31(1): 9-20 (1999)
Available online at http://www.idealibrary.com on IDE^-L
MAPPING OF AMMONIA POLLUTION WITH
EPIPHYTIC LICHENS IN THE NETHERLANDS
M. van HERK*
Abstract: In the Netherlands a monitoring programme is in operation to map the
effects of ammonia pollution with epiphytic lichens. The method is presented here
and the results are statistically correlated with abiotic data. The abundance of
appears to be a useful parameter. Detailed spatial
patterns of ammonia pollution can be obtained with lichens. To avoid interference,
important to consider other influences, for example dust, climate, exposure, age
of the trees and other pollutants. [, 1999 The British Lichen Society
Since the 1950s lichens have often been used to map sulphur dioxide (SO2) air
pollution in the Netherlands (Barkman 1958; de Wit 1976). During recent
decades a progressive recovery of species sensitive to SO2 took place (van
Dobben 1993), due presumably to the falling levels of SO2. Now there are
several records of species that had not been seen for nearly
century (van Herk
& Aptroot 1996). There are even species new to science that were absent
before (Aptroot & van Herk 1998).
Some changes, however, do not fit within the spatial patterns and temporal
changes in SO2. In the course often years a spectacular increase in nitrophytic
species has taken place in all parts of the country with a high cattle density (van
der Knaap 1984; de Bakker 1987; van Dijk 1988). In these areas the trees
have become covered with such species as
This phenomenon is especially apparent
on trees with acid bark
on which nitrophytes were absent or
scarce before. In the same period several acidophytes, for example Evernia
and Pseudevernia furfura-
rapidly decreased (van Dijk 1988; van Herk 1990). A large number of
stations formerly covered with these species are now totally devoid of them.
Outside the areas with intensive cattle breeding these changes are less
Air pollution with ammonia (NH3) is considered to be the most important
cause of these changes. In the Netherlands the correlation between ammonia
and lichens has been studied repeatedly. Correlations are reported by de
Bakker & van Dobben (1988), van Dijk (1988), de Bakker (1989), Aptroot
van Herk (e.g. 1990, 1991, 1993, 1995, 1996), van Dobben (e.g.
1993) and van Dobben
Wamelink (1992). In Belgium (Vlaanderen)
*Lichenologisch Onderzoekbureau Nederland, Goudvink 47, NL-3766 WK Soest, The
0024-2829/99/010009+12 S30.00/0 © 1999 The British Lichen Society
10 THE LICHENOLOGIST Vol. 31
the effects of ammonia have been studied by Hoffmann (1993). In Great
Britain effects of intensive cattle breeding have been reported from Devon
Field observations show a clear relationship between the distance from a
livestock farm and the abundance of nitrophytes on trees (Fig. 1A-C). Some
of the species are more dominant, whereas other species are present only in
small quantities in the immediate surroundings of the farms, for example
Phaeophyscia nigricans, Candelariella aurella and Caloplaca holocarpa (Fig. 2).
Very polluted sites show a striking resemblance to epilithic vegetation of
calcareous substrata such as concrete. Even
have been found at such stations on trees.
The transition zone surrounding a livestock farm is usually more or less
compressed at the west side and a little elongated at the east side, indicating
that westerly winds are more frequent. The effects are definitely not caused
only by slurry. Even in woods small branches at the tops of trees are now
covered with Physcia tenella and Xanthoria polycarpa.
The atmospheric behaviour of ammonia supplies an explanation for the
close transitions. At 100 m distance from a source, c. 10% of the ammonia is
deposited and at 1000 m this is c. 20% (Asman & van Jaarsveld 1990a).
However, the greater part of the ammonia disappears into the atmosphere
close to the source so gradients of ammonia concentrations may be abrupt at
Until 1980 epiphytic nitrophytes on acid bark were largely confined to
farmyards, present in small quantities on trees surrounding dunghills. There
was no indication that gaseous ammonia was important for their occurrence,
only the direct influence of dung was apparent. At the end of the 1970s most
farmers switched over from a heavy solid straw-mixed product to liquid
manure. This switch might be an important cause of the observed changes, as
already suggested by Benfield (1994).
