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Bark pH and susceptibility to toxic air pollutants as independent causes of change in epiphytic lichen composition in space and time

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The lichen composition on wayside Quercus robur in the Netherlands was related to bark properties (pH, EC, NH4+, SO42-, NO3-) and levels of air pollution (SO2 and NH3). The pH of the bark and the susceptibility to toxic substances appear to be the two major primary factors affecting epiphytic lichen composition. These factors have independent effects on the lichen composition. Most of the so-called nitrophytic species appear to have a low sensitivity to toxic effects of SO2; their only requirement being a high bark pH. An increased bark pH appears to be the primary cause of the enormous increase in nitrophytic species and the disappearance of acidophytic species over the last decade in the Netherlands. Measurements of ambient NH3 concentrations in the air show that there is a nearly linear relationship between the NH3 concentration and the abundance of nitrophytes on Quercus. The abundance of nitrophytes was not correlated with SO2 concentrations. Most of the acidophytic species appear very sensitive to NH3 since in areas with concentrations on 35 microgr. m-3 or more, all acidophytic species have disappeared. Current methods using species diversity to estimate or monitor SO2 air pollution need some modification, otherwise the air quality may be erroneously considered to be relatively good in areas with high NH3 levels.
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Lichenologist
33(5): 419-441 (2001)
doi:10.1006/lich.2001.0337, available online at http://www.idealibrary.com on
Bark pH and susceptibility to toxic air pollutants as independent
causes of changes in epiphytic lichen composition in space and
time
C. M. van HERK
Abstract: The lichen composition on wayside
Quercus robur
in the Netherlands was related to bark
properties (pH, EC, NH4+, SO42~, NO3~) and levels of air pollution (SO2 and NH3). The pH of
the bark and the susceptibility to toxic substances appear to be the two major primary factors affecting
epiphytic lichen composition. These factors have independent effects on the lichen composition.
Most of the so-called nitrophytic species appear to have a low sensitivity to toxic effects of
SO
2
;
their
only requirement being a high bark pH. An increased bark pH appears to be the primary cause of the
enormous increase in nitrophytic species and the disappearance of acidophytic species over the last
decade in the Netherlands. Measurements of ambient NH3 concentrations in air show that there is
a nearly linear relationship between the NH3 concentration and the abundance of nitrophytes on
Quercus.
The abundance of nitrophytes was not correlated with SO2 concentrations. Most of the
acidophytic species appear very sensitive to NH3 since in areas with concentrations of
35
|ig m
~
3 or
more, all acidophytic species have disappeared. Current methods using species diversity to estimate
or monitor SO2 air pollution need some modification, otherwise the air quality may be erroneously
considered to be relatively good in areas with high NH3 levels. ©
2001
The British Lichen Society
Introduction
During the last century numerous studies
have successfully used epiphytic lichens to
estimate sulphur dioxide (SO2) air pollution
levels.
Several methods were introduced,
such as de Sloover & Leblanc's (1968)
Indices of Atmospheric Purity and
Hawksworth & Rose's (1970) qualitative
scale. In recent decades, however, with
decreasing SO2 concentrations and other
factors apparently becoming more import-
ant, species diversity counts and distri-
bution patterns no longer demonstrate a
clear correlation with SO2 (Seaward 1997).
The effect of SO2 air pollution on epi-
phytic lichens is well-known and the number
of published and unpublished studies on this
C. M. van Herk: Lichenologisch Onderzoekbureau
Nederland, Goudvink 47, NL-3766 WK Soest, The
Netherlands.
0024-2829/01/050419
+ 23
$35.00/0
topic is very
large.
During the second half
of
the last century, several sensitivity scales
were introduced for a number of epiphytic
lichen species (e.g. Barkman 1958;
Hawksworth & Rose 1970; de Wit 1976).
Hawksworth & Rose related their scale to
absolute SO2 concentrations, indicating that
the toxic nature of SO2 is probably the
primary factor affecting lichen species
rather than acidified bark. Several workers
attempted to find a physiological basis for
the drastic effects of SO2 on lichens. The
sensitivity of lichen species from acid bark,
tested in the laboratory for their respiratory
responses to sulphur dioxide, appeared to
correlate well with the data on field sensi-
tivity. For species from eutrophicated bark,
however, the correlation appeared to be
poor (Baddeley
et
al.
1972; Ferry
&
Coppins
1979).
Unlike the toxic effects of
SO2,
acidity is a
natural phenomenon. It proves to be highly
© 2001 The British Lichen Society
420THE LICHENOLOGISTVol. 33
influential to species composition and is
probably the most important factor deter-
mining the natural lichen floras of tree
species (Bates & Brown 1981). Many
studies have shown a switch of lichen species
from trees with acid bark to trees with a
normally neutral bark in the presence of
increasing SO2 pollution. Harmful effects of
the acid nature of SO2 resulting in a very
acid bark with only a few lichen species have
also been reported.
