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Changes in the Epiphytic Flora on Four Tilia Trees in Belgium Over59 YearsAuthor(s): André AptrootSource: Herzogia, 25(1):39-45. 2010.Published By: Bryological and Lichenological Association for Central EuropeDOI: http://dx.doi.org/10.13158/heia.25.1.2010.39URL: http://www.bioone.org/doi/full/10.13158/heia.25.1.2010.39

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Herzogia 25 (1), 2012: 39 – 45 39

Changes in the epiphytic flora on four Tilia trees in Belgium over 59 years

André Aptroot

Abstract: Aptroot, A. 2012. Changes in the epiphytic flora on four Tilia trees in Belgium over 59 years. – Herzogia 25: 39 – 45.The epiphytes on four Tilia trees in southern Belgium, which were studied by Barkman in 1952, were re-investigated in 1999 and 2011. In 1952, 19 species of epiphytes (including 12 lichen species) were recorded; in 1999, there were 65 epiphyte species (including 49 lichens), and in 2011, 53 epiphyte species (including 41 lichens) were found. The enor-mous increase in species between 1952 and 1999 is primarily attributable to colonization by additional species, which is an early stage of natural succession, whereas the reduction in species between 1999 and 2011 is most probably due to competition, the next step in the natural succession, when larger mosses and foliose lichens became dominant over crustose lichens and the whole bark surface had been covered by epiphytes. Global warming also may have influenced the species composition in the last decades.

Zusammenfassung: Aptroot, A. 2012. Veränderungen der epiphytischen Flora von vier Linden in Belgien innerhalb von 59 Jahren. – Herzogia 25: 39 – 45.Die Epiphyten von vier Linden in Südbelgien, die 1952 von Barkman untersucht wurden, wurden 1999 und 2011 erneut erfasst. 1952 wurden 19 Epiphytenarten (darunter 12 Flechtenarten) nachgewiesen; 1999 waren es 65 Epiphytenarten (darunter 49 Flechtenarten) und 2011 53 Epihytenarten (darunter 41 Flechtenarten). Der starke Anstieg an Flechtenarten zwischen 1952 und 1999 kann vor allem durch die Besiedlung durch zusätzliche Arten, eine frühe Phase der natürlichen Sukzession, erklärt werden. Der Artenverlust zwischen 1999 und 2011 ist höchstwahr-scheinlich auf Konkurrenz, den nächsten Schritt in der natürlichen Sukzession, zurückzuführen, da große Laubmoose sowie Blatt- und Strauchflechten die Krustenflechten verdrängen und nunmehr die gesamte Borkenoberfläche von Epiphyten besiedelt ist. Die globale Klimaerwärmung mag einen zusätzlichen Einfluss auf die Artenzusammensetzung in den letzten Jahrzehnten ausgeübt haben.

Key words: Lichens, bryophytes, succession, colonization, competition, long-term monitoring, global warming, air pollution.

IntroductionEpiphytic lichens have been in use as biological monitors for air pollution effects for over a century, leading to a vast body of literature. However, only rarely are individual trees monitored for any prolonged time. It was therefore a pleasant surprise to find that a group of four roadside Tilia trees, from which Barkman (1958) recorded the epiphytic vegetation in 1952, is still standing in an es-sentially unchanged habitat in southern Belgium (Fig. 1A). The opportunity presented itself to make a detailed comparison with the situation of nearly 60 years ago. This small case study is the first re-port on a re-investigation of a lichen-dominated epiphytic vegetation on trees outside a forest span-ning more than 50 years. Previous reports on long-term monitoring of epiphytic lichens only rarely span more than 20 years. Examples include 22 years (van Herk et al. 2002), 25 years (Stapper & Aptroot 2012), 29 years (Will-Wolf et al. 2010) and 35 years (Kirschbaum et al. 2006).