A few studies on bark chemistry demonstrate that the effects of ammonia on
nitrophytes are not primarily caused by the increased availability of nitrogen
van Dobben 1988; van Herk 1990). More important is the rise
in bark pH, caused by the adsorption of NH3. In areas with a high cattle
density the pH of the Common Oak
pH 4-5, can
rise to c. 6-5. At pH 6-5 most acidophytes are replaced by nitrophytes. The
term, ' nitrophytic ' assumes that such species require some form of nitrogen.
However, a high pH seems to be a more direct reason for their occurrence. A
better name should be ' neutrophytic ' but this name is already used for
another ecological group. Real neutrophytic lichens (indifferent species), for
example most Parmelia and Ramalina species seem not to be affected
significantly by ammonia, although a slight positive reaction on ammonia
might be possible.
The Netherlands is one of the most polluted parts of Europe with respect to
ammonia. Ammonia is especially a huge problem in regions with acid sandy
In large areas of the Netherlands the emission values exceed 10 000 kg
(Asman & van Jaarsveld 1990a). Surprisingly ammonia
contributes to about 45% of the total acidification in the Netherlands.
Although ammonia is not acid in
nitrification transforms most of the
* NIW 4-5
1. Spatial patterns in a hypothetical area with four livestock farms. A. Topography; B. Quantity of nitrophytes (NIW) on trees (all
C. Reconstruction of ammonia pollution isolines based on nitrophytes.
Lecanora dispersa (incl. L. hageni)
2. Schematic reaction of several nitrophytic species to ammonia pollution in the Netherlands based on
The degree of pollution at which a species appears is called the threshold. Most of the
species become more common at a higher ammonia pollution.
1999 Ammonia pollution in the Netherlands—van Herk 13
ammonia into nitric acid (HNO3) after deposition. As far as is known, this
process only takes place in the soil, not on the bark of trees (van Dobben
Not all emitted ammonia appears to be deposited unchanged.
Some ammonia reacts in the atmosphere with acids, leading to the deposition
of, for example, ammonium sulphate [(NH4)2SO4], thus part of the emitted
ammonia will be transformed into ammonium (NH4+).
Regional ammonia and ammonium concentration and deposition calcu-
lations are available by means of mathematical models based on cattle density
(Asman & Jaarsveld 19906). Figure 3A, B shows the ammonia and ammo-
nium concentrations based on these calculations. Real measurements of
ammonia and ammonium are only acquired at a limited number of stations
because the costs are very high.
To fill a gap in our knowledge of ammonia pollution, most of
authorities charged with reducing their pollution have taken the initiative to
map parts of their territory using
From 1989 onwards every year a part
of Holland has been mapped using nitrophytes and acidophytes. This
information is now used to take measures; for example, state-aided removal of
livestock farms from the surroundings of nature reserves.
Materials and Methods
The imponant role of bark pH as an intermediate factor requires that the effects of ammonia are
mapped with only one tree species, preferably one with acid bark. Therefore only
used. A limited area (province of Utrecht) has been mapped with several different tree species in
order to investigate the effect of the tree species used. Some tree species have been compared by
means of regression analyses (Table 1).
At the moment about 5500 sampling sites, each consisting often trees, have been investigated,
on average one site per 4 km2, covering about half of the Netherlands (Fig. 4). Sampling sites are
at least at a 100 m distance from a livestock farm. Only straight and exposed trees, without low
branches or shrubs in front, are used. Usually wayside trees are suitable. During subsequent years
additional regions will be mapped. Although all epiphytic lichens have been examined, only
selected results on nitrophytes and acidophytes are considered here.
