Further evidence of the effects of global warming on lichens, particularly those with Trentepohlia phycobionts

Article · April 2007with249 Reads
DOI: 10.1016/j.envpol.2006.03.018 · Source: PubMed
Abstract
Increasing evidence suggests that lichens are responding to climate change in Western Europe. More epiphytic species appear to be increasing, rather than declining, as a result of global warming. Many terricolous species, in contrast, are declining. Changes to epiphytic floras are markedly more rapid in formerly heavily polluted, generally built-up or open rural areas, as compared to forested regions. Both the distribution (southern) and ecology (warmth-loving) of the newly established or increasing species seem to be determined by global warming. Epiphytic temperate to boreo-montane species appear to be relatively unaffected. Vacant niches caused by other environmental changes are showing the most pronounced effects of global warming. Species most rapidly increasing in forests, although taxonomically unrelated, all contain Trentepohlia as phycobiont in addition to having a southern distribution. This suggests that in this habitat, Trentepohlia algae, rather than the different lichen symbioses, are affected by global warming.
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Further evidence of the effects of global warming on lichens,
particularly those with Trentepohlia phycobionts
A. Aptroot
a,
*
, C.M. van Herk
b
a
ABL Herbarium, G.v.d. Veenstraat 107, NL-3762 XK Soest, The Netherlands
b
Lichenologisch Onderzoeksbureau Nederland, Goudvink 47, NL-3766 WK Soest, The Netherlands
Received 15 October 2005; accepted 10 March 2006
Epiphytic and terr icolous lichens in Western Europe respond to global warming through their Trentepohlia algae.
Abstract
Increasing evidence suggests that lichens are responding to climate change in Western Europe. More epiphytic species appear to be increas-
ing, rather than declining, as a result of global warming. Many terricolous species, in contrast, are declining. Changes to epiphytic floras are
markedly more rapid in formerly heavily polluted, generally built-up or open rural areas, as compared to forested regions. Both the distribution
(southern) and ecology (warmth-loving) of the newly established or increasing species seem to be determined by global warming. Epiphytic
temperate to boreo-montane species appear to be relatively unaffected. Vacant niches caused by other environmental changes are showing
the most pronouced effects of global warming. Species most rapidly increasing in forests, although taxonomically unrelated, all contain
Trentepohlia as phycobiont in addition to having a southern distribution. This suggests that in this habitat, Trentepohlia algae, rather than
the different lichen symbioses, are affected by global warming.
Ó 2006 Elsevier Ltd. All rights reserved.
Keywords: Algae; Biomonitoring; Climate change; Europe
1. Introduction
Lichens have certain ecological and physiological require-
ments that make them very sensitive to atmospheric changes
and are thus excellent indicators of air pollution. Lichen mon-
itoring has become a widely used sta ndard to evaluate air qual-
ity and is an effective early-warning system, including the
accumulation of heavy metals and radioactivity in terrestrial
ecosystems (for a review see Nimis et al., 2002). Monitoring
has hitherto focused on air pollution effects, because most
lichens are highly sensitive to SO
2
(Hawksworth and Rose,
1970; Seaward, 1993). Classic lichen-based monitoring has
generated pollution maps showing areas largely devoid of
epiphytic lichens, the so-called lichen deserts, in and around
cities in, for example, Britain (Hawksworth and Rose, 1970),
Germany (Kirschbaum et al., 1996; Stapper and Kricke,
2004) and the Netherlands (Barkman, 1958).
In some parts of Europe, the use of lichens to monitor
environmental changes has been facilitated by the long-term
attention paid to these organisms, with data extending back
over several decades. For instance, in the Netherlands, detailed
data on the epiphytic lichen flora are available since the 1950s
(Barkman, 1958; de Wit, 1976). In recent decades, air quality
in most of Western Europe has improved as a result of socio-
economic changes and pollution abatement strategies. In par-
ticular, SO
2
levels have dramatically decreased and as a result,
a recovery of the lichen flora became apparent in the 1980s
(Hawksworth and McManus, 1989; van Dobben and de
Bakker, 1996). Although this recovery is still in progress
(van Herk and Aptroot, 1998), the regenerating lichen flora
differs from the flora that disappeared. Major shifts in commu-
nity structure are nowadays linked to changes in atmospheric
* Corresponding author. Tel.: þ31 35 6027417; fax: þ31 30 2512097.
