488. States. Utah Agr. Exp. Sta. Spec. Rept. 23. Rangeland Entomology. Range Sci. Series Anonymous. 1996. Grasshopper IPM User 64 pp. No. 2. 2nd ed. 388 pp. Handbook. Tech. Bull. No. 1809. Hewitt, G.B. 1980. Tolerance of ten species of Wildermuth, V.L. and D.T. Caffrey. 1916. USDAÐAPHIS. Agropyron to feeding by Labops hesperins. The New Mexico range caterpillar and its Ansley, R.J. and C.M. McKell. 1982. Crested J. Econ. Entomol. 73:779Ð782. control. USDA Bull. 443. 12 pp. wheatgrass vigor as affected by black grass Higgins, K.M., J.E. Browns and B.A. Haws. bug and cattle grazing. J. Range Manage. 1977. The black grass bug, Labops hesperins 35:586Ð590. Uhler; its effect on several native and intro- Bauernfeind, R.J. and L.D. Breeden. 1994. duced grasses. J. Range Manage. 30:380Ð84. Blister beetles. Kans. St. Univ. Ext. Ser. Ag Huddleston, E.W., E.M. Dressel, and J.G. Facts Entomol. 111. 4 pp. Watts. 1976. Economic thresholds for range Bellows, T.S., J.C. Owens, and E.W. caterpillar larvae on bluegramma pasture in Huddleston. 1983. Model for simulating northeastern Lincoln County, New Mexico in consumption and economic injury level for 1975. N. Mex. Agr. Exp. Sta. Res. Rept. 314. the range caterpillar. (Lepidoptera: 4 pp. Saturniidae). J. Econ. Entomol. 76:1231Ð38. Kamm, J.A. and J.R. Fuxa. 1977. Campbell, J.B., P.E. Reece, and G.L. Hein. Management practices to manipulate popula- 1998. Range and pasture insects. Chap. 19. tions of the plant bug Labops hesperins High Plains integrated pest management Uhler. J. Range Manage. 30:385Ð87. guide—Colorado, western Nebraska and Kelton, L.A. 1980. The insects and arachnids Wyoming. Bull. 564A. pp. 1Ð6. of Canada, Part 8. The plant bugs of the Campbell, J.B., W. Harold Arnett, J.D. Prairie Provinces of Can. Res. Brit. Agr. Can. Lambley, O.K. Jantz, and H. Knutson. Pub. 1703. 401 pp. 1974. Grasshoppers (Acrididae) of the Flint Kumer, R., R.J. Lavigne, J.E. Lloyd, and Hills native prairie in Kansas. Kans. St. Univ. R.E. Pfadt. 1976. Insects of the Central Agr. Exp. Sta. Res. Paper No. 19. 147 pp. Plains experimental range, Pawnee National Capinera, J.L. 1978. Studies of host plant Grassland. Wyo. Agr. Exp. Sta. Div. preference and suitability exhibited by early Monogr. 32. 74 pp. instar range caterpillar larvae. Environ. Lavigne, R.J. and H.G. Fisser. 1966. Entomol. 7:738Ð40. Controlling western harvester ants. Mtn. Sta. Capinera, J.L., J.K. Detling, and W.J. Reg. Publ. No. 3. 4 pp. Parton. 1983. Assessment of range caterpil- Malechek, J.C., A.M. Gray, and B.A. Haws. lar (Lepidoptera:Saturniidae) effects with a 1977. Yield and nutritional quality of inter- grassland simulation model. J. Econ. mediate wheatgrass infested with black grass Entomol. 76:1088Ð1094. bugs at low population densities. J. Range. Capinera, J.L., D.R. Gardner, and F.R. Manage. 30:128Ð131. Stermitz. 1985. Cantharidin levels in blister Pfadt, R.E. 1994. Field guide to common west- beetles (Coleoptera:Meloidae) associated ern grasshoppers. Wyo. Agr. Exp. Sta. Bull. with alfalfa in Colorado. J. Econ. Entomol. 912. 40 pp. 78:1052Ð55. Randolph, N.M. and C.F. Garner. 1961. Cole, C., Jr. 1968. Pogonomyrmex Harvester Insects attacking forage crops. Tex. Agr. Ext. Ants: A study of the genus in North America. Ser. Bull. B-975. 2 pp. Tenn. Press; Knoxville, Tenn. 222 pp. Riley, S.L., T.S. Bellows, Jr., J.C. Owens, Cowan, F.T. and H. Shipman. 1947. Quantity and E.W. Huddleston. 1984. Consumption of food consumed by Morman crickets. J. and utilization of bluegramma grass Econ. Entomol. 40:825Ð828. Bontelona gracilis by range caterpillar larvae. Dickerson, G.W. 1978. Control of black grass Hemilenca oliviae (Lepidoptera:Saturniidae). bugs (Labops hesperins Uhler) in northern Environ. Entomol. 13:29Ð35. New Mexico. J. Range Man. 3:398Ð99. Shaw, P.B., D.B. Richman, J.C. Owens and Drake, C. 1964. The relationship of white E.W. Huddleston. 1987. Ecology of the grubs, facultative fungi and bacteria on the range caterpillar, Hemilenca oliviae Cockrell. decline of birdsfoot trefoil. Plant Dis. Rept. In: Capinera, J.L. Ed. Integrated pest man- 48:406Ð8. agement on rangeland. A shortgrass prospec- Dubach, J.M., D.B. Richman, and R.B. tive. Westview Press, Boulder Colo. pp. Turner. 1988. Genetic and morphological 234Ð247. variation among geographical populations of Thomas, D.B. and F.G. Werner. 1981. Grass the range caterpillar Hemilenca oliviae feeding insects of the Western ranges: an (Lepidoptera:Saturniidae) Ann. Entomol. annotated checklist. Univ. of Ariz. Agr. Exp. Soc. Amer. 81:132Ð7. Stat. Tech. Bull. No. 243. 50 pp. Hagen, A.F. 1975. Crested wheatgrass. L. hes- Ueckert, D.N. 1970. Seasonal dry-weight com- perins control. Insect and Acar. Tests. 1:102. position in diets of Morman crickets. J. Econ. Entomol. 63:96Ð98.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 465 J. Range Manage. 54: 466Ð473 July 2001 Effects of proanthocyanidins on digestion of fiber in forages

JESS D. REED

Author is associate professor, Department of Animal Sciences, University of Wisconsin-Madison, Madison, Wisc. 93706.

Abstract Resumen

The ability of proanthocyanidins (PA) to form insoluble com- La capacidad de las proantocianidinas (PA) para formar complexes with proteins and polysaccharides affects fiber digestion plejos insolubles con proteínas y polisacáridos afectan la and analysis. This review discusses these effects in relationship to digestión de la fibra y su análisis. Esta revisión discute estos efec- the application of the detergent system of forage analysis. A frac- tos en relación a la aplicación del sistema de detergente del tion of the PA in plants remains after extraction for analysis. análisis de forrajes. Una fracción de las PA en las plantas per- Insoluble PA may be a natural part of the plant cell wall or may be manecen después de la extracción para el análisis. Las PA insol- insoluble because of high molecular weight and post harvest reac- ubles pueden ser una parte natural de la pared celular de la tions. These reactions increase the amount of insoluble PA and planta o pueden ser insolubles debido al alto peso molecular y decrease the amount of soluble PA. The butanol-HCl assay is the reacciones post-cosecha. Estas reacciones aumentan la cantidad most suitable method for analysis of insoluble PA. Insoluble PA de PA insoluble y disminuyen la cantidad de PA soluble. El are associated with negative apparent digestion coefficients for método de Butanol-HCL es el mas apropiados para el análisis de acid-detergent lignin (ADL), neutral-detergent insoluble N and PA insolubles. Las PA insolubles son asociadas con coeficientes acid-detergent insoluble N. The addition of sodium sulfite to neu- negativos de digestión aparente de la lignina acido detergente tral detergent eliminates insoluble PA from NDF. However, the (ADL), N insoluble neutro detergente y N insoluble acido deter- addition of sodium sulfite to neutral detergent will give misleading gente. La adición de sulfito de sodio a l detergente neutro elimina results in relationship to true digestibility of protein. The differ- las PA insolubles de la NDF. Sin embargo, la adición de sulfito de ence between fiber fractions that are prepared with and without sodio al detergente neutro producirá resultados erróneos en the addition of sodium sulfite to neutral-detergent may estimate relación a la digestibilidad verdadera de la proteína. La diferen- the amount of PA/protein complex associated with NDF. A better cia entre las fracciones de fibra que son preparadas con y sin la understanding of the relationship between PA structure and func- adición de sulfito de sodio al detergente neutro pueden estimar la tion is necessary to manipulate PA in forages through breeding or cantidad del complejo PA/proteína asociado con la NDF. Se genetic engineering. The interaction between PA and fiber analysis necesita un mejor entendimiento de la relación entre la estruc- and digestion is an important component of this research. tura y función de las PA para manipular las PA en los forrajes a través del mejoramiento o ingeniería genética. La interacción entre las PA,el análisis de fibra y la digestión es un componente Key Words: condensed tannins, neutral detergent, acid deter- importante de esta investigación. gent, lignin, polyphenolics

Proanthocyanidins (PA) are naturally occurring plant polyphe- et al. 1987, McNabb et al. 1993). The positive effects of tannins on nols that strongly influence the nutritive value of forages. In gen- protein utilization have practical importance because problems eral, PA and condensed tannins are synonyms. Phytochemists associated with extensive proteolysis and (or) deamination in the prefer to use proanthocyanidin because, as discussed below, this rumen limit production in modern feeding systems (Beever et al. term is more closely related to their chemical structure. Most 1989). Proanthocyanidins may also protect ruminants against nutritionists use “condensed tannins” because tannins are defined helminthiasis. Undrenched lambs grazing sulla (Hedysarum coro- as water-soluble polymeric phenolics that precipitate proteins narium L.), a forage that contains PA, had lower fecal egg counts (Haslam 1989). However, many soluble phenolics that have and Trichostrongylus colubriformis worm burdens and higher aver- structural and chemical properties that are similar to PA do not age daily gains than undrenched lambs grazing alfalfa (Medicago precipitate proteins. There are also high molecular weight PA that sativa L.), which does not contain PA (Niezen et al. 1995). Several have structures related to tannins but that are not water-soluble useful reviews on the nutritional effects of PA and tannins in the (Bate-Smith 1973, Stafford and Cheng 1980). diets of ruminants have been written in recent years (Mueller- Proanthocyanidins in forages have both negative and positive Harvey and McAllan 1992, Reed 1995, Waghorn et al. 1999). effects on nutritive value (Reed et al. 1990, Mueller-Harvey and Research on the relationship between concentration of PA in McAllan 1992). In high concentrations, PA reduce intake, forages and parameters of nutritive value is complicated by inad- digestibility of protein and carbohydrates, and animal perfor- equate methodology for quantification and structural analysis. mance (Barry and Duncan 1984, Reed et al. 1990). In low to The ability of PA to form strong complexes with proteins is the moderate concentrations, PA prevent bloat and increase the flow most important aspect of their nutritional and toxic effects of non-ammonia nitrogen and essential amino acids from the (Hagerman and Butler 1981). The strength of these complexes rumen (Egan and Ulyatt 1980, Barry and Manley 1984, Waghorn depends on characteristics of the PA and protein (molecular weight, tertiary structure, isoelectric point, and compatibility of binding sites). Proanthocyanidins have a large number of free Manuscript accepted 25 Nov. 00. phenolic hydroxyl groups that form strong hydrogen bonds with

466 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 proteins and carbohydrates (Haslam 1989). Proanthocyanidins also complex with proteins through hydrophobic bond- ing (Oh et al. 1980). In addition, PA form covalent bonds with proteins through oxidative polymerization reactions as a result of heating, exposure to ultraviolet radiation and the action of polyphenol oxidase (Haslam 1989). The ability of PA to form insoluble complexes with proteins and polysaccharides leads to several effects on fiber digestion and analysis. This review discusses these effects in relationship to the application of the detergent system of forage analysis.

Chemistry and Nomenclature of Proanthocyanidins

Proanthocyanidins are polymers that belong to the class of secondary plant compounds known as flavonoids (Harborne 1994, Haslam 1989, Stafford 1990, Foo et al 1982). Monomeric and polymeric flavonoids are ubiquitous in higher land plants and have many ecological and nutritional effects on animals Fig. 1. Structure of proanthocyanidin polymers. (Harborne 1993). The principal structure of PA is based on repeating units of poly- with glycosylation, acylation with gallic In species such as sainfoin (Onobrychis hydroxy flavan units linked by C bonds acid, and other substitutions (Porter 1994). viciifolia Scop) and Gliricidia sepium between carbons 4 and 8 of the ring struc- The solubility and extraction of PA in (Jacq.) Stewd., the insoluble fraction rep- tures (Fig. 1). These covalent bonds are forage legumes were initially studied by resents the greatest amount (Bate-Smith resistant to hydrolysis and no known Bate-Smith (1973). This research demon- 1973, Giner-Chavez et al. 1997, Jackson et enzyme is capable of cleaving the interfla- strated that substantial amounts of PA are al. 1996). van bond. not extracted by aqueous organic solvents The proportion of insoluble PA in plants However, PA undergo a cleavage reac- and remain in the fibrous residue after also appears to be under genetic control. tion upon heating with strong acids. This extraction. The origin of these insoluble In group II genotypes of sorghum all of reaction is an auto-oxidation to form an PA remains somewhat controversial. the PA in the grain are insoluble in aque- intermediate that undergoes oxidation to Haslam (1989) proposed that PA are a nat- ous organic solvents unless HCl is added an anthocyanidin. The term proantho- ural part of the plant cell wall with cova- to the extraction procedure (Price et al. cyanidin (PA) is prefered over condensed lent bonds to cell wall polysaccharides. On 1978). Our research on the inheritance of tannin because their discovery and distrib- the other hand Stafford (1988) suggests PA among interspecific crosses of ution in plants was determined by this that PA are insoluble because of high mol- Sesbania sesban (L.) Merr. and S. goetzei characteristic auto-oxidation reaction. ecular weight and post harvest condensa- Harms also indicates that insoluble PA is a Therefore, PA are defined as colorless tion reactions with proteins and cell wall heritable characteristic (Table 1). Sesbania plant compounds that form anthocyanidins polysaccharides. Regardless of the mecha- goetzei has a large quantity of insoluble nism, a fraction of the PA in most plants upon heating in solutions of strong acids. PA in comparison to S. sesban. The hybrid remains after extraction for analysis. This had the same levels of insoluble PA as S. Specific names for PA are given based on fraction has a large effect on the analysis the type of anthocyanidin formed during goetzei and a higher amount of soluble PA of fiber and its relationship to nutritive in comparison to S. sesban (Table 1). the autoxidation reaction. Proantho- value and is the main topic of this paper. cyanidins that yield cyanidin are termed procyanidins and those that yield delphini- Table 1. Extractable and insoluble proanthocyanidins (PA) in leaves from Sesbania sesban and S. din are termed prodelphinidin (Fig. 2). goetzei and their interspecific crosses. These 2 PA are the most common but many diverse PA occur in plants including Species Extractable PA Insoluble PA propelargonidin and proluteolinidin. One 1 2 (A550) (A550) problem with this nomenclature is that it S. sesban 0.503 0.263 implies that the proanthocyanidins are S. goetzei 0.556 0.727 homopolymers. However, as we learn S. sesban x S. goetzei 0.928 0.821 more about the structure of PA it is clear S. goetzei x S. sesban 0.807 1.029 that many heteropolymers occur in nature. 1Absorbance at 550 nm from the butanolÐHCl reaction of the extract of 100 mg of DM in 15 ml of aqueous acetone. Proanthocyanidins have been described 2Absorbance at 550 nm from the butanol HCl reaction on 5 mg of neutralÐdetergent fiber.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 467 Fig. 2. ButanolÐHCl reaction of proanthocyanidins.

Analytical Methods above 60¡ C, heat damage and polymer- are different than the compounds from the ization may occur (Haslam 1966). These plant extracts. This difference can lead to post harvest reactions increase the amount large under and over estimations of the The quantification of PA in plants is of insoluble PA and decrease the amount content of PA and is probably the single essential to studies on their nutritional and of soluble PA. If the researcher does not ecological effects (Feeny and Bostock largest cause for the great deviation in attempt to assay for insoluble PA then the concentrations that are reported in the lit- 1968, Swain 1979, Horvath 1981, Martin total amount will be severely underesti- and Martin 1982, Waterman and Mole erature (Giner-Chavez et al. 1997). mated in the case of oven drying. Another problem is that the mechanism 1994). However, the commonly used The most commonly used colorimetric methods of colorimetric analysis have that leads to the reaction of PA with the procedures for the analysis of PA are the many problems (Tempel 1982, Martin and analytical reagent is unrelated to the the vanillin-HCl reaction (Broadhurst and Martin 1982). There are a growing number mechanism underlying their nutritional of analytical methods for the determina- Jones 1978) and the butanol-HCl reaction effects (Reed 1995). The most suitable tion of PA in plants (Waterman and Mole (Bate-Smith 1973, 1975). The vanillin- method is to use the butanol-HCl assay 1994). However, no single method will HCl reagent is specific for flavan-3-ols and isolate the PA from the plant species give satisfactory results for quantitative and proanthocyanidins. The reaction is under investigation for use as a standard. analysis in relationship to nutritional based on the condensation of the phenolic Reversible adsorption of PA from plant effects because the chemical properties aldehyde (vanillin) with the phlorogluci- extracts onto Sephadex LH-20 is a com- that are involved in the reactivity of PA in nol structure of flavan-3-ols and proantho- monly used method for isolating PA from colorimetric and (or) precipitation assays cyanidins under acidic conditions in plants (Hagerman 1991, Giner-Chavez et differ from the properties that underlie methanol or ethanol. The butanol-HCl al. 1997). Reed et al. (1985) developed a their nutritional or toxic effect. Animal reaction is specific to the proanthocyani- gravimetric method based on the ability of species also differ in nutritional response dins and is the prefered method because of trivalent ytterbium to selectively precipi- ingesting plants that contain PA its close relationship to the accepted tate PA from plant extracts. The advantage (Hagerman et al. 1992). Sample prepara- nomenclature. The butanol-HCl method of Yb precipitation is that the precipitate tion also has a large influence on the can also be applied to insoluble PA by can be easily dissolved to yield a solution determination of PA and related polyphe- placing the fibrous residues after extrac- of the PA. These solutions are used for nols in plants. Proanthocyanidins in fresh tion into the solution. After heating, the colorimetric analysis (Giner-Chavez et al. samples are likely to have low complex red pigments formed during the auto-oxi- 1997), chromatography, enzyme inhibition formation and oxidative polymerization dation reaction go into solution. studies and in vitro and in vivo assays for and high solubility in aqueous organic sol- These colorimetric procedures share the inhibition (Reed et al. 1985). The results vents. If storage is necessary, freezing is analytical problem of lack of suitable stan- preferred over other methods as long as from the assays on the dissolved PA also dards. The most commonly used standards relate to an equivalent weight of PA pre- the samples are not allowed to thaw before are catechin for the vanillin-HCl reaction extraction (Mould and Robbins 1981). In cipitate. The 2 methods for isolating PA and quebracho tannins for the butanol-HCl give similar results for several species of some situations, drying is the only means reaction. However, the extinction coeffi- of preserving material. At low tempera- forages (Giner-Chavez et al. 1997). cients for the chromophores produced in tures (< 40¡ C), enzymes may still func- the reaction with these standards usually tion leading to oxidation. At temperatures

468 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Effects of Proanthocyanidins Table 2. Extractable, protein-bound and fiber-bound proanthocyanidins in species of forages.

