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Associations of the hemiparasite, Castilleja christii N.H. Holmgren (Orobanchaceae).

ABSTRACT

Castilleja christii is known from a single, 80 hectare population in the subalpine zone of Mt. Harrison, of the Albion Mountains, Cassia County, Idaho. All known Castilleja species are hemiparasites capable of utilizing broad range of hosts, yet nothing is known about the host(s) of C. christii. A recent invasion of a non-native weed, smooth brome (Bromus inermis), has raised conservation concerns regarding the long-term persistence of C. christii in the face of a more variable and potentially less stable host community. The study found one C. christii with a haustorial attachment on a mountain big sagebrush (Artemisia tridentata. ssp. vaseyana), and another C. christii with a haustorial attachment from Pedicularis contorta, a parasitic coastal adjunct found on Mt. Harrison. The remainder of plants growing on Mt. Harrison could not be verified as hosts for C. christii, and there was no evidence that C. christii had adopted B. inermis as a host.

KEY WORDS:

Castilleja christii, Mt. Harrison, conservation, hemiparasite

INTRODUCTION:

Castilleja christii N.H. Holmgren (Orobanchaceae) (Christ's Indian paintbrush) is a rare endemic species known from a single 80 hectare population in the subalpine zone of Mt. Harrison, of the Albion Mountains, Cassia County, Idaho (Holmgren 1973). It is assumed that like most members of Castilleja, C. christii is a hemiparasite that forms root associations with one or more hosts to obtain water, nutrients and photosynthates to augment its growth (Heckard 1962). Additonally, secondary compounds from the host plant can confer protection of Castilleja species from herbivores (Adler 2000), increase pollinator atractiveness (Adler et al. 2001) and increase seed set (Adler 2003). However, nothing is known about the host(s) of C. christii.

The Idaho Native Plant Society's Rare Plant List (2011) and Nature Serve (2012) consider C. christii to be globally rare and assign it a conservation rank of G1 (Critically Imperiled). Due to the threats of disturbance and limited distribution, C. christii is a candidate for listing under the Endangered Species Act and is on the U.S. Fish and Wildlife Service Notice of Review list (USDA-NRCS 2011). The majority of research on parasitic plants focuses on damages sustained by the host (Marvier and Smith 1997). Conserving a rare parasitic or hemiparasitic plant requires an understanding of host preferences, and assurance of available hosts (Marvier and Smith 1997, Phoenix and Press 2005).

A Candidate Conservation Agreement was established between the Burley Ranger District of the Sawtooth National Forest (NF) and the U.S. Fish and Wildlife Service for purposes of protecting C. christii and managing activities atop Mt. Harrison (USFWS 1995). The Candidate Conservation Agreement between the NF and USFWS established a rigorous monitoring program allowing the regulating agencies to make informed decisions pertaining to the management and recreational uses permitted on Mt. Harrison.

In the three sub-habitat types where C. christii is found: graminoid, snowbed, and Artemisia tridentata Nutt. ssp. vaseyana (Rydb.) Beetle/Festuca idahoensis Elmer (Moseley 1993), the first 10 years of monitoring showed that the C. christii population "suffered a significant decline" over this period (USFS and USFWS 2005). These data also show that C. christii has different densities and reproductive output in the three habitat types, and that densities of C. christii have fluctuated the most in graminoid communities (USFS and USFWS 2005).

The fluctuations and overall decline of the C. christii population have generated both interest and concern. Factors causing the C. christii population to fluctuate may include biological interactions, direct human disturbances, and environmental effects (USFS and USFWS 2005). With regard to biological interactions, special attention has been paid to non-native weeds. The presence of Bromus inermis Leyss. (smooth brome), and a wheatgrass cultivar (Agropyron sp.) was detected during monitoring and reported in 2001 (USFS and USFWS 2005); B. inermis is the more robust species and spread quickly between 2001 and 2005. The source of the invasion was most likely a seed mix that was used following road work that occurred in 1997 (USFS and USFWS 2005). Monitoring data from 2004 and 2005 showed a positive relationship between C. christii and B. inermis (USFS and USFWS 2005). Despite the initial findings that the B. inermis has had no negative impacts on C. christii, there remain lingering concerns that B. inermis will ultimately destabilize the native habitat and compromise the C. christii population (USFS and USFWS 2005).

This research was performed to identify hosts of C. christii in order to better understand the life history and habitat requirements of this rare plant.