E-mail addresses: andreaptroot@wanadoo.nl (A. Aptroot), lonsoest@wxs.
nl (C.M. van Herk).
0269-7491/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.envpol.2006.03.018
Environmental Pollution 146 (2007) 293e298
www.elsevier.com/locate/envpol
pollutant levels, especially ammonia (NH
3
)asSO
2
concentra-
tions have decreased in many areas (van Herk, 1999, 2001 ).
Changes in the epiphytic lichen flora of the Province of
Utrecht in the Netherlands appear significant for all separate
intervals (usually 5 years) of investi gation.
Many lichen species are heavily dependent on climate, of-
ten influenced by minor fluctuations. Climate change has a
profound influence on the distributions of these sensitive
organisms (Watson et al., 2004). A recent study in the Nether-
lands, based on monitoring at five-year intervals since 1979,
has identified recent major changes in epiphyte distribution
independent of pollution. Warm-temperate species have signif-
icantly increased, and species characteristic of cold environ-
ments have either decreased or disappeared (van Herk et al.,
2002). Climate change was statistically found to be the most
probable explanation for these patterns. This study, one of
the first long-term biological monitoring programmes to detect
the influence of global warming on terrestrial communities,
strongly suggests that this phenomenon has affected lichen
populations. Duly cited and used by Parmesan and Yohe
(2003) in their recent impressive meta-study, it is the only
such lichenological data set. The conclusion can thus be drawn
that lichens are among the most sensitive organisms respond-
ing to global warming. Some base-line studies have recently
been set up to specifically target the effects of climate change
on lichens (Insarov and Schroeter, 2002; Aptroot and van
Herk, 2003). This paper reports further evidence of lichen re-
sponses attributable to global warming and highlights the sig-
nificance of Trentepohlia phycobionts.
2. Data and methods
Fieldwork was carried out by the authors in four regions within the Nether-
lands, viz. the provinces of Utrecht in 1979, 1984, 1989, 1995 and 2001 (van
Herk, 2002), Zeeland in 1997, 2000 and 2003 (van Herk, 2004a), Gelderland
in 1990 and 2002 (van Herk, 2004b), and the Noordhollands Duinreservaat in
1990, 1993 and 2000 (Sparrius and Aptroot, 2001), the latter being a forested
coastal dune area NW of Amsterdam. Each monitoring site usually consisted
of ten trees of the same species, for which all lichen species were recorded per
individual tree. This method allows monitoring of species’ abundances both at
separate sites and at study areas as a whole. At each of the four study areas,
250e1500 localities are involved.
For each species, the latitudinal distribution was derived from a wide range
of lichen checklists and floras, e.g. Purvis et al. (1992) and Wirth (1995). Four
categories were distinguished:
1. predominantly pan-tropical species, often extending into (warm-) temper-
ate areas;
2. species with a warm-temperate to (sub)tropical distribution, i.e. with the
majority of the distribution well south of the Netherlands;
3. predominantly (or only) cool-temperate, often very widespread over all
vegetation zones in at least the northern hemisphere;
4. boreo-montane/arctic-alpine species, the majority distributed far north of
the Netherlands or at altitudes well above sea level, mainly in the mon-
tane and/or alpine belt.
Temperature preferences were taken from Wirth (1991) where listed. Other
species (including many new arrivals) were excluded from this analysis.
Wirth’s temperature classes 3, 4, 5, 6, 7 and 8/9 have been translated and
abbreviated into the terms ‘cold’, ‘cool’, ‘average’, ‘rather warm’, ‘warm’
and ‘very warm’, respectively.
3. Results and discussion
3.1. Epiphytic lichens on free-standing trees respond to
global warming
Most of the observed changes are very similar in all four
study areas. For example, many lichens that are increasing
in frequency are warm-temperate or subtropical. One example
is Flavoparmelia soredians, a drought-resistant, warm-temperate
species which until recently had its northernmost limit in
southern England (Seaward and Coppins, 2004). It was very
rare in the Netherlands before 1900 (only known from one
record), absent during 1900e1987, and recently became com-
mon throughout the country (van Herk and Aptroot, 1996,
2004) as well as in adjacent countries. A similar ecology
and a comparable rapid increase were observed for Punctelia
borreri (Spier and van Herk, 1997). Both species now occur
throughout the country, although not in equal abundance.
