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Tropical Bryology 31: 1-4, 2010 

Looking back on 15 years of research on bioindication with 

Jan-Peter Frahm in Bonn 

Norbert J. Stapper 1 & Isabelle Franzen-Reuter 2 

1 Büro für Ökologische Studien, Monheim, Germany (nstapper@t-online.de) 

2 Burgbrohl, Germany (franzen-reuter@web.de) 

Abstract: The article summarizes 15 years of research activity of Jan-Peter Frahm at Bonn University in the 

field of bioindication of environmental pollution with bryophytes and lichens as sensitive monitoring organisms. 

Keywords: bioindication, lichen, bryophyte, atmospheric pollution, eutrophication, climate change. 

Jan-Peter Frahm's transfer from the Pedagogical 

University in Duisburg to the venerable University of 

Bonn in 1994 coincided with the first observable 

reduction in decades of annual means of sulphur 

dioxide immissions below the level of 25µg/m 3 . 

Investment in flue gas desulphurization and the use of 

low sulphur fuel helped to stop the "acid rain" 

(Vestreng et al. 2007). This represents a landmark in 

European industrial history. At the same time, a few 

mosses and lichens spread into rural parts of the Ruhr 

district and started colonizing tree bark. Shortly 

before, the centers of the big cities along the Rhine 

and Ruhr were "epiphyte deserts", because epiphytic 

bryophytes and lichens were most affected due to the 

low buffer capacity of tree bark. 

In Duisburg, Jan-Peter had lived close to the major 

source of the acid rain. Already in 1974, he had 

studied the impact of acidic immissions on 

transplanted mosses (Frahm 1976). Transplanted 

Dicranoweisia cirrata e.g. rapidly died within four 

weeks. Twenty years later, however, it survived for an 

entire year of exposure outside the lab, and when the 

experiment was stopped, sporophytes had formed. 

Under non-experimental conditions, however, this 

species did neither occur in Duisburg, nor in Bonn at 

this time. This was soon to change radically. 

On weekends at the Lower Rhine in the vicinity of the 

Dutch border and on local walks around Bonn, Jan- 

Peter found the first small cushions of Orthotrichum 

affine, and shortly afterwards, Ulota bruchii - 

indicating that the return of the epiphytes had begun. 

To document this phenomenon, Jan-Peter - in the 

summer term of 1996 - started giving lectures and lab 

classes focusing on "mosses as bioindicators". 

Somewhat later, lichens were included in the curricula 

and the first diploma thesis was initiated: Claudia 

Dilg (Dilg 1998) mapped epiphytic lichens and 

TROPICAL BRYOLOGY 31 (2010) 

bryophytes in the city of Bonn. She recorded 38 

bryophytes and 54 lichens, among them were 

sensitive species such as Frullania dilatata, Bryoria 

fuscescens, and Ramalina pollinaria. At that time, 

epiphytic species’ diversity still correlated well with 

winter levels of sulphur dioxide immissions, but Dilg 

(1998) already postulated that air pollution by 

eutrophicating compounds like dust and reactive 

nitrogen were growing in significance. 

The bioindication lab class soon became particularly 

popular at graduate students of biology. In addition to 

techniques for mapping epiphytes, analyses of heavy 

metal content in Sphagnum samples ("Sphagnum 

bags"); tests with water mosses in aquariums, or 

estimates of the water quality in the River Ahr by use 

of aquatic mosses became part of the study program. 

Subsequently, the cooperation with the State Institute 

for Ecology, Agriculture and Forestry of North Rhine- 

Westphalia (LÖBF NRW) gave more momentum. On 

behalf of the LÖBF, epiphytic lichens and bryophytes 

were mapped along three transects through Duisburg, 

Bochum and Dortmund. Not only many species were 

recorded, but a significant gradient was observed, 

indicating stronger pollution impact on the northern 

parts of the transects. While pollution tolerant 

Lecanora conizaeoides dominated in the north, 

several Orthotrichum mosses and Parmelia lichens 

were monitored in the south, and last but not least, 

there was no longer evidence of lichen deserts 

(Stapper et al. 2000). We were indeed proud when the 

Environmental Secretary showcased our results as a 

testimony of better air quality in the Ruhr district and 

proof that investment in environmental protection had 

been sensible. 

