Noteworthy records of the lichens associated with Juniperus phoenicea L. die-off in El-Jabal El-Akhdar region, NE Libya Manam W B SAAED1,2, *, Yacoub M EL-BARASI2, 3, Ahmed A EL-SHAIKHY2 1. Department of Botany, Faculty of Arts and Science, Al-Abyar Branch, Benghazi University, Libya. 2. Department of Environmental Science and Engineering, The Libyan Academy of postgraduate studies, Benghazi Branch, Benghazi, Libya 3. Department of Botany, Faculty of Science, Benghazi University, Benghazi, Libya * Corresponding Author: manam.saaed@uob.edu.ly Received: 25 September, 2021; First decision: 25 November, 2021; Revised: 4 December, 2021; Final decision: 9 December, 2021. Abstract El-Jabal El-Akhdar region is the most vegetated area in Libya dominated by a Mediterranean evergreen maquis; the juniper trees (Juniperus phoenicea L.) consist of about 70-80% of the vegetation cover. These trees suffer a wide die-off phenomenon for a few decades, which put extra pressure on the ecosystems, in addition to climate change and unsustainable management. Notably, this phenomenon in El-Jabal El-Akhdar region is associated with a dense growth of lichens. This study aimed to identify the lichens on the juniper trees and record some ecological notes. According to our results, a total of 15 taxa belonging to six families and eight genera were recognized on the J. phoenicea trees. The main lichen life-forms were crustose, fruticose, and foliose. However, the densest growth was recorded for Ramalina maciformis (Delile) Bory and Tornabea scutellifera (With.) J.R. Laundon., which appear in most of the infected areas. However, Lecanora gr. subfusca (L.) Ach. has dense growth in only a few areas south El-Jabal El-Akhdar region. This needs further investigation to understand why they grow in such a way on the juniper in the study area. The present study provides baseline information for further progressions in understanding Libyan lichens’ species richness and community composition at local and regional scales. Keywords: lichenology, list of species, Juniperus phoenicea subsp. turbinata (Guss.) Nyman, Mediterranean Maquis, Mediterranean shrubland, Libya. ecologia mediterranea – Vol. 47 (2) – 2021 Introduction El-Jabal El-Akhdar region (Figure 1) is the only remaining natural dense vegetated zone in the whole way from Tunisia to Sinai in eastern Egypt, in the southern part of the Mediterranean Sea. This region consists of about 1% of the Libyan territory but contains about 65% of the country’s flora (El-Barasi & Saaed, 2013). El-Jabal El-Akhdar region is a part of the Mediterranean Basin biodiversity hot spot (Myers et al. 2000; Mittermeier et al. 2004, 2011). The Juniper tree (Juniperus phoenicea L.), a member of the cypress family (Cupressaceae), most probably J. phoenicea subsp. turbinata (Guss.) Nyman (Pavon et al. 2020), makes up 70-80% of the vegetation cover in El-Jabal El-Akhdar region. This region is characterized by a higher cryptogamic richness and diversity, especially lichens, compared to other Libyan areas. However, there is a growing concern that the widespread of Juniper tree die-off in this region may lead to a significant decline in the green areas in a country while about 95% of its land is a hot desert (Great Sahara). J. phoenicea has a wide geographical range and is not globally threatened. However, its range in Libya is shrinking to a dangerous level due to climate change, anthropogenic pressures, and lately 41 MANAM W B SAAED, YACOUB M EL-BARASI, AHMED A EL-SHAIKHY Figure 1 – The geographical location of the study area (El-Jabal El-Akhdar region) showing the 14 study sites. the tree die-off phenomenon. Despite the fact that J. phoenicea can be a host plant for many epiphytic lichens (Jüriado et al. 2015) and is often incorporated into the group of epiphytes on coniferous trees (Jüriado et al. 2015), the El-Jabal El-Akhdar’s tree die-off is unique in that it associated with a dense growth of lichens (Figure 2). Lichens can be found almost anywhere worldwide. They grow readily on rocks, soils, and trees (bark, wood, leaves). Lichens can withstand harsh conditions such as freezing, high light, and intense heat. Many of them can dry out for long periods, then quickly become active again when rehydrated. Trees can provide a broad spectrum of microhabitats for epiphytic vegetation (Peard 1983). The physical and biotic factors that