on Fiber Analysis Source and Species Extractable ProteinÐbound FiberÐBound ------(g/kg) ------The extraction of PA from plant samples Terrill et al 1992: is a problem that is often overlooked in Lotus pedunculatus 59 14 1 PA analysis. Bate-Smith (1973) showed Lotus corniculatus 7 13 1 that, in sainfoin (Onobrychis viciaefolia), Hedysarum coronarium 23 13 1 a significant percentage of the PA is not Jackson et al 1996: extracted by aqueous organic solvents. Calliandra calothyrsus 103 to 158 10 to 28 4 to 8 Flemingia macrophylla 19 to 198 1 6 to 98 3 to 32 The extraction is improved by fine milling Desmodium ovalifolium 82 to 197 16 to 30 8 to 10 and using hot methanol, but there is GinerÐChavez et al 1997: always a substantial amount of PA which Desmodium ovalifolium 63 to 272 1 4 to 35 1 to 10 remains in the fibrous residue after extrac- Gliricidia sepium 0 to 43 21 to 120 2 to 29 tion. High molecular weight PA may be Manihot esculenta 22 to 126 12 to 22 0 to 1 completely insoluble in aqueous organic solvents (Stafford and Cheng 1980). Much of the PA remains in the neutral- cal tree, shrub and forage legumes by Effect on Fiber Digestion detergent fiber (NDF) after sequential using this method (Jackson et al. 1996). extraction of several browse species with Similar results were also obtained by Giner-Chavez et al. (1997) by using a dif- Proanthocyanidins reduce cell wall aqueous acetone (7:3, acetone:H2O) fol- digestibility by binding bacterial enzymes lowed by neutral detergent (Reed et al. ferent methodology. Gliricidia sepium had the highest proportion of protein-bound and (or) forming indigestible complexes 1982, Reed 1986). This problem is com- with cell wall polysaccharides (Barry and mon in several types of feeds that contain and fiber-bound PA in the studies of Jackson et al. (1996) and Giner-Chavez et Manley 1984, Barry et al. 1986, Reed et PA (Terrill et al. 1992). Insoluble PA in al. 1990). Digestibility of fiber fractions the NDF of sorghum grain was inversely al. (1997). The assumption in the butanol HCl reac- was low for sheep fed Acacia cyanophylla correlated with soluble PA (r = -.69, p < Lindl., a tree legume with a high content .01, n = 16) in brown and red varieties tion of the insoluble and fiber bound PA is that the stoichiometry of the reaction is of PA when compared to sheep fed for- (Reed 1987). These results suggest that ages that did not contain PA. Digestibility analysis of extractable PA may underesti- identical to the extractable PA that was isolated from the plant species for use as a of acid detergent lignin in A. cyanophylla mate the total PA content in many samples. was negative (Reed et al. 1990). The amount of PA in the fiber fractions standard. This is unlikely to be the case. The butanol HCl reactivity for the fiber The recovery of PA in digestion balance can be estimated by using the butanol-HCl studies with forage legumes that contain assay (Bate-Smith 1973, Reed et al. 1982, bound PA is likely to be much lower than the extractable PA that was used as a stan- PA also presents an analytical problem. Terrill et al. 1992). The nutritional effects Studies carried out with 14C labeled PA of the insoluble PA have not been ade- dard. The formation of an insoluble complex between PA and protein or polysac- indicate that they are not absorbed from quately studied. They are associated with the digestive tract of chickens (Jimenez- negative apparent digestion coefficients charide is likely to decrease the reactivity of the PA in the auto-oxidation reaction Ramsey et al. 1994) and sheep (Terrill et for acid-detergent lignin (ADL), neutral- al. 1994). Terrill et al. (1994) recovered detergent insoluble N and acid-detergent that occurs in the butanol HCl reagent. This difference in reactivity would lead to 92% of the labeled PA in the digesta and insoluble N in browse legumes (Reed et no label was found in the blood. However, al. 1990, Wiegand et al. 1995). Increased an underestimation of the amount of fiber- bound PA. only 42% of the PA could be accounted total fecal excretion and increased fecal for by direct analysis of PA by butanol- excretion of water, fat, and nitrogen were observed in rats fed carob pod concentrate Table 3. Soluble and insoluble proanthocyanidins and digestibility of acidÐdetergent lignin (ADL) that contained non-extractable condensed by rams in 3 accessions of Sesbania sesban (10865, 15019, and 15036) and 1 accession of S. goetzei tannins (Bravo et al. 1993). (15007). Rams were supplemented with leaves from S. sesban or S. goetzei to supply 3 levels of Terrill et al. (1992) developed a method crude protein. to determine the extractable PA, protein- bound PA and fiber-bound PA in forages Sesbania accession and protein concentrate meals. The 10865 15019 15036 15007 method uses a modified butanol-HCl pro- Soluble PAs1 cedure. Protein-bound PA in the fiber (A550/g DM) 13 35 93 95 Insoluble PAs1 24 48 71 271 remaining after extraction with aqueous (A /g DM) acetone is extracted with a solution of 550 sodium dodecyl sulphate (SDS) and 2- Level of CP from mean mercaptoethanol. The fiber-bound PA is Sesbania (g/day) determined directly on the residue after ------% ADL ------extraction with SDS. The ratio of 25 15.1 Ð26.8 Ð69.3 Ð100.2 Ð45.3 extractable PA to protein-bound PA to 50 7.1 Ð40.2 Ð95.2 Ð163.4 Ð72.9 fiber-bound PA was highly variable 75 11.2 Ð46.1 Ð110.7 Ð166.7 Ð78.1 mean 11.2 Ð37.7 Ð91.7 Ð143.4 Ð65.4 among these feeds but in each case the 1 fiber-bound fraction was the lowest (Table Values for proanthocyanidins were determined by analysis with butanolÐHCl and expressed as absorbance units per g of dry matter analyzed. 2). Similar results were obtained for tropi-

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 469 HCl analysis of feed and digesta. The reactivity of PA in butanol-HCl is most likely altered in the process of digestion. This change in reactivity may be related to the increase in ADL and detergent insoluble nitrogen fractions of digesta and feces that is observed in ruminants fed forages that contain PA (Reed et al. 1990, Yocum and Reed 1994, Yocum 1995, Wiegand et al. 1995).

Proanthocyanidins and the Detergent System of Forage Analysis

Research on the use of 3 accessions of Sesbania sesban and 1 accession of S. goetzei as sources of protein in diets for Fig. 3. Excretion of acidÐdetergent lignin (ADL) and intake of insoluble proanthocyanidins sheep demonstrated the effects of PA on (PA) in sheep fed 3 accessions of Sesbania sesban (10865, squares; 15019, circles; and the application of the detergent system of 15036, triangles) and 1 accession of S. goetzii (15007, diamonds) at 3 levels of crude protein forage analysis (Wiegand et al. 1995). offered from each accession. Accessions with a high content of PA had negative digestion coefficients for neutral- sions was not digested in a nutritionally The increased excretion of fecal NDIN detergent insoluble nitrogen (NDIN) and uniform manner. These results indicate and negative digestion coefficients also acid-detergent lignin (ADL) (Table 3). that, as the level of PA increase, forage N indicates that the N in the sesbania acces- Higher amounts of ADL and NDIN becomes nutritionally non-uniform and sions that contain high levels of PA is excreted in the feces than consumed are a true digestibility of N can not be predicted digested in a nutritionally non-uniform result of the formation of these fractions in by regression analysis. Similar effects of manner. Fecal excretion of NDIN was the digestive tract. The origin of the NDIN PA on true digestibility of N were highly correlated to intake of insoluble in the feces may be from dietary or observed for Acacia cyanophylla, A. siebe- PA. These results indicate that PA cause endogenous sources. Reed et al. (1990) riana and A. seyal Del. that contained high the formation of detergent insoluble com- also observed negative digestion coeffi- levels of PA (Reed et al. 1990). plexes in the digestive tract. Intake of PA cients for NDIN in sheep fed diets containing forage from 2 tree species, Acacia cyanophylla and A. sieberiana DC., that had high levels of PA. Linear regression of the apparent digestible amount of N and the amount of N in the diet can estimate true digestibility of nitrogen. Uniform feed fractions have a constant true digestibility and the metabolic amount in the feces is estimated by the intercept of this linear regression. The slope of this regression in forages that do not contain PA is approximately 0.88 and indicates that the forage N has uniform nutritional availability and high true digestibility (Van Soest 1967). The negative intercept is an estimate of N of endogenous origin and is approximately 0.5% of dry matter intake. The slope and intercept of the regression analysis for the accession of S. sesban with the lowest content of PA were similar to the expected values. The high r2 and low standard error indicates that the N in this accession was digested in a nutritionally uniform manner. The lower slope and r2 and higher standard error for the regression analysis Fig. 4. Excretion of neutralÐdetergentÐinsoluble N (NDIN) and intake of insoluble proantho- of accessions that contained higher levels cyanidins (PA) in sheep fed 3 accessions of Sesbania sesban (10865, squares; 15019, circles; of PA indicated that the N in these acces- and 15036, triangles) and 1 accession of S. goetzii (15007, diamonds) at 3 levels of crude protein offered from each accession.

470 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 4. Insoluble PA (A550 gÐ1) with (+) and without (Ð) addition of sodium sulfite to neutral (Astragalus cicer L.), sericea lespedeza detergent (Krueger et al 1999). [Lespedeza cuneata (Dum.-Cours) G. Don], and kura clover (Trifolium ambigu- Neutral Detergent Insoluble um M. Bieb. ) were subjected to sequential Proanthocyanidin detergent fiber analysis to investigate the Sulfite Trt. effects that the addition of 0.5 g sodium Ð + Difference sulfite to neutral detergent has on the (g/kg) recovery and composition of fiber and Sericea (AU Donnely) 130 1 129 Sericea (Serala) 216 2 215 lignin from forage legumes that vary in Crownvetch 38 2 36 levels of PA (Krueger et al. 1999). Sainfoin (Eski) 36 3 33 Soluble, insoluble, and neutral detergent Sainfoin (Remont) 27 3 24 insoluble PA (NDIPA) concentrations Birdsfoot trefoil (Viking) 21 2 19 were highest in sericea, moderate in Birdsfoot trefoil (Norcen) 17 1 16 crownvetch, sainfoin, and birdsfoot trefoil and absent in alfalfa, cicer milkvetch, red clover, and kura clover. Addition of sodi- was highly correlated to fecal excretion of gent system may be a useful technique to um sulfite reduced levels of neutral deter- ADL and NDIN, and fecal ADL and determine the effects of PA on protein gent fiber (NDF), acid detergent fiber NDIN were also highly correlated. digestion. This conclusion is supported by (ADF), acid detergent lignin (ADL), neu- Proanthocyanidins cause the formation the high correlation between intake of tral detergent insoluble nitrogen (NDIN), of detergent insoluble complexes that ele- insoluble PA and fecal excretion of ADL and acid detergent insoluble nitrogen vate fecal excretion of NDIN and ADL. (r = .88, p < .01, n = 36) (Fig. 3), and (ADIN) recovered from most forages test- The formation of these complexes violates NDIN (r = .94, p < .01, n = 36; Wiegand ed. The addition of sodium sulfite effec- 2 of the basic principles of the application et al 1995; Fig. 4). tively eliminated NDIPA from NDF (Table of detergent analysis for estimating the 4). The difference between fiber fractions nutritive value of forages. The first princi- prepared without and with the addition of ple is that neutral-detergent solubles and Sodium Sulphite in Neutral sodium sulfite during the neutral detergent crude protein are nutritionally uniform and Detergent and Insoluble procedure was related to PA concentration. have high true digestibility. The second is Proanthocyanidins Neutral detergent fiber difference was pos- that fiber fractions are of plant origin and itively correlated with insoluble PA (r = cannot originate in the digestive tract (Van 0.905, p = 0.0001) and NDIPA (r = 0.913, Soest 1967). The violation of these princi- Alfalfa (Medicago sativa L.), red clover p = 0.0001; Fig. 5). The addition of sodium ples in forages that contain PA does not (Trifolium pratense L.), birdsfoot trefoil sulfite to neutral detergent in sequential invalidate the use of the detergent system (Lotus corniculatus L.), sainfoin detergent analysis of PA containing of analysis. These results suggest that the (Onobrychis viciifolia Scop), crownvetch species eliminates the insoluble PA frac- deviation from ideal behavior in the deter- (Coronilla varia L.), cicer milkvetch

Fig. 5. Difference in sequential acidÐdetergent lignin (ADL) and insoluble PA with and without addition of Na2SO3 to Neutral Detergent.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 471 tion and decreases the amount of lignin shrubs and seed coats to determine PA GinerÐChavez, B. I., P. J. Van Soest, J. B. and detergent insoluble N. concentration and reactivity. The effect of Robertson, C. Lascano, J. D. Reed and A. There are 2 applications for the detergent PA on the nutritive value and adaptation N. Pell. 1997. A method for isolating con- system of analysis. First, NDF provides an of rangeland species in the diets of rumi- densed tannins from crude plant extracts with trivalent ytterbium. J. Sci. Food Agr. estimate of the plant cell wall fractions. nant herbivores is another important 74:359Ð368. Acid detergent fiber estimates the cellulose research topic. Products to overcome the Hagerman, A. E. 1991. Tannin Analysis. and lignin, while ADL estimates lignin. negative effects of PA and related Miami University, Oxford, Ohio, USA. For this application the presence of polyphenols on ruminant production on Hagerman, A. E. and L. G. Butler. 1981. The PA/protein complexes in the fiber residues rangelands are sold in South Africa, specificity of proanthocyanidinÐprotein interferes with the estimate of the plant cell Australia and Zimbabwe. However, the interactions. J. of Biol. Chem. wall and the addition of sodium sulfite to manipulation of range vegetation in rela- 256:4494Ð4497. neutral detergent when analyzing plant tionship to PA content would be very dif- Hagerman, A. E., C. T. Robbins, Y. Weerasuriya, T. C. Wilson and C. species that contain PA may be advisable. ficult because many dominant woody McArthur. 1992. Tannin chemistry in rela- The second application of neutral deter- species contain high levels of PA and tion to digestion. J. Range Manage. gent is to partition feed into fractions that related polyphenolic compounds. 54:57Ð62. reflect their bioavailability and nutritional Harborne, J.B. 1993. Introduction to uniformity. Protein in forages that do not Ecological Biochemistry. Academic Press contain PA are nutritionally uniform, have Limited, London. p. 318. high true digestibility and are soluble in Harborne, J. B. 1994. The Flavonoids Literature Cited Advances in Research Since 1986. Chapman neutral detergent (Van Soest 1967). and Hall, London. P. 676. However, the true digestibility of protein is Haslam, E. 1966. Chemistry of Vegetable reduced in forages that contain PA and the Barry, T. N. and S. J. Duncan. 1984. The role of condensed tannins in the nutritional value Tannins. Academic Press, New York. protein is nutritionally non-uniform. This of Lotus pedunculatus 1. voluntary intake. Haslam, E. 1989. Plant Polyphenols-Vegetable behavior of protein in forages containing Br. J. Nutr. 51:485Ð491. Tannins Revisited. Cambridge University Press, Cambridge, U.K. PA is associated with an increase in NDIN, Barry, T. N. and T. R. Manley. 1984. The Horvath, P. J. 1981. The nutritional and eco- ADIN and ADL in both forages and feces. role of condensed tannins in the nutritional The recovery of PA/protein complexes in logical significance of AcerÐtannins and value of Lotus pedunculatus for sheep 2. related polyphenols. M. S. Thesis, Cornell NDF reflects the nutritional non-uniformi- quantitative digestion of carbohydrates and University, Ithaca, New York. ty of protein. The addition of sodium sul- protein. Br. J. Nutr. 51:493Ð504. Jackson, F. S., T. N. Barry, C. Lascano, and fite to neutral detergent will therefore give Barry, T. N., T. R. Manley, and S. J. B. Palmer. 1996. The extractable and bound misleading results in relationship to the Duncan. 1986. The role of condensed tan- condensed tannin content of leaves from true digestibility of protein. On the other nins in the nutritional value of Lotus pedun- tropical tree, shrub and forage legumes. J. hand, the difference between fiber frac- culatus for sheep. 4. sites of carbohydrate Sci. Food Agr. 71:103Ð110. tions that are prepared with and without and protein digestion as influenced by dietary JimenezÐRamsey, L. M., J. C. Rogler, T. L. the addition of sodium sulfite to neutral- reactive tannin concentration. Br. J. Nutr. Housley, L. G. Butler and R. G. Elkin. 1994. Absorption and distribution of detergent may estimate the actual amount 55:123Ð137. BateÐSmith, E. C. 1973. Tannins in herba- 14CÐlabeled condensed tannins and related of PA/protein complex associated with the ceous leguminosae. Phytochemistry sorghum phenolics in chickens. J. Agr. Food NDF. Therefore, both analytical approach- 12:1809Ð1812. Chem. 42:963Ð967. es may be used to study the effects of PA BateÐSmith, E. C. 1975. Phytochemistry of Krueger, C. G., K. A. Albrecht, J. D. Reed, on protein digestion in forages. proanthocyanidins. Phytochemistry 16: E. J. Bures, and V. N. Owens. 1999. 1107Ð1113. Sodium sulfite effects on recovery and composition of detergent fiber and lignin from Beever, D. E., M. Gill and J. D. Sutton. 1989. forage legumes varying in levels of proantho- Management Implications Limits to animal production with high forage cyanidins. J. Sci. Food Agr. 79:1351Ð1356. diets. J. Anim. Sci. 67(supp 1):298. (Abstr.). Martin, J. S. and M. M. Martin. 1982. A better understanding of the relation- Bravo, L., E. Mañas and F. Saura–Calixto. Tannin assays in ecological studies: lack of 1993. Dietary nonÐextractable condensed ship between PA structure and function is correlation between phenolics, proantho- tannins as indigestible compounds: effects on cyanidins and proteinÐprecipitating con- necessary to manipulate PA in forages faecal weight, and protein and fat excretion. through breeding and selection or through stituents in mature foliage of six oak species. J. Sci. Food Agr. 63:63Ð68. Oecology 54:205Ð211. genetic engineering. The interaction Broadhurst, R. B. and W. T. Jones. 1978. McNabb, W. C., G. C. Waghorn, T. N. Barry between PA and fiber analysis and diges- Analysis of condensed tannins using acidi- and I. D. Shelton. 1993. The effect of con- tion is an important component of this fied vanillin. J. Sci. Food Agr. 29:788Ð794. densed tannins in Lotus pedunculatus on the research. There is a fine line between the Egan, A. R. and M. J. Ulyatt. 1980. digestion and metabolism of methionine, cys- potentially positive effects of PA and their Quantitative digestion of fresh herbage by tine and inorganic sulphur in sheep. Br. J. negative effects on intake, digestion and sheep VI. utilization of nitrogen in five Nutr. 70:647Ð661. animal performance. The review by herbages. J. Agr. Sci. Camb. 94:47Ð56. Mould, E. D. and C. T. Robbins. 1981. Evaluation of detergent analysis in estimat- Waghorn et al. (1999) clearly outlines the Feeny, P. P. and H. Bostock. 1968. Seasonal changes in the tannin content of oak leaves. ing nutritional value of browse. J. Wildl. magnitude of the problem and the research Manage. 45:937Ð947. required. Topics include defining the Phytochemistry 7:871Ð880. Foo, L. Y., W. T. Jones, L. J. Porter and V. MuellerÐHarvey, I. and A. B. McAllan. 1992. chemical structure of PA in relationship to Tannins: their biochemistry and nutritional M. Williams. 1982. Proanthocyanidin poly- properties. Advances in Plant Cell reactivity with proteins and enzymes, mers from fodder legumes. Phytochemistry Biochemistry and Biotechnology 1:151Ð217. determining optimal concentrations and 21:933Ð935. types of PA for ruminants, surveys of grasses, herbaceous plants, trees, browse

472 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Niezen, J.H., Waghorn, T.S., Charleston, Reed, J. D., P. J. Horvath, M. S. Allen and P. Van Soest, P. J. 1967. Development of a com- W.A.G. and G.C. Waghorn. 1995. Growth J. Van Soest. 1985. Gravimetric determina- prehensive system of feed analysis and its and gastrointestinal nematode parasitism in tion of soluble phenolics including tannins application to forages. J. Anim. Sci. lambs grazing either lucerne (Medicago sati- from leaves by precipitation with trivalent 26:119Ð128. va) or sulla (Hedysarum coronarium) which ytterbium. J. Sci. Food Agr. 36:255Ð261. Waghorn, G. C., J. D. Reed and L. R. contains condensed tannins. J. Agr. Sci. Reed, J. D., R. E. McDowell, P. J. Van Soest, Ndlovu. 1999. Condensed tannins and herbi- (Camb.) 125:281Ð289. and P. J. Horvath. 1982. Condensed tan- vore nutrition. Proceedings of the XVIII Oh, H. I., J. E. Hoff, G. S. Armstrong, and L. nins: a factor limiting the use of cassava for- International Grassland Congress. Volume A. Haff. 1980. Hydrophobic interaction in age. J. Sci. Food Agr. 33: 213Ð220. IIIÐInvited Papers and Opening and Closing tanninÐprotein complexes. J. Agr. Food Stafford, H. A. 1988. Proanthocyanidins and Sessions. P. 153. Association Management Chem. 28:394Ð398. the lignin connection. Phytochemistry Centre, Calgary, Canada. Porter, L. J. 1994. Flavans and proanthocyani- 27:1Ð6. Waghorn, G. C., M. J. Ulyatt, A. John and dins. In: J. B. Harborne (Ed.) The Flavonoids Stafford, H. A. 1990. Flavonoid Metabolism. M. T. Fisher. 1987. The effect of condensed Advances in Research Since 1986. p. 23. CRC Press Inc., Boca Raton, Fla. tannins on the site of digestion of amino Chapman and Hall, London. Stafford, H. A. and T. Y. Cheng. 1980. The acids and other nutrients in sheep fed on Price, M. l., S. Van Scoyoc and L. G. Butler. procyanidins of Douglas fir seedlings, callus Lotus corniculatus L. Br. J. Nutr. 1978. A Critical evaluation of the vannillin and cell suspension cultures derived from 57:115Ð126. as an assay for tannin in sorghum grain. J. cotyledons. Phytochem. 19: 131Ð135. Waterman P. G., and S. Mole. 1994. Analysis Agr. Food Chem. 26:1214Ð1218. Swain T. 1979. Tannins and lignins. In: G. A. of Phenolic Plant Metabolites. Blackwell Reed, J. D. 1986. Relationships among soluble Rosenthal and D. H. Janzen (Ed.) Scientific Publications, Oxford, U.K. phenolics, insoluble proanthocyanidins and Herbivores, Their Interaction with Secondary Wiegand, R. O., J. D. Reed, A. N. Said and fiber in East African browse species. J. Plant Metabolites. p 657. Academic Press, V. N. Ummuna. 1995. Proantocyanidins Range Manage. 39:5Ð7. New York. (condensed tannins) and the use of leaves Reed, J. D. 1987. Phenolics, fiber and fiber Tempel, A. S. 1982. Tannin measuring tech- from Sesbania sesban and Sesbania goetzei digestibility in bird resistant and nonÐbird niques: a review. J. Chem. Ecol. as protein supplements. Anim. Feed Sci. resistant sorghum grain. J. Agr. Food Chem. 8:1289Ð1298. Technol. 54:175Ð192. 35:461Ð464. Terrill, T. H., A. M. Rowan, G. B. Douglas Yocum, F. 1995. Proanthocyanidins and Reed, J. D. 1995. Nutritional toxicology of tan- and T. N. Barry. 1992. Determination of polyphenols in ensiled forage legumes and nins and related polyphenols in forage extractable and bound condensed tannin con- nitrogen digestion by sheep. M. S. Thesis, legumes. Invited Paper. Pharmacology/- centrations in forage plants, protein concen- University of WisconsinÐMadison, Madison, Toxicology Symposium on Toxic Legumes. trate meals and cereal grains. J. Sci. Food Wisc. J. Anim. Sci. 73:1516Ð1528. Agr. 58:321Ð329. Yocum, F. D., and J. D. Reed. 1994. Reed, J. D., H. Soller and A. Woodward. Terrill, T. H., G. C. Waghorn, D. J. Wooley, Proanthocyanidins and polyphenols in 1990. Fodder tree and straw diets for sheep: W. C. McNabb and T. N. Barry. 1994. ensiled forage legumes and nitrogen diges- intake, growth, digestibility and the effects of Assay and digestion of 14CÐlabelled con- tion by sheep. J. Dairy Sci. 77 (Suppl.):385. phenolics on nitrogen utilisation. Anim. Feed densed tannins in the gastrointestinal tract of (Abstr.). Sci. Technol. 30:39Ð50. sheep. Br. J. Nutr. 72:467Ð477.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 473 J. Range Manage. 54: 474Ð489 July 2001 Anti-quality factors associated with alkaloids in eastern temperate pasture

F.N. THOMPSON, J.A. STUEDEMANN, AND N.S. HILL

Authors are professor emeritus of physiology, College of Veterinary Medicine University of Georgia, Athens, Ga 30602, animal scientist, J.Phil Campbell, Sr., Natural Resource Conservation Center, USDA-ARS, Watkinsville, Ga 30677 and professor Department of Crop and Soil Sciences, University of Georgia, Athens, Ga 30602.

