W1193: Locoweed and its Fungal Endophyte: Impact, Ecology, and Management

(Multistate Research Project)

Status: Inactive/Terminating

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Locoweeds are the most widespread group of poisonous plants in the western United States (Allred, 1991; Graham et al., 2009). Consumption of toxic species within the plant genera of Astragalus and Oxytropis, within the Fabaceae, cause locoism to grazing animals (Knight and Walter, 2003). Locoism is caused by consumption of the indolizidine alkaloid swainsonine (SWA), an alpha-mannosidase inhibitor (Dorling et al., 1980). Locoism symptoms include reproductive problems, cellular vacuolization, neurological damage, and lack of coordination (James, 1970; James et al., 1981; James et al., 1992). Livestock poisoning from locoweeds causes major economic losses in several western states. While the magnitude of economic loss depends on the degree of intoxication, losses from locoweeds due to poor animal health, low reproductive performance, increased death and reduced weight can cause reductions in cattle prices from 10% to 85%. In New Mexico in 1985, over 10% of the cow/calf and 40% of the cow stocker operations reported losses of over $20 million from locoism (Torell et al., 2000).

Most plants in natural ecosystems are hypothesized to interact in symbioses with fungal endophytes (Rodriguez et al., 2009), often in mutualism because the fungal endophyte gains a home, a source of nitrogen and carbon resourses, while providing a variety of benefits to the plant host. Fungal endophytes of locoweeds (genus Undifilum) produce the alkaloid swainsonine and are thus responsible for the locoism disease symptoms (Braun et al., 2003; Pryor et al., 2009). The endophytes are seed transmitted and generally do not cause disease to their plant host (Oldrup et al., 2010). Similarly, fungal endophytes of grasses produce alkaloids toxic to grazing mammals. Research on the grass-fungal endophyte system has shown host benefits including herbivore defense (Clay 1990), increased heat and drought tolerance (Bacon and White., 2000), and improved plant vigor and resistance to some pathogens (Molyneux et al., 2007). In contrast, the benefits provided by the fungal endophytes to locoweed plants are not known. As a consequence, the ecological relationship between the endophytes and locoweeds has not been well-defined. However, plants grown without the endophytes are non-toxic high quality forage. A better understanding of the endophytic fungi, including how they produce swainsonine and how they interact with their plant hosts, will contribute toward long term management solutions with understanding of the toxic compound quantity and accumulation in hosts and locoweed population establishment and occurrence, respectively.

Locoism causes severe life and economic losses to domestic and wild ungulates. Locoism is caused by the consumption of the toxic alkaloid SWA which is produced by a fungal endophyte associated with locoweeds of the Astragalus and Oxytropis genus. However, the biosynthetic pathway for swainsonine production remains unknown. A better understanding of factors that affect SWA levels within the host plant as well as between populations on range lands needs to consider both the locoweed host plant and its fungal endophyte. This is because although the fungal endophyte produces SWA, it most likely receives its nutrients from its host plant to do so (Delaney et al., 2011; Vallotton et al., 2012). Also, the success of the fungal endophyte, and its distribution, depends on the success of the locoweed host since the fungus is only vertically transmitted through seed coats. Finally, although vertebrate herbivores may not be deterred by SWA when preferred food plants are unavailable, 20% of cattle tested were willing to consume new plants like locoweed and social interactions among cattle can promote many individuals to consume locoweeds in a relatively short time (Graham et al, 2009). With the small yet pervasive populations of many species of locoweed throughout many western rangelands, providing non-toxic forage for grazing can only be accomplished by a thorough understanding of the interaction between host plants and their corresponding endophytes.
Effective management of locoweeds and locoism has been difficult to implement and costly despite the prevalance of locoism in the United States for over a century (Marsh, 1909). Recommendations include restricting access to pastures for grazing in the spring, supplementing cattle feed so that they don’t graze on locoweeds, spraying herbicides during locoweed flowering, and using insects for biocontrol (Graham et al., 2009). Behavior modification of cattle and horses shows promise as a management option, although large scale feasibility has not been determined. A valuable, sustainable management program that can be implemented in multiple states is needed for this difficult problem.

Understanding locoweed-fungal endophyte interactions can significantly impact several research areas: plant/microbe interactions, microbe-induced plant defense against herbivores, rangeland management, secondary metabolite production (plant or fungal production control), plant resource investment into an asymptomatic endophyte, plant abiotic and biotic stress tolerance, plant biogeography, and the continuum between mutualistic and commensalistic interactions where locoweed/endophyte system seems to fall. Locoweed-fungal endophyte interactions are also of interest by being quite different from the tall fescue-fungal endophyte complex where the fungus produces a toxic alkaloid, but also enhances plant growth.

We propose establishment of a regional project to study locoweeds and their fungal endophytes to monitor locoism impacts on the rangeland grazing communities and collaborate for management solutions. Locoweeds and locoism cause problems over a large area and the researchers that are experts in the field that address the problem are spread over several states and over different agencies, ie. ARS and USDA. A multistate project will improve communication and research efficiency. This group will meet annually to discuss, assess, and prioritize research topics such as locoweed genetics, endophyte genetics, plant and fungal ecology and physiology, and locoism detection and management. The group will develop an action plan to determine who will accomplish which aspects of the research, including identifying research of high impact for locoism management, and who will work together to seek funding for the highest priority research. The group will coordinate research to provide preliminary information needed to secure grant funding. The group will also bring together research resources including plant and fungal samples collected from various locations and seed of various locoweed species, and provide periodic written documents reviewing the status of locoweeds, endophytes, and management both for dissemination among collaborating institutions and throughout range communities.

This research will lead to a better understanding of the interaction of plant and endophyte on swainsonine concentrations and subsequent effects on grazing animals. Through increased understanding of this tripartite interaction of fungus-plant-animal, we may be able to develop strategies to eliminate swainsonine or change the dynamics of the endophyte in naturally occurring populations of locoweed. Incorporating research from multiple states will contribute to management solutions for local, state-wide, and national locoism problems as well as decreasing duplication of research and increasing dissemination of results. This work can benefit society by helping to more completely understand locoweeds and how a toxic alkaloid is produced by a fungus, which in turn may ultimately protect the food supply by aiding ranchers whose livestock suffer from locoism.
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