The distribution and ecological factors of aerial algae inhabiting stoneworks in Korea

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  • ABSTRACT

    The physico-chemical and environmental factors of stoneworks were examined from March 2009 to October 2010, and aerial algae living on 24 stoneworks in Korea were identified. Fifty aerial algae were found in 24 stoneworks. Of the 50 taxa, 30 taxa were cyanophytes, 16 taxa were bacillariophytes, 3 taxa were chlorophytes, and 1 taxon was a xanthophyte. Nine species, including Aphanocapsa rivularis, which is known to only live in aquatic conditions, inhabited both aquatic and aerial environments. Synechococcus aeruginosus, Scytonema coactile var. thermalis, S. coactile var. minor, Stigonema ocellatum f. ocellatum, and Oscillatoria boryana were newly recorded in Korea. As a result of a correlation analysis between algae and the physico-chemical and ecological environmental factors, the taxa were divided into the bryophyte group, the humidity group, and the dry group. Although the bryophyte group was included within the humidity group, it was separated from the dry group. Taxa in the bryophyte group including Nostoc commune which was distributed in more humid areas than those in the humidity group. However, dry group taxa including Chroococcus pallidus were distributed in lower humidity than that of the two other groups. Correlations among other environmental factors were tested to identify other factors that could substitute for humidity and light intensity. As a result, tree distance, water distance, and plant coverage were replaceable environmental factors.


  • KEYWORD

    aerial algae , bacillariophytes , chlorophytes , cyanophytes , stoneworks , xanthophytes

  • INTRODUCTION

    Aerial algae are algae that live in rock faces, earthen rocks, stone walls, and plants but not in water. Edaphophytes can also be included as aerial algae (Chung 1993). Studies on algae have mostly concentrated on aquatic algae, and studies conducted on aerial algae have mostly focused on biological pollution and preventive stone cultural heritage research (National Research Institute of Cultural Heritage 2008). Some taxa in Protococcus, Trentepholia, Cephaleuros, Scytonema, Nostoc, Schizothrix, Stigonema, Chlorococcum, and Trentepholia are known as aerial algae. According to Chung (1979), 90 taxa are listed as aerial algae, and 45 taxa were identified in Korea in Chung (1993). Additionally, 41 aerial algae taxa have been identified in Korea in studies by Chang et al. (1998), but only a few studies have been conducted on aerial algae.