Some species, such as Lecanora confusa are clearly expand-
ing, but they are still largely confined to the relatively warm
and wet southwestern part of the country, mainly the province
of Zeeland. This species was known from only one record be-
fore 1950 and was absent during the period 1950e1990. Some
species are currently increasing that were never previously
reported from the Netherlands, e.g. Physcia tribacioides and
Heterodermia obscurata (Wolfskeel and van Herk, 2000).
Newly established lichens include many species which were
previously unknown to science.
Several epiphytic species new to science have been de-
scribed recently from the Netherlands, viz. Protoparmelia
hypotremella (Aptroot et al., 1997), Fellhanera viridisorediata
(Aptroot et al., 1998), Lecanora barkmaniana (Aptroot and
van Herk, 1999a), Bacidia neosquamulosa (Aptroot and van
Herk, 1999b), Lecanora compallens and L. sinuosa (van
Herk and Aptroot, 1999), Fellhanera ochracea (Sparrius and
Aptroot, 2000) and Bacidia adastra (Sparrius and Aptroot,
2003). These are unlikely to have been previously overlooked,
as most are now common, and tree bark has been int ensively
studied for lichens since the 1950s (Barkman, 1958; de Wit,
1976). Most of these species are currently invading various
countries in Western Europe, but their origin is unclear.
Lecanora barkmaniana was found to be common and abun-
dantly fertile in warm valleys in the Alps (Aptroot et al.,
2001), after it had been described as new to science in 1999
on the basis of many sterile and only two fertile populations
in the Netherlands. Several of the newly described species,
especially Fellhanera viridisorediata, which is described in a
predominantly tropical genus of mostly foliicolous taxa, with
up to 1998 only one extra-tropical species, have close relatives
in warm-temperate to wide-tropical regions (Lu
¨
cking et al.,
1994). Some of the new species may turn out to actually occur
in these areas.
About 10% of the more-or-less common epiphytic species
have recently decreased. Most are acidophytes with a boreo-
montane centre of distribution. For example, Tuckermannopsis
chlorophylla was so common in the 19th century that it had
a Dutch vernacular name. According to very recent fieldwork
294 A. Aptroot, C.M. van Herk / Environmental Pollution 146 (2007) 293e298
in the province of Drenthe, it continues to rapidly decline in
abundance. In this relatively cool northeastern part of the
country, the presently estimated population size on wayside
trees is only some 10% of that found in 1996. The same holds
for Platismatia glauca, which is now rapidly disappearing
from forest trees. Some of the change of these species in the
Netherlands over the last decades can definitely also be attrib-
uted to the high NH
3
levels. However, recently (after 1997)
NH
3
levels decreased, as have nitrophytes (van Herk,
2004a,b), but species like T. chlorophylla and P. glauca con-
tinue to become increasingly rare. Global warming is the
most probable explanation for this.
Of all epiphytic and terricolous lichen species in the Neth-
erlands, many more have increased rather than decreased in
abundance (137 versus 79 since 1980; 113 remained the
same), and it appears that the country is regaining its original
lichen flora, which was largely lost due to heavy air pollut ion.
However, a close examination of the changes in lichen com-
munities reveals distinct trends from the expected patterns
in response to eutrophication (NH
3
) and decreasing SO
2
concentrations alon e e.g. some pan-tropical epiphytes (e.g.
Anisomeridium polypori, Fellhanera species, P. borreri and
F. soredians) are among the fastest spreading species. For
example, the following species expanded rapidly (>5%, abso-
lute) and increasingly during the period 1995e 2001 in the
province of Utrecht (van Herk et al., 2002): Candelaria con-
color (þ24.7%), Hyperphyscia adglutinata (þ18.9%), Lecanora
barkmaniana (þ16.0%), Parmotrema chinense (þ11.8%),
Physconia grisea (þ11.8%), Lecidella scabra (þ11.6%),
Micarea micrococca (þ11.1%), B. neosquamulosa (þ10.0%),
Diploicia canescens (þ9.6%), Candelariella xanthostigma
(þ7.8%), F. viridisorediata (þ6.8%), and P. borreri (þ6.0%).