A
low bark pH, however,
is not the principal reason for a poor lichen
flora because in areas with low SO2 air
pollution levels, well developed lichen com-
munities may occur at a pH of 4 or even
lower (Gauslaa 1985). Damage by SO2 to
lichen species appears to be more severe at
low pH values (Turk & Wirth 1975). In
addition to this, many acidophytic species
seem to be more susceptible to toxic effects
of SO2 than species preferring eutrophic
conditions. Gilbert (1976) described an
SO2-polluted environment with Fraxinus
trees having a very acid bark (pH 3) and only
few lichens. In the surroundings of a lime-
stone quarry the situation appeared to be
quite different due to alkaline dust. Here a
Xanthorion occurred with more than 20
species at a bark pH of more than 6. A
species-poor situation apparently occurred
only at high SO2 levels in combination with
low pH values.
More recently, ammonia (NH3) air pol-
lution caused by intensive cattle breeding
has been recognized as an important factor
affecting epiphytic lichen vegetation, first
and principally in the Netherlands (van der
Knaap 1984; de Bakker & van Dobben
1988;
van Herk 1990), but to a lesser extent
also in other European countries such as
Denmark (Sechting 1991), Italy (Nimis
et al. 1991), Spain (Berdowski & Aptroot
1991),
Belgium (Hoffmann 1993), Great
Britain (Benfield 1994; Wolseley & Pryor
1999),
Switzerland (Ruoss 1999) and
Germany (Zimmer 2000). The epiphytic
lichens of large parts of the Netherlands
have already been mapped to investigate
the effects of NH3 (van Herk 1999). Most
authors observed a positive response of ni-
trophytic species to NH3, usually combined
with a negative response of acidophytic
species.
Although a response of nitrophytic species
to ammonia air pollution may be a relatively
new and increasingly important phenom-
enon, the influence of nitrogen in general
has been known for a long time and dis-
cussed by many authors. Barkman (1958)
summarized the most important circum-
stances encouraging nitrophytic species: (1)
bark
wounds;
(2) salt spray; (3) dust; and (4)
dung from birds, cattle and dogs. Other
agricultural practices that have an impact on
lichens have been discussed by Brown
(1992).
According to Nienburg (1919) the
ammonium (NH4+) content of sources
encouraging nitrophytes is more important
than the nitrate (NO3 ~) content. As a
consequence, Rasanen (1927) suggested the
adjective 'ammoniophytic' instead of 'nitro-
phytic'. Recent measurements of bark pH,
however, suggest that the effect of airborne
ammonia on nitrophytic lichens is probably
caused by producing high pH values rather
than an increased availability of ammonium
on the bark (de Bakker
&
van Dobben 1988;
van Herk 1990). This is supported by field
observations since species that react to alka-
line dust (Gilbert 1976) are largely the same
as those now reacting positively to ammonia
(van Herk 1999), i.e., mainly Xanthorion
species.
Van Dobben & ter Braak (1999) calcu-
lated a sensitivity scale to NH3, calibrated
with abiotic data from the Dutch Air Quality
Network (Asman & van Jaarsveld 1990a).
On their scale, not only the usual
Xanthorion
species such as Xanthoria parietina and
Phaeophyscia orbicularis are recognized as
reacting to ammonia, but surprisingly the
Lecanorion carpineae species of neutral to
slightly basic bark such as Lecanora carpinea,
Lecidella
elaeochroma
and Cliostomum griffithii
yielded also very high NH3 indicator values.
These latter species are most often not
considered as nitrophytic (see for example
Wirth 1991). This seeming paradox can be
explained by hypothesizing that in the Dutch
situation nitrogen sources are not limiting
growth because there is an excess available.
In such an environment, acidity is probably
2001Causes of change in epiphytic lichen composition—van Herk 421
the limiting factor for the growth of nitro-
phytic species and the difference between
species needing nitrogen (Xanthorion) and
species tolerating nitrogen (Lecanorion
carpineae)
may not be detectable. Therefore,
the species reacting positively to ammonia
on the scale of van Dobben & ter Braak are
primarily basiphytic species.
The effect of nitrogen oxides (NOX),
mainly emitted by road traffic, on lichens
remains poorly understood. In some recent
studies an increase in nitrophytic species in
urban areas has been observed, which was
attributed to NOX. Van Dobben & ter Braak
(1999) went as far as to calculate a sensitivity
scale for NOX. However, attempts to find
correlations between lichen distribution and
NOX
concentrations may be confounded by
strong positive correlations between SO2
and NOX concentrations. Accordingly, more
fundamental work is probably necessary
to decide whether NOX encourages or is
harmful to certain lichen species.
This paper is based on a statistical treat-
ment of data on lichen community compos-
ition, chemical properties of bark, and SO2
and NH3 air pollution. Results of this work
were first described in some internal Dutch
reports (van Herk 1990, 1991). A more or
less similar approach was chosen by van
Dobben
&
Wamelink (1992) and Hoffmann
(1993).
In 1996 field measurements of NH3
became feasible and were carried out at
selected lichen monitoring sites (van Herk
1998).
This paper integrates data on bark
properties, measurements of ambient NH3
concentrations in air and long-term moni-
toring of epiphytic lichens on wayside trees.