40 Herzogia 25 (1), 2012

Materials and methodsThe four investigated Tilia trees are old landmark trees near a small statue halfway between Nismes and Olloy-sur-Viroin in the Thierache in southern Belgium (50°5'N/5°35'E), close to the border with France. Barkman recorded the epiphytes on these trees on June 6th, 1952 and published them in 1958 as relevée 7 in his Table XLV of the Physcietum ascendentis, with some additional taxa mentioned in Barkman (1958: 571–572). The location of the present study site is not given in the main publication on the data (Barkman 1958), but was found in a mimeographed document (produced in at most a dozen copies) which the author received from Barkman on a visit to him in 1978. In 1952, Barkman investigated the exposed sides of all trees, with a total surface of 160 dm2. On May 5th, 1999, the author investigated the whole lower trunk of the same trees. On June 16th, 2011, the whole lower trunk of these trees was investigated by the author for the second time. In all cases, all known epiphytic lichens, bryophytes and some conspicuous non-lichenized ascomycetes and algae were recorded. Taxonomy and nomenclature follows Smith et al. (2009) for lichens and Siebel & During (2006) for bryophytes.

ResultsIn total, 19 epiphytes, including 12 lichen species, were recorded in 1952. In contrast, 65 epi-phytes, including 49 lichens, were present in 1999, whereas 53 species, including 41 lichens, were found in 2011 (Table 1). The species found in 1999 included all species found in 1952, except for Physcia aipolia, which is a pioneer species indeed. Two species, viz. Lecanora laevis and Peridiothelia fuliguncta, were found both in 1952 and in 1999, but vanished afterwards. Both are characteristic of smooth bark.

DiscussionThere is a whole variety of reasons why the monitoring of epiphytes on individual trees rarely surmounts a few decades: – trees are cut for old age (especially fast-senescing tree species like Populus and Salix), – trees are cut for diseases (especially Ulmus), – trees are cut for road improvement or urban development,

– trees cannot be exactly refound (especially if only an unmarked proportion of a row of trees was sampled),

– the scope and the aim of the research changes, requiring other sample trees. There is some question about the comparability of the data from 1952, 1999 and 2011, as the scope of Barkman’s study was different from that of the present study. Barkman wanted to docu-ment a representative relevée of a community and was not aiming at a complete list of species on the four trees. It is likely that the tree base was included in all years, as one of the rare and prominent species recorded in all years, Caloplaca pyracea, was in 1999 and 2011 only present on one tree base. It is however possible that it occurred higher up the trunk in 1952. The sheltered side of the trees was not included in Barkman’s relevée, as he considered that the species assem-blage there belongs to a different community. While making the 1999 and 2011 investigations, special attention was therefore paid to the exposition of the various species. Only one species, Chaenotheca ferruginea, was only present at the sheltered side of the trees, and is absent from the 1952 records. However, this species is very probably new to the trees, as it has been rapidly increasing during the past decennia and only recently started to occur outside forested areas. The

Aptroot: Changes in the epiphytic flora on four Tilia trees in Belgium over 59 years 41

Fig. 1: The studied trees. A – Aspect of the trees fom the SW; at the right the SW tree, left the NE tree, extreme left hanging branches of the NW tree. B – Detail of the NW tree with Frullania dilatata (dark), Punctelia subrudecta (grey) and Lecanora compallens (pale). C – Detail of the NE tree with Radula complanata (dark), Anaptychia ciliaris (grey) and Pertusaria albescens (white). D – Detail of the base region of the SW tree with Leucodon sciuroides (dark) and Caloplaca pyracea (pale). E – Detail of the SE tree with Orthotrichum lyellii (dark), Homolathecium sericeum (slightly paler) and Parmelina tiliacea (pale).

location of the trees is beyond doubt. The studied surface area on the trees has increased some-what as the trees grew. The age of the trees is unknown, but in 1952 they were already mature trees, because otherwise they would have been noted as young trees in the remarks to the relevée. In 2011, the trees were still healthy and not senescent.

The overall epiphytic community in 1999 and in 2011 can still be classified as belonging to the Physcietum ascendentis in the sense of Barkman (1958), albeit a much species-richer represen-tation. In fact, all four trees contain a somewhat different species composition: The NW tree (Fig. 1B) has much Frullania dilatata and contains Lecanora compallens. The NE tree (Fig. 1C) has much Anaptychia ciliaris (present since 1952) and Porella platyphylla. The SW tree (Fig. 1D) has Leucodon sciuroides and Caloplaca pyracea (present since 1952), especially at the base. The SE tree (Fig. 1E) has Orthotrichum lyellii and (only in 2011) Parmelina tiliacea. Most species present are epiphytes with a wide ecological amplitude, often even also occurring on rock. Only a few species, such as Hyperphyscia adglutinata and the Xanthoria species, are nitrophytes. All species are resistant to drought.