interact to create these environments have been discussed in great detail by Barkman (1958). Horizontal and vertical gradients of light, water, and temperature depend upon the direction of trunk exposure and height above ground; this along with the tree vigour influence the presence and growth of lichens. Bark hardness, texture, water-holding capacity, and pH vary among tree species and within species according to the age of tree bark (Peard 1983). In general, most lichen species grow best with sufficient light and moisture within moderate temperature zones. Figure 2 – Dense growth of lichens on Juniperus phoenicea L. trees from different locations in the study area (El-Jabal El-Akhdar region). 42 ecologia mediterranea – Vol. 47 (2) – 2021 Noteworthy records of the lichens associated with Juniperus phoenicea L. die-off in El-Jabal El-Akhdar region, NE Libya Lichens are a vital component of tree epiphytic (lichens, bryophytes, and vascular plants) biodiversity with critical ecological roles in the ecosystems and occupy small econiches from the canopy to trunks (Gonzáles-Montelongo & Pérez-Varga 2021). Lichens are, by definition, symbiotic organisms, usually composed of a fungal partner, the mycobiont, and one or more photosynthetic partners, the photobionts, which are most often either a green alga or cyanobacterium or both (Maphangwa 2010). This complex association makes it difficult to classify these organisms (Karagünlü & Tufan-Çetin 2020). Lichens are perennials and maintain a uniform morphology over time. They grow slowly, have a large-scale dependence upon the environment for their nutrition, and in contrast to vascular plants, they do not shed their leaves during growth (Maphangwa 2010). Traditionally, lichens are classified into four primary growth forms: crustose, squamulose, foliose, and fruticose. These forms, which are in no sense natural divisions, are at best points on a scale of continuous differentiation from primitive to highly structured thalli with many intermediates. Each form is characterized by a particular arrangement of cortical, algal, and medullary tissues and different modes of attachment to the substrate (Maphangwa 2010). Not surprisingly, many people mistakenly blame lichens for the decline and death of shrubs and trees in El-Jabal El-Akhdar region. Because these unusual plant-like organisms are commonly seen on the exposed limbs and trunks of declining or dead trees and shrubs, especially J. phoenicea and, to a relatively less degree, on many other species, such as Pistacia lentiscus L., Olea europaea L., Rhamnus oleoides L. However, lichens are not responsible for the poor top growth or death of shrubs and trees. Instead, their appearance is often related to damage from environmental stress or poor management. Exposed limbs on damaged plants simply give lichens access to the sunlight they need for growth with little competition (Hagan 2004). With few exceptions, research has shown that lichens are not parasitic or pathogenic on higher plants. However, their growth may increase due to increased light levels when branches lose leaves and die (Hagan 2004). The botanical exploration of the Libyan flora has a long history dating back to the beginning of the 18th century (Saaed et al., 2019), which ecologia mediterranea – Vol. 47 (2) – 2021 has provided the basis for the compilation of the checklist of Libyan vascular plants. Despite the favourable natural conditions for lichens in the northern parts of the country, e.g., El-Jabal El-Akhdar region, the data on the Libyan lichen biota are limited and scanty, and lacking a comprehensive approach. The exploration is still a work in progress, and most of the country is still underexplored from a lichenological point of view and almost certainly contains many lichen taxa yet to be discovered. Only a few lichenological collections were conducted in Libya (e.g., Baroni 1892 Durand & Barrate, 1910, Zanfrognini 1913a, b, Mameli 1913, Pampanini 1914, 1930, Thor & Nascimbene 2010). The lichen and lichenicolous fungi biota of Libya probably remains largely unknown (Thor & Nascimbene 2010). A checklist compiled from literature up to the year 1950 includes 151 taxa, and Thor & Nascimbene (2010) added another 49 taxa. A realistic estimate of the total number of Libyan lichens and lichenicolous fungi could exceed 1,000 species (Thor & Nascimbene 2010). The lack