Most are warm-temperate and some are even frequent in tropi-
cal regions. Trees in parks in tropical cities (e.g. Cape Town,
Quito, Singapore, Hong Kong) are often covered with assem-
blages dominated by C. concolor and Hyperphyscia adglutinata.
Three of these species were only recently described (Aptroot
et al., 1998; Aptroot and van Herk, 1999a,b). Fewer species
decreased over the same period. These were often acidophytes,
including several boreo-montane ones. The following species
rapidly decreased: Lecanora conizaeoides (68.3%), Hypogym-
nia physodes (26.8%), Evernia prunastri (17.1%), and Plat-
ismatia glauca (7.1%).
Recorded changes in the species composition at epiphytic
monitoring sites over the last decade are shown in Fig. 1.As
can be seen from the graphs, changes in the various provinces
are comparable. In all cases, species with a warm-temperate to
tropical distribution, as well as warmth-loving species (those
with a high temperature preference value) have dramatically
increased. Cold-loving species have usually declined, but not
at the same rate as the increase in warmth-loving species. So
far, the total numbers of boreo-montane species have remained
approximately the same, despite the decline of T. chlorophylla.
Boreo-montane species have, however, always been rare in
Zeeland, in the southwestern part of the country. The graphs
suggest that global warming mainly determines from where
(southern) or what ecology (warmth-loving) the newly
established species are derived. The existing epiphytic temper-
ate to boreo-montane species (with a few exceptions) appear
not to be seriously affected, but are at the same time un able
to increas e, e.g. by occupying vacant niches. This phenome-
non might explain why the effects of global warming have
so far not been observed in natural or more-or-less stable epi-
phytic lichen communities. At least some vacant niches caused
by other environmental changes are probably required to con-
firm the influence of global warming.
3.2. Terricolous lichens respond to global warming
Drift-sand areas at terminal moraines dating from the pen-
ultimate glaciation form a unique habitat for terricolous
lichens at sea level. Vegetation here is usually dominated by
Cladonia species and has a typically boreo-alpine character.
Monitoring of these species-rich areas in the Netherlands
(Sparrius et al., 2001) has shown that these are very stable
communities, with changes in species composition occur ring
only very slowly and probably not being attributable to com-
petition. In general, the age of exposure determines the species
richness.
Nevertheless, several species are currently disappearing
from otherwise stable and well-developed drift-sand commu-
nities. No change in management is apparent, and the pattern
of the species loss is not correlated with any pattern of air pol-
lution. The single factor shared by these taxa is that they all
have a predominantly boreo-alpine distribution. Some species,
such as Cladonia rangiferina, and C. sulphurina, most proba-
bly became extinct only recently in the Netherlands. Others,
like Cetraria islandica, which was formerly rather common,
were until recently known from a dozen localities, and now
only have a few remaining populations. Another shift is shown
by Cladonia squamosa, formerly a common species in drift-
sand vegetations until ca. 1980, but disappeared completely
from that habitat and currently only grows on dead wood.
This is an unstable habitat from which it has to constantly
relocate.
3.3. Global warming effects in forests
Effects of air pollution on lichens have been up to now pre-
dominantly recorded from relatively open environments, espe-
cially from wayside trees or drift-sand areas. The same holds
true for the observed effects of global warming. Although
many lichens occur in closed habitats, especially forests, their
response to global warm ing is less pronounced. Most of the
rapidly increasing species mentioned above are absent or un-
common in forests, with the exception of Micarea micrococca
and B. neosquamulosa. However, the re-investigation in 2000
of the epip hytic lichen flora in the Noordhollands Duinreser-
vaat determined marked changes between 199 0 and 2000
(Table 1). Some newly described species, including Fellhanera
ochracea and F. viridisorediata, were found, but only
infrequently. The three species most dramatically expanding
(more than 4 times) all have a southern distribution, and also
share another character, namely they all contain the alga
295A. Aptroot, C.M. van Herk / Environmental Pollution 146 (2007) 293e298
Trentepohlia as photobiont. In fact, all lichens containing
Trentepohlia occurring in the area have increased in abun-
dance. Increases in lichen abundance can be attributed to a rel-
atively few species containing Trentepohlia. This suggests
global warming may have affected Trentepohlia directly rather
than the fungal components. This phenomenon has also been
recently observed in other areas of the Netherlands and in
adjacent Germany (N. Stapper, personal communication).