To achieve the mapping an integrated parameter was designed, the NIW (' Nitrofiele Indicatie
Waarde '). The NIW is defined as the mean number of nitrophytes found on the bark of one
Species covering more than
dm2 count as double. The following species are considered
to be nitrophytes: Caloplaca citrina, C. holocarpa, Candelariella aurella, C. reflexa, C. vitellina,
C. xanthostigma, Lecanora muralis, L dispersa s. lat. (inc. L. hageni), Phaeophyscia orbicularis,
nigricans, Physcia adscendens, P. caesta, P. dubia, P. tenetta, Rinodina gennarii, Xanthoria
X. parietina and X. polycarpa. Note that common species present on all
trees add much more to the NIW (2 points) than species present in small numbers on one out of
ten trees only (0-1 point), thus quantity is an important element in the NIW. All common
nitrophytes are used; only a few nitrophytes for which interference with sulphur dioxide is
have been omitted.
The above calculation has also been carried out with acidophytes, mainly to investigate whether
acidophytes reveal matching results. The species united into the AIW (' Acidofiele Indicatie
Waarde ') are Cetraria chlorophytta, Chaenotheca ferruginea, Cladonia (all species taken together),
Evemia prunastri, Hypocenomyce scalaris, Hypogymnia physodes, H. tubulosa, Lecanora aitema, L.
L. pulicans, Lepraria incana
ambigua, Placynthidla icmalea, Platismatia glauca, Pseudevemia furfuracea, Trapeliopsis flexuosa,
(all species taken together). At all sites the NIW and AIW have been
calculated and both NIW and AIW have been used to produce detailed maps by means of linear
To investigate statistical significance, the NIW was related by means of multiple regression to
several abiotic parameters,
ammonia air concentration, ammonium air concentration, sulphur
isolines 2.0 6.0 10.0 14.0 18.0isolines3.0 4.0 5.0 6.0 7.0
3. Ammon,a (A) and ammonium (B) ah' concentrate in the Netherlands in 1988 (,gm
[source: National Institute of Public
Health and Environmental Protection (RIVM)].<
the Netherlands—van Herk 15
Nitrofiele Indicate Waaide
Netherlands derived from
Quercus robur (NIW).
concentration, the structure
the landscape, distance from livestock farms, distance
from maize fields, the girth
the geographical position
nitrophytes. Both tree species yield
500 mol ha~
Furthermore, with both tree species there
There was insufficient data from
but the explained variance
only small, which means that factors other than
ammonia might dominate
16THE LICHENOLOGISTVol. 31
1. Calculated linear
for the abundance of
(NIW) on Quercus robur and
Populus x canadensis against ammonia (NHJ deposition values (after van Herk 1996)*
Linear model: Y = a+bXExplained variance Degrees of freedom Probability level
= - 2-1 x 0-0020 NH,
= - 1-5 x 0-0028 NH,
*Dependent variables: Nitrofiele Indicatie Waarde with Quercus robur (NIW
) and Nitrofiele
Indicatie Waarde with Populus x canadensis (NIW
). Independent variable: ammonia deposition
with the abundance of
on Quercus robur (NIW) as
variable and nine
parameters as independent variables (after van Herk 1995)*
Girth of trees
Not in model
*A total of 2349 sampling sites throughout the Netherlands were analysed. A variable enters the
model when F-Enter is at least 4-00 (corresponds to /><0-05). The contribution of the variables
on the left-hand side ('in model') is significant (.P<0-05). No significant contribution to the
model could be proved for the variables on the right-hand side (' not in model'). Dependent
Nitrofiele Indicatie Waarde (NIW). Explained variance
47-l%, degrees of free-
^Explanation of variables:
mean ammonia (NH
) air concentration per 5x5 km
(ug . m~
) [taken from the
National Institute of Public Health and Environmental Protection (RIVM)];
mean ammonium (NH
) air concentration per 5x5 km
(|ig . m~
) (taken from
girth 0/wees=girth of the sampled trees (dm);
roughness ' of the landscape, parameter to express to what rate the landscape causes
turbulence and dilution (taken from RIVM);
maize fields=presence of maize fields in the surroundings (—m distance);
farms=presence of livestock farms in the surroundings (—m distance);
sulphur dioxide=mean SO
air concentration per 5x5 km
(n . m~
) (taken from RIVM);
X-co-ordinate/Y-co-ordinate=^West-Rast/l>lorth-So\ith position in the Netherlands.