Jan-Peter strongly “infected” both of us with his 

enthusiasm for this topic, so that currently one of us 

(IFR) is now responsible for drafting technical

2 

guidelines for the Association of German Engineers 

(VDI), while the other (NJS) has become a selfemployed 

surveyor specializing in bioindication with 

lower plants. 

During the last years, epiphyte recolonization 

proceeded at a faster pace. In less than two years, 

epiphitic species’ diversity doubled within the 

transects. Moreover, frequency and cover increased 

substantially. When remapping the transects, we 

observed that especially nitrophytic species like 

Orthotrichum diaphanum, Phaeophyscia spp. and 

Xanthoria spp. were rapidly spreading, even Bryum 

argenteum as well as dense tomenta of filamentous 

algae had become prevalent on trunks (Frahm 1999, 

Franzen 2001a) while species adapted to nutrient-poor 

or acidic substrata, e.g. Hypogymnia physodes, 

rapidly receded. 

Thus the improvement for epiphytes was not only due 

to a decrease of acidic immissions, but also to (the 

influence of) airborne nutrients. Epiphyte monitoring 

within the level II programme that was also promoted 

by the LÖBF, yielded confirmatory results (Stetzka & 

Stapper 2001). 

Two doctoral dissertations, partially financed by the 

ministry of the environment of North Rhine- 

Westphalia and the Deutsche Bundesstiftung Umwelt, 

were initiated to conduct research on the cause of the 

apparent changes of epiphyte flora: What are the 

causes for the increase of nitrophytes? Which nitrogen 

compounds are of importance ("reactive nitrogen")? 

Are there further factors affecting epiphytes? A 

comprehensive epiphyte mapping of North Rhine- 

Westphalia gave an overview of the occurrence of 

epiphytic lichens and bryophytes (Franzen et al. 2002, 

Franzen-Reuter & Stapper 2003, Stapper & Franzen- 

Reuter 2004). Data interpretation according to VDI 

3799 Part 1 (VDI 1995) resulted in high „air quality 

values“ indicating low pollution levels also for those 

parts of the state of which airborne nutrient supply 

was already known to be high (Frahm et al. 2006). 

Closer analysis, however, showed that the high „air 

quality values“ were caused by the abundance of 

nitrophytes, epiphytes promoted by pollution with 

airborne nutrients falsified the results. When, in lieu 

of lichen frequency, we simply plotted the mean 

number of epiphytes per tree, a much more realistic 

pattern was obtained. The Dutch colleagues call this 

figure "Nitrifiele Indicatie Waarde" (van Herk 1999). 