3.4. Global warming and lichens in adjacent countries
The examples given above were all from the Netherlands,
where because of intensive lichen monitoring considerable
data are available and already evaluated. However, if the
changes are indeed at least in part attributable to global warm-
ing, similar changes are to be expected in other countries. In-
deed, increasingly such changes are being reported, although
not yet at such a large scale. An example is in England, where
changes possibly attributable to global warming have been
reported in the lichen flora of the formerly heavily polluted
regions (Seaward and Coppins, 2004). For instance, in Kew
Gardens in London, where 20 years ago only one epiphytic
lichen (Lecanora conizaeoides) survived, over 40 species can
now be observed, including thermophilous species like
F. soredians and P. borreri, and of the recently described spe-
cies Bacidia adastra, B. neosquamulosa and Lecanora com-
pallens (Aptroot, 2005). In Denmark, the first signs of global
warming effects on lichen distribution have been recently re-
ported (Søchting, 2004). Th e situation in the adjacent parts
of Belgium (van den Broeck and Aptroot, 2003; van den
Broeck et al., 2005) and Germany ( de Bruyn et al., 2005) is,
not surprisingly, also very similar. Chan ges (including the
occurrences of the recently described species) can at least be
observed in a wide lowland belt ranging from England through
0
10
20
30
40
50
60
70
80
90
100
1997 2000 2003
percentage
0
10
20
30
40
50
60
70
80
90
100
percentage
0
10
20
30
40
50
60
70
80
90
100
percentage
cold %
cool %
average %
rather warm %
warm %
very warm %
1979 1984 1989 1995 2001
1990 2002
0
2
4
6
8
10
12
14
16
1997 2000 2003
number of species / sitenumber of species / site
boreo-montane
cool-temperate
warm-temperate
tropical
0
2
4
6
8
10
12
14
16
18
20
1979 1984 1989 1995 2001
A
B
D
number of species / site
0
2
4
6
8
10
12
14
16
18
20
F
C
E
1990 2002
Fig. 1. (A, C, E) Temperature preferences according to Wirth (1991) of epiphytic lichens in the given years at monitoring sites in the provinces of (A) Zeeland, (C)
Utrecht and (E) Gelderland. The total number of species for which a temperature preference is known is given as 100%. The respective number of sites and the
number of species involved per province is for Zeeland: sites ¼ 225, species ¼ 135; Utrecht: sites ¼ 950, species ¼ 178; Gelderland: sites ¼ 715, species ¼ 160. (B,
D, F) Main distribution areas of epiphytic lichens in the given years at monitoring sites in the provinces of (B) Zeeland, (D) Utrecht and (F) Gelderland. The
number is the average number of species at a monitoring site.
296 A. Aptroot, C.M. van Herk / Environmental Pollution 146 (2007) 293e298
to the border between Germany and Poland (Aptroot, in press)
and even further along the Baltic Sea into Estonia (Aptroot
et al., 2005). On the other hand, few, if any, changes in the li-
chen flora attributable to global warming have been noted in
areas that are either more moun tainous (e.g. the Vosges, the
Alps, most of Scandinavia) and/or experienced fewer losses
due to air pollution in the past (e.g. the Eifel, Scotland, Wales).
Similar effects have also been observed on bryophytes in
Germany (Frahm and Klaus, 2001) and elsewhere (Gignac,
2001).
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Table 1
Comparison between 1990 and 2000 of identical epiphytic monitoring sites in
the Noordhollands Duinreservaat
1990 2000
Species that increased over 4 times
Anisomeridium polypori 152
Arthonia spadicea 17 83
Gyalideopsis anastomosans 111
Remaining species with Trentepohlia
Arthonia radiata 23
Dimerella pineti 64 95
Enterographa crassa 11
Graphis scripta 34
Opegrapha species 5 17
Porina aenea 16 25
Schismatomma decolorans 35
Change
Total of lichens with Trentepohlia 113 296 þ186
Total of all lichen occurrences 3586 3765 þ189
Listed are the species that increased over four times, and the remaining species
with Trentepohlia as photobiont. The numbers are the number of monitoring
sites with the respective species.