Abstract Resumen

The greatest anti-quality associated with eastern temperature El principal factor anti-calidad asociado con los de zacates pasture grasses is the result of ergot alkaloids found in endo- templados del este que se utilizan para praderas es el resultado phyte-infected (Neotyphodium ceonophialum) tall fescue (Festuca de los alcaloides Ergot encontrados en el pasto Alta fescue infec- arundinacea Schreb.) The relationship between the grass and the tado de hongo endófito (Neotyphodium ceonophialum). La endophyte is mutalistic with greater persistence and herbage relación entre el pasto y el endófito es mutualista, con mayor mass as a result of the endophyte. Ergot alkaloids reduce growth persistencia y masa de forraje como resultado del endófito. Los rate, lactation, and reproduction in livestock. Significant effects alcaloides Ergot reducen la tasa de crecimiento, la lactación y la are the result of elevated body temperature and reduced periph- reproducción del ganado. Los efectos críticos son el resultado de eral blood flow such that necrosis may result. Perturbations also la elevada temperatura corporal y el reducido flujo periférico de occur in a variety of body systems. Planting new pastures with sangre que puede ocasionar en necrosis. También ocurren per- seed containing a “non-toxic” endophyte appears to be a poten- turbaciones en una variedad de sistemas corporales. El plantar tial solution. Ergotism results from the ingestion of the scelerotia praderas nuevas con semilla libre del hongo endófito parece ser of Claviceps purpurea containing ergot alkaloids found on seed una solución potencial El Ergotismo resulta de la ingestión de la heads. Ergotism resembles the effects of endophyte-infected tall esclerotia de Claviceps purpuerea que contiene alcaloides Ergot fescue. Endophyte-infected perennial ryegrass (Lolium perenne la cual se encuentra en las estructuras de la planta que contienen L.) contains ergot and lotirem alkaloids that result in reduced las semillas. El Ergotismo asemeja los efectos producidos por el growth and tremors. Reed canarygrass (Phalaris Anundinacba zacate Alta fescue infectado por el hongo endófito. El ryegrass L.) contains tryptamine, hordenine and gramine alkaloids that perenne infectado con el endófito contiene alcaloides ergot y reduce growth. Annual ryegrass (Lolium multiplorum L. may lotirem que resultan en un crecimiento reducido y temblores. El contain galls with cornetoxins which result in neurological signs. zacate “Reed canarygrass” contiene los alcaloides triptamina, hordenina y gramina los cuales reducen el crecimiento. El rye grass anual puede contener agallas con cornetoxinas las cuales resultan en síntomas necrológicos. Key Words: tall fescue, ergotism, perennial ryegrass, reed canarygrass, annual ryegrass Tall Fescue The term “eastern temperature grass” is somewhat subjective and could be defined to include any grass species grown in tem- The most notorious grass-related livestock anomaly in the United perate zones or species that originate and predominate within the States is fescue toxicosis, affecting over 8.5 million beef cows and temperate regions of the world. Numerous grass species contain 700,000 horses (Ball et al. 1996). The economic impact of grazing anti-quality compounds as defense mechanisms, so this discus- endophyte-infected (E+) tall fescue upon the beef industry has been sion will be limited to grasses that are utilized in the eastern half estimated to exceed $700 million per annum (Hoveland 1990). of the United States, have origins in temperature climatic Further economic impacts occur upon the horse and sheep industry. regimes, and contain the C3 photosynthetic pathway common to The agronomic attributes of tall fescue (Festuca arundinacea cool-season grasses. Using this definition of the term, this discus- Schreb.) make it an attractive forage species because of its ability sion will focus on 2 grass species, i.e., tall fescue (Festuca arund- to withstand drought, poor soil conditions, and intensive defolia- inacea Schreb.) and perennial ryegrass (Lolium perenne L.) that tion from grazing. It is utilized on approximately 14 million form mutualistic associations with other organisms resulting in hectares of pasture and hayfields, most of which are located in the anti-quality products, and 1 grass species, reed canarygrass eastern half of the United States. Fescue toxicosis occurs when the (Phalaris anundinacea L.), in which anti-quality products are an plant is infected with the constitutive clavicipitaceous endophytic endemic function of the plant genome. In addition, ergotism and fungus, Neotyphodium coenophialum (Glenn et al. 1996, formerly annual ryegrass (Lolium multiflorum L.) toxicosis are the result of called Acremonium). The endophyte lives in intercellular spaces of organisms parasitizing forages. sheath, stem, leaf, and seed tissues. There is no invasion of plant cells nor does the endophyte become pathogenic. It is passed from Manuscript accepted 24 Mar. 01. generation to generation via seed, so infected plants beget infected

474 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 offspring and thus perpetuate the association. In a survey of over 1500 pasture samples obtained throughout the United States, more than 70% of the samples had 60% or more endophyte infection rates (Shelby and Dalrymple 1987). Seeds which were tested generally had the same rate of presence as pasture samples, but nearly 90% of the seed samples had less than 20% viable (living) endophyte. The obvious question then is, “Why are fields highly infected if the endophyte does not survive in the seed from which they were planted?” Older tall fescue stands are typically highly infected because in mixed stands of endophyte-free (E-) and E+ plants, E+ plants choke out and replace the E- plants and hence, pastures convert from low-infection rates to high-infection rates as the process continues. Fig. 2. Loline alkaloids found in endophyteÐinfected tall fescue (Porter 1994). The grass benefits from the endophyte- grass association in part by a group of alkaloids produced by the endophyte or by The endophyte receives a home and a (animal behavior), 3 (physiological) and 4 the plant in response to the endophyte. food supply in return for its contribution to (sera or plasma). In cases where extensive Ergot (Fig. 1) and clavine alkaloids, the plant. This means the endophyte is data exist, only a few selected articles peramine, and saturated aminopy- never subjected to environmental forces were referenced to illustrate effects. rrolizidine (lolines) alkaloids (Fig. 2) are and is only dependent upon plant health The presence of ergot and perhaps other all biologically active compounds that for its survival (Hill 1994). Hence, it is in alkaloids in forage resulting in depressed serve as feeding deterrents and decrease the plant’s interest to provide the needs for body weight gains in livestock grazing E+ reproduction and growth by both mam- the endophyte; and the endophyte to pro- tall fescue particularly during the warm mals (Porter 1994, Stuedemann et al. vide protection to the plant against climat- season is often referred to as summer fes- 1989) and insects (Clay et al. 1985, Clay ic and biological forces (e.g., insects) that cue toxicosis. Affected animals have an 1989, Siegel et al. 1991, Porter 1994). may be threatening. unthrifty appearance, long rough hair Protection from defoliation suggests solar coats, excessive salivation and elevated energy capture and retention is a para- Animal Toxicosis-Tall Fescue respiratory rates and spend less time graz- mount priority in this association. The impact or effects of consumption of ing during daylight hours (Stuedemann Reduced insect or livestock grazing results E+ tall fescue have been reviewed (Bush and Hoveland 1988). Calving rates are in more photosynthetically active leaf et al. 1979, Stuedemann and Hoveland also decreased (Porter and Thompson area, resulting in greater energy capture, 1988, Schmidt and Osborn 1993, 1992) as well as milk yield in dairy cows greater energy reserves, and greater re- Stuedemann and Thompson 1993). (Strahan et al. 1987). Fescue foot and fat growth capacity when infected with the Readers are referred to those reviews for necrosis are 2 other conditions in cattle endophyte (Hill et al. 1990). Endophyte- specific information on the impact of E+ associated with E+ tall fescue. Fescue foot infected tall fescue has greater forage and tall fescue on animal response. A com- is a gangrenous condition of the hooves, seed productivity than the E- form (Hill et pendium of the effects of the endophyte on tail and occasionally ears that occurs pri- al. 1991) and is more drought tolerant animal response variables is presented in marily during the winter months (Yates (West et al. 1993). Tables 1 (performance and production), 2 1983). Fat necrosis occurs in mature cows and is associated with masses of hard fat in the abdomen, leading to poor digestion and calving problems (Bush et al. 1979). We postulate that both fat necrosis and fescue foot are symptoms of fescue toxicosis. Milk Production and Calf Growth. Milk production was reduced as much as 60% in dairy cows consuming an E+ ryegrass- tall fescue hybrid compared to the same E- hybrid (Hemken et al. 1979). There was also an associated decrease in forage intake. In a subsequent study daily milk production was significantly reduced in mid-lactation Holsteins on E+ compared to E- tall fescue (Strahan et al. 1987). There was also an associated significant decrease in daily dry matter intake on E+ Fig. 1. Ergot alkaloids found in endophyteÐinfected tall fescue (Porter 1994). (7.1 kg) compared to E- (9.1 kg) tall fes-

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 475 Table 1. Effects of endophyteÐinfected fescue on animal performance criteria.

Response Endophyte Ergovaline Response criteria level Low E High E Low E High E Low E High E Feedstuff Animal Referencea Average daily gain (%) (mg dÐ1) (Kg dayÐ1) 0 100 .96 .20 Seed Steers Schmidt el al. 1982 2 >90 .83 .45 Pasture Steers Hoveland et al. 1983 8 91 .97 .46 Pasture Steers Read and Camp 1986 <1 98 .21 Ð.05 Pasture Cows Gay et al. 1988 <10 >70 .66 .43 Pasture Steers Tolley et al. 1990 0 >85 .45 3.50 Ð.08 Ð3.5 Pasture Cows Peters et al. 1992 0 >85 .89 72 Pasture Suckling Peters et al. 1992 calves 25 58 .46 30 Pasture Steers Stuedemann et al. 1993 Pregnancy Rate (%) 1 98 95 55 Pasture Cows Gay et al. 1988 21 77 89 74 Pasture Cows Tucker et al. 1989 0 >85 1.45 3.50 91 72 Pasture Cows Peters et al. 1992 a Some values were adapted from specific research reports. cue. Cows receiving E- tall fescue gained reduction in calf weights associated with grazing E+ tall fescue both lost weight and 12.0 kg during the experiment compared nursing cows grazing E+ tall fescue was had reduced pregnancy rates compared to to a weight loss (Ð11.7 kg) in cows fed E+ reported by Gay et al. (1988). These cows grazing E- tall fescue. A decline in tall fescue. The authors suggested that effects of E+ tall fescue are most detri- cow body condition postpartum negatively there was no endophyte threshold level mental to calf-weaning weights consider- affects reproduction and results in a pro- below which milk production in dairy ing that cow-milk production accounts for longed interval from parturition to first cows would not be adversely affected. approximately 66% of the variance in calf- estrus (Wiltbank et al. 1964). In a 3-yr Milk production was 75% greater in weaning weight. In this regard Danilson et cow study Gay et al. (1988) reported calv- beef cows grazing E- compared to E+ tall al. (1986) calculated a 0.15 kg reduction in ing rates were 95 and 55% for the E- and fescue (Schmidt et al. 1984). At 100 days milk production for each 10% increase in E+ tall fescue groups, respectively. In postpartum, primiparous beef cows graz- pasture endophyte-infection level. Grazing another 3-yr study Washburn and Green ing E+ tall fescue had 50% lower milk E+ tall fescue also reduced milk produc- (1991) reported that 65% and 39% of production than those grazing E- tall fes- tion in ewes (Stidham et al. 1982). cows on low vs. high endophyte, respec- cue (Schmidt et al. 1986). Beef cows graz- The effect of grazing E+ tall fescue on tively, raised a calf each year. Similarly, ing E+ KY 31 tall fescue had a 25% calf-birth weight either had no effect Boling (1985) reported cows grazing low- reduction in milk production compared to (Schmidt et al. 1986) or there was a reduc- endophyte infected Kenhy tall fescue had cows grazing E- Mozark tall fescue or tion in birth weight (Bolt and Bond 1989). calving rates of 86% compared to 67% for orchard grass, (6.0 and 8.0 kg/day, respec- Reproduction in Beef Cattle. This sub- E+ tall fescue. tively) (Peters et al. 1992). Calf growth ject has been reviewed (Porter and A greater negative effect from grazing associated with nursing cows grazing E+ Thompson 1992, Schmidt and Osborn E+ tall fescue upon reproduction occurred tall fescue was also significantly reduced 1993). In studies summarized by Schmidt in beef heifers compared to cows. Heifers compared to the other 2 groups. A similar and Osborn (1993), lactating beef cows raised on E+ tall fescue had delayed onset

Table 2. Effects of endophyteÐinfected tall fescue on behavioral response criteria.

Response Endophyte Ergovaline Response criteria level Low E High E Low E High E Low E High E Feedstuff Animal Referencea Intake (%) Kg dayÐ1 0.0 100 6.6 4.2 Pasture Steers Stuedemann et al. 1989 0.0 96 6.0 3.2 Seed Steers Osborn et al. 1992 (mg/d) (% of BW) 0.0 >85 1.45 3.50 2.40 2.25 Pasture Cows Peters et al. 1992

(mg/kg BW.75 ) 0.0 0.053 2.55 1.76 Seed Sheep Aldrich et al. 1993b & hay Water (Lis in dayÐ1) intake 0.0 0.053 4.2 5.3 Seed Sheep Aldrich et al. 1993b & hay 0.0 0.05 49.3 48.9 Seed Heifers Aldrich et al. 1993b a Some values were adapted from specific research reports.

476 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Table 3. Effects of endophyteÐinfected fescue on physiological response criteria.

Response Endophyte Ergovaline Response criteria level Low E High E Low E High E Low E High E Feedstuff Animal Referencea Skin (%) (ppb) Kcal m2 hourÐ1 Vaporization <50 381 113.7 91.3 Seed Heifers Aldrich et al. 1993a <50 285 41.9 34.4 Seed Steers Aldrich et al. 1993b (at 22¡C) <50 285 87.2 47.1 Seed Steers Aldrich et al. 1993b (at 32¡C) Respiration (breath minÐ1) rate 0.0 96 62 70 Seed Steers Osborn et al. 1992 & hay Heart rate (beats minÐ1) 0.0 96 68 51 Seed Steers Osborn et al. 1992 & hay Rectal temperature (¡C ) 0.0 96 39.4 39.7 Seed Steers Osborn et al. 1992 & hay (mg/kg BW.75) 0.0 0.053 40.0 40.4 Seed Sheep Aldrich et al. 1993b & hay Core body Temperature 0.0 0.053 38.3 39.3 Seed Sheep Aldrich et al. 1993b & hay a Some values were adapted from specific research reports. of puberty and decreased first-service con- experienced dystocia. Supplementing ier (Monroe et al. 1988, Brendemuehl et ception rates (Washburn et al. 1989). pregnant mares on E+ tall fescue with al. 1994b). Surviving foals were large- Similarly, in another study there was a shelled corn had no effect on gestation framed and emaciated in appearance, with 96% conception rate in beef heifers raised length or incidence of dystocia (Earle et premature eruption of teeth and overgrown on E- tall fescue compared to a conception al. 1990). Placentas from affected mares hooves (Monroe et al. 1988, Putnam et al. rate of 55% on E+ tall fescue (Schmidt et were thickened, reddish colored and heav- 1991). Mares should be removed from E+ al. 1986). In the following year, only 33% of the then primiparous cows grazing E+ Table 4. Effect of ingestion of endophyteÐinfected tall fescue on sera or plasma constituents of cattle. tall fescue were successfully rebred compared to 93% on E- tall fescue. Response criteria Direction Reference The adverse effect of the endophyte Alkaline phosphatase reduced Bond et al. 1984 upon reproduction in cattle is mediated Boling et al. 1989 partially at least, by increased early Amylase increased Nutting et al. 1992 embryonic mortality. Cattle embryos Asparatate aminotransferase reduced Dougherty et al. 1991 transferred into heifers grazing E+ tall fes- Cholesterol reduced Bond et al. 1984 cue had decreased survival compared to Stuedemann et al. 1985a embryos transferred into heifers grazing Lipham et al. 1989 Tolley et al. 1990 E- tall fescue (Rahe et al. 1991). Similarly, Cortisol unchanged Aldrich et al. 1993a cattle embryos taken from cows grazing Creatine kinase reduced Dougherty et al. 1991 E+ tall fescue had decreased in vitro Growth hormone unchanged Elsasser and Bolt, 1987 cleavage, rate of development and quality Lipham et al. 1989 increased Thompson et al. 1987 compared to those from cows grazing E- Ð1 tall fescue (Nasti et al. 1994). InsulinÐlike growth factor reduced Filipov et al. 1999 Lactic dehydrogenase reduced Dougherty et al. 1991 Impact on Horses. The pregnant mare is Luteinizing hormone unchanged Mizinga et al. 1992 very sensitive to the effects of grazing E+ Melatonin reduced Hurley et al. 1981 tall fescue (Cross 1997). Mean gestation Porter et al. 1990 length in mares consuming E+ tall fescue Prolactin decreased Hurley et al. 1981 was lengthened 27 days (Monroe et al. Elsasser and Bolt, 1987 1988). Others reported similar effects Thompson et al. 1987 Lipham et al. 1989 (Putnam et al. 1991, Redmond et al. Thyroid stimulating hormone unchanged Elsasser and Bolt, 1987 1994). Severe dystocia frequently occurs Thyroxine unchanged Aldrich et al. 1993a with prolonged gestation in mares on E+ Triiodothyronine unchanged Aldrich et al. 1993a tall fescue. Putnam et al. (1991) reported that 10 of 11 mares grazing E+ tall fescue