of information added to the increased die-off phenomenon associated with a dense growth of lichens, mainly on J. phoenicea were the main incentive to conduct this study. The present article focused on lichen identification with some notes on their ecological characteristics. It aims to start new lichenological studies in Libya and provide baseline information of the lichens known to grow on J. phoenicea associated with the die-off phenomenon in El-Jabal El-Akhdar region. Material and methods Study area Libya is one of the largest countries in North Africa, covering about 1.75 million km2. Its territory is mainly covered by deserts or semideserts, whereas the Mediterranean vegetation is restricted to the coastal areas (Thor & Nascimbene 2010). El-Jabal El-Akhdar (The Green Mountain) is the most vegetated region in Libya. It is a low to medium mountainous region located in the country’s north-eastern part at the Mediterranean Sea (Figure 1). It is divided by many valleys that vary in depth and length, and are oriented either towards the sea in the north, or towards the south to end in the desert (Sahara) (El-Barasi and Saaed 2013). 43 MANAM W B SAAED, YACOUB M EL-BARASI, AHMED A EL-SHAIKHY El-Jabal El-Akhdar region covers an area of about 8000 km2, and the dense vegetation covers about 5000 km2. The vegetation consists mainly of Mediterranean Maquis, e.g., short trees, shrubs, sub-shrubs, and annuals after rainfall in winter and spring in open areas. Tall trees can be found in many valleys and seasonal rivers. The flora of El-Jabal El-Akhdar comprises more than 1,350 species, which consist of about 70% of the total number of Libyan flora (El-Barasi & Saaed 2013; Saaed et al. 2019). Important canopy species are met like: Juniperus phoenicea L., Arbutus pavarii Pamp., Olea europaea L., Ceratonia siliqua L., Pistacia lentiscus L., Rhamnus lycioides L., Pinus halepensis Mill., Cistus parviflorus Lam., Quercus coccifera L., Searsia tripartita (Ucria) Moffett (El-Barasi & Saaed 2013). The northern parts of the study area are influenced by the Mediterranean climate, which is characterized by hot, dry summers and mild, rainy winters. About 75% of the rain falls during the winter season (October to February), while the dry period extends for a period of six months (from April to September). (El-Barasi & Saaed 2013). The rainfall in the northern parts of El-Jabal El-Akhdar ranges between 400 to 600mm/year and the evaporation rate about 2000mm/year. The southern parts have a semi-desert climate showing low and irregular rainfall, usually below 200mm/ year, and high evaporation rates that exceed 2000mm/year. (El-Barasi et al. 2011). El-Jabal El-Akhdar region has been inhabited since ancient times. The main human activities that have influenced the natural vegetation in this region are: gathering firewood, charcoal production, collecting of medical and aromatic species, and vegetation clearing for agriculture practices, as well as grazing (El-Barasi et al. 2011). Lichen collection and identification The study area was divided into three parts: the northern, middle, and southern parts according to the distance from the coast and altitude (m asl), which mainly influence the area’s climate and other environmental factors. There were 14 survey sites selected carefully to cover the whole areas of J. phoenicea distribution in El-Jabal El-Akhdar region; four in the northern part, five in the middle, and the other five in the southern part (Table 1, Figure 1). In the northern part (locations 1-4), the altitude of the survey locations ranged between 27 and 139 m asl, and 44 their distance from the coast between 0.23 to 3.15km. In the middle part (locations 5-9), the altitude ranged between 334 and 517m asl, and the distance from the coast between 5.81 and 24.77km. And in the southern part (locations 10-14), the altitude ranged between 310 and 779m asl, and the distance from the coast between 11.60 and 40.10km. The fieldwork was performed during the year 2020; several trips were conducted to each site to collect lichen specimens only from J. phoenicea trees (from trunks and limbs). In each site, all different types of lichens were described and collected carefully from the juniper trees in a circular plot of 100 meters in diameter. The lichen specimens were put in a plastic cube (7 × 7cm) with a lid to ensure maximum protection and then transferred