The Bryologist 103(2), pp. 353-356Copyright © 2000 by the American Bryological and Lichenological Society, Inc.

INWTED ESSAY

New Frontiers in Bry^logy and Lichen^logy

Lichen Communities as Indicators of Forest Health

BRUCE MCCUNE

Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331-2902, U.S.A. e-mail:mccuneb@bcc.orst.edu

BACKGROUNDForest health: what is it? "Health" is an inher-

ently fuzzy concept, even when applied to our-selves. And forests (and other ecosystems) are fuzz-ier than organisms, being weakly bounded andloosely organized. So the concept of "foresthealth" can seem hopelessly vague. Nevertheless,in extreme cases anyone can spot a "sick" forest.Despite forest health being a fuzzy concept, peoplewant healthy forests and expect resource manage-ment agencies to monitor them.

The concept of ecosystem health is contentiousnot only because it is fuzzy, but also because itembodies societal values and preferences (Lackey1998). The more that people disagree on these val-ues, the more contentious the concept of ecosystemhealth.

One way ecologists make progress on inherentlyfuzzy concepts is to make them practical with op-erational definitions (Peters 1992). For example, wecould define a person's health by a combination oftheir internal temperature, blood pressure, and cho-lesterol levels. These are indicators of health, not acomprehensive examination. Nor do the indicatorsin themselves usually allow the diagnosis of a spe-cific problem. Rather, these indicators tell us whenwe need to examine a problem more closely. Thesedata are easy to obtain, yet tell us a lot.

Similarly we want to identify indicators of foresthealth. The indicators should point to ecosystemswhere a problem exists or is emerging. They shouldalso tell us when and where forest health is im-proving. Lichen communities have the honor of be-ing included as indicators of forest health by theU.S. Forest Service and other government agencies.

WHAT IT TAKES

All organismal biologists would like to see theirgroups of special interest incorporated into long-term monitoring programs. But what does it actu-ally take to accomplish this, beyond stable long-

term funding? Some key components of the scienceare:

Simple field method that is usable by nonspe-cialists (much as we would like to see profes-sional lichenologists collect the field data, thatoption is financially hopeless).Repeatable field method.Meaningful data.Collaboration among many scientists and gov-ernment agencies.Compelling links between the organisms and so-cietal values (the public must value either theorganisms themselves or ecosystem conditionsthat they indicate).Timely, clear, interesting products (reports, sci-entific papers, web sites, etc.).

The lichen part of the Forest Health Monitoring(FHM) program has accomplished the first threeitems (McCune et al. 1997a,b; Stolte 1997; http://willow.ncfes.umn.edu/fhm_fact/overview.htm); thelast three items are ongoing challenges.

H ISTORY

The FHM program seeks to assess the conditionand trend of forests of the United States. FHM usesthe national sampling grid established by the En-vironmental Monitoring and Assessment Program(EMAP) of the Environmental Protection Agency(Messer et al. 1991). The sampling design is un-usual for forest ecology in that plots are chosen atrandom with respect to disturbance history, envi-ronment, internal homogeneity, and stand charac-teristics. The sampling design is ideal for charac-terizing a whole region.

Epiphytic lichen communities were included inFHM because they inform us about ecosystem con-taminants and biodiversity. Hundreds of papersworldwide and dozens of review papers and booksdocument the close relationship between lichencommunities and air pollution, especially SO 2 and

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TABLE 1. Selected lichen community biomonitoring efforts. A sample unit (SU) is an individual plot representinga grid point.

PlannedDuration, resampling Resolution, Number of

Country Extent, km' years interval, years SU/100 km2

SU'sNetherlands 2 X 104 30 5 18 ca 5,000Switzerland 4 X 104 4 101' 24 826U.S.A.* 8 X 106 8 4 0.16 2,600§

* Conterminous 48 states; includes many non-forested areas not part of FHM.Uncertain.Not a regular grid: area stratified by elevation and forest cover, then sampled 2% of the kilometer intersections in

each stratum.§ Currently 3,860 forested plots; ca 2,600 of those sampled for lichens; total of 6,441 plots anticipated after merger

with FIA (Forest Inventory and Analysis).

acidifying or fertilizing nitrogen- and sulfur-basedpollutants. Much of the sensitivity of epiphytic li-chens to air quality apparently results from theirlack of a cuticle and their total reliance on atmo-spheric sources of nutrition. Although trees may re-spond to moderate, chronic air pollution, all of theother influences on tree growth, such as variationin soils, make the responses of trees to pollutantsdifficult to measure in the field. So lichen com-munities provide not only a measure of air pollutionimpacts upon lichens, but also suggest air pollutionimpacts on aspects of forest health that are difficultto measure directly.