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    • Climate changes, atmospheric pollution, green areas fragmentation, and other environmental changes may also affect lichen communities, due to the physiological response of each individual. Such changes have been directly influencing lichens over the years, changing their habitats or the interaction of each specimen with other organisms (Insarov & Schroeter 2002, Aptroot & Van Herk 2007, Käffer et al. 2011). In Brazil, few studies relate lichen community structure to host tree structure, and the existing ones are restricted to non-urban areas (Marcelli 1992, Cáceres et al. 2008, Fleig & Grüninger 2008, Käffer et al. 2009, Martins & Marcelli 2011).
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    Full-text · Article · May 2016 · Plant Disease
    • Batı Avrupa'da küresel ısınmaya cevap olarak epifitik likenlerde artış gözlenirken buna karşılık terrikollerde ise azalma kaydedilmiştir. Kirlilliğin etkisindeki bölgelerde ormanlara oranla daha hızlı bir değişimle, Trentepohlia alg bileşenli ve güney yayılışlı liken türlerinde bolca artış rapor edilmiştir [98]. İsviçre'de sıcaklık artışlarının belirginleştiği, SO 2 'in azalmasına karşılık NH 3 'ün arttığı yıllarda (1989199019911992199319941995) yapılan çalışmada [99], liken florasında 22 yılda meydana gelen değişimler incelenmiş ve sub-tropikal türlerde büyük yükseliş olurken (%83), arktik-alpin/boreal türlerde ise %50 oranda düşüş görüldüğü tespit edilmiştir.
    Article · Dec 2015 · Plant Disease
    • Lichens can be saxicolous, i.e. growing on rocks, terricolous, i.e. on soil, muscicolous or hepaticolous on bryophytes, foliicolous on the surface of living leaves, and corticolous on the bark of trees, which is the majority of epiphytic species. Substrate features and abiotic factors have been shown to influence the distribution and occurrence of lichen species (Purvis 2000; Aptroot & Herk 2007; Dyer & Letourneau 2007; Käffer et al. 2007; Bunnell et al. 2008; Mezaka et al. 2008; Morales et al. 2009). Ecological studies on lichens in northeastern Brazil have been undertaken, first with foliicolous (Cáceres et al. 2000), and then corticolous microlichens (Cáceres et al. 2007; 2008a; b; Cavalcante 2012; Rodrigues 2012).
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    Full-text · Article · Dec 2015
    • It has recently been documented that global warming has influenced the migration of trentepohlialean algae and the tropical lichens that associate with them. A study conducted by Aptroot and vanHerk (2007)noted that a majority of the epiphytic lichens rapidly colonizing forests in Western Europe are associated with the Trentepohliales. Temperature and disease distribution.
    [Show abstract] [Hide abstract] ABSTRACT: Most plant pathologists know certain algae can be used as gelling agents in culture media. Pathologists practicing in tropical or subtropical environments also know that some algae damage plants. The five genera in the order Trentepohliales (Chlorophyta) are unique and fascinating. Among other characteristics they are subaerial, bright orange to red in color and one genus, Cephaleuros, is a plant pathogen while another, Stomatochroon, is a space parasite. Cephaleuros causes algal spot and includes 17 accepted species. Of these, 13 develop between the cuticle and the epidermis of their hosts and 4 grow intercellularly. The latter are especially damaging, causing chlorosis and branch dieback. Zoospores and gametes germinate on plant surfaces during the rainy season and probably penetrate through breaks in the host cuticle. Their filamentous growth forms thalli that produce sporangiophores and spherical gametangia the following year. Several species of Cephaleuros have a broad host range and though their damage is usually superficial it can be economically important on certain crops. Plant stress is the greatest predisposing factor to this algal disease. Management includes providing plants with sufficient moisture and nutrients, modifying cultural and harvesting practices, and planting resistant cultivars when available.
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