Therefore, most of the enormous increase in species number of the epiphytes may most probably be attributable to other effects and is probably the result of more than one factor. The four main factors include the natural succession and global warming, whereas changes in microclimate and air pollution might have been of subordinate significance:

1) Intrinsic succession. In epiphytic vegetation, succession usually begins with colonization, which means a constant addition of extra species, because there is relatively little competi-tion. This is at least true for the first several decades, as it takes a long time before the bark surface is totally covered by epiphytes. Water, nutrition and irradiation are available more or

E

A B C

D

42 Herzogia 25 (1), 2012

Table 1: Epiphytes on four Tilia trees in the Thierache, Belgium (in brackets: synonyms used by Barkman).

Lichens n = 12 n = 49 n = 41Amandinea punctata 1999 2011Anaptychia ciliaris 1952 1999 2011Anisomeridium polypori 1999Bacidia caligans 1999Bacidia subincompta 1999Buellia griseovirens 1999 2011Caloplaca obscurella 1999Caloplaca pyracea 1952 1999 2011Candelariella reflexa 1999 2011Candelariella vitellina 1952 1999 2011Chaenotheca ferruginea 1999 2011Cladonia fimbriata 1999Dimerella pineti 1999Evernia prunastri 1999 2011Flavoparmelia caperata (Parmelia caperata) 1952 1999 2011Flavoparmelia soredians 1999 2011Hyperphyscia adglutinata 1999 2011Lecanora carpinea 1999 2011Lecanora chlarotera 1999Lecanora compallens 1999 2011Lecanora dispersa 1999 2011Lecanora expallens 1999 2011Lecanora hageni 1999 2011Lecanora horiza (Lecanora laevis) 1952 1999Lecidella elaeochroma 1999 2011Lecidella scabra 2011Lepraria incana 1999 2011Melanelixia fuliginosa 1999 2011Melanelixia subaurifera 1999 2011Parmelia saxatilis 1999 2011Parmelia sulcata 1999 2011Parmelina tiliacea 2011Pertusaria albescens 1999 2011Pertusaria amara 1999 2011Pertusaria pertusa 2011Phaeophyscia orbicularis (Physcia orbicularis) 1952 1999 2011Phlyctis argena 1999 2011Physcia adscendens 1952 1999 2011Physcia aipolia 1952Physcia tenella 1999 2011Physconia distorta (Physcia pulverulenta) 1952 1999 2011Physconia grisea (Physcia grisea) 1952 1999 2011

Aptroot: Changes in the epiphytic flora on four Tilia trees in Belgium over 59 years 43

less equally to all individuals present, because there is no deep stratification (like root zones) and all sources are superficial. Natural succession in the form of colonization may be the most likely explanation for much of the enormous increase in species between 1952 and 1999. Natural succession in the form of competition is the logical explanation for the reduction in species between 1999 and 2011, because in 2011 the bark surface was on most places totally covered (Figs 1B–E) by relatively large moss colonies and foliose lichens. Obviously, pioneer species can be expected to disappear over time. Most of the vanished species are small crus-tose lichens which cannot compete with the larger species. It is significant that several of these species, such as Lecanora chlarotera, which were lost from the stem between 1999 and 2011, still occur in 2011 on the branches of the same trees. Together with Lecanora chlarotera also its lichenicolous fungus Vouauxiella lichenicola vanished.