Other calculations (Table 2) make clear that Q. robur is very useful
for mapping ammonia. Unfortunately, Q.
is absent or sparse in the
western part of the Netherlands. Investigations are being carried out to
is an appropriate alternative in areas where
Figure 4 shows the abundance of nitrophytes in the area mapped so far.
Detailed patterns of NIW are notable; areas with high and low values are
situated close to each other. The overall similarity of the spatial patterns of
NIW and the ammonia air concentration (Fig. 3A) is striking. There is not
only a good correspondence concerning the polluted areas (e.g. Gelderse
1999 Ammonia pollution in the Netherlands—van Herk 17
Vallei) and the cleaner areas (e.g. Drenthe). The size and position of the
smaller polluted regions like Friese Wouden and Kempen is also clearly
visible. It was not attempted to map individual livestock farms, although
clusters of big farms are often visible in Fig. 4. The pattern derived from the
lichen composition (Fig. 4) is obviously much more detailed than the pattern
calculated using cattle density (Fig. 3A). Therefore, the lichen method is
much more informative.
The similarity between the NIW and the ammonium air concentration
(Fig. 3B) is only slight. Multiple regression confirms this. The ammonia air
concentration contributes considerably to the explained variance of the NIW,
but the contribution of the ammonium air concentration is not significant
(Table 2). The explanation is that ammonium has no effect on bark pH. Thus,
only the effects of ammonia are visible with nitrophytes because ammonia
gives rise to an increase in the pH. The increased nitrogen availability caused
by ammonium apparently has no effect on the occurrence of nitrophytes, as
already concluded in connection with bark chemistry. Neither has nitrogen
oxide (NOX), emitted mainly by traffic, any effect on the occurrence of
nitrophytes (statistical calculation not presented).
The presence of livestock farms in the surroundings adds considerably to
the variance (Table 2). Both parameters ' ammonia ' and ' livestock farms ' are
good for 43% explained variance. The remaining four variables with a
significant contribution in Table 2 add only 4%.
Maize fields are usually spread heavily with slurry. The presence of
maize fields, however, has only a slight effect on the presence of nitrophytes
(Table 2). Perhaps only sources of ammonia with a continuous character have
a clear effect, as maize fields are spread with slurry only once or twice a year.
More important is the structure of the landscape. Very open ' windy'
landscapes with only exposed trees yield more nitrophytes than landscapes
with many hedges, bushes and ' hidden ' rows of trees. In the last case the
ammonia is probably spread over a lot of objects resulting in a dilution effect.
An important cause of interference is the age of the trees. The NIW appears
to be higher on young (slender) trees (see below). Nitrophytes (NIW) and
acidophytes (AIW) appear to have oppositing behaviour (r=
Thus, on trees with high NIW values, AIW values are usually low
and vice versa.
There are also other differences in behaviour between nitrophytes and
acidophytes. Multiple regression shows that acidophytes are sensitive to both
ammonia and ammonium (whereas nitrophytes react only to ammonia). This
phenomenon is confirmed by field observations. At a lot of stations acido-
phytes (e.g. Hypogymnia physodes and Pseudevernia furfuracea) have disap-
peared on a large scale without any or only a small increase of nitrophytes.
This is especially the case at some distance from the well-known areas with a
high cattle density. (Fig. 3A) but within the areas for which a high ammonium
deposition is calculated (Fig. 3B). This suggests that (at least some) acido-
phytes are not only sensitive to a rise of the pH, but also sensitive to an
increase in the ammonium content of the bark. Competition with other
lichens, for instance increasing nitrophytes, is in most cases not an important
reason for their disappearance.
18 THE LICHENOLOGIST Vol.31
The abundance of epiphytic nitrophytes can be used effectively to map spatial
patterns of ammonia pollution. Lichens have the advantage that very detailed
maps can be produced at relatively low costs. Only (expensive) direct
measurement of the ammonia air concentration reveals comparable detailed
information. At this moment permanent measurements are carried out at
about 100 lichen monitoring stations by a Dutch institute for technical
research (TNO). For this purpose special measuring tubes were developed,
which can be suspended from a monitored tree. Once a month these tubes
are collected and the mean ammonia concentration during the preceding
month can be calculated. In the near future a comparison between lichen
composition and these ammonia air concentrations will be carried out. These
calculations are important for a further validation of the detailed patterns of
ammonia pollution observed with nitrophytic lichens (Fig. 4).