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 477 tall fescue at least 30 days prior to expect- al. 1989, Osborn et al. 1992) and sheep found in sheep on E+ diets (Zanzalari et ed foaling (Taylor 1993). (Hemken et al. 1979, Aldrich et al. 1989). al. 1989). Following foal delivery mares grazing An 8% depression in intake in steers fed Body Temperature, Respiratory and E+ tall fescue had a high incidence of E+ tall fescue hay resulted in a 58% sup- Heart Rates. Inclusion of the endophyte either agalactia or reduced milk yield pression in average daily gains (Schmidt in fed diets has resulted in increased rectal (Monroe et al. 1988, Putnam et al. 1991). et al. 1982). Steers grazing E- tall fescue temperature and respiratory rate. In this The milk from such mares was off-colored had a 43Ð69% greater dry matter intake regard, the effects of the endophyte were (straw-colored with an oily appearance), compared to steers on E+ tall fescue investigated using temperature controlled rather than the white milk of normal (Stuedemann et al. 1989). rooms (Hemken et al. 1981, Rhodes et al. mares. This milk lacked normal While the negative effect of the endo- 1991, Osborn et al. 1992, Aldrich et al. immunoglobulin concentrations and, con- phyte upon intake may due to palatability 1993b, Cornell et al. 1990). Calves consequently, foals did not have normal pas- or secondarily to increased body tempera- suming a toxic ryegrass-tall fescue hybrid sive immunity (Cross 1997). ture (Beede and Collier 1986), a separate at increased ambient temperatures had Grazing E+ tall fescue alters the repro- neural mechanism is probable. increased rectal temperatures, respiratory ductive endocrinology of the pregnant Metoclopramide, primarily a dopaminer- rates and depressed body weight gains mare (reviewed by Cross 1997). Serum gic antagonist with some anti-serotinergic compared to those fed a non-toxic hybrid concentrations of the pituitary hormone, activity (Freeman et al. 1992), increased (Hemken et al. 1981); however, at lower prolactin, that is necessary for the onset of intake in lambs held at 32¡C fed a high ambient temperatures there were no differ- lactation (lactogenesis) were depressed. endophyte diet with no alteration in body ences in respiratory rate and rectal temper- Serum progesterone concentrations were temperature (Aldrich et al. 1989). atures. In a later experiment using steers also lowered, but serum concentrations of The effect of E+ tall fescue on intake is fed E-, E+ or E- diets plus ergotamine at estradiol were increased. This indicates exacerbated by elevated environmental both a thermoneutral temperature (21¡C) that placental function is altered because temperatures (Hemken et al. 1981). When and a heat stressed environment (32¡C), progesterone and estradiol are secreted calf intake of E+ and E- tall fescue forage Osborn et al. (1992) reported both temper- from that organ. was compared in environmental chambers, ature and endophyte increased rectal tem- Grazing E+ tall fescue did not increase the E+ forage decreased intake only when perature and decreased heart rate, but no body temperature in horses (Monroe et al. environmental temperatures exceeded significant interaction occurred between 1988), perhaps because of the ability of 31¡C. In a similar experiment with calves endophyte and temperature. Respiratory horses to dissipate heat by sweating. in environmental chambers at 21¡C and rate was increased with the endophyte Putnam et al. (1991) observed increased 32¡C, and fed an endophyte-free tall fes- only at the elevated temperature. sweating in pregnant mares grazing E+ tall cue diet with added ergotamine resulted in Ergotamine induced changes similar to fescue. A relationship between grazing E+ reduced intake at both temperatures those found by feeding E+ diets. Both the tall fescue and laminitis has been suggest- (Osborn et al. 1992). endophyte and added ergotamine ed based upon epidemiologic and patho- In vitro dry matter digestibility was decreased peripheral body temperature; logic reports (Rhorbach et al. 1995). superior for E+ hay compared to E- tall this was attributed to reduced peripheral McCann et al. (1992a) reported no reduc- fescue hay (Schmidt et al. 1982). Chestnut blood flow. Similar changes in rectal tem- tion in growth of yearling horses grazing et al. (1991) found no difference in organ- perature in cattle resulted from feeding E+ E+ tall fescue supplemented with concen- ic matter digestibility of E+ and E- tall or E- tall fescue diets when animals were trate. In contrast, average daily gain was fescue in steers and Harmon et al. (1991) exposed to diurnal temperature changes reduced by 57% in yearling horses grazing found no endophyte effect on dry matter (Aldrich et al. 1993a). Interestingly, this E+ tall fescue without supplementation and nitrogen digestibility in steers. Others, experiment also revealed that there was a (Aiken et al. 1993). Relative to mare fertil- however, found that diets containing E+ significant interaction between diet and ity (Brendemuehl et al. 1994a) reported tall fescue had reduced dry matter and environmental temperature on skin vapor- that mares grazing E+ tall fescue had organic matter digestibility in sheep ization; with skin vaporization increased reduced fertility and increased early (Hannah et al. 1990, Fiorito et al. 1991, only in the E- group at an elevated temper- embryonic mortality rates. Westendorf et al. 1993), cattle (Aldrich et ature. Therefore the effect of the endo- Behavior, Intake and Digestibility. al. 1993a), and rats (Larson et al. 1991), phyte reduces the ability to remove excess During daylight, cattle on E+ tall fescue which could be ambient temperature- body heat. A relationship was established pastures spent less time grazing dependent (Hannah et al. 1990). between dietary ergovaline concentrations (Stuedemann et al. 1985b, Lipham et al. A metabolic cost has been associated fed to cattle and rectal temperatures 1989). In sunlight, steers on E+ tall fescue with the endophyte. This was revealed by (Cornell et al. 1990). Ergovaline at 50 grazed 5Ð21% of the time between 1200 pair-fed experiments where the intake of ppb, lowest concentration, resulted in and 1600 hours compared to 43Ð65% for animals receiving E- diet was maintained increased rectal temperature only at 30¡C steers grazing E- tall fescue (Stuedemann at the intake level of the E+ tall fescue ambient temperature and above. et al. 1985b). This effect persisted for at seed-based diet group. Using this strategy Ergot alkaloids can increase body tem- least 26 days after the steers were moved with rats and cows, a depression in body perature by a direct effect upon the tem- from E+ to E- pastures. There is no known weight gains occurred in the animals perature regulating areas in the brain explanation for this residual behavior. receiving E+ diets (Mizinga et al. 1992, (Nickerson 1970, Loew et al. 1978). This Much of the reduction in animal perfor- 1993). Therefore, growth in rats and cattle central effect upon body temperature mance has been attributed to reduced are affected by the endophyte in some occurs at a lower dosage compared to that intake. The presence of the endophyte manner beyond intake. This could be due necessary to mediate vasoconstriction. reduced intake in cattle (Hemken et al. to increased hepatic mixed function oxi- Spiers et al. (1995) investigated the effects 1981, Schmidt et al. 1982, Stuedemann et dase activity related to detoxification as of injecting rats with ergovaline in both a

478 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 cold environment (7Ð9¡C) and hot envi- vasoconstriction is found in the thickening effect upon GH secretion. The effects of ronment (31Ð33¡C). Treatment in the cold of the smooth muscle layer of the arteri- E+ tall fescue intake on serum GH have environment resulted in a decrease in both oles in cattle following ingestion of the been variable (Oliver 1997). Both ergota- rectal and tail temperature whereas treat- endophyte (Oliver and Schultze 1997). In mine and ergonovine elevated plasma GH ment in the hot environment resulted in an this regard bovine vascular smooth muscle in steers (Browning et al. 1997). Serum elevation of rectal temperature, but a proliferated in vitro in response to both IGF was reduced in steers grazing E+ tall reduction in tail temperature. ergot alkaloids and N-acetyl loloine fescue (Filipov et al.1999, Hazlett et al. The effects of ergot alkaloids are com- (Strickland et al. 1996). 1998 ), suggesting this may be an impor- plicated as they are adrenergic and Prolactin, Neural Function and Hair tant mechanistic effect whereby the ergot dopaminergic agonists as well as both Coat. Serum prolactin is reduced in live- alkaloids suppress growth. serotinergic agonists and antagonists stock species consuming E+ diets (Hurley Ergot alkaloids may also alter energy (Muller-Schweintzer and Weidmann et al. 1981, Bolt et al. 1983, Thompson et metabolism and electrolyte movement in 1978). Receptors for these activities are al. 1987, Lipham et al. 1989, McCann et the liver, as both ergonovine and ergota- widely dispersed. In this regard treatment al. 1992b). Pituitary secretion of prolactin mine inhibited Ca2++-activated bovine of previously dewormed heifers fed E+ is inhibited by dopamine and ergot alka- mitochondrial ATPase activity (Moubarak diets treated with ivermectin, an loids are potent dopaminergic agents et al. 1998). As previously mentioned, E+ anthelmintic that binds to g-amino butyric (Lamberts and Macleod 1990). Ergot alka- intake increased mixed function oxidases neural receptors (Barragry 1984), had loids were ranked relative to competitive in the liver of sheep (Zanzalari et al. reduced core body temperature and binding to dopamine receptors on pituitary 1989). increased intake upon heat exposure (Dr. cells (Larson 1997). Ergovaline shared Fat Metabolism. Serum cholesterol is Spiers, University of Missouri, personal potency with other ergopeptines in this reduced by grazing E+ tall fescue in cattle communication). Treatment of cattle graz- regard and the ergopeptine alkaloids had (Stuedemann et al. 1985a, Lipham et al. ing E+ tall fescue with ivermectin topical- 10-fold greater activity compared to ergine 1989) and sheep (Bond et al. 1988). It is ly before grazing and again at 56 days and ergonovine. unknown whether this was the result of after beginning the experiment had Depressed serum prolactin with E+ diets increased cholesterol uptake by the tissues increased weight gains (Bransby 1997). In indicates an impact of ergot alkaloids on or decreased hepatic secretion. The ergot some experiments this treatment resulted both pituitary and neural function. While alkaloids may decrease lipolysis by an in increased gains in cattle on E- tall fes- prolactin is required for the onset of lacta- adrenergic receptor activity in the liver cue in spite of very low fecal egg counts. tion, it is not importantly related to growth (Oliver 1997). An association was made Therefore, while ivermectin resulted in a (Eisemann et al. 1984). The central ner- between high-nitrogen fertilization of E+ tall positive effect in cattle on E+ tall fescue, vous system and pituitary have an abun- fescue, reduced serum cholesterol and the this effect may not have a specific effect dance of dopamine receptors. Meto- incidence of fat necrosis in cattle against alkaloids in the forage. clopramide (dopamine antagonist) given (Stuedemann et al. 1985a). Serum triglyc- Interestingly, a combination of an anabolic to steers grazing E+ tall fescue increased eride levels were also reported to be ear implant containing estradiol and prog- serum prolactin, improved hair coat quali- decreased in cattle on E+ diets (Oliver esterone plus ivermectin to cattle over- ty, body weight gains and more time was 1997). Together these studies indicate that came the growth depressant effect of E+ spent grazing (Lipham et al. 1989). The ingestion of E+ diets alters lipid metabolism. tall fescue. dull and shaggy hair coat changes associ- Serum Enzymes. Several serum Vasoconstriction. In vitro ergot alka- ated with fescue toxicosis may also result enzymes, alkaline phosphatase, aspartate loids mediated vasoconstriction of bovine from depressed serum prolactin. amino transferase, alanine amino trans- dorsal pedal veins via α-2 adrenergic Administration of prolactin to hamsters ferase, and lactic dehydrogenase, are fre- properties (Solomons et al. 1989). N- following pituitary removal resulted in quently reduced in cattle on E+ diets acetyl loline had some effect in this regard hair changes appropriate for the photoperi- (reviewed by Stuedemann and Thompson (Oliver et al. 1990). A subsequent study od under which they were maintained 1993, Oliver 1997). This general decrease (Dr. Jack Oliver, University of Tennessee, (Niklowitz and Hoffmann 1988). In sheep, in enzymatic activity by E+ diets has been personal communication) demonstrated increased daylight length that results in attributed to increased hepatic α-2 adren- extreme potency of ergovaline in this increased serum prolactin, which is impor- ergic activity (Oliver 1997). Other possi- regard. Most interestingly, Oliver et al. tantly related to a spring moult and pro- ble mechanisms include inhibitors of (1998) demonstrated that venous prepara- duction of a summer coat (Lincoln 1990). enzymatic action, effects on cell prolifera- tions from cattle on E+ diets had an As a specific cellular mechanism upon tion, increased clearance via the liver or enhanced contractility to an alpha-2 adren- neural function, ergovaline inhibited kidney, loss of enzymatic cofactors and ergic agonist. Dyer (1993) reported ergot Na+/K+ ATPase activity in a dose depen- alterations in conditions that might inhibit alkaloids mediated vasoconstriction upon dent manner in rat brain homogenates enzymatic action, e.g. pH and tonicity cattle uterine and umbilical veins via a (Moubarak et al. 1993). (Schultze et al. 1999). Dougherty et al. serotinergic mechanism. Hepatic/Insulin-Like Growth Factor/- (1991) reported that circulating gamma Vasoconstriction is important in the Energy Production. The major anabolic glutamyltransferase, as well as aspartate pathogenesis of fescue foot. Yates et al. effect of growth hormone (GH) secreted aminotransferase and creatinine kinase (1979) showed that administration of toxic from the pituitary is expressed via stimu- were reduced in cows fed E+ tall fescue anion fractions from fescue resulted in lating secretion of insulin-like growth fac- seed. Gamma glutamyltransferase is pro- decreased coronary band temperatures in tor-1 (IGF) prominently from the liver duced specifically in the liver in the cattle. Decreased blood flow to the digit (Hossner et al. 1997). Secretion of IGF is bovine species (Duncan et al. 1994). It is would result in decreased nutrient delivery modulated by diet and intake (Elsasser et pertinent to recognize that only an and tissue death. A mechanism for the al. 1989). Circulating IGF has a negative increase in the circulating concentration of

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 479 these enzymes is an indication of inflam- meters. Oliver (1997) indicated both total Willibrand factor, and angiotensin con- mation of the organ(s) of origin. circulating leukocytes and individual types verting enzyme, were elevated in sera of The reduction of alkaline phosphatase as of leukocytes (neutrophils, lymphocytes, cattle grazing E+ tall fescue (Oliver 1997). the result of E+ diets is rather consistently eosinophils and monocytes) were lowered Endothelin is a potent vasoconstrictor observed (Bond et al. 1984, Boling et al. in calves on E+ tall fescue, suggesting agent and is mitogenic (Anggard et al. 1989, Jackson et al. 1997, Gould and lowered immunocompetence. However, in 1990). Angiotensin converting enzyme Hohenboken 1993, Schultze et al. 1999). a later report (Oliver et al. 2000) only results in the production of angiotensin II, A steady decrease in the concentration of eosinophil numbers were reduced by E+ a potent vasoconstrictor enzyme (Hoorn alkaline phosphatase was observed in tall fescue. and Roth 1993). Von Willibrand factor is steers grazing E+ tall fescue (Schultze et Immunological effects. Saker et al. an adhesion molecule for platelets during al. 1999). This enzyme catalyzes the (1998) indicated cattle on E+ tall fescue vascular injury (Blann 1993). hydrolysis of monophosphate esters under had lowered indices of immunological Additionally, thromboxane B2a (stable alkaline conditions (Duncan et al. 1994). function. Additionally, a decreased anti- metabolite of thromboxane A2) a potent Quantitative isoenzyme determinations of body titer in response to tetanus toxin vasoconstrictor from platelets, was report- this enzyme obtained from cattle grazing occurred in steers grazing on E+ tall fes- edly elevated in the sera of cattle on E+ E+ indicated that the decrease in this cue (Dawe et al. 1997) and in rats on E+ tall fescue (Oliver 1997). This agent also enzyme was due to lowered activities of diets challenged with sheep red blood cells has bronchoconstrictive effects in the lung intestinal and bone isoenzymes (Schultze (Dew et al. 1990). In contrast, Rice et al. (Campbell 1990). Recently, it was found et al. 1999). Therefore, an effect upon (1997) reported greater antibody response that steers grazing E+ compared to E- tall serum enzymes extends beyond the liver. in challenged cattle grazing E+ tall fescue. fescue had a greater response to Copper Status. Consumption of pre- Further evidence of immunosuppression is lipopolysaccharide as measured by sumably high-endophyte tall fescue result- indicated by the decreased serum globulin increases in tumor necrosis factor, a cata- ed in rapidly decreased circulating copper concentrations in steers grazing E+ bolic agent (Filipov et al. 1999); indicating (Cu) and ceruloplasmin oxidase activity in (Schultze et al. 1999). Both the alpha and that E+ tall fescue sensitizes the animal to cattle (Stoszek et al. 1979); however, body gamma globulin fraction decreased, but other excitatory agents. weight gains were not improved by Cu the largest decrease occurred in the In summary, the pathogenesis of fescue supplementation. Recent work indicates gamma globulin fraction. Since gamma toxicosis appears to originate from dam- serum Cu concentrations were decreased globulins are of lymphoid origin (Duncan age to the vascular endothelium. in E+ compared to E- tall fescue (Dennis et al. 1994), this could explain decreased Endothelial cells release mediators that et al. 1998, Oliver et al. 2000). In a related immune responses. In support of these result in smooth muscle cell proliferation report, steers grazing E+ compared to E- experimental observations, Purdy et al. in the arterioles. Further exposure of blood tall fescue had reduced ceruloplasmin and (1989) reported that steers that had been vessels results in vaso-constriction with serum Cu (Saker et al. 1998). The steers on E+ had increased morbidity and mor- ischemia so that nutrient flux is altered grazing E+ tall fescue also had lowered tality following movements to feedlots. and dissipation of heat is reduced. The indices of immunological competency Pathogenesis. Necropsy changes decrease in blood perfusion to the skin and (lowered phagocytic activity and MHC observed in cattle that had grazed E+ tall lungs would contribute to heat stress while class II expression). Copper supplementa- fescue were mostly limited to a thickening the same effect upon the GI tract would tion increased the MHC class II expres- of the smooth muscle layer of the arteri- result in altered nutrient flux. The more sion regardless of forage endophyte status. oles (Oliver and Schultze 1997). There distal portions of the body would be most Additionally, Cu is required for hair pig- were GI tract lesions in several animals compromised by this scenario with the mentation and red blood cell production indicating abscesses, enteritis and colitis. resultant loss of tail tips and limb digits. (Barragry 1994). Perhaps the decreased Similarly, in earlier findings in cattle that The effects upon reproduction could be circulating Cu levels contributes to the had grazed E+ tall fescue, Garner and either as a direct effect of ergot alkaloids bronzed hair coat observed in Angus cattle Cornell (1985) reported swollen arterioles upon embryos, decreased nutient delivery grazing E+ tall fescue. upon necropsy. Therefore, changes in cat- to the uterus, or altered uterine environ- Blood Cells. The results of a 3 year tle on E+ tall fescue are largely referable ment. A direct effect of ergot alkaloids grazing study indicate that the effect of E+ to the cardiovascular system. The patho- upon the brain may lead to increased body tall fescue was an increase in numbers of genesis associated with ergotism is also temperature and decreased intake. circulating red blood cells, however, there described as due to stimulation of smooth was a reduction in both mean red blood muscles in blood vessels (primarily arteri- cell volume and hemoglobin concentration oles) with congestion proximal to the Ergotism in each cell (Oliver et al. 2000). These resulting vasoconstriction and ischemia changes in red blood cell volume and distal to the vessel spasm (Osweiler 1981). Ergot toxicity or ergotism occurs as the hemoglobin are congruous with a decrease Ergot alkaloids mediated cytotoxicity result of ingestion of the scelerotia of in circulating Cu. Earlier work (Steen et upon the endothelial portion of blood ves- Claviceps purpurea found on feed grains al. 1979, Bond et al. 1984) indicated the sels in cattle grazing E+ tall fescue (Oliver and pasture grasses. Ergot alkaloids identi- hematocrit was likely suppressed in cattle 1997). The vascular endothelium is a fied with the toxicosis have been identi- grazing E+ tall fescue. In contrast, circu- known target for the ergot alkaloids fied (Porter et al. 1987). The major ergot lating numbers of red blood cells were not (Thompson et al. 1950). The endothelial alkaloids found in sclerotia on fescue, reduced in cattle on endophyte containing cells are metabolically active and serve as wheat, and barley were ergotamine, diets (Rhodes et al. 1991). Since Cu is an interface for toxic agents (Gimbrone ergocristine and ergosine. Additionally, related to red blood cell production, a Cu 1986). Biologically active agents of ergocornine and ergocryptine were associ- deficiency could alter red blood cell para- endothelial origin, endothelin, von ated ergotized annual ryegrass (Schneider