to the laboratory. In the field, other comments were recorded such as site coordinates and altitude, distance from the coast, lichen type, number of infected trees, infection percentage for each tree, lichen growth density on the Juniper tree, which part of the tree is infected, and any other infected plants. Table 1 – Information about survey localities in the study area (El-Jabal El-Akhdar region). Locality Coordinate Altitude Distance (m asl) from sea coast (km) Location 1 32 40 553 N 20 55 388 E 139 1.95 Location 2 32 51 928 N 21 55 248 E 324 3.15 Location 3 32 54 817 N 22 04 911 E 27 0.23 Location 4 32 52 172 N 22 19 945 E 34 0.28 Location 5 32 50 227 N 22 09 604 E 517 5.81 Location 6 32 42 361 N 21 25 247 E 354 8.97 Location 7 32 34 065 N 21 12 385 E 336 22.49 Location 8 32 32 535 N 21 06 667 E 465 24.77 Location 9 32 17 500 N 20 32 631 E 334 20.88 Location 10 32 19 710 N 20 54 971 E 539 35.43 Location 11 32 32 555 N 21 17 220 E 407 25.59 Location 12 32 34 274 N 21 40 250 E 779 40.10 Location 13 32 36 676 N 21 55 222 E 778 31.35 Location 14 32 40 609 N 22 33 841 E 310 11.60 ecologia mediterranea – Vol. 47 (2) – 2021 Noteworthy records of the lichens associated with Juniperus phoenicea L. die-off in El-Jabal El-Akhdar region, NE Libya In the laboratory, the specimens were studied in the usual way. First, the specimens were cleaned with tap water and air-dried, then examined with a stereomicroscope and a compound microscope with different objective lenses up to 100x. Morphological and anatomical traits were inspected in an aqueous solution, especially lichen growth form, colour, type of photobiont and its pigmentation, mycobiont fruiting bodies, presence and type of rhizines, presence of cifel or pseudocifels, size of spores, and the number of spores per ascus, among others. With a razor blade, all cuts were freehand performed. The chemical reagents as K test (potassium hydroxide 10%), C test (commercial bleach), P test (alcohol solution of para-phenylenediamine), were used for the analyses of secondary metabolic substances present in lichens (Maphangwa 2010). The change in colour resulting from the reaction with these chemicals is an indication of the presence of a certain lichen substance with a critical taxonomic key. The Chemotaxonomic tests were carried out under the stereomicroscope using white light and performed on part of young thallus as available. Lichen specimens were identified according to several sources (Pampanini 1914, 1930; Llimona 1982; Seaward & Sipman 2006; Thor & Nascimbene 2010; Roux et al. 2021; Nimis 2021). The lichen classification was confirmed through communication with Professor Göran Thor (Department of Ecology, University of Agricultural Sciences, Uppsala, Sweden). Also, a matching process of the classification was carried out in cooperation with Professor Sipman M. J Harrie (Dr. Honorary Curator of Lichens, Botanical Garden and Botanical Museum in Berlin, Dahlem, Germany). Dubious status for some lichens was also reported. GBIF (2021) and Index Fungorum (2021) websites were used to update lichen taxa names. In addition, the obtained list of the lichens was compared with the work of Durand & Barrate (1910), Pampanini (1914, 1930) and Thor & Nascimbene (2010). Results and discussion Lichen existence and distribution In the study area, lichens are an indication of poor plant health. Good plant vigour is the best protection against the presence of ecologia mediterranea – Vol. 47 (2) – 2021 lichens. Heavy invasions of lichens are most common on trees and shrubs in declining or poor health due to other factors (Hagan 2004), e.g., prolonged drought, nutrient deficiency, severe anthropogenic pressure, and sufficient exposure of the lichen to the sun as a result of the decline or fall of the tree foliage. Therefore, the dense lichen growth on J. phoenicea and other trees and shrubs in El-Jabal El-Akhdar is probably a sign of vegetation degradation due to prolonged drought and climate change (Ali & El Shatshat 2015) and unfavourable anthropogenic impacts (El-Barasi & Saaed 2013). Climatic, geographic, and environmental conditions are quite heterogeneous across El-Jabal El-Akhdar region, leading to substantial ecoregional diversity. This is reflected in distinctive lichen distribution patterns mainly between the northern, middle, and southern parts of the study area, resulting in significant