In other countries, on other substrata, or under other circumstances the
occurrence of nitrophytes may be less obviously linked to nitrogenous
emissions. The way in which nitrophytes react to the pH of the substratum
means that the observations cannot be compared with the straight reaction of
lichens to SO2. Interference from other factors, which might even be dominant
must be considered. To avoid interference it is important to consider the
influence of other factors such as climate, dust, the age of the trees, other
pollutants, dogs, bark wounds, and salt spray. Each of
will be discussed.
Climate is considered to be an important interfering factor. Within the
Netherlands a slight shift in climatic conditions is evident, from dry in the
South and East to slightly wetter near the coast and in the North. Some species
are more drought resistant (Xanthoria parietina, Physcia adscendens), whereas
other species are slightly more common in areas with higher precipitation
Within the area studied the effect of the climate as
a whole is probably negligible on the NIW. However a slight shift along
the Y-co-ordinate is apparent (Table 2), which might be due to climatic
Epiphytic nitrophytes also occur on the base of trees on calcareous soils,
especially under dusty circumstances. As most of the soils in the Netherlands
are non-calcareous and oligotrophic, dust is probably only a minor cause of
interference in the area studied. In countries with a very dry climate, drought
and dust might be dominant factors, preventing the use of nitrophytes as
indicators of ammonia pollution.
The age of the trees investigated appears to be important. Multiple
regression shows that on old trees fewer nitrophytes occur than on young trees
with the same NH3 pollution (Table 2). On young trees the NIW is about 0-7
NIW unit higher than on old
To avoid interference, trees with only slight
differences in age should be compared.
Nitrophytes are also common on trees polluted by dogs. In built-up areas it
is sometimes difficult to find ' clean ' trees. A practical solution might be not
to use the base of trees since such pollution generally reaches no higher than
50 cm. Near bark wounds nitrophytes are also common, especially on
and Fagus. Trees with bark wounds should be avoided.
1999 Ammonia pollution in the Netherlands—van Herk 19
However, on Q.
usually very few nitrophytes are to be found near bark
wounds. Finally, salt spray causes some influence in coastal areas, but the
effects seem to be restricted to a few kilometres along the coast.
Table 2 shows that there appears to be no effect of
on the NIW: in areas
with a high SO2 concentration there is no ' deficit' of
If the (not
significant) effect is calculated in a regression equation, the effect appears to be
only 0-01 unit, thus negligible. It is surprising that SO2 levels have no effect
on the spatial pattern of nitrophytes on oaks (NIWQu) in the Netherlands.
At the moment the SO2 level is very low; even in the most polluted areas
the concentration now rarely exceeds 30
3. It is likely that SO2 is not
limiting the occurrence of common nitrophytes any more. Furthermore no
effect of SO2 on the pH of the bark of Q.
could be traced (van Herk
Even trees in the centre of cities with only
appeared to have the same pH as trees in large woods with lush
pH 3-9). Only the effect of ammonia on the pH is apparent. However, the pH
of tree species with neutral bark may be influenced by SO2 levels. A
calculation carried out with
shows that this indeed seems to be the
Multiple regression with SO2 and NH3 on NIWPo shows a just
significant (but not dominant) effect of SO2 (van Herk 1997).
A sensitivity scale based on separate species has not been used to estimate
ammonia pollution, although clear differences in the species response exist
(Fig. 2). It is obvious that in the area studied the total quantity of nitrophytes
and acidophytes (NIW and AIW) at sampling sites are useful and sufficient
indicators. The use of separate species as indicators of pollution zones has the
disadvantage that a shift in response of a single species can disrupt the scale
Such a shift could be caused by spatial differences of other pollutants,
the climate or the ecology, as stated for X. parietina in connection with
I am grateful to Dr A. Aptroot and L. Spier for discussions on this subject and useful comments
on the manuscript. Furthermore, I am grateful to the provincial administrations of Groningen,
Friesland, Drenthe, Overijssel, Gelderland, Utrecht and Noord-Brabant for making this research
possible and giving me the opportunity to publish this paper.