480 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Animal ToxicosisÐPerennial Ryegrass. The effect of grazing endophyte-infected (E+), lolitrem B-free E+ and E- varieties of perennial ryegrass upon animal performance and the incidence of ryegrass staggers has been reported (Fletcher 1993, Cunningham et al. 1993). Animal Performance. Live weight gains were reduced in sheep grazing E+ perennial ryegrass in the absence of ryegrass staggers (Fletcher and Barrell 1984); indicating a direct effect of the endophyte. Fig. 3. Alkaloids found in endophyteÐinfected perennial ryegrass (ergot alkaloids not shown)(Porter Depressed body weight gains occurred 1994). only in association with summer conditions and the endophyte. Reduced serum et al. 1996). The scelerotia of the fungus viable and non-viable tissue. In another prolactin also was associated with the replaces some of the seedhead and appear report, gangreneous lesions on the rear of endophyte, presumably as the result of as elongated dark-brown bodies of vari- the fetlock characterized ergotism in cattle ergovaline (Davies et al. 1993b). Grazing able size. (Woods et al. 1966). Intestinal inflamma- the lolitrem B-free varieties of E+ perenni- The signs of ergotism resemble fescue tion has been observed in both cattle and al ryegrass over an extended period did toxicosis (Robbins et al. 1986, Schneider sheep with ergotism (Coppock et al. 1989, not result in improved live weight gains et al. 1996). This similarity in signs is nat- Greatorex and Mantle 1973). The patho- over other perennial ryegrass endophyte ural as both are the result of ergot alkaloid genesis of ergotism and fescue toxicosis is associations, however, animals grazing the toxicity. Hyperthermia, decreased intake, identical with the disturbances resulting endophyte-free variety had the greatest peripheral vasoconstriction leading to from endothelial damage to the vascular gain (Fletcher and Sutherland 1993a). lameness and gangrene of distal portions system. Reference is made to the pathogen- Therefore, other anti-quality factor(s) of the body especially in the hind limb esis of fescue toxicosis for this discussion. associated with the endophyte depressed characterize both conditions in cattle gains in the absence of lolitrem B. (Coppock et al. 1989, Mantle 1978a, Staggers. Ryegrass staggers is a neuro- Robbins et al. 1986). Barley ergot fed to Perennial Ryegrass muscular disease that is of major animal heifers resulted in tail sloughing, retained health significance in sheep, cattle and winter coats, increased salivation, and res- Perennial ryegrass (Lolium perenne L.) horses in New Zealand and Australia. It is piratory rates during hot weather is of minor significance as an eastern tem- most prevalent in warm drought condi- (Skarland and Thomas 1972). Cold weath- perate forage grass (Balasko et al. 1995). tions and is associated with close grazing er predisposed cattle fed ergot to lameness It’s primary region of adaptation is the wet (less than 2.5 cm) and when animals are and gangrene (Mantle 1978b). Pregnant and cool climate of the northeastern disturbed (Keogh 1973). Ryegrass stag- heifers fed ergot failed to abort (Mantle United States and seed production regions gers occurs sporadically in most years on 1978b), however, some ewes aborted fol- of the Willamette Valley in Oregon. As E+ perennial ryegrass in Australia lowing ergot feeding (Greatorex and with tall fescue, perennial ryegrass is (Cunningham et al. 1993). Severe out- Mantle 1974). Sheep fed either ergot or infected with a mutualistic endophyte, breaks have resulted in substantial live- ergotamine had anorexia, hyperventilation, Neotyphodium lolii, and E+ ryegrass has stock losses with the greatest loss in young excessive salivation, cold extremities, and increased growth and density compared to lambs suggesting altered lactation (Foot et some had necrosis of the tongue the non-infected forms (Cunningham et al. al. 1988). (Greatorex and Mantle 1973). Ergotism 1993). Insect resistance mediated by the Animals with ryegrass staggers may has resulted in severe loss of milk produc- endophyte can have a significant impact appear normal or have a fine tremor of the tion associated with loss of body mass and on the agronomic qualities of a pasture, as head and neck at rest. When affected ani- infertility occurred in dairy cows Argentine stem weevil (Listronotus bona- mals are excited they move with a stiff, (Schneider et al. 1996). A reduction in nensis) kills the growing points of the E- uncoordinated, jerky gait that affects serum prolactin was associated with the grass plant (Prestidge and Gallagher either the front limbs or all limbs. toxicity. 1988). The alkaloids found in N. Severely affected animals may collapse Gross and microscopic changes associat- coenophialum infected tall fescue are also with tetanic seizures, but rise and move ed with ergot resemble the vascular found in N. lolii infected perennial rye- normally within a few minutes once the changes in fescue toxicosis. In cattle, con- grass, but in addition, N. lolii produces source of excitement is removed striction of arterioles, endothelial damage, tremorgenic indolediterpene alkaloids (Mortimer and di Menna 1985). Generally vascular stasis, thrombosis, ischemia, and (lolitrems) (Fig. 3). These tremorgenic there are few deaths in affected livestock gangrene are described (Burfening 1973). alkaloids produce involuntary convulsing unless associated with misadventure and Another cattle report included areas of skin when animals are stressed by excitation animals generally recover when moved to necrosis at the base of the ear, flanks, tail- (Fletcher 1982). Hence, livestock produc- E- pastures (Cunningham et al. 1993). head, and around the distal portions of the ers utilizing perennial ryegrass are faced Lesions associated with this condition are limbs (Coppock et al. 1989). Micro- with the same dilemma as those utilizing primarily biochemical, however, muscle scopically arterioles were thickened. tall fescue in that they can use a toxic for- fiber degeneration and degeneration of Grossly there was distal swelling of the age base (endophyte-infected) or a non- Purkinje’s cells in the cerebellum have limbs with a demarcating line between sustainable endophyte free variety. been microscopically described (Munday

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 481 et al. 1985). These changes are considered the result of altered neuronal metabolism, neuronal exhaustion, and anoxic conditions during seizures. The tremorgenic action of several mycotoxins including paxilline have been attributed to binding to the gamma amino butyric acid (GABA) receptors in neural tissue and inhibiting GABA stimulation of Cl- uptake (Gant et al. 1987). The significance of this inhibitory effect is found in the fact that GABA is the major inhibitory neurotransmitter in the nervous system. Consequently, receptor blockade of the GABA system results in increased sensitivity to stimulii. Heat Stress. Increased respiratory rates and rectal temperatures have been associated with grazing E+ perennial ryegrass (Fletcher 1993). The rectal temperature increase in a stressed environment was greatest in the animals grazing E+ ryegrass compared to E-, however, rectal temperatures were intermediate in lambs Fig. 4. Alkaloids found in reed canary grass (Phalaris sp.) that are similar to serotonin (Cheeke on E+ lolitrem B-free ryegrass. This 1998). increase in rectal temperature was attributed to ergovaline in the E+ lolitrem-free boline, hordenine, and gramine alkaloids (Gallagher and Koch 1964). The problem forage. Animals with the greatest increase (Marten 1973). Structures of these alka- occurred when P. aquatica L. dominated in respiratory rates grazed forage with the loids are in Fig. 4 (Cheeke 1998). These the pasture with rapidly growing plants largest concentration of ergovaline. It is alkaloids are concentrated in the immature (Blood and Radostits 1989). Signs have presumed that the presence of ergovaline leaf sheaths and blades (Woods et al. occurred within 4 hours of going on pas- results in the effects as described for fes- 1979). They reduce palatability of the ture but usually between 12 and 72 hours cue toxicosis. grass, and thus serve as animal deterrants after exposure. The cardiac disorder asso- Fecal Contamination and Fly Strike. to prevent overgrazing (Marten et al. ciated with “sudden death” has been Fecal contamination of wool and flystrike 1976). The tryptamine and carboline alka- attributed to an unknown toxin other than involving flies laying eggs in the skin loids create digestive disorders resulting in the tryptamine alkaloids (Bourke et al. beneath fecal contaminated areas is a a greater incidence of diarrhea in sheep 1988). The cardiac syndrome or “sudden major economic problem in New Zealand compared to either the hordenine or death” was regarded to be the result of associated with grazing E+ perennial rye- gramine alkaloids (Marten et al. 1981). forced exercise in sheep already exhibiting grass (Fletcher and Sutherland 1993b). Hordenine and gramine alkaloids simply nervous signs. Anderton et al. (1994) sug- Lambs grazing E- perennial ryegrass did reduce average daily gains. Hence, there gested N-methyltyramine (structurally not have these problems whereas this are metabolic differences in modes of related to hordenine) is causative. Both occurred in 29Ð31% of the animals on E+ action; however, forage refusal correlates tryptamine and tyramine alkaloids being perennial ryegrass. better with total alkaloid concentration monoamine oxidase inhibitors provides a than with the individual alkaloid classes mechanism for a cardiotoxic effect. (Marten et al. 1976). The alkaloids in reed The typical nervous form occurs after Phalaris Species (Reed canarygrass are under simple genetic con- more protracted exposure, usually 2Ð3 Canarygrass) trol and are highly heritable (Marum et al. weeks after sheep are put on new growth 1979, Woods et al. 1979). Fortunately, pasture (Blood and Radostits 1989). The low alkaloid cultivars are commercially following signs were described: thoracic Reed canarygrass (Phalaris arundi- available. Therefore, the obvious solution limb paresis, pelvic limb paresis, disturbed nacea L.) is utilized primarily in the north- for prevention of Phalaris staggers is to equilibrium, hypermetria of the thoracic ern half of the United States (Sheaffer and replant with low-alkaloid cultivars. limbs, fine mild tremors and a bounding Martin 1995). It is adapted to poorly Field outbreaks of Phalaris toxicity pelvic gait (Bourke et al. 1990). Affected drained or flooded areas and can be inva- have been reported for sheep and cattle sheep often are conscious and frightened sive in these habitats (Merigliano and (Bourke et al. 1990, Nicholson et al. when approached. If they are recumbent, Lesica 1998). Its primary utilization is in 1989). In sheep 2 toxicological entities they struggle in an attempt to rise. New low lying areas where spring melting occur: a “sudden death” syndrome and a cases have occurred in association with snows or streambanks provide moist habi- nervous syndrome (Bourke et al. 1988). forced exercise for as long as 12 weeks tats. Reed canarygrass is also drought The “sudden death” is characterized by after removing sheep from the pasture intolerant and, therefore, has limited use in sudden collapse especially when excited (Blood and Radostits 1989). The nervous the southeastern U.S. (Sheaffer and Martin and is associated with cardiac abnormali- signs were replicated following adminis- 1995). Reed canarygrass may contain ties, cyanotic mucous membranes and dis- tration of the Phalaris alkaloids, 5- methoxy-methyl tryptamine, 2 methyl turbed respiration. Affected sheep either methoxy dimethyltryptamine, gramine and tryptamine, 2 methoxy-tetrahydro-b-car- die immediately or recover spontaneously hordenine, with the former being the most

482 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 potent (Bourke et al. 1990). Phalaris alka- factor that reduced gains in Rival and bacteria to be infected with a bacterio- loids act by binding to neural serotinergic Venture in the latter half of the grazing phage before the toxin can be produced receptors that inhibit neurotransmission in season. (Ophel et al. 1993). The bacterium pro- those pathways. Provision of cobalt to duces a yellow slime on the seed heads. iodinized salt is preventive (Duynisveld Toxic nematode galls are orange in color and Wittenberg 1993). Ryegrass Toxicosis whereas, the non-toxic gall is dark brown Signs of toxicosis in cattle include stiff- or black. Nematodes in the gall may be ness of the hocks, dragging the hind feet, Annual ryegrass (Lolium multiflorum visualized microscopically following addi- incoordination of the tongue and lips Lam., Lolium rigidum Gaud. in Australia) tion of water to the dry gall (McKay and which results in eating difficulty. is grown on approximately 1 million Riley 1993). Consequently, affected bulls died after a hectares in the United States, of which The mechanism of action of the coryne- wasting disease associated with P. car- over 90% is found in the southeast toxins involves inhibition of an enzyme, oliniana (Nicholson et al. 1989). (Balasko et al. 1995). Annual ryegrass is uridine diphospho-N-acetylglucosa- Microscopically degenerative lesions of infected with an endophytic fungus whose mine:dolichol-phosphate N-acetyl-glu- spinal cord tracts and in the cerebellum of dissemination is fastidious compared to cosamine phosphate transferase (UDT) sheep have been observed (Blood and endophytes belonging to the genus necessary for glycosylation of proteins Radostits 1989). Also, an abnormal green- Neotyphodium. The endophyte resides in (Jago et al. 1983). Therefore, toxicity ish pigment has been seen in the renal the basal 2 mm of the tiller, and is trouble- results from depletion or reduced activity medulla and in parts of the brain. some to locate in developing seedheads, of essential glycoproteins found in Animal Production. Total indole alka- but it is passed from one generation to the enzymes, hormones, components of the loid concentration (gramine, tryptamines next in a limited number of seed within cell membrane and membrane receptors and carbolines) was inversely correlated the raceme (Latch et al. 1987, Nelson and (Jago et al. 1983). with weight gains in lambs and steers Ward 1990). The endophyte has no Toxicosis may appear as soon as 2 days (Marten et al. 1976). Marten et al. (1981) adverse effects on livestock (Hickey and or as late as 12 weeks after grazing the indicated that a total alkaloid concentra- Hume 1994) nor does it provide resistance toxic forage. Signs in sheep associated tion greater than 2.0 mg/g dry weight of to insect predation (Prestidge 1991). with this toxicosis include a high stepping forage reduces animal gains. Similarly, While the endophye is termed gait, lack of coordination and convulsions palatability was correlated with total alka- “Acremonium-like” there is no taxonomic (Cheeke 1998). An animal may have a loid concentration (Simons and Marten evidence suggesting a common ancestry convulsion and recover or remain recum- 1971). Recently released cultivars of reed with Neotyphodium. bent and die with their feet in a paddling canarygrass, ‘Rival’ and ‘Venture’, con- Animal Toxicosis. Annual ryegrass motion. Signs appear most obvious when tain only gramine and hordenine (Lolium rigidum) toxicosis in livestock is the animals are excited and resemble rye- (Duynisveld and Wittenberg 1993). Lamb a neurological disease caused by grazing grass staggers, however, a substantial mor- gains were superior on these cultivars annual ryegrass parasitized by the nema- tality is associated with annual ryegrass early in the grazing season compared to tode, Anguina agrostis (McIntosh et al. toxicosis. Convulsions and lack of coordi- ‘Frontier’ reed canarygrass, a cultivar con- 1967). The causative agents are coryne- nation has been described for cattle and taining the methoxy derivatives of the toxins (Fig. 5) produced by the bacterium, horses that had access to galls found on tryptamines and B-carbolines; however, Clavibacter toxicus, which is carried into chewing red fescue (Festuca rubra com- overall ADG was similar for the 3 culti- the seedhead by the nematode (Riley and mutata Gaud.) (Galloway 1961). Annual vars. Gramine concentration exceeded 2.0 Ophel 1992). The infected flower does not ryegrass toxicosis per se has also been mg/g during a portion of the trial in all 3 produce seed, but is replaced by a gall. reported in horses (Creeper et al. 1996). cultivars and this was assumed to be the There appears to be a requirement for the The lethal dose of corynetoxins given orally to sheep was 5 mg/kg. This total lethal dose was the same whether administered as a single dose or as repeated smaller doses with a maximum interval of 9 weeks between doses being examined (Jago and Culvenor 1987). Therefore, the toxic effect is cumulative. Corynetoxins result in extensive damage to the cerebellum via damage to the endothelial cells in capillaries (Finnie and Mukherjee 1987). Gross and microscopic pathology includes lipid deposition in the liver, diffuse hemorrhages, and perivascular edema particularly in the cerebellar meninges (Blood and Radostits 1989). Hepatic damage determined by increases in the serum concentration of 2 hepatic enzymes, aspartate amino transferase (AST) and glutamate dehydrogenase Fig. 5. Corynetoxin alkaloids found in toxic galls on annual ryegrass (Cheeke 1998). (GLDH) occurred in ewes given sublethal doses of corynetoxins (Davies et al. 1996).

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 483 There was no effect of this treatment on tion with selenum or copper have not Aldrich, C.G., J.A. Paterson, J.L. Tate, and body weight and reproduction was not given consistent results. Research with MS. Kerley. 1993a. The effects of endo- adversely affected. However, wool growth other mineral supplements is either lim- phyteÐinfected tall fescue consumption on and wool fiber diameter were reduced. ited or non-existent. diet utilization and thermal regulation in cat- Anorexia and rumen stasis has been 4. Ensiling. Limited research suggests it tle. J. Anim. Sci. 71:164Ð170. Aldrich, C.G., M.T. Rhodes, J.A. Paterson, reported in acutely affected sheep (Berry does not overcome the toxicosis. and MS. Kerley. 1989. The effects of tall et al. 1976). 5. Others. The use of thiamine supplemen- fescue endophyteÐfungus and the dopamine Some protective effect from corynetox- tation, zeranol, aluminosiliates and acti- antagonist metoclopramide on voluntary diet ins was found by dosing sheep with cobalt vated charcoal have either given nega- consumption, digestibility and body tempera- sulfate (4.0 Mg/Day-1) (Davies et al. tive results, inconsistent results or have ture in lambs. J. Anim. Sci. 67(Suppl.1):695. 1993a). Cobalt treatment prevented the not been researched. Aldrich, C.G., M.T. Rhodes, J.L. Miner, MS. rise in the serum concentration of AST Kerley, and JA. Paterson. 1993b. The and GLDH but did not prevent the sup- C. Pharmacologic compounds effects of endophyteÐinfected tall fescue con- pression of UDT in the liver. It was 1. Ivermectin. The anthelmintic appears to sumption and use of a dopamine antagonist on intake, digestibility, body temperature, thought that cobalt treatment would have some positive effect, although its and blood constituents in sheep. J. Anim. Sci. enhance the growth of microorganisms in mechanism of action and method of 71:158Ð163. the rumen that would metabolize coryne- administration has not been fully Anderton, N., PA. Cockrum, and J.A. toxins, although there was no evidence researched. Edgar. 1994. Identification of a toxin sus- presented to indicate cobalt had this effect. 2. Domperidone. It appears domperidone pected of causing sudden death in livestock Normally corynetoxins are not readily is an effective treatment for equine fes- grazing Phabaris pastures. p. 269Ð274. P.R. metabolized in the rumen (Vogel and cue toxicosis. Dorling and S.M. Colegate (eds.), McGrath 1986). PlantÐassociated toxins. Agricultural, phyto- D. Immunologic protection chemical and ecological aspects. CAB International, Wallingford, UK. 1. Although experimentation with vac- Anggard, E.E., R.M. Botting, and J.R. Vane. Management Options to cines has resulted in positive effects, 1990. EndotheliumÐderived vasoconstricting Overcome or Reduce Fescue none are commercially available. factors. p. 7Ð20. In: J.B. Warren (ed.), The Toxicosis endothelium, an introduction to current Management Options to Overcome research. Wiley Liss, New York. Balasko, JA., G.W. Evers, and R.W. Duell. Ergotism 1995. Bluegrasses, ryegrasses and bentgrass- A. Pasture and/or animal management 1. Graze intensely enough to prevent seed 1. Dilution with other forages including es. p. 357Ð370. In: R.F. Barnes, D.A. Miller, head development. and C.J. Nelson (eds.), Forages. Volume I: Bermudagrass or clovers. The major 2. Avoid grazing or consuming ergotized problem associated with dilution with An introduction to grassland agriculture. seed heads. Iowa State Univ. Press, Ames, Ia. clovers is that the potential for utilizing Ball, D.M., C.S. Hoveland, and GD. clover varies greatly among regions. Management Options to Overcome Lacefield. 1996. Southern Forages. p. Clovers are sensitive to viruses and 169Ð174. Potash and Phosphate Institute. other diseases, plus, they are compara- Perennial Ryegrass Toxicosis 1. Plant endophyte-infected lolitrem B free Atlanta, Ga. tively shallow rooted and are conse- Barragry, T. 1984. Anthelmintics: A review. quently subject to drought stress which varieties N.Z. Vet. J. 32:161Ð164. often occurs during summer months. Barragry, T.B. 1994. Veterinary drug therapy. 2. Although research is limited, it appears Management Options to Phalaris sp. p. 737Ð743. In: Lea & Febiger, Philadelphia, that increased stocking rates on E+ tall Toxicosis Penn. fescue may improve animal perfor- 1. The long-term solution is to plant low Beede, D.K. and R.J. Collier. 1986. Potential mance and production. alkaloid cultivars. nutritional strategies for intensively managed 2. The most common option utilized is to cattle during thermal stress. J. Anim. Sci. 3. Friendly endophytes. Endophyte infect- 62:543Ð554. ed cultivars, i.e., those containing non- avoid planting reed canarygrass and utilizing another cool-season perennial. Berry, P.H., R.D. Cook, J. McHoweH, R.R. toxic endophytes will be commercially White, and D.A. Purcell. 1976. Lesions in available. Limited research suggests sheep and guinea pigs pen fed parasitised they will improve animal productivity; Management Options to Annual annual ryegrass (Lobium rigidum). Aust. Vet. however, knowledge regarding stand Ryegrass Toxicosis J. 52:540Ð541. persistance is unknown. 1. First of all, it doesn’t appear to be a Blann, A.D. 1993. Is raised von Willebrand 4. Withdrawal of pregnant mares from E+ major problem in the U.S. factor a marker of endothelial cell damage? tall fescue at least 30 to 60 days prior to 2. In outbreak situations, dosing, sheep Med. Hypotheses 41:419Ð424. expected foaling date should reduce with cobalt sulfate appears to have Blood, D.C. and OM. Radostits. 1989. some benefit. Veterinary medicine: A textbook of the dis- problems assocated with foaling. eases of cattle, sheep, pigs, goats and horses. p. 1328Ð1329. 7th edition. Bailliere Tindall, B. Feed treatment and/or dietary additives Philadelphia, Penn. 1. Ammoniation of hay. Ammoniation of Boling, J.A. 1985. Endophytic fungus and tall hay has resulted in consistent improve- Literature Cited fescue utilization by ruminants. Prof. Anim. ment in animal performance. Sci. 1:19. 2. Energy supplementation. Supplementa- Boling, J.A., L.D. Bunting, G.M. Davenport, Aiken, G.E., D.I. Bransby, and C.A. McCall. J.L. Van der Veen, K.M. Meekins, NW. tion with concentrated feedstuffs may 1993. Growth of yearling horses compared to overcome much of the negative effects. Bradley, and R.E. Kohls. 1989. steers on highÐ and lowÐendophyte infected Physiological responses of cattle consuming 3. Mineral supplementation. Supplementa- tall fescue. J. Equine Vet. Sci. 13:26Ð28.

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JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 489 J. Range Manage. 54: 490Ð493 July 2001 Practical measures for reducing risk of alfalfa bloat in cattle

WALTER MAJAK, JOHN W. HALL AND TIM A. MCALLISTER

Authors are toxic plant biochemist, biostatistician and rumen microbiologist, Agriculture & Agri-Food Canada, Range Research Unit, Kamloops, B.C. V2B 8A9; Research Centre, Summerland, B.C. VOH 1ZO; and Research Centre, Lethbridge, AB. T1J 4B1.