In addition to their utility as indicators of airquality, epiphytic lichens are an important and spe-cies-rich component of the biodiversity many for-ests. Lichens have numerous functional roles intemperate forests, including nutrient cycling (es-pecially nitrogen fixation in moist forests) and ascomponents of food webs. The complete depen-dence of epiphytes on woody plants makes themsensitive to forest management practices.

Other countries also use large scale monitoringof lichen communities (Table 1). The program inthe Netherlands (van Dobben & de Bakker 1996;van Dobben & ter Braak 1998; and van Herk 1999)is outstanding for its length of record, fine spatialresolution of the sampling grid, high density of cor-responding physical measurements of pollutants,and illuminating analyses of trends in lichen com-munities in response to the changing compositionof air pollutants. The recently created program inSwitzerland (Dietrich & Scheidegger 1997a,b,1998) emphasizes detecting and evaluating rare li-chen species. It will also be extremely useful fordetecting human impacts on lichen communities.

Analysis of elemental content of lichen tissues isanother common approach to biomonitoring of airquality (Stolte et al. 1993). After a two year trial,the FHM program rejected this as an indicator offorest health, for two reasons. First, high within-plot variability led to high repeat-measurement er-

rot Subtle pollution signals were difficult to detectagainst the background of this statistical noise. Sec-ond, the ecological heterogeneity of North Americaprecluded a simple standardization of the targetspecies. Standardization is necessary because dif-ferent species in the same environment differ mark-edly in their elemental contents. Even such candi-date species as the seemingly ubiquitous Parmeliasulcata are rare or absent in large parts of the for-ested US.

The lichen community indicator for FHM (Fig.1) is implemented in three phases 1) collect fielddata on the sampling grid and special plots in urbanand industrial areas; 2) construct a gradient modelof lichen communities to isolate and describe cli-matic and air quality gradients; and 3) apply themodel to calculate gradient scores for additionalplots. Scores for these plots are then used to de-scribe the regional condition of lichen communities.Repeated sampling of these permanent plots willdocument changes in lichen communities over timeand allow us to infer changes in regional air quality.

The FHM lichen community method determinesthe presence and abundance of macrolichen specieson all standing woody plants in each FHM plot.The field crew collects samples for mailing to li-chen specialists for naming. The field methods andquality assurance procedures are described inMcCune et al. (1997a).

SYNTHESIS OF IMPORTANT DISCOVERIES

In the southeastern U.S. we found two major re-gional gradients in lichen communities (McCune etal. 1997b). The strongest gradient in the lichencommunities corresponded to a macroclimatic gra-dient from the coast through the Piedmont to theAppalachian Mountains, primarily related to tem-perature. The second major gradient was correlatedwith air quality, with pollution-tolerant species andlower species richness in urban and industrial areas,and pollution-sensitive species and high species

2000] 355

No dataOn-frame dataData + gradient model

FIGURE 1. Status of lichen communities in FHM in the U.S. Shaded states have lichen data; blackened states alsohave a gradient model representing lichen communities in relationship to climate and air quality

MCCUNE: NEW FRONTIERS

richness in cleaner areas. Epiphytic macrolichenswere sparse in urban areas with heavy industry. Inmany rural areas lichens were luxuriant and di-verse.

The northeastern U.S. required a somewhat morecomplex model, with two climatic gradients (lati-tude and elevation) and an air quality gradient (S.Will-Wolf, unpubl. data). Lichens have low diver-sity and abundance in urban and industrial areas inthe northeastern U.S. In Central Park of New YorkCity, a single macrolichen species, Physcia mine-grana, was found. This is the most pollutant tol-erant macrolichen in eastern North America.