differences in regional lichen distribution and local community compositions. The northern locations of the study area showed very little or no lichen growth on J. phoenicea, the middle locations showed little, moderate, dense, and very dense growth, and the southern locations showed little, moderate, and dense growth. The very low or absence of lichens growth in the northern parts that are very close to the sea is most likely attributed to the salt sprays that come with wind from the sea, particularly in winter, which affect lichen growth as they depend on air moisture to get water and nutrients as well. Previous findings (e.g., Roux & Sigoillot 1987, Stammitti 1992) indicated the effect of sea spray polluted by anionic surfactants and hydrocarbons as a factor responsible for the die-off of conifers and declining lichen growth in European Mediterranean regions. Meanwhile, the highest lichen growth was in the middle locations of the mountain, which have the highest rate of precipitation, air humidity, and dew. Lichens, mainly fruticose and foliose, are usually abundant in forests, where fog is the predominant source of water (Gonzáles-Montelongo & Pérez-Vargas 2021). This is not the case in the southern locations of the study area, which have relatively higher temperatures and lower precipitation and air humidity rates. Lichens are most numerous on limbs and trunks of large mature trees and shrubs in full sun, particularly those plants with badly thinned canopies. As lichens love sunlight and moisture, they are often found in sunny, wet 45 MANAM W B SAAED, YACOUB M EL-BARASI, AHMED A EL-SHAIKHY spots and most lichens do not thrive on heavily shaded twigs and branches of healthy woody plants. It is noteworthy to mention that young J. phoenicea trees and the new growth and branches on old ones in all the survey sites are devoid of significant lichen growth. This could be related to the vigour of the young trees and new growths. Also, young junipers have a papery bark that is smooth and flaky, exfoliating in long vertical stripes, which may not be suitable for the establishment and growth of lichen colonies, because they do not retain water from rains and mists for long enough. Another important factor is the slow growth of lichens, which takes many years to become visible, this is infeasible in young trees and new branches. This is consistent with the finding of Peard (1983) in a forest area in Colorado, in the USA, mainly composed of Pinus ponderosa Laws. and Juniperus scopulorum Sarg. Jüriado et al. (2015) who studied the lichens on Juniperus communis L. in calcareous grasslands north Europe found that the composition and richness of lichens were influenced by the vitality of the phorophyte (proportion of dead branches) and its size (height and width, and stem circumference). This indicates the inter-correlated effects of juniper age and size as well as indirect effects of exogenous disturbances (like flooding, drought, fire), which are known to influence juniper vitality. Table 2 – Information about survey localities in the study area (El-Jabal El-Akhdar region). Family Species 1. Cladoniaceae Cladonia foliacea subsp. endiviifolia (Dicks.) Boistel 2. Lecanoraceae Lecanora gr. subfusca (L.) Ach. 3. Lecanoraceae Lecanora horiza (Ach.) Röhl. 4. Lecanoraceae Lecanora sp. 5. Pertusariaceae Pertusaria hymenea (Ach.) Schaer. 6. Pertusariaceae Pertusaria sp. 7. Physciaceae Tornabea scutellifera (With.) J.R.Laundon. 8. Ramalinaceae Ramalina maciformis (Delile) Bory 9. Teloschistaceae Polycauliona polycarpa (Hoffm.) Frödén, Arup & Søchting Synonym: Xanthoria polycarpa (Hoffm.) Rieber. 10. Teloschistaceae Seirophora lacunosa (Rupr.) Frödén 11. Teloschistaceae Seirophora villosa (Ach.) Frödén 12. Teloschistaceae Seirophora sp. 13. Teloschistaceae Seirophora sp. 14. Teloschistaceae 15. Teloschistaceae Seirophora sp. Xanthoria parietina (L.) Beltr. 