Aptroot, A. (1989) Veranderingen in de epifytenflora van de Provincie Utrecht over de periode
1984-1989. Utrecht: Provincie Utrecht.
Aptroot, A. & van Herk, C. M. (1998) Lecanora barkmaneana, a new nitrophilous sorediate
corticolous lichen from The Netherlands. Lichenologist 31: 3-8.
Asman, W. A. H. & van Jaarsveld, J. A. (1990a) Gedrag van atmosferisch ammoniak.
Symposium Dierlijke Mest:
Den Haag: K. N. C. V.
Asman, W. A. H. & van Jaarsveld, J. A. (19906) A Variable-Resolution Statistical Transport Model
Applied for Ammonia and Ammonium. RIVM report no. 228471007. Bilthoven.
Barkman, J. J. (1958)
of Crypwgamic Epiphytes. Assen: Van Gorcum.
Benfield, B. (1994) Impact of agriculture on epiphytic lichens at Plymtree, East Devon.
de Bakker, A. J. (1987) Verslag van de herinventarisatie van Noord-Brabant en Limburg op
epifytische lichenen in 1986. Buxbaumiella 20: 36-39.
de Bakker, A. J. (1989) Monitoring van epifytische korstmossen in 1988. RIN-rapport 89/14:
1-53. Leersum: Rijksinstituut voor Natuurbeheer.
20 THE LICHENOLOGIST Vol. 31
de Bakker, A. J. & van Dobben, H. F. (1988) Effecten van ammoniakemissie op epifytische
korstmossen, een correlatief onderzoek inde Peel. RIN-rapport 88/35: 1-48. Leersum:
Rijksinstituut voor Natuurbeheer.
de Wit, T. (1976) Epiphytic lichens and air pollution in The Netherlands.
Hoffmann, M. (1993) Verspreiding, Fytosociologie en Ecologie van Epifyten en Epifytengemeen-
schappen in Oost- en West-Vlaanderen. Proefschrift Universiteit Gent,
van Dijk, H. W. J. (1988) Epifytische Kortstmossen, zure Regen en Ammoniak. Zwolle: Provincie
van Dobben, H. F. (1991) Monitoring van epifytische korstmossen in 1989. RIN-rapport 91/8:
1-62. Leersum: Rijksinstituut voor Natuurbeheer.
van Dobben, H. F. (1993) Vegetation as a monitor for
and acidity. Proefschrift
van Dobben, H. F. & Wamelink, W. (1992) Effects of atmospheric chemistry and bark chemistry
on epiphitic lichen vegetation in The Netherlands. RIN-rapport 92/23: 1-34. Wageningen:
Instituut voor Bos- en Natuuronderzoek.
van Herk, C. M. (1990) Epifytische Korstmossen in de Provincies Drenthe,
Zwolle: Provincie Overijssel.
van Herk, C. M. (1991) Korstmossen als Indicator voor zure Depositie, Basisrapport. Arnhem:
van Herk, C. M. (1993) Korstmossen en zure
in Drenthe en Friesland. Assen/Leeuwarden:
Provincie Drenthe & Provincie Friesland.
van Herk, C. M. (1995) Korstmossen en ammoniak. Buxbaumiella 36: 43-49.
van Herk, C. M. (1996) Monitoring van Ammoniak en Zwaveldioxide met
Utrecht. Soest: LON by order of Provincie Utrecht,
van Herk, C. M. (1997) Monitoring van Ammoniak met Korstmossen in Zeeland. Soest: LON by
order of Provincie Zeeland.
van Herk, C. M. & Aptroot, A. (1996) Epifytische korstmossen komen weer terug. Natura 93:
van der Knaap, W. O. (1984) Epifyten in de provincie Utrecht 1979-1984. Buxbaumiella 16:
Accepted for publication 16 January 1998