Abstract Resumen

Frothy bloat in cattle is a serious problem and is difficult to El timpanismo espumoso es un problema serio en ganado y es manage under field conditions as it progresses rapidly from early difícil de manejar bajo las condiciones de campo conforme pro- signs of distension to acute distress. Scientists at Agriculture and gresa rápidamente de los signos iniciales de distensión aguda. Agri-Food Canada centres in Western Canada are committed to Científicos en los centros Agricultre and Agri-Food Canada del the development of bloat-free alfalfa grazing systems, which may oeste de Canadá estan comprometidos al desarrollo de sistemas require feed additives or supplements. As well, a new cultivar of de apacentamiento de alfalfa libres de timpanismo, los cuales alfalfa (AC Grazeland), selected for a low initial rate of digestion, pueden requerir alimentos aditivos o suplementos. También un will soon be available. In grazing trials the cultivar reduced the nuevo cultivar (AC Grazeland), seleccionado para una tasa ini- incidence of bloat by an average of 56% compared with the con- cial baja de digestión pronto estará disponible. En ensayos de trol cultivar (Beaver). Commonly accepted mineral mixes for the apacentamiento el cultivar redujo la incidencia de timpanismo prevention of bloat were tested and found ineffective but we have en promedio de 62% comparado con el cultivar control (Beaver). confirmed that poloxalene (Bloatguard¨) is 100% effective if it is Se probaron mezclas minerales comúnmente aceptadas para evi- given intraruminally at the prescribed dose. However, under tar timpanismo y se encontró que fueron inefectivas, pero hemos practical conditions, poloxalene can only be offered free choice confirmado que el Poloxeno (Bloatguard¨) es 100% efectivo si es and protection from bloat cannot be guaranteed. We have also administrado intraruminalmente a la dosis recomendada. Sin shown that the water soluble polymer, Blocare¨ 4511, when used embargo, bajo las condiciones practicas el poloxeno puede ser in the water supply is 100% effective in bloat prevention. This solo ofrecido a libre acceso y la protección contra timpanismo no product is not yet registered in North America. Other strategies puede ser garantizada. Tambiém hemos mostrado que cuando el for bloat prevention will be discussed, including the selection of polímero soluble en agua Blocare ® 4511 se utiliza en el sumin- growth stages and grazing schedules, and the reduction of risk by istro de agua es 100% efectivo para evitar el timpanismo. Este wilting alfalfa or combining it with tannin-containing forages. producto aun no es registrado en Norte América. Otras estrategias para evitar el timpanismo serán discutidas, incluyendo la selección de etapas de estados de crecimiento y calendarios de Key Words: pasture management, frothy bloat, legumes, feed apacentamiento y la reducción del riesgo mediante el marchita- additives miento de la alfalfa o combinandola con forrajes que contienen taninos. The incidence of frothy bloat in cattle increases worldwide as legume forages gain popularity in cultivated pastures and, more cal and climatic variables involved in bloat. Feed additives for the recently, in land reclamation. In North America, alfalfa control and prevention of bloat have also been tested. This paper (Medicago sativa L.) is the predominant legume forage and is will summarize research results on bloat in Western Canada with favoured for its high yield, nutritional quality and winter hardi- a view of providing practical information on pasture manage- ness. The economic benefits of alfalfa in grazing systems for cat- ment. It will also report on recent bloat trials with cattle that tle are not fully realized because of the risk of frothy bloat. This yielded further strategies for reducing the risk of alfalfa bloat. digestive disorder is difficult to manage under field conditions as it progresses rapidly and unpredictably from early signs of discomfort and distension to acute distress and pronounced swelling Materials and Methods of the left flank. The inability to expel fermentation gases and the resultant formation of a stable foam in the rumen can have fatal consequences. Each trial was conducted with 2 to 4 groups of ruminally fistu- Bloat research with ruminally fistulated cattle at Kamloops, lated Jersey steers, 7 to 10 years old. There were 3 to 5 animals B.C. and more recently at Lethbridge, AB has been designed to per group, with 4 animals per group used in most studies. Studies better understand the plant, animal and microbial factors involved were conducted either in confinement, where animals were fed in the etiology of bloat. Feeding regimens in both pens and pas- freshly harvested alfalfa cut daily at 0700 hours (58 kg head-1, tures have been developed to express bloat in cattle reliably and fresh weight), or in alfalfa pastures under grazing conditions. The reproducibly thereby permitting evaluation of chemical, biologi- alfalfa, which was irrigated, was cut with a flail-type harvester (New Holland, Crop-Chopper¨ Forage Harvester 38). Except for the stage of growth studies, the alfalfa was usually at the vegeta- Manuscript accepted 27 Nov. 00. tive to early bud stage. The average crude protein and acid deter-

490 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 gent fibre contents were 21.4 ± 0.49 and potential for grazing management through tests were conducted under confinement 29.1 ± 0.81% (n=79), respectively, on a selection of plant phenology as a method conditions. Our experience suggests that dry matter basis. Studies were conducted of bloat control. In practice, it would be unlike continuous grazing conditions, har- during the summer growing season and in essential to recognize the predominant vesting and feeding fresh herbage daily in the fall at Kamloops, B.C. (lat. 50¡ 42' N, stage of growth of the stand before turning confinement is a much more vigorous and long. 120¡ 27' W). Animals were cared for out cattle to pasture. The leaf to stem ratio reliable test of the efficacy of a treatment under the guidelines of the Canadian should also be recognized as a factor in owing to the higher incidence of bloat that Council on Animal Care. An animal was bloat throughout all stages of growth is generated (Majak et al. 1995). In a classified as bloated if it showed 1) visible (Thompson et al. 2000). An exceptional crossover experiment at Kamloops during distension of one or both flanks prior to leafy bloom stage can also cause bloat (W. 1999, more bloat (P < 0.05) occurred in removing the cannula plug and 2) release Majak, unpublished results). confinement (30 cases) than during contin- of internal pressure and ejection of a uous grazing (21 cases). stream of frothy ruminal contents after AC Grazeland As reviewed by Majak et al. (1995), plug removal. This event could occur The quest for a cultivar of alfalfa that numerous theories on the use of mineral within 1 hour of feeding in confinement or was bloat-free began over 30 years ago supplements, household detergents and within 2 hours of grazing on the pasture. when attempts were made to select an flocculants were tested for the prevention Each trial was designed as a crossover alfalfa strain with a low soluble protein of alfalfa bloat and most were found to be experiment in which animal groups were ineffective. The surfactant poloxalene content (Majak et al. 1995). Subsequently, ¨ switched after each test period to deter- extensive studies were conducted compar- (Bloat Guard ) was 100% effective if mine the effect of the treatment on all ani- ing legumes that do and those that do not given intraruminally at the prescribed dose mals on test. In these trials, the length of cause bloat in order to elucidate the chem- even under severe bloat challenge. The each test period was not specified but was ical and morphological features that distin- major difficulty is that it is expensive and determined by the total number of cases of guish the 2 types of species (Goplen et al. must be fed daily with a feed supplement, bloat observed. A single animal bloating 1993). The net result of the investigation or with a salt or mineral mix. Protection on 1 day was counted as 1 case but the suggested that an alfalfa with a lower from bloat cannot be guaranteed with animal may have distended more than potential for bloat might be produced by poloxalene or other insoluble anti-bloat once on that day. A minimum of 24 cases reducing its initial rate of digestion (IRD). agents because they are given free choice of bloat per crossover period provided rea- Selection for this trait was feasible using a and animal intake is highly variable. A sonable power for detecting treatment dif- modified nylon bag technique. The low more effective approach for administering ferences. All of the steers were susceptible IRD was mainly expressed at earlier anti-bloat agents to grazing cattle would to bloat as determined in previous trials stages of growth, when the potential for be to administer them through the water but none were chronic bloaters. Statistical bloat was highest (Goplen et al. 1993, supply. This would provide a uniform comparisons of the effects of treatments Berg et al. 1995). Low IRD selections intake and rapid dispersal of the agent took into account the daily fluctuations in were tested in grazing trials at Lethbridge throughout the rumen. Such water-soluble the bloat potential of the alfalfa, which and Kamloops. The resulting new alfalfa products are available in New Zealand and affected the susceptibility of each animal Australia but they are not registered in cultivar (AC Grazeland) reduced the inci- ¨ on test (Majak et al. 1995). A significance dence of bloat by an average of 56% com- North America. One such agent, Blocare level of 0.05 was used throughout to compared with the control cultivar Beaver 4511, was recently tested at Kamloops pare treatment effects. (Berg et al. 2000). As well, these initial under severe bloat challenge using 2 studies suggested that the severity of bloat groups of 4 steers in a crossover design. was reduced as indicated by the reduction The soluble agent was administered at Results and Discussion 0.1% in the water supply. As shown in in multiple distensions of the rumen with ¨ AC Grazeland (Majak et al. 1999). Table 1, Blocare 4511 was 100% effec- Stage of Growth The efficacy of AC Grazeland in the It has long been accepted that the proba- reduction of bloat could be further Table 1. Effect of Blocare¨ 4511 treatment on bility of legume bloat decreases with enhanced with the use of the ionophore the incidence of bloat in cattle fed alfalfa advancing stages of plant maturity. The monensin given intraruminally as a con- herbage during 1995. ¨ decrease has been mainly attributed to a trolled release capsule (Rumensin CRC ). 1 decrease in the soluble protein content of On average, a 50% reduction in bloat was Treatment ¨ the legume (Majak et al. 1995). Alfalfa obtained if the bolus was used in combina- Cross-over period Control Blocare 4511 proteins can contribute to the frothiness of tion with AC Grazeland (Hall et al. 2001). - - (Number of bloat cases) - - rumen contents (Howarth et al. 1986). The The bolus reduced bloat by 50% in earlier 29 JuneÐ23 July 24 0 effect of plant maturity on the incidence of trials with unspecified cultivars of alfalfa 27 JulyÐ5 August 24 0 2 frothy bloat in cattle was examined in at unspecified stages of growth (Merrill Total 48 0 feeding trials. Alfalfa at the vegetative, and Stobbs 1993). 1Two groups of 4 cattle were fed fresh alfalfa daily, with bud and bloom stages of growth was or without Blocare¨ 4511 in drinking water (100 ml Blocare¨ 100 litres-1 water). 2 simultaneously harvested and fed to 3 Feed Additives P<0.01. groups of cattle in a 3-way crossover In response to producers’ inquiries and experiment (Thompson et al. 2000). The demands over the last decade, we have vegetative stage yielded the highest inci- tive in the prevention of alfalfa bloat, even tested, under experimental conditions, a dence of bloat as compared with the bud under conditions of severe bloat where number of feed additives and supplements or bloom stage. The bloom stage had no many cases were designated at a rating of reputed to be effective in the prevention of cases of bloat. These results indicate the 4 on a scale of 1 to 5 (Majak et al. 1995). pasture bloat. It should be noted that these

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 491 It is generally accepted that high-molecu- Table 2. Effect of barley or molasses top dressing on the incidence of bloat in cattle fed alfalfa lar weight synthetic polymers such as herbage during 1996. poloxalene and Blocare¨ 4511 are non- 1 toxic at the recommended formulations Treatment and that they are excreted intact from the Cross-over period Control Barley Molasses ruminant digestive system. Recently the ------(Number of bloat cases) ------complete efficacy of Blocare¨ 4511 was 13Ð18 June 8 12 13 substantiated in alfalfa grazing trials at 3 20Ð24 June 9 10 14 locations in Western Canada (Stanford et 1Ð11 July 6 0 25 Total2 23 22 52 al. 2001). Clearly this product has the 1Three groups of 4 cattle were fed fresh alfalfa daily, with or without a top dressing of barley (2.72 kg head-1) or potential to protect livestock from alfalfa molasses (1.36 kg head-1). bloat and its registration in North America 2P < 0.01 (molasses). should be promoted. composed of approximately 50% glucose Alfalfa silage is virtually bloat-free owing Diet Manipulation and fructose (Harris et al. 1981) and these in part, to protein degradation by proteoly- Non-bloating legumes such as sainfoin simple invert sugars are highly fer- sis during ensilage. Wilting alfalfa for 24 (Onobrychis viciifolia Scop.) have mentable. A study was conducted in 1996 hours also produced changes in protein endogenous chemical and morphological to compare the effects of 2 supplementary configuration as evidenced by increases in features that render them digestible in the carbohydrate sources on the occurrence of the sulfhydryl and disulfide content of rumen without causing the rapid fermenta- alfalfa bloat in cattle (Table 2). More than alfalfa proteins (Makoni et al. 1993). tion and excessive gas production con- twice as many cases of bloat occurred with Studies were conducted recently to deter- ducive to foam formation. Sainfoin con- molasses supplements (P < 0.01) than with mine whether the changes in protein struc- tains high levels of condensed tannins, barley, which was not significantly differ- ture attributed to swathing and wilting polyphenolic polymers that can interact ent from the control. The energy source in could reduce the incidence of bloat in cat- with feed, microbial and plant proteins. barley is starch, which ferments at a slow- tle. It should be emphasized that swathing Unlike alfalfa, legumes that have high lev- er rate. differs from the regular harvesting of els of condensed tannins are bloat-free alfalfa for confinement studies. The latter due, in part to the protein binding capacity Swathing and Wilting yields chopped herbage using a flail-type of the endogenous tannins. In recent stud- It is clear that alfalfa leaf proteins are harvester while the former is cut once usu- ies, fresh alfalfa was fed alone or with intimately involved in the onset of bloat. ally for hay production using a swather. In sainfoin herbage (at 10 to 20% on a dry A significant decrease in the frequency of our studies, a John Deere 1209 Mower- matter basis) to determine the impact of bloat can occur if the alfalfa protein chem- Conditioner was used for swathing. sainfoin tannins on the occurrence of alfal- istry is modified through complex forma- Compared with feeding a fresh swath, fa bloat. Sainfoin supplements were also tion with tannins or during senescence. wilting a swath for 24 or 48 hours signifi- given as hay or pellets. The crossover cantly reduced (P < 0.01) the incidence of experiment utilized 2 groups of 4 steers during 1994 to 1997. Including sainfoin in Table 3. Effect of swathing and wilting alfalfa on the incidence of bloat in cattle fed alfalfa herbage the diet reduced (P < 0.001) the incidence during 1994, 1997, and 1999. of bloat by 45 to 93% in 3 of the 4 years 1 irrespective of the form in which sainfoin Treatment was supplied (McMahon et al. 1999). The Cross-over period Control Wilted 24 hours Wilted 48 hours variation in the response to sainfoin sup------(Number of bloat cases) ------plements could be partly attributed to the 1994: chemistry of sainfoin tannin polymers, 18Ð23 Aug 19 8 --- 25 AugÐ7 Sept 22 10 --- which show considerable variation with Total2 41 18 --- stage of leaf development (Koupai-Abyazani 4Ð7 Sept 19 --- 8 et al. 1993). Nevertheless, there is potential 9Ð13 Sept 8 --- 1 for reducing bloat by cultivation of pastures Total3 27 --- 9 containing mixtures of alfalfa and sainfoin or 1997: other bloat-free legumes. 5Ð16 Aug 19 8 0 In contrast to condensed tannins, which 17Ð29 Aug 14 14 0 can depress the incidence of alfalfa bloat, 30 AugÐ3 Sept 14 13 0 other feed supplements have the capacity Total4 47 35 0 to increase the risk of bloat. The escalation 1999: is usually caused by an excessive release 19Ð30 Aug 19 (81)6 --- 0 (50)7 and availability of nutrients in the rumen 31 AugÐ 5 Sept 17 (82) --- 6 (59) with a resultant burst of microbial fermen- Total5 36 --- 6 tation and gas production. Where bloat 1Two groups of 5 cattle in 1994, 3 groups of 4 in 1997, and 2 groups of 4 in 1999 were fed a fresh swath of alfalfa (WL problems are encountered and the diet 225) or a swath that was wilted 24 or 48 hours. contains rapidly fermentable feedstuffs, 2P < 0.01. 3P < 0.01. such as beet pulp or molasses, the removal 4P < 0.05 (24 hours), P < 0.01 (48 hours). of these components from the diet is often 5P < 0.01. sufficient to control bloat. Molasses is 6,7Average moisture content (%) in alfalfa herbage. 6SE = 1.2, 7SE = 8.2

492 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 alfalfa bloat in each year of the study on grass pasture would be desirable before Majak, W., J.W. Hall, and W.P. (Table 3). The reduction was greater (P < turning out cattle on alfalfa. As well, turn- McCaughey. 1995. Pasture management 0.01) if the alfalfa was wilted for 48 hours ing out onto alfalfa pasture in the after- strategies for reducing the risk of legume and in 1997 bloat was eliminated after a noon is much less likely to cause bloat bloat in cattle. J. Anim. Sci. 73:1493Ð1498. 48 hour wilt. The difference between years than turning out in the morning (Hall and Majak, W., B. Berg, T. McAllister, J.W. Hall, D. McCartney, K.-J. Cheng, and B. in the response to the 48 hour treatment Majak 1995). In summary, pasture man- Coulman. 1999. Bloat in cattle fed AC could be attributed to the swathing dates agement can be used to minimize the risk Grazeland selected for a low initial rate of of the alfalfa. In 1994, the swaths were cut of bloat and the strategies involve an digestion. Abstr. Can. J. Plant Sci. later in the season and the morning dew appreciation of the plant, animal, micro- 79:118Ð119. may have impeded wilting. A similar trend bial and environmental factors that con- McMahon, L.R., W. Majak, T.A. McAllister, was observed in 1999. The moisture contribute to frothy bloat. J.W. Hall, G.A. Jones, J.D. Popp, and K.- tent of the wilted swath was lower in the J. Cheng. 1999. Effect of sainfoin on in vitro first part of the crossover experiment digestion of fresh alfalfa and bloat in steers. when bloat was eliminated after a 48 hour Literature Cited Can. J. Anim. Sci. 79:203Ð212. Makoni, N.F., J.A. Shelford, S. Nakai, L.J. wilt (Table 3). The results for 1999 sug- Fisher, and W. Majak. 1993. gest that a 30% reduction in moisture dur- Berg, B.P., W. Majak, T.A. McAllister, J.W. Characterization of protein fractions in fresh, ing wilting may be sufficient to eliminate Hall, D. McCartney, B.E. Coulman, B.P. wilted and ensiled alfalfa. J. Dairy Sci. the risk of bloat. Grazing alfalfa pastures Goplen, S.N. Acharya, R.M. Tait, and K.- 76:1934Ð1944. that have been swathed and wilted pro- J. Cheng. 2000. Bloat in cattle grazing alfal- Merrill, J.K. and L.A. Stobbs. 1993. The vides yet another strategy for reducing the fa cultivars selected for a low initial rate of effect of the monensin controlled release cap- risk of bloat. digestion: A review. Can. J. Plant Sci. sule on the incidence and severity of bloat 80:493Ð502. and average daily gain in animals grazing Berg, B.P. , T.A. McAllister, S.N. Acharya, legumes. Abstr. J. Anim. Sci. 71 (Suppl. Climate W. Majak, J.W. Hall, R.M. Tait, and K.-J. 1):181. It is obvious that the growing conditions Cheng. 1995. Influence of maturity and cul- Stanford, K., Y. Wang, B.P. Berg, W. of the alfalfa can affect the protein content tivar of alfalfa on the initial rate of ruminal Majak, D.H. McCartney, V. Baron, and of the plant and the content of other plant digestion. Abstr. J. Anim. Sci. 73 (Suppl T.A. McAllister. 2001. Effects of alcohol constituents that may contribute to the 1):340. ethoxylate and pluronic detergents on the Goplen, B.P., R.E. Howarth, and G.L. Lees. development of pasture bloat in cattle and onset of bloat. At Kamloops, alfalfa is 1993. Selection of alfalfa for a lower initial grown under irrigation and the impact of sheep. J. Diary Sci. 84:167Ð176. rate of digestion and corresponding changes Thompson, D.J., B.M. Brooke, G.J. Garland, seasonal rainfall patterns on the incidence in epidermal and mesophyll cell wall thick- J.W. Hall, and W. Majak. 2000. Effect of of bloat cannot be assessed. Other climatic ness. Can. J. Plant Sci. 73:111Ð122. stage of growth of alfalfa on the incidence of variables were screened at Kamloops but Hall, J.W. and W. Majak. 1995. Effect of bloat in cattle. Can. J. Anim. Sci. none were found to be useful indicators or time of grazing or cutting and feeding on the 80:725Ð727. predictors of the occurrence of bloat (Hall incidence of alfalfa bloat in cattle. Can. J. et al. 1984). The commonly held opinion Anim. Sci. 75:271Ð273. that alfalfa is bloat-safe after a killing frost Hall, J.W. and W. Majak. 1991. Relationship was also refuted (Hall and Majak 1991). of weather and plant factors to alfalfa bloat in autumn. Can. J. Anim. Sci. 71:861-866. More recently in Kamloops, an atypical Hall, J.W., W. Majak, R.J. Williams, and cool, wet spring was associated with an R.E. Howarth. 1984. Effect of daily weather extremely high incidence of bloat (Hall et conditions on bloat in cattle fed fresh alfalfa. al. 2001). Can. J. Anim. Sci. 64:943-950. Hall, J.W., W. Majak, T.A. McAllister, and J.K. Merrill. 2001. Efficacy of Rumensin Feeding Regimens controlled release capsule for the control of Lastly, the feeding habits of the grazer alfalfa bloat in cattle. Can. J. Anim. Sci. (in need to be considered to further under- press). stand the etiology of alfalfa bloat. It is Harris, L.E., L.C. Kearl, and P.V. well established that feeding regimens that Fonnesbeck. 1981. A rationale for naming are continuous and uninterrupted are less feeds. Bulletin 501. Inter. Feedstuffs Inst., likely to cause bloat (Majak et al. 1995). Utah Agr. Res. Sta., Utah State Univ., Logan, The key is to promote continuous and Ut. rapid turnover of the rumen and to prevent Howarth, R.E., K.-J. Cheng, W. Majak, and J.W. Costerton. 1986. Ruminant bloat, p. distortions of the natural processes of 516Ð527. In: L.P. Milligan, W.L. Grovum, microbial fermentation that increase gas and A. Dobson (eds.), Control of digestion formation and reduce rumen bypass. and metabolism in ruminants. Prentice-Hall, When shifting from a pen to a pasture, it is Englewood Cliffs, N.J. essential to adapt cattle to a continuous Koupai-Abyazani, M.R., J. McCallum, A.D. grazing system where the intake is gradual Muir, B.A. Bohm, G.H.N. Towers, and and unimpeded. For example, a sudden M.Y. Gruber. 1993. Developmental changes change from a 6 hour grazing system to a in the composition of proanthocyanidins continuous regimen resulted in a rash of from leaves of sainfoin (Onobrychis viciifo- bloat cases during the first few days of the lia) as determined by HPLC analysis. J. Agr. Food Chem. 41:1066-1070. new system (Majak, unpublished results). A 3 day adaptation to continuous grazing

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 493 J. Range Manage. 54: 494Ð498 July 2001 Review of toxic glycosides in rangeland and pasture forages

WALTER MAJAK

Author is toxic plant biochemist, Agriculture and Agri-Food Canada Range Research Unit, Kamloops, B.C. V2B 8A9.