46 Species composition Describing and identifying the lichen flora of Libya is problematic since all of the previous works were done by European scientists, and most of the collections were deposited in different herbaria outside the country. In addition, the literature about the Libyan lichen biota is very scarce. In this study, 15 different lichens (Figures 3-14) were collected from J. phoenicea trees belonging to six families and eight genera (Table 2). Five of the lichens could not be fully identified to the species level. Seven lichens belonging to the family Teloschistaceae, three to Lecanoraceae, two to Pertusariaceae, and the Cladoniaceae, Physciaceae, and Ramalinaceae each represented by only one taxon. Most of the recorded lichens have a usual growth form except for three species. Ramalina maciformis and Tornabea scutellifera (With.) J.R. Laundon. appear in most affected areas with die-off phenomenon and have dense growth on infected J. phoenicea. Lecanora gr. subfusca (L.) Ach. has dense growth in few areas south El-Jabal El-Akhdar region. These lichen species are more related to the juniper die-off to the extent that their abnormal growth indicates the infected trees. Our list contains only two species in common with the 15 lichens mentioned by Durand and Barrate (1910); Xanthoria parietina (L.) Beltr. and Cladonia foliacea subsp. endiviifolia (Dicks.) Boistel. Durand & Barrate materials were mainly collected by P.H. Taubert in 1887 from different localities and from various sources; soil, rocks, and plants, both in Cyrenaica and Tripolitania (Thor & Nascimbene 2010). Pamapnini (1930) mentioned 49 lichens collected from Cyrenaica, 12 taxa collected from different tree types, including J. phoenicea, of which five taxa are shared with our list: Cladonia foliacea subsp. endiviifolia [= Cladonia endiviaefolia (Dicks.) Fr.], Ramalina maciformis, Xanthoria parietina, Tornabea scutellifera (With.) J.R. Laundon.[= Anaptychia intricata (DC.) A. Massal.], and Lecanora gr. subfusca [= Lecanora allophana (Ach.)]. Nine taxa are shared with the list of Thor & Nascimbene (2010); Cladonia foliacea subsp. endiviifolia, Lecanora gr. subfusca, Lecanora horiza (Ach.) Röhl., Tornabea scutellifera, Ramalina maciformis, Polycauliona polycarpa (Hoffm.) Frödén, Arup & Søchting [= Xanthoria polycarpa (Hoffm.) Rieber.], Seirophora lacunosa (Rupr.) Frödén, Seirophora villosa (Ach.) ecologia mediterranea – Vol. 47 (2) – 2021 Noteworthy records of the lichens associated with Juniperus phoenicea L. die-off in El-Jabal El-Akhdar region, NE Libya Figure 3 – Xanthoria parietina (L.) Beltr. Figure 4 – Seirophora villosa (Ach.) Frödén. Figure 5 – Seirophora lacunosa (Rupr.) Frödén. Figure 6 – Polycauliona polycarpa (Hoffm.) Frödén, Arup & Søchting. Figure 7 – Seirophora sp. Figure 8 – Seirophora sp. Figure 9 – Ramalina maciformis (Delile) Bory. Figure 10 – Tornabea scutellifera (With.) J.R. Laundon. ecologia mediterranea – Vol. 47 (2) – 2021 47 MANAM W B SAAED, YACOUB M EL-BARASI, AHMED A EL-SHAIKHY Figure 11 – Lecanora horiza (Ach.) Röhl. Figure 12 – Lecanora gr. subfusca (L.) Ach. Figure 13 – Pertusaria hymenea (Ach.) Schaer. Figure 14 – Cladonia foliacea subsp. endiviifolia (Dicks.) Boistel. Frödén, and Xanthoria parietina. Only one taxon in our list, Pertusaria hymenea (Ach.) Schaer., has not been mentioned by Durand & Barrate (1910), Pampanini (1930), or Thor & Nascimbene (2010). In our list, only the remarkable species are listed. Several species could not be determined at the species level (Lecanora gr. subfusca, Lecanora sp., Pertusaria sp., Seirophora sp.) and it is likely that several species barely visible and/or poorly known have gone unnoticed. These species will need to be reviewed or researched for further study. Further surveys are recommended to develop a more detailed picture of the floristic composition and distribution of the lichen biota in El-Jabal El-Akhdar region and Libya. However, the remaining unanswered question is why only three lichens, Ramalina maciformis, Tornabea scutellifera, and Lecanora gr. subfusca have dense growth associated with juniper die-off? 48 Acknowledgement The authors are indebted to Professor Göran Thor from the Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden, for confirming some lichens classification. Also, our thanks are due to Professor M. J. Harrie Sipman., Dr. Honorary Curator of Lichens in the Botanical Garden and Botanical Museum in Berlin, Dahlem, Germany, for his insightful comments and matching process of the lichen classification. References Ali, M. & El Shatshat, S. (2015). Ecological study of Juniperus phoenicea L. in El-Gabal El-Akhdar area, Libya. European Journal of Experimental Biology, 5(7), 71-76. AFL (2021). Association française de lichénologie, Available at: http://www.afl-lichenologie.fr/. 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