It supplements an earlier paper in which a
mapping programme on NH3 effects was
reported (van Herk 1999). The aims of this
paper are (1) to discuss the effects of differ-
ent air pollutants on lichen composition, (2)
to find primary factors affecting the lichen
community composition, (3) to evaluate
bioindicators for NH3 proposed earlier
(NIW and AIW in van Herk 1999), and (4)
to find an explanation for observed changes
in lichen composition with time.
Multivariate analysis is used to gain an
insight into the relative influence of several
sources of air pollution and bark properties
as possible intermediate factors. Evidence
will be provided for the increasing
importance of ammonia as an air pollutant.
Materials and Methods
Lichen recording
Each monitoring site consists of 10 wayside
Quercus
robur
trees on which all lichen species were recorded.
Lichens were identified to species level where possible
using standard microscopic techniques and spot tests
for their chemistry. Nomenclature follows Aptroot
et
al.
(1999).
The following abundance scale was used: (1)
only one thallus present; (2) more thalli present on one
tree;
(3) present on 2-5 trees, less than ldm2 per tree;
(4) present on 2-5 trees, more than
1
dm2 per tree; (5)
present on 6-10 trees, less than ldm2 per tree; (6)
present on 6-10 trees, more than ldm2 per tree. From
1989 onwards approximately 6000 sites were surveyed.
The sites are widely distributed over areas with acid
sandy soils (poor in nutrients and calcium) in the
eastern parts of the Netherlands (Fig. 1A). Approxi-
mately 3500 of these sites continue to be involved
in a monitoring programme with re-assessment at
approximately 5 yearly intervals.
At each site abundance of nitrophytic species was
taken as a measure for species reacting positively to
NH3 and abundance of acidophytic species was taken as
a measure for species sensitive to NH3. Both species
groups were united into the integrated parameters,
NIW (derived from Dutch 'Nitrofiele Indicatie
Waarde') and AIW ('Acidofiele Indicatie Waarde') re-
spectively, both calculated in accordance with van Herk
(1999).
NIW and AIW are denned as the mean number
of nitrophytic and acidophytic species respectively,
found on one tree. Species covering more than 1 dm2
(class 4 and 6 on the abundance scale), however, were
counted twice (i.e. 2-0 points when present on all trees).
Thus,
common species present on all trees add much
more to NIW or AIW scores than species present in
small numbers on one out of ten trees only (i.e. 0-1
point).
The following species were considered as nitrophytes
and used to calculate the NIW:
Caloplaca
citrina,
C.
holocarpa, Candelariella aurella, C. reflexa, C. vitellina, C.
xanihostigma, Lecanora muralis, L.
dispersa
s.lat.
(incl. L.
hagenii),
Phaeophyscia orbicularis, P. nigricans, Physcia
adscendens, P. caesia, P. dubia, P. tenella, Rinodina
gennarii, Xanthoria candelaria, X. calcicola, X. parietina
and X.
polycarpa.
The species used to calculate the AIW
were Cetraria chlorophylla, Chamotheca fetruginea, Cla-
donia
spp. (all species taken together),
Evernia
prunastri,
Hypocenomyce scalaris, Hypogymnia physodes, H. tubu-
losa, Lecanora aitema, L. conizaeoides, L. pulicaris,
Le-praria incana, Ochrolechia microstictoides, Parmelia
saxatilis, Parmeliopsis ambigua, Placynthiella icmalea,
Platismatia glauca, Pseudevemia furfuracea, Trapeliopsis
flexuosa, T. granulosa and Usnea spp. (all species taken
together).
to
to
C*
c^?
H
n
33
w
§
r
o
o
on
H
FIG.
1. A, lichen survey sites with
Quercus robur
as phorophyte in the Netherlands; B, sites where bark properties were also determined; C, sites where NH3
concentrations in air were also determined.
2001Causes of change in epiphytic lichen composition—van Herk 423
Bark samples
Bark samples were collected from 76 lichen monitor-
ing sites (Fig. IB) in October 1989 from a wide range of
habitats: from areas with mainly arable land (5), from
moderately (31) to very intensively (21) used agricul-
tural areas, villages (6), towns (6) and forests (7). The
number of sites per habitat reflect its relative abun-
dance. Only standard
Quercus robur
wayside plots were
sampled and, wherever possible, only trees from ex-
posed and well-illuminated sites. Within these restric-
tions,
the sampled sites were selected at random in the
area mapped for lichens in 1989 (van Herk 1990).
Bark slices
c.
3 mm thick were taken from the south-
west side of the trunk of all 10 trees at a height of 1-5 m
(c.
20
g
bark in total per
site).
Sampling was undertaken
under dry, uniform weather conditions over a period of
four days and each sample was stored in a separate
plastic bag. In the laboratory the samples were dried at
20°C for
two
weeks, then ground with knife and grinder
to <3 mm and 5-00 g of each suspended in 50 ml
distilled water. The suspensions were shaken for one
hour, left to stand for one day, then shaken again for
one hour and centrifuged. The supernatant was ana-
lysed for electrical conductivity (EC) and pH using
appropriate digital measuring instruments with plati-
num and glass electrodes, respectively. Soluble NH4+,
SO
42