A climatic gradient was also strong in Colorado(McCune and others, unpubl. data). An elevation-moisture gradient explained over half of the varia-tion in lichen communities. Because air qualityscores, as expressed by lichen communities, werepositively related to elevation, we needed to re-ex-press air quality as a number of standard deviationsaway from expectation for a given elevation, usingresiduals from the regression of raw air qualityscores on elevation. Lichen communities indicatedpoor air quality on the east side of the Front Rangenear Denver and Boulder, the Steamboat Springsarea, and the Grand Junction area.

In all three models, use of special plots from ur-ban and industrial areas was essential for fitting anair quality gradient. Application of the models in

the future will allow us to monitor regional changesin air quality and climate.

WHY THIS TOPIC WILL YIELD SIGNIFICANT ADVANCESIN THE NEXT MILLENNIUM

The FHM program and similar efforts in othercountries give us the first opportunity to documentsystematically the changing biota of a region. Themain challenge facing that vision is the reluctanceof government agencies to make long-term finan-cial commitments to monitoring our biota—the samecommitment given to monitoring weather andstream flows.

If FHM discontinues, we will still have a lichensnapshot of many forested areas of the country.This will provide the basis for follow-up compari-sons. Think of the tremendous value that would beplaced today on systematic lichen data from a hun-dred years ago.

Regional lichen community data have potentialfor many significant by-products, beyond the pri-mary purpose. Some of the spinoffs are: docu-menting the invasion and extinction of species, en-hancing our knowledge of the distribution andabundance of macrolichens (the data have alreadyyielded many surprises), increasing appreciation bynon-lichenologists for the importance of lichens ascontributors to ecosystem function and diversity,

356 THE BRYOLOGIST [VOL. 103

contributing data to meet survey-and-manage man-dates in the Northwest Forest Plan (USDA & USDI1994), training numerous people in the basics oflichenology,. and building collections from poorlystudied areas.

The FHM program is giving a big boost to li-chenology in the U.S. With support from the li-chenological community, it has great potential toadvance our understanding, and perhaps even influ-ence the fate of our lichens and forests in NorthAmerica.

ACKNOWLEDGMENTS

Peter Neitlich, Paul Rogers, Ken Stolte, and Susan Will-Wolf shared the lead with me in developing the lichenpart of the FHM program and adopted the leadership afterI moved to other work. Other lichenological contributorsinclude Ann DeBolt, Jonathan Dey, Karin Heiman, JeriPeck, Roger Rosentreter, Andrea Ruchty, and Bruce Ryan.Philippe Clerc and Theodore Esslinger assisted with dif-ficult specimens. Han van Dobben and Christoph Schei-degger provided information on lichen monitoring in theNetherlands and Switzerland, respectively. Bill Smith pro-vided data on the FHM grid. Funding was provided bythe Forest Health Monitoring Program, an interagencyprogram including the USDA Forest Service, the U.S. En-vironmental Protection Agency, USDI Bureau of LandManagement, USDA Natural Resource Conservation Ser-vice, Tennessee Valley Authority, and participating stateagencies. This paper has not been subjected to reviews byany of those agencies, therefore it does not necessarilyreflect the views of the agencies. No official endorsementshould be inferred.

LITERATURE CITED

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quency of epiphytic lichens at the regional and na-tional levels and its use for the red list of Switzerland,pp. 145-154. In R. Tiirk & R. Zorer (eds.), Progress

and Problems in Lichenology in the Nineties. Biblio-theca Lichenologica, J. Cramer, Berlin, Stuttgart. . 1998. Diversity of forest lichens in

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PETERS, R. H. 1992. A Critique for Ecology. CambridgeUniversity Press, Cambridge.

STOLTE, K. W. 1997. 1996 National Technical Report onForest Health. USDA Forest Service, AdministrativeReport FS-605. , D. MANGIS, R. DOTY, K. TONNESSEN & L. S.

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VAN DOBBEN, H. E, & A. J. DE BAKKER. 1996. Re-mappingepiphytic lichen biodiversity in the Netherlands: ef-fects of decreasing SO 2 and increasing NH 3 . Acta Bo-tanica Neerlandica 45: 55-71. , C. J. F TER BRAAK. 1998. Effects of atmospheric

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