METHODS:

On 23 July 2008, twelve C. christii plants were excavated, four in each of the three habitats where C. christii occurs (snowbed, mountain big sage/Idaho fescue, and graminoid). In each of the three habitats, the specimens of C. christii, and the plants growing directly adjacent, were excavated with attention to the preservation of the clod surrounding the roots. The plants co-occurring with C. christii included: Achillea millefolium L., Pedicularis contorta Benth., Artemisia tridentata ssp. vaseyana, Penstemon rydbergii A. Nelson, Festuca idahoensis, Solidago multiradiata Aiton, Lupinus argenteus Pursh, and Bromus inermis. One to several associated species were excavated along with each C. christii specimen; the assemblage of associated species excavated with each specimen were different both inter and intra sub-habitat types. In the graminoid community attention was given to collecting C. christii specimens that were within 20 cm of B. inermis; only one such specimen meeting this criterion was found.

The roots were gently washed by soaking for three hours, followed by lightly spraying the dirt away. The cleaned roots were microscopically examined to identify and photograph haustorial attachments between C. christii and associated plants.

RESULTS:

Definitive haustorial connections were observed on two of the twelve C. christii specimens examined. One haustorial attachment was observed between C. christii and host A.t. vaseyana (Figure 1). Another haustorial attachment was observed between a different C. christii and P. contorta (Figure 2). In this case, it appeared that the haustorial attachment between the two plants was initiated by R contorta. No other haustorial attachments between C. christii and associated plants could be positively identified. The roots of C. christii were tightly intertwined with the roots of many of the other associated plants.

DISCUSSION:

The data indicate that C. christii is a facultative root parasite of A.t. ssp. vaseyana. Artemisia tridentata ssp. vaseyana is not present in all of the sub-habitats where C. christii occurs, and given the broad range of plant families which Castilleja is known to parasitize (Heckard 1962), it is likely that C. christii may parasitize hosts that were not identified. Reasons that other hosts may not have been identified are: small sample size, facultative nature of the relationship, and methodology. In a controlled greenhouse study of another rare hemiparasite, Schwalbea americana L. (Orobanchaceae), there were also relatively low instances of parasitism (less than 30%) of 3 of the 5 hosts tested (Helton et al. 2000). Similarly, in another controlled experiment four species of Castilleja were able to grow, and in the case of Castilleja angustifolia (Nutt.) G. Don var. dubia A. Nelson produce flowers, without a host (Matthies 1997). Additionally, in a range of experiments, Heckard (1962) found that eleven species of Castilleja could complete their life cycles growing singly without a host, albeit at a decreased vigor compared to plants growing parasitically. These examples illustrate the facultative nature of parasite-host interactions in Castilleja and further explain the limited number of hosts detected in this study. Further studies under more controlled conditions are warranted.

The threat of B. inermis acting as a novel, and potentially inferior, host (USFS and USFWS 2005) was not evident. However, small sample size (n = 1) may have limited the detection of a parasitic relationship with B. inermis. Consistent with observations that control efforts had curtailed some of the B. inermis invasion (USFWS 2010), the fact that simply locating C. christii specimens growing near B. inermis proved difficult suggests that persistence of C. christii is not dependent upon B. inermis. These results also imply that active control of B. inermis would most likely not harm C. christii in a host-parasite context. This research did not investigate the indirect effects that the B. inermis invasion might have on the other potential hosts of C. christii.

While it does not initially seem to be a conservation threat to C. christii, it would be interesting to know if parasitism by P. contorta impacts fitness of C. christii.

ACKNOWLEDGMENTS:

This work was performed under U.S. Fish and Wildlife Service PO 101818M539 Mod #0001. The authors wish to acknowledge the past and present staff at Conservation Seeding and Restoration, Inc. and friends without whom this project would not have been possible. Julie Riddle processed the photos that became the figures in this manuscript. Thanks are due to the two anonymous reviewers who provided comments that vastly improved this manuscript.

REFERENCES:

Adler, L. S. 2000. Alkaloid uptake increases fitness in a hemiparasitic plant via reduced herbivory and increased pollination. American Naturalist 156(1): 92-99.

Adler, L.S. 2003. Host species affects herbivory, pollination, and reproduction in experiments with parasitic Castilleja. Ecology 84(8): 2083-2091.