Abstract Resumen

Los rumiantes son un grupo diverso de mamíferos, que tanto Ruminants are a diverse group of mammals, both domestic especies domésticas como salvajes, que presentan fermentación and wild species, that exhibit microbial fermentation prior to microbiana antes de la actividad gastrointestinal. Durante el gastrointestinal activity. During the digestive process, glycosides proceso digestivo los glicosidos y otros productos naturales son and other natural products are exposed to ruminal microorgan- expuestos a los microorganismos ruminales y metabolizados isms and metabolised as substrates. Most compounds are con- como substratos. Muchos compuestos son convertidos en nutri- verted into nutrients but some become toxic metabolites. At least entes pero algunos llegan a ser metabolitos tóxicos. Al menos 10 10 types of toxic glycosides occur in forage species. Glycosides tipos de glicosidos tóxicos ocurren en las especies forrajeras. Los are characterized by the presence of one or more sugars linked to glicosidos son caracterizados por la presencia de uno o mas azú- the alcohol or thiol functions of the non-sugar portion of the mol- cares encadenados a las funciones alcohol o tiol de la porción no- ecule, which is called the aglycone. The biological activity of the azúcar de la molécula, la cual es llamada aglicone. La actividad glycoside is usually determined by the chemical nature of the biológica del glicosido usualmente es determinada por la natu- aglycone. The aglycones are released by microbial enzymes and raleza química del aglicone. Los aglicones son liberados por las may undergo further enzymatic or non-enzymatic transforma- enzimas microbianas y pueden llegar sufrir mas transformations to yield toxic metabolites that can be absorbed from the ciones enzimáticas o no-enzimáticas para producir metabolitos gastrointestinal tract. Microbial detoxification of the aglycone is tóxicos que pueden ser absorbidos del tracto gastrointestinal. La also possible. Further biotransformation of the aglycone can detoxificación microbiana del aglicone también es posible. Mas occur in the liver. A review is presented on glycosides that are biotransformaciones del aglicone pueden ocurrir en el hígado. Se toxic to ruminants. The discussion covers aliphatic nitrocom- presenta una revisión de los glicosidos que son tóxicos para los pounds, cyanogenic glycosides, cardiac glycosides, saponins, glu- rumiantes. La discusión cubre compuestos nitrogenados alifáti- cosinolates, diterpenoid glycosides, bracken glycosides, calcino- co, glicosidos cianogénicos, glicosidos cardíacos, saponinas, glu- gens, phenolic glycosides and ranunculin. Clinical signs of poi- cosinolatos, glicosidos diterpenoides, calcinógenos, glicosidos soning and treatment of livestock as well as management strate- fenólicos y ranuculina. Se consideran los signos clínicos de enve- gies for the prevention of poisoning are considered. nenamiento y tratamiento del ganado, así como las estrategias de manejo para la prevención del envenenamiento. Key Words: poisonous plants, ruminants, cattle, rumen microbes Glycosides are conjugated alcohols formed when the alcoholic A diverse array of toxic glycosides occurs in higher plants, the function of the aglycone adds to a sugar such as D-glucose. The most abundant of these being the glucosinolates (thioglycosides), biological activity of the glycosides is usually determined by the the cyanogenic glycosides, the aliphatic nitrotoxins, and the car- chemical nature of the aglycone, which is the non-sugar portion diac glycosides. Glycosides are secondary plant products, many of the molecule. Glycosides most commonly occur as O-§-D-glu- of which are recognized as active metabolites or allelochemicals that interact with other plants, microorganisms, insects, and ani- cosides. The glycosidic bond renders the glycosides innocuous mals. The roles of these compounds include the attraction of pol- through stabilization of the reactive aglycone (Majak and Benn linators or seed dispersers and the repulsion or inhibition of her- 2000). In ruminants, an important feature of the digestive system bivores and microorganisms (Rhoades 1979). Concentrations of is the occurrence of microbial fermentation in the rumen prior to toxic glycosides in plants can be affected significantly by physio- gastrointestinal activity. About 50% of rumen bacteria possess logical stress, such as water deficits or nutrient deficiencies. §-glucosidase activity and the hydrolytic enzyme is also widely Other factors that may affect glycoside levels include stage of distributed among species of rumen ciliate protozoa and anaero- growth, accumulation in specific plant tissues, geographic or bic fungi (Chesson and Forsberg 1988). Hydrolysis of the glyco- topographic location, and seasonal effects of soil and climate. sidic bond is essential for the toxic expression of cyanogenic gly- This review will focus on the distribution of toxic glycosides in cosides as well as aliphatic nitrotoxins such as miserotoxin. In forage species and their mode of action in ruminants. monogastric animals the upper regions of the digestive tract are Management strategies for the prevention and treatment of poi- largely devoid of §-glucosidase activity; §-D-glucosides are not soning are also considered. usually hydrolysed but are absorbed and excreted intact in the urine. Chemical inhibitors of §-glucosidase are known. These The author wishes to thank Ruth McDiarmid for her contributions in the prepa- inhibitory compounds, both naturally-occurrring and synthetic, ration of this manuscript. are structural analogues of glucose that bind tightly to the active Manuscript accepted 27 Nov. 00.

494 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 site of the enzyme; however, if absorbed causative agent of neuronal degeneration been attributed to the slower release of from the rumen they can be toxic to live- in mammals (Alexi et al. 1998). HCN from the glycoside. The delayed stock (Nash et al. 1998). The major clinical signs in the acute release of HCN permits a greater degree of Glucosinolates are S-§-D-glucosides syndrome include incoordination, distress, detoxification through thiocyanate forma- and thus not substrates for O-§-D-glucosi- labored breathing, cyanosis, muscular tion. Clinical signs of subacute and acute dase. Both ovine and bovine rumen fluids weakness, and collapse, with death occur- poisoning in cattle resulting from adminis- are devoid of myrosinase, the hydrolytic ring from a few hours to a day after inges- tration of prunasin include tachycardia, enzyme that releases the thiol aglycone tion of the toxin. In chronic poisoning, the hyperpnea, recumbency, increased pink- (Majak 1992); however, glucosinolate- animals lose weight and develop respirato- ness of the mucous membranes, and tonic containing plants all contain myrosinase. ry distress, a poor hair coat, hind limb convulsive contractions (Majak et al. Thus the hydrolysis of glucosinolates in paresis progressing to paralysis, and a 1980). The classic nitrite-thiosulfate treat- the rumen is contingent upon the activity nasal discharge. Early signs of poisoning ment is still the preferred therapeutic of endogenous plant enzymes (Majak in cattle under field conditions include method, especially if it is supplemented 1992, Majak et al. 1991). The thiol agly- frothy salivation, stupefaction, diarrhea with oxygen (Majak et al. 1980, Way cone is unstable at physiologic pH and and labored breathing (Majak and Pass 1984). undergoes a non-enzymatic rearrangement 1989, Maricle et al. 1996). When forced to The distribution of cyanogenic glyco- to form isothiocyanates. move as part of a group they exhibit signs sides in the plant kingdom has been exten- Hydrolysis of the glycosidic bond is not of incoordination and will lag behind. sively reviewed (Poulton 1983). The a prerequisite for the biological activity of Recent field observations do not support Leguminosae (Trifolium spp.), Rosaceae polycyclic glycosides such as glycoalka- the concept of livestock addiction to (Prunus spp. and Amelanchier spp.), and loids, saponins, and cardenolides. In fact, NPOH-containing plants (Majak et al. Juncaginaceae (Triglochin spp.) have been removal of the sugar units results in 1996). No specific antidote is available for particularly rich sources where the glyco- reduced activity with saponins and carde- the treatment of livestock poisoned with sides occur in white clover, wild cherry, nolides, and loss of activity with glycoal- aliphatic nitrotoxins but dietary protein serviceberry and arrowgrass, respectively. kaloids (Majak and Benn 2000). supplements can enhance the activity of unique rumen bacteria capable of NPOH Cardiac glycosides Nitrocompounds detoxification (Majak et al. 1996). These As a consequence of their powerful Relatively few natural products contain bacteria reduce the nitro group to the effect on the heart, preparations containing the nitro group, but of those that do, 2 much less toxic amino group (Anderson et cardiac glycosides have a long history as important sets correspond to sugar conju- al. 1998). medicinals and poisons. Probably most gates of 3-nitropropanol (NPOH) and 3- famous in the Western world is the intro- nitropropionic acid (NPA). Although the Cyanogenic glycosides duction of digitalis, an extract of Digitalis latter are not glycosides, they often resem- In plants, cyanogenesis or the release of purpurea L. (foxglove), for the treatment ble them structurally and their mammalian HCN is associated with the disruption of of heart disease, but similar usage of Scilla toxicities are similar; it is for these reasons cells followed by autolysis as the glyco- maritima L. (squill; sea onion) dates back that they receive attention here (Majak and sides are exposed to endogenous plant to ancient civilizations. Cardiac glycosides Pass 1989). The toxin karakin [1,2,6-tris- enzymes. The resulting aglycones are are characterized by a steroidal aglycone O-(3-nitropropanoyl)-§-D-glucopyranose] unstable cyanohydrins. At physiologic pH which is 1 of 2 structural types: cardeno- was the first nitrocompound to be isolated. they undergo a rapid dissociation to yield lides, such as digitalin, or bufadienolides The identification of miserotoxin (3-nitro- HCN and either an aldehyde (e.g.ben- such as scilleroside. Both cardenolides and propyl-§-D-glucopyranoside) followed the zaldehyde in the case of prunasin) or a bufadienolides are plant products, com- observation that Astragalus miser var. ketone (e.g. acetone, in the case of lina- mon particularly in the Asclepiadaceae oblongifolius (Rydb.) Cronq. was respon- marin). The dissociation is a pH-depen- (milkweeds), Apocynaceae, and Liliaceae. sible for losses of stock on rangelands of dent reaction with higher rates of HCN Dogbane (Apocynum cannabinum L.) con- the western United States. Glucose esters formation occurring at a pH greater than 6 tains high concentrations of the cardeno- of NPA such as karakin are found in the and much slower rates at pH 5-6. Cattle lide cymarin (0.1% on a dry wt basis, W. Leguminosae (Astragalus, Coronilla, should be least susceptible to poisoning Majak unpublished results). Bufadienolides Indigofera, and Lotus) and miserotoxin during feeding and digestion when the pH are also associated with the poison glands occurs in numerous species of Astragalus of rumen fluid is depressed and most sus- of toads (Joubert 1989, Majak and Benn (milkvetch). It has become well estab- ceptible after a 24 hour fast (Majak et al. 2000). lished that NPA is the lethal metabolite 1990). It is generally accepted that the Na+- formed in the biotransformation of nitro- The HCN is extremely toxic because it K+-adenosinetriphosphatase in cardiac propyl glycosides or nitropropanoyl glu- blocks aerobic cellular respiration. The muscle is the major pharmacological cose esters. The esters yield NPA directly toxic effect is mainly attributed to inhibi- receptor of cardiac glycosides. Inhibition upon hydrolysis, but the bioactivation of tion of cytochrome oxidase but other by cardenolides such as ouabain and digi- the glycosides requires a second metabolic metabolic processes may also be affected. toxin affects intracellular electrolyte con- step; after hydrolytic release of the agly- Physiologically, HCN poisoning results in centrations, resulting in more forceful con- cone, NPOH is oxidized to NPA, probably histotoxic anoxia with the initial manifes- tractions of the myocardium. Therapeutic by liver alcohol dehydrogenase (Majak tation of hyperpnea, followed by dyspnea, at medicinal doses for the treatment of and Pass 1989). The NPA is a potent and then convulsive seizures. Clinical congestive heart failure in humans, they inhibitor of Krebs (tricarboxylic acid) signs of poisoning with cyanogenic glyco- are toxic to domestic herbivores when cycle enzymes essential to respiration and, sides develop at a much slower rate than consumed at the natural concentrations in more recently it has been implicated as a they do for sodium cyanide, which has plants. Sub-acute to acute signs of poison-

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 495 ing in cattle and sheep include restless- Glucosinolates erated anaerobic glycolysis, lactate pro- ness, dyspnea, ruminal atony, frequent uri- The glucosinolates, precursors of organic duction, and glycogenolysis. Clinical signs nation and defecation, tachycardia, isothiocyanates (mustard oils) are mainly of poisoning in livestock include acute arrhythmia, and ventricular fibrillation. constituents of members of the depression, weakness, and convulsions, The closely related bufadienolides pro- Brassicaceae (Cruciferae), but they are also and the accompanying pathologic changes duced similar signs of poisoning in cattle. found in other smaller tropical families. include nephrosis, gastric irritation, hepat- All cardiac glycosides may be regarded as Some glucosinolate breakdown products ic necrosis, and marked hypoglycemia highly toxic (Joubert 1989, Majak and are goitrogenic agents that cause hyperpla- (Cole et al. 1989). A current and compre- Benn 2000). sia and hypertrophy of the thyroid gland. hensive review on the biochemistry and Various treatments for cardiac glycoside Two types of goitrogens are derived from toxicology of atractylosides is available poisoning in humans and livestock have glucosinolates, which act on the thyroid (Obatomi and Bach 1998). been reviewed (Joubert 1989); these gland in different ways. The thiocyanate include the use of activated charcoal, ion, the less potent of the 2, is derived from Bracken glycosides potassium chloride, atropine, digoxin-spe- the breakdown of alkyl isothiocyanates or Poisoning of cattle by bracken (species cific antibodies, §-adrenergic blocking indole isothiocyanates. It inhibits uptake of of the fern Pteridium) had been suspected agents, procainamide and phenytoin. inorganic iodide by the thyroid gland, for many years, but the first report of apparently in a competitive way since the lesions in experimental animals on a diet Saponins inhibition can be reversed with iodide sup- including bracken did not appear until Saponins are glycosidic conjugates of plements. The cyclic thiouracils, such as 1965, when rats were found to develop triterpenes. The name derives from their goitrin, are derived from the hydrolysis of cancers. Another 18 years passed before soap like property of forming stable foams glucosinolates containing a §-hydroxyl the carcinogenic agent was isolated and when shaken in dilute aqueous solutions. substituent. Goitrin and other thiouracil identified as the sesquiterpene glycoside They are also noted for their ability to analogues interfere with tyrosine iodina- ptaquiloside. Ptaquiloside and several ana- hemolyse red blood cells, even at high tion and the coupling reactions that sythe- logues have since been isolated from other dilution. Historically, Medicago sativa L. size thyroxine or triiodothyronine, and ferns. The prominent feature of “bracken (alfalfa) and Dioscorea species (yams) their effects cannot be reversed. poisoning” in cattle is depressed bone have been recognized as rich in saponins Antithyroid drugs are available for the marrow activity that results in leukopenia, but they are widely distributed throughout treatment of hyperthyroidism; these thrombocytopenia, and hemorrhages of the the plant kingdom, to the point that they include methimazole, propylthiouracil, and urinary bladder that give rise to hematuria. appear to be ubiquitous. In spite of their such other antithyroid drugs as the sulfon- Ptaquiloside is apparently transferred to wide distribution, only a small number of amides, amphenone, and chlorpromazine cows’ milk, and could pose a human species contain saponins that are toxic to (Fenwick et al. 1989). health hazard (Hirono 1986, 1989). mammals (Cheeke 1998). This has been Ingestion of mustard (Brassica spp.) Bracken also contains the enzyme thiami- attributed to their negligible degree of seeds by cattle and the release of mustard nase, which can induce polioencephaloma- absorption from the gastrointestinal tract. oils can result in lesions in the gastroin- lacia in monogastric animals and rumi- There appears to be a growing list of testinal tract including profuse edema of nants (Chick et al. 1989, Cheeke 1998). saponin-containing forages that are impli- the forestomachs and abomasum and mucosal necrosis and hemorrhage of the cated in hepatogenous photosensitization Calcinogenic glycosides of livestock, with sapogenins being detect- cecum and colon. In addition to the isoth- Pathological calcinogenesis, calcinosis, ed as crystals in obstructed bile ducts iocyanates, episulfides, thiocyanates and refers to the deposition of calcium salts in (Cheeke 1998). nitriles also are produced during autolysis soft tissues. A causative link between the The toxic saponin effect is usually initi- of glucosinolates. Allylthiocyanate is ingestion of Solanum glaucophyllum ated by interaction with mucosal mem- formed during stinkweed (Thlaspi arvense Desf. (S. malacoxylon Sm.) and the inci- branes, causing permeability changes or L.) autolysis, and the irritant oil may cause dence of a calcinotic disease of livestock loss of membrane-bound enzymes severe gastric distress. Nitriles having in Argentina and Brazil was suspected for (Oakenfull and Sidhu 1989). Lysis of the pancreatotoxic and nephrotoxic effects can some time, as it was for Cestrum diurnum mucosal cell membranes results in intesti- be generated during the autolysis of L. in Florida and Trisetum flavescens (L.) nal lesions and severe gastroenteritis. Brassica species and other crucifers Beauv. in the European alps. An isolation Under these conditions, saponins may be (Majak 1992, Majak and Benn 2000). absorbed from the gastrointestinal tract of the biologically active fraction from S. and produce systemic effects such as liver glaucophyllum, treated with §-glucosidase, Diterpenoid glycosides released calcitriol (1α, 25-dihydroxy vita- damage, respiratory failure, violent con- The 1970-1980 decade saw the isolation min D3). Subsequently, vitamin D3 and its vulsions, and coma. The ability of and characterization of hypoglycemic α saponins to disrupt and lyse cell mem- 25-hydroxy and 1 ,24,25-trihydroxy agents from species of the Compositae derivatives were also found. The calcino- branes enhances their activity when given such as Atractylis, Xanthium (cocklebur), intravenously. Saponins are also anti- genic glycosides of C. diurnum and T. and Wedelia. The toxic diterpenoid glyco- flavescens also proved to be derivatives of nutritional factors in swine and poultry sides from these sources were respective- vitamin D3 (Weissenberg 1989, Majak feeds such as alfalfa (Cheeke 1998). The ly named atractyloside, carboxyatractylo- adverse effects of saponins have been and Benn 2000). side, and wedeloside. These glycosides reversed by the inclusion of dietary cho- Dietary or endogenous vitamin D3 is can block the mitochondrial ADP/ATP lesterol, presumably because saponins hydroxylated at C25 and stored in the energy-carrier system and the resultant form insoluble complexes with cholesterol liver. It is activated further in the kidney cellular dysfunction is characterized by or they perturb cholesterol-containing by hydroxylation at C1. This active form inhibited oxidative phosphorylation, accel- micelles (Oakenfull and Sidhu 1989). is required for the synthesis of calcium