Finally, we participated in the revision of the 

guideline for lichen mapping; the current version is 

VDI 3957 Part 13 (VDI 2005). IFR examined the 

effects on and metabolism of experimentally applied 

nitrogen compounds on epiphytic lichens and 

bryophytes (Franzen-Reuter 2004, Franzen-Reuter et 

al. 2006, Franzen-Reuter & Frahm 2007), while 

landscape ecologist Andreas Solga, who had joined 

the Frahm group, made similar experiments with 

STAPPER & FRANZEN-REUTER: BIOINDICATION IN BONN 

terrestrial and saxicolous bryophytes (Solga 2003, 

Solga et al. 2005, 2006b). They discovered that 

reactive nitrogen is preferentially taken up in its 

reduced form. Both, nitrate and ammonia are taken up 

by organisms, and ammonia is instantly incorporated 

into amino acids and other metabolites, whereas the 

conversion of nitrate is rather energy consuming, 

making oxidized N a less efficient nutrient. Mapping 

results showed a strong correlation between the 

frequency of nitrophytes and both agricultural activity 

or traffic intensity. We initially suspected dust 

(Vorbeck & Windisch 2001) and nitrogen oxides from 

cars (Franzen et al. 2002) as the principal nutrients for 

nitrophytes downtown, but in view of the rapid 

decline of traffic impact with distance from road 

edges, ammonia produced in catalytic converters 

(Cape et al. 2004, Frahm 2008), appeared as more 

likely candidate. Consequently, we analyzed 

specimens of the foliose lichen Parmelia sulcata 

collected at different sites in Düsseldorf, and 

discovered a strong correlation between total tissue 

nitrogen content and traffic intensity at the collecting 

site (Stapper et al. 2005). At the same sites, Jan-Peter 

estimated ammonia using FERM samplers (Frahm 

2006, 2007a) showing that sites with both high 

nitrogen content in lichens and traffic intensity were 

the ones with high ammonia levels, too. 

Compared to livestock farming, traffic is a small 

source for ammonia, and for this reason, its potential 

impact on the urban ecosystem has been 

underestimated or ignored so far. In congested and 

canyonlike downtown streets, only mosses and 

lichens which are most resistant to airborne nutrients 

hold out if any (Stapper & Kricke 2004). At these 

sites, the influence of eutrophicating pollutants is 

particularly strong. In the Netherlands, the trafficrelated 

impact on epiphytes has become noticeable 

with declining levels of ammonia emitted from the 

agricultural sector (van Herk 2009). There are several 

explanations for the effects of ammonia on the 

composition of epiphytic lichen and bryophyte 

communities, (1) altered substrate, i.e. increased pH 

of bark caused by ammonia (van Herk 2001), and (2), 

higher tolerance of (some) nitrophytes to drought and 

osmotic stress, imputing ammonia derived 

compounds to act (Janßen et al. 2007, Frahm 2008, 

Frahm et al. 2009). 

Drought resistence appears to be a cause of the 

increase of Phaeophyscia nigricans and P. 

orbicularis, because they predominantly do not only 

survive at highly congested sites but also at heated 

sites in urban areas, where most others cannot be 

found. Furthermore, Jan-Peter Frahm and his students 

demonstrated that the frequency of nitrophytes 

declines with increasing humidity at the investigated 

sites (Frahm et al. 2007a,b). Some of the nitrophyte 

species used as indicators for eutrophication by VDI 

3957 Part 13 suffer much less from low humidity than 

TROPICAL BRYOLOGY 31 (2010)

acidophytes and neutrophytes. Frahm & Stapper 

(2008) consequently introduced a humidity related 

correction factor for lichen mappings of large areas. 

The activities of Jan-Peter Frahm in the field of 

bioindication with bryophytes are numerous and 

diverse, and resulted in two amply illustrated 

textbooks (Frahm 1998, Frahm et al. 2007a). The 

experience gathered in many studies and observations 

during field trips are, for instance, included in a VDI 

guideline for mapping of diversity of epiphytic 

bryophytes as indicators of air quality (Franzen 

2001b, VDI 2006). 

Investigating the effects of climate change on 

bryophytes and lichens is another focus of research of 

the "Bonn group". First scientific findings were 

published already 10 years ago (Frahm & Klaus 2000, 

Frahm 2003, 2007b). Here again, epiphytes are of 

main interest, because their properties are well 

known. The rapid increase - particularly in northwest 

Germany - of lichens originally limited to the 

Mediterranean or Atlantic parts of Europe appears to 

be caused by climate change, even if one keeps in 

mind that the return of many species due to reduced 

pollution is not completed (unpublished observation). 

Research has largely been focusing on epiphytes. For 

the sake of completeness it has, however, to be 

mentioned that some results of studies on aquatic or 

terrestrial mosses are used or will soon be used in 

standards and technical guidelines. The sampling 

procedure developed by Solga et al. (2006a) and 

Solga & Frahm (2006), for instance, has been made 

standard practice in VDI 3957 Part 19 (VDI 2009). 

Acknowledgements: We are indebted to our colleague 

Walter Erhardt (Karlsruhe) for helpful comments. 

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