Adler, L. S., R. Karban, and S. Y. Strauss. 2001. Direct and indirect effects of alkaloids on plant fitness via herbivory and pollination. Ecology 82(7): 2032-2044.

Heckard, L.R. 1962. Root parasitism in Castilleja. Botanical Gazette 124(1): 21-29.

Helton R.C., Kirkman, L.K, and L.J. Musselman. 2000. Host preference of the federally endangered hemiparasite Schwalbea americana L. (Scrophulariaceae). Journal of the Torrey Botanical Society 127(4): 300-306.

Holmgren, N.H. 1973. Five new species of Castilleja (Scrophulariaceae) from the Intermountain Region. Bulletin of the Torrey Botanical Club 100(2): 83-93.

(INPS) Idaho Native Plant Society. 2011. Results of the twenty-fifth Idaho rare plant conference. Boise, ID. 9 pp.

Marvier, M.A. and D.L. Smith. 1997. Conservation implications of host use for rare parasitic plants. Conservation Biology. 11(4): 839-848.

Matthies, D. 1997. Parasite-host interactions in Castilleja and Orthocarpus. Canadian Journal of Botany. 75(8): 1252-1260.

Moseley, R.K. 1993. The status and distribution of Christ's Indian paintbrush (Castilleja christii) and Davis' wavewing (Cymopterus davisii) in the Albion Mountains, Sawtooth National Forest and City of Rocks National Reserve. Unpublished report on file at the Conservation Data Center, Idaho Department of Fish and Game, Boise, ID. 18 p. plus appendices.

NatureServe. 2012. NatureServe Explorer: An online encyclopedia of life [web application]. Version 7.1. NatureServe, Arlington, Virginia. Available http://www.natureserve.org/explorer. (Accessed: 22 October, 2012).

Phoenix G.K. and M.C. Press. 2005. Linking physiological traits to impacts on community structure and function: the role of root hemiparasitic Orobanchaceae (ex-Scrophulariaceae). J. Ecology. 93: 67-78.

St. John, L. and D.G. Ogle. 2009. Plant Guide for Christ's Indian paintbrush (Castilleja christii). USDA Natural Resources Conservation Service, Plant Materials Center, Aberdeen, ID. Available: ftp://ftp-fc.sc.egov.usda.gov/ID/programs/plant/christs_paintbrush.pdf (Accessed: 22 October 2012).

(USDA and NRCS) U.S. Department of Agriculture and Natural Resources Conservation Service. 2011. Plant guide: Christ's Indian paintbrush, Castilleja christii N.H. Holmgren. Available ftp://ftp-fc.sc.egov.usda.gov/ID/programs/plant/christs_paintbrush.pdf. (Accessed: January 3, 2011).

(USFS and USFWS) U.S. Forest Service and U.S. Fish and Wildlife Service. 2005. Candidate Conservation Agreement for Castilleja christii, Christ's Indian paintbrush. U.S. Forest Service, Minidoka Ranger District, Sawtooth National Forest, Twin Falls and Burley, Idaho. 60 p.

(USFWS) U.S. Fish and Wildlife Service. 1995. Conservation Agreement: Castilleja christii/ Christ's Indian paintbrush. Unpublished document on file at the Conservation Data Center, Idaho Department of Fish and Game, Boise, ID. 12 p.

(USFWS) U.S. Fish and Wildlife Service. 2010. Species assessment and listing priority assignment form: Castilleja christii. 26 p. Available http://ecos.fws.gov/docs/candidate/assessments/2010/r1/Q0CI_P01.pdf (Accessed: January 3, 2011)

Michael Clancy (1), Kent Fothergill (1,2), Jeff Motychak (3), and Kim Pierson (4)

(1) Conservation Seeding and Restoration, Inc., 506 Center Street West, Kimberly, ID. 83341 (2) Orma J. Smith Museum of Natural History, The College of Idaho, 2112 Cleveland Blvd., Caldwell, ID. 83605 (3) McCall College 106 East Park Street, Suite 220, McCall, ID. 83638 (4) United States Forest Service, Payette National Forest, New Meadows Ranger District, P.O. Box J, 3674 Highway 95, New Meadows, ID. 83654
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Author:Clancy, Michael; Fothergill, Kent; Motychak, Jeff; Pierson, Kim
Publication:Journal of the Idaho Academy of Science
Article Type:Report
Geographic Code:1USA
Date:Jun 1, 2013
Words:2042
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