496 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 carrier proteins involved in the transport successful under experimental and field Cycasin of the cation from the intestine under con- conditions (Adams 1989). Two distinct field diseases have been ditions of calcium deprivation. It is this Melilotoside, coumarinic acid §-D-gluco- recognized in livestock poisoning by dihydroxylated active form of vitamin D3 side, is the bound form of coumarin that cycads and zamias. One is a neurotoxic that occurs in glycosidic forms in Solanum can be found in high concentrations in syndrome characterized by ataxia and per- glaucophyllum and Cestrum diurnum. sweet clover (Melilotus spp.). Sweet clover manent weakness of the hindquarters. A Consequently, consumption of this exoge- poisoning is associated with moldy hay or rare amino acid was implicated but others nous form of vitamin D3 results in excess silage where enzymes of fungal origin have excluded this agent (Charlton et al. absorption of calcium and phosphate from metabolize coumarin to dicoumarol, a 1992). The second syndrome is a hepatic the intestine leading to calcification of soft potent anticoagulant. Dicoumarol interferes and gastrointestinal disease attributed to tissues. Symptoms of calcinogenesis in with the synthesis of thrombin, which is cycasin, methylazoxymethanol-§-D-glu- both livestock and laboratory animals have required for fibrin formation and blood coside (Hooper 1983). Acute cycasin toxi- been reviewed comprehensively clotting. Signs of poisoning in cattle city in sheep and cattle is characterized by (Weissenberg 1989). include lethargy, anemia, and the develop- hepatitis, gastroenteritis, hemorrhages, and ment of subdermal swelling in reponse to liver cirrhosis. In chronic poisoning, ani- Phenolic glycosides internal hemorrhaging, which is the cause mals lose appetite and develop mild liver A very large number of phenolic glyco- of death (Kingsbury 1964). The induced cirrhosis and nephrosis. The labile agly- sides have been isolated from plants, and deficiency can be ameliorated with cone is the lethal metabolite. their aglycones exhibit considerable struc- increased vitamin K, especially vitamin K1 In summary, 11 classes of toxic glyco- tural diversity and biological activity. given intramuscularly (Alstad et al. 1985). sides have been examined in this review. There is evidence to suggest that the phe- “Low coumarin” cultivars of sweet clover Bioactivation and toxicity of the glyco- nolic glycosides of plants provide a are available but “high coumarin” Melilotus sides mainly depend on 1) the rate of defense against herbivorous insects but persists in pastures and as a weed. release of the aglycone by rumen only a few are regarded as dangerously microbes, 2) the rate of detoxification of toxic to mammals. In most cases, the toxic Ranunculin the aglycone, and 3) the degree of absorp- agents have been identified as the phenolic The recognition that chewing the fresh tion of the aglycone from the gastrointesti- aglycones. Classic examples include the leaves or blossoms of buttercups released nal tract. Plant enzymes may also be isoflavonoid daidzein and formononetin, a vesicant substance must be prehistoric. involved in the mode of action of toxic found in subterranean clover (Trifolium The toxin has been identified as the unsat- glycosides. Clearly, these results indicate subterraneum L.), and coumestrol, which urated ϒ-lactone protoanemonin (5-meth- that the rumen ecosystem is the first line occurs in alfalfa (Medicago sativa L.). ylene-2-oxodihydrofuran), but the storage of defense and it should be further exploit- Both of these phytoestrogens induce abor- form of this unstable compound remained ed for pathways of detoxification. tions in sheep. Reproductive problems in doubt until recently when the parent §- were first encountered over 50 years ago D-glucoside was re-isolated by different with the establishment of subterranean extraction protocols and identified as Literature Cited clover on pastures in western Australia. A ranunculin (Bai et al. 1996). Ingestion of dramatic decrease in the fertility of sheep the plant material can cause gastric dis- Adams, N.R. 1989. Phytoestrogens, p. 23Ð51. was noted. The failure to conceive was tress, including irritation of the digestive In: P.R. Cheeke (ed.) Toxicants of Plant attributed to a change in the viscosity of tract, abdominal pain, and diarrhea. When Origin, Vol. IV, Phenolics. CRC Press Inc., the cervical mucus and the resultant Ceratocephalus testiculatus Crantz. (bur Boca Raton, Fla. impaired passage of spermatozoa. The buttercup) was given to sheep, clinical Alexi, A., P.E. Hughes, R.L.M. Faull, and condition was accompanied by cystic signs of poisoning included weakness, C.E. Williams. 1998. 3-Nitropropionic acid’s lethal triplet: cooperative pathways of glandular hyperplasia of the cervix and depression, tachycardia, dyspnea, anorex- neurodegeneration. NeuroReport 9:57Ð64. uterus and lactation in nonpregnant ewes ia, diarrhea, and sometimes fever (Olsen et Alstad, A.D., H.H. Caspar, and L.J. and wethers. Clinical signs of reproduc- al. 1983). Ranunculin has been obtained Johnson. 1985. Vitamin K treatment of tive disorders diminished with the intro- from numerous species of the buttercup sweet clover poisoning in calves. J. Amer. duction of new cultivars of clover that family (Ranunculaceae) (Bai et al. 1996). Vet. Med. Assoc. 187:729Ð731. were low in formononetin, but a tempo- The purified glycoside is a substrate for §- Anderson, R.C., W. Majak, M.A. Rasmussen rary infertility still prevailed among ewes glucosidase which can release the agly- and M.J. Allison. 1998. Detoxification potential of a new species of ruminal bacteria exposed to phytoestrogen-containing pas- cone; however, during the autolysis of that metabolize nitrate and naturally occur- tures. Reproductive disorders on alfalfa ranunculin-containing forages, pro- ring nitrotoxins, p. 154Ð158. In: Tam pastures usually are associated with toanemonin is released and not the agly- Garland and A. Catherine Barr (eds.), Toxic increases in coumestrol concentrations cone. Two competing reactions occurred plants and other natural toxicants. CAB resulting from fungal infections, often in rumen fluid when Ranunculus cym- International. referred to as a phytoalexin response. balaria Pursh. was incubated in vitro: Bai, Y., M.H. Benn, W. Majak, and R. Coumestrol and related coumestans microbial hydrolases yielded the aglycone McDiarmid. 1996. Extraction and HPLC decrease the ovulation rate in ewes. There and the endogenous plant enzyme yielded determination of ranunculin in species of the buttercup family. J. Agr. Food Chem. is no satisfactory explanation for the protoanemonin (Majak et al., unpublished 44:2235Ð2238. reduced susceptibility of cattle as com- data). This is another example where the Charlton, T.S., A.M. Marini, S.P. Markey, pared to sheep to the effects of phytoestro- release of the toxic metabolite, pro- K. Norstog, and M.W. Duncan. 1992. gen-containing pastures. Immunological toanemonin, is contingent upon the specif- Quantification of the neurotoxin approaches for the prevention of phytoe- ic activity of endogenous plant enzyme. 2ÐaminoÐ3Ð(methylamino)Ðpropanoic acid strogenic disorders have been partially (BMAA) in Cycadales. Phytochemistry 31:3429Ð3432.

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 497 Cheeke, Peter R. 1998. Natural toxicants in Kingsbury, J.M. 1964. Poisonous plants of the Nash, R.J., A.A. Watson, A.L. Winters, feeds, forages, and poisonous plants. Second United States and Canada. Prentice Hall Inc., G.W.J. Fleet, M.R. Wormald, S. Dealler, Edition. Interstate Publishers Inc., Danville, Englewood Cliffs, N.J. E. Lees, N. Asano, and R.J. Molyneux. Ill. Majak, W. 1992. Biotransformation of toxic 1998. Glycosidase inhibitors in British plants Chesson, A. and C.W. Forsberg. 1988. glycosides by ruminal microorganisms, p. as causes of livestock disorders, p. 276Ð284. Polysaccharide degradation by rumen 86Ð103. In: R.F. Keeler, N.B. Mandava, and In: Tam Garland and A. Catherine Barr microorganisms, p. 251Ð284. In: P.N. A.T. Tu (eds.), Natural toxins: toxicology, (eds.), Toxic plants and other natural toxi- Hobson (ed.), The rumen microbial ecosys- chemistry and safety. Alaken Inc., Fort cants. CAB International. tem. Elsevier Appl. Sci., London and New Collins, Colo. Oakenfull, D. and G.S. Sidhu. 1989. York. Majak, W. and M.H. Benn. 2000. Glycosides, Saponins, p. 97Ð142. In: P.R. Cheeke (ed.), Chick, B.F., B.V. McCleary, and R.J. p. 299Ð349. In: Y.H. Hui, R.A. Smith, D.G. Toxicants of plant origin, Vol. II, Glycosides. Becket. 1989. Thiaminases, p. 73Ð91. In: Spoerke (eds.), Foodborne disease handbook, CRC Press Inc., Boca Raton, Fla. P.R. Cheeke (ed.), Toxicants of plant origin, Vol. 3, Plant Toxicants. Marcel Dekker Inc., Obatomi, D.K. and P.H. Bach. 1998. Vol. III, Proteins and amino acids. CRC New York, N.Y. Biochemistry and toxicology of the diter- Press, Inc., Boca Raton, Fla. Majak, W. and M.A. Pass, 1989. Aliphatic penoid glycoside atractyloside. Food Chem. Cole, R.J., H.G. Cutler, and B.P. Stuart. nitrocompounds, p. 143Ð159. In: P.R. Toxicol. 36:335Ð346. 1989. Carboxyatractyloside, p. 253Ð263. In: Cheeke (ed.), Toxicants of plant origin, Vol. Olsen, J.D., T.E. Anderson, J.C. Murphy P.R. Cheeke (ed.), Toxicants of plant origin, II, Glycosides. CRC Press Inc., Boca Raton, and G. Madsen. 1983. Bur buttercup poi- Vol. II, Glycosides. CRC Press Inc., Boca Fla. soning of sheep. J. Amer. Vet. Med. Assoc. Raton, Fla. Majak, W., R.E. McDiarmid, M.H. Benn, 183:538Ð543. Fenwick, G.R., R.K. Heaney, and R. and W.D. Willms. 1991. Autolysis of Poulton, J.E. 1983. Cyanogenic compounds in Mawson. 1989. Glucosinolates, p. 1Ð41. In: Thlaspi arvense in bovine rumen fluid. plants and their toxic effects, p. 117Ð157. In: P.R. Cheeke (ed.), Toxicants of plant origin, Phytochemistry 30:127Ð129. Richard F. Keeler and Anthony T. Tu (eds.), Vol. II, Glycosides. CRC Press Inc., Boca Majak, W., R.E. McDiarmid, J.W. Hall, and Handbook of natural toxins, Vol. 1, Plant and Raton, Fla. K.ÐJ. Cheng. 1990. Factors that determine fungal toxins. Marcel Dekker Inc., New Hirono, I. 1986. Carcinogenic principles iso- rates of cyanogenesis in bovine ruminal fluid York, N.Y. lated from bracken fern. CRC Crit. Rev. in vitro. J. Anim. Sci. 68:1648Ð1655. Rhoades, D.F. 1979. Evolution of plant chem- Toxicol. 17:1Ð22. Majak, W., T. Udenberg, L.J. Clark, and A. ical defense against herbivores, p. 3Ð54. In: Hirono, I. 1989. Carcinogenic bracken glyco- McLean. 1980. Toxicity of saskatoon ser- Gerald A. Rosenthal and Daniel H. Janzen sides, p. 239Ð251. In: P.R. Cheeke (ed.), viceberry to cattle. Can. Vet. J. 21:74Ð76. (eds.), Herbivores, Their interaction with sec- Toxicants of Plant Origin, Vol. II, Majak, W., L. Stroesser, J.W. Hall, D.A. ondary plant metabolites. Academic Press, Glycosides. CRC Press Inc., Boca Raton, Quinton, and H.E. Douwes. 1996. Seasonal New York, N.Y. Fla. grazing of Columbia milkvetch by cattle on Way, J.L. 1984. Cyanide intoxication and its Hooper, P.T. 1983. Cycad poisoning, p. rangelands in British Columbia. J. Range mechanism of antagonism. Ann. Rev. 463Ð471. In: R.F. Keeler and A.T. Tu (eds.), Manage. 49:223Ð227. Pharmacol. Toxicol. 24:451Ð481. Handbook of natural toxins, Vol. I, Plant and Maricle, B., J. Tobey, W. Majak, and J.W. Weissenberg, M. 1989. Calcinogenic glyco- fungal toxins. Marcel Dekker Inc., New Hall. 1996. Evaluation of clinicopathological sides, p. 201Ð238. In: P.R. Cheeke (ed.), York, N.Y. parameters in cattle grazing timber Toxicants of plant origin, Vol. II, Glycosides. Joubert, J.P.J. 1989. Cardiac glycosides, p. milkvetch. Can. Vet. J. 37:153Ð156. CRC Press Inc., Boca Raton, Fla. 61Ð69. In: P.R. Cheeke (ed.), Toxicants of plant origin, Vol. II, Glycosides. CRC Press Inc., Boca Raton, Fla.

498 JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 Book Review

The New Ranch Handbook: A Guide to Restoring tion by manipulating access to water. They purchase all Western Rangelands. By Nathan F. Sayre. Edited by replacement heifers and run yearling stockers in years of high Barbara H. Johnson. 2001. The Quivira Coalition, 551 forage production to keep stocking rates conservative and Cordova Road, #423, Santa Fe, New Mexico 87501, USA. very flexible (600Ð1,400 head). Recreation management is 102 + x p. US$10.00 (+ 3.00 S&H) paper. ISBN 0-9708264- replacing grazing management as the most difficult planning 0-0. issue. Western cattle producers are in chronic economic trouble Roger Bowe (San Jon, N.M.) switched from continuous and some extreme environmentalists are demanding total grazing to SDG in response to poor distribution and slowly removal of livestock from arid and semiarid public range- declining production. With an intensive, 62-pasture rotation, lands. Yet there are many examples where ranchers, range distribution has improved and stocking rate has more than managers, and conservationists are working together to pro- doubled. Bowe reports that less labor is required, variable cost duce livestock while simultaneously sustaining and restoring per lb of beef has decreased by > 50%, and net annual income rangelands and rural communities. per acre has tripled. Unfortunately the analysis does not The Quivira Coalition (http://www.quiviracoalition.org) is a include the sunk cost of the initial capital improvements. New Mexico based organization of producers, agency range Bowe also employs a monitoring system tailored to his opera- managers and environmentalists dedicated to promoting sus- tion. No information on cattle herd management is provided. tainable ranching and “sharing common-sense solutions to the Jim Winder also practices management-intensive SDG, on rangeland conflict.” They call this stance the “New Ranch.” semiarid desert grassland near Nutt, N.M. With 66 pastures Their first major publication, The New Ranch Handbook by divided by electric fences, and moving his herd every one to Nathan Sayre, is intended to describe the management prac- three days during the growing season, Winder has doubled his tices that have improved economic and ecological sustainabil- stocking rate to well over the official carrying capacity. He is ity in the Southwest, to place these in a scientific framework, able to stock flexibly with a cow-calf-yearling operation; on and in so doing to offer a common vocabulary for, and average he maintains a herd of 60% mother cows and 40% increase awareness of the complexity of, sustainable grazing stockers. Both the range (especially the riparian areas, which management. are grazed mostly in the winter and only for short periods) and The book is organized around 6 concise case studies of the cattle are in substantially better condition than they were innovative cattle producers, each followed by chapters outlin- prior to implementing planned, controlled grazing. Winder ing the basic ecological processes which sustain the range plans for drought every year by making stocking decisions at livestock operation. Although Sayre states that half of the the beginning of the dormant season and throughout the year, ranchers use short-duration grazing (SDG) and half use rest- rather than at the beginning of the growing season. rotation grazing, it is clear from the text that none uses rest- Jim Williams (Quemado, N.M.) recently implemented rotation as developed by Gus Hormay; all 6 use some form of planned rotational grazing and monitoring on his Cibola intensive rotational grazing during the growing season, with National Forest allotment, such that every pasture receives 90 longer grazing periods in the dormant season. days of rest during the growing season. Conditions have Sid Goodloe, the first holistic range manager in the U.S., improved dramatically, especially along the Largo Creek has doubled the carrying capacity of his ranch near Capitan, riparian corridor. Relations with the Forest Service have also N. M., through a combination of chaining junipers, prescribed improved, and Williams is hopeful that a 1995 stocking rate burning, and SDG in the growing season. He stocks his ranch reduction will be restored. No information on herd manage- conservatively (slightly less than the official carrying capaci- ment is provided. ty) with moderate size “Alpine Black” (3/4 Black Angus and Chapter 1, “Ranching as Sustainable Agriculture,” explains 1/4 Brown Swiss) cattle. The breeding season is matched to that grazing is a disturbance and that rangelands must be peak forage conditions, and weaning is timed to occur before resilient to disturbance if grazing is to be sustainable. The dis- the first frost reduces the nutritional quality of the forage. cussion on disturbance stops just short of internalizing the David Ogilvie (Silver City and Gila, N.M.) uses a combina- idea in the larger concept of the ecosystem. Rangeland tion of SDG and high intensity-low frequency grazing tactics ecosystems are highly variable, and exhibit nonlinear dynam- during the growing season, such that each of his 18 pastures ics and qualitative differences across scales; thus the linear receives nearly yearlong rest and goes to seed every year. He tools of historic range management (estimates of carrying has also implemented a small-scale burning program to con- capacity, utilization, and range condition) are inadequate for trol piñon-juniper encroachment into grasslands. The U Bar large-scale management because they assume that the whole Ranch now boasts the largest concentration of endangered is simply the sum of the parts. Sayre suggests that a new view Southwestern willow flycatchers in the U.S. No information of grazing that focuses not simply on condition and trend but on stocking rates or cattle herd management is provided. on the basic ecological processes underlying plant and animal John and Mac Donaldson manage the Empire Ranch, most production is necessary to avoid problems of scale. of which is on the BLM’s Empire-Cienega National Chapter 2 examines “Grazing as a Natural Process” to Conservation Area near Sonoita, Ariz. They practice flexible which forage plants and herbivores have adapted. In a short rotational grazing with long rest periods, and control distribu- discussion of the debate over compensatory growth in response to grazing, Sayre concludes that compensation is more

JOURNAL OF RANGE MANAGEMENT 54(4), July 2001 499 likely at larger scales (plant communities) and over longer (suc- part. Grazing managers must find ways to work with natural cessional) timeframesÐ the scales most important to manage- processes, not against them; and most importantly, they must ment. There is no distinct difference between “natural” and manage for the whole rather than just a few parts. “unnatural” herbivory, except that the former is less likely to be The Conclusion admonishes the reader to “Find and expand characterized by sedentary, highly selective grazers. Grasses the radical center.” Both extremes in the rangeland conflict are tolerate defoliation, but recover faster when more leaf area wrong; reasonable people who set their differences aside and remains. The grazing disturbance needs to be understood and collaborate to develop shared visions can effect successful, managed in terms of timing, frequency, and intensity. on-the-ground management that benefits all involved. Chapter 3, “The Spatial and Temporal Distribution of Water Stewardship is a bottom-up social process as well as an eco- and Nutrients,” discusses how nutrient and especially water logical one. cycles affect plant community persistence. Total precipitation This book is by no means a complete treatise on sustainable is not as important as the effectiveness of the precipitation. livestock production in the arid and semiarid West. The artic- The more water retained in the soil, the more resilient is the ulation of grazing impacts in terms of timing, frequency, and system. Where soils are stable and watersheds are properly intensity focuses on temporal aspects to the exclusion of the functioning, the potential for long-term sustainable livestock spatial dimension. It does not focus on matching cattle breeds production is high. to the harsh and variable conditions of rangeland environ- Chapter 4, “Thresholds and Monitoring,” revisits the nonlin- ments, or timing the annual livestock production cycle of earity of ecological processes. Understanding state and transi- calving, breeding, weaning and sale to forage conditions, or tion models of vegetation change and patch dynamics is nutritional management. Without discussion of livestock man- important for the appropriate use of the tools of timing, fre- agement per se, the book falls somewhat short of a truly holis- quency, and intensity of grazing to maintain or enhance long tic approach. That the author is an anthropologist and not a term forage and livestock production. Because the crossing of range or animal scientist shows, but it also frees the book of thresholds leads to self-reinforcing changes, monitoring is traditional professional worldviews. The book is a primer of critical to gauging the success of management strategies. modern range science, with a minimum of esoteric jargon, and Monitoring is a way of measuring ecological processes indi- as such is a valuable introduction to sustainable grazing land rectly: litter cover as an indicator of nutrient cycling, and bare management for conservationists, range managers, and espe- ground or total cover as an indicator of the water cycle. Body cially cattle ranchers. The synthesis and application of older condition score is an important index of cattle herd nutrition and more recent ideas is indeed new and continually evolving. and production, but not necessarily of vegetation trend It is especially important that it comes from within the live- because animals may continue to perform satisfactorily after stock community. The ranches profiled in The New Ranch ecological conditions begin to deteriorate. Monitoring must be Handbook demonstrate that livestock grazing can be ecologi- consistent, practicable, and related to management goals; it is cally and economically sustainable, compatible with native no longer optional but a cost of doing business. For technical biodiversity, even on Western rangelands that receive less assistance in designing a monitoring program, the reader is than 12 inches of rain per year. Perhaps the book’s greatest directed to the Monitoring Manual for Grassland, Shrubland contribution is that it suggests a systems approach of planned and Savanna Ecosystems developed by scientists at the yet adaptive management, responsive to opportunities and Jornada Experimental Range in 2000. synergisms, that fosters productive and resilient rangelands Chapter 5, “New Ranch Management,” discusses the appli- and ranching operations.—Matthew K. Barnes, Utah State cation of the concepts developed previously to sustainable University, Logan, Utah. livestock production. The profiled ranchers have combined scientific knowledge with insights gained from living and working on the land—the integration that distinguishes sustainable range management as an art as well as a science. Sayre acknowledges that there is no scientific “proof” of the superiority of any one management program, including SDG, but points out that all 6 ranchers control timing, frequency, and intensity with frequent moves, high numbers of pastures, and rest periods sufficient for recovery. The ranchers with the highest management intensity (Bowe and Winder) also have the highest stocking rates. The ranchers manage their cattle in a single herd (or 2 herds to separate replacement heifers from mature cows). Distribution is controlled with fences, access to water, mineral blocks, and herding with low-stress livestock management methods. The ranchers all plan extensively, especially for drought. In years of high forage production they hold over some calves, run stockers, lease pastures, or engage in prescribed burning. Chapter 6 discusses “Making the Leap” to New Ranch management. Sayre advises ranchers considering substantial changes to begin by examining their goals and then considering the resources of the current operation. Planning is the hard

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