Platismatia glauca 1999Pleurosticta acetabulum (Parmelia acetabulum) 1952 1999 2011Porina aenea 1999 2011Punctelia jeckeri 1999 2011Punctelia subrudecta 1999 2011Pyrrhospora quernea 1999 2011Ramalina farinacea 1999 2011Ramalina fastigiata 1999Xanthoria candelaria 1999Xanthoria parietina 1952 1999 2011Xanthoria polycarpa 1999 2011

Mosses n = 3 n = 8 n = 8Dicranoweisia cirrata 1999 2011Homalothecium sericeum 1999 2011Hypnum cupressiforme 1999 2011Leucodon sciuroides 1999 2011Orthotrichum diaphanum 1952 1999 2011Orthotrichum lyellii 1952 1999 2011Syntrichia laevipila (Tortula laevipila) 1952 1999 2011Tortella flavovirens 1999 2011

Hepatics n = 1 n = 3 n = 3Frullania dilatata 1952 1999 2011Metzgeria furcata 1999 2011Porella platyphylla 1999 2011

Corticolous fungi n = 2 n = 3 n = 1Hysterium pulicare 1952 1999 2011Massarina corticola 1999Peridiothelia fuliguncta (Didymosphaeria micula) 1952 1999

Lichenicolous fungi n = 0 n = 1 n = 0Vouauxiella lichenicola (on Lecanora chlarotera) 1999

Algae (not complete) n = 1 n = 1 n = 0Trentepohlia umbrina 1952 1999

Total number of species n = 19 n = 65 n = 53

44 Herzogia 25 (1), 2012

2) Global warming. Several of the species that colonized the trees after 1952 have their centre of distribution in warm-temperate regions south of Belgium. The appearance in recent years of many southern lichens is striking. In the present locality, global warming has probably been the other main influence (next to intrinsic succession), and the explanation for the appearance of e.g. Flavoparmelia soredians and Leucodon sciuroides, which are southern elements in western Europe. Interestingly, the alga Trentepohlia umbrina, which is reported to increase in many places and habitats as a result of global warming (Aptroot & van Herk 2007), was present already in 1952, but vanished since 1999 from the site.3) Changed land use affecting microclimate. There is little doubt that the microclimatical situ-ation, which is quite stable in such a group of four trees with long, hanging branches near a local road and 20 m from a forest, is largely unchanged. However, the fact that all species are drought-resistant and the epiphyte community is still referable to the same association, sug-gests that no major change in microclimate has occurred.4) Improved air quality. This is often given as an explanation for increasing species numbers. Here however, the most sensitive species present, e.g. Anaptychia ciliaris, Flavoparmelia caperata and Physconia distorta, were already present in 1952, when the air quality was still relatively good. The region has never been heavily affected by air pollution and it is question-able whether the air quality has been a significant factor.A factor that is not of direct importance here is the inadverted introduction of species by means of planting trees that have been grown in other areas or countries. This seems to be a common phe-nomenom, and several cases have been reported recently, and many more are suspected. It may well be of indirect relevance here, as certain species that are increasing may have been originally introducted in an area.The difference in the epiphytic flora between the four sample trees cannot be explained with the information available to the author. Two of the species found in 1999 (and still present in 2011) were at that time never previously recorded from Belgium. These are Lecanora compal-lens, which has been reported from Belgium from these trees in the publication with the original description of the species by van Herk & Aptroot (1999), and Flavoparmelia soredians, which was reported as new for Belgium from these trees by Diederich & Sérusiaux (2000). Both are southern species in Europe, which apparently reached Belgium rather recently, following global climate change (van Herk et al. 2002).

ConclusionsThe re-investigation in an unchanged study site of four trees after 47 and 59 years, respectively, provided a unique opportunity for the study of epiphytic vegetation over a long-term period. The enormous increase in species between 1999 and 2011 is mostly attributed to colonization, the first step of the natural succession, while the reduction in species between 1999 and 2011 is mostly attributed to competition, the next step in the natural succession, when larger mosses and foliose lichens become dominant and the whole bark is covered by epiphytes. Global warming may well have influenced the species composition in the last decades. Effects of air pollution or changes in land use or microclimate were not apparent.The difference between the epiphytic vegetation on four such close trees of the same species shows that Barkman was probably right in including all four trees in one relevée in order to show the total variation present. Smaller relevées may have led to fragmentary samples. Studies on individual trees or even parts thereof may underestimate the species diversity, while studies combining the data of a series of trees are probably more robust.

Aptroot: Changes in the epiphytic flora on four Tilia trees in Belgium over 59 years 45

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Manuscript accepted: 13 April 2012.

Address of the authorAndré Aptroot, ABL Herbarium, Gerrit van der Veenstraat 107, 3762 XK Soest, The Netherlands. E-mail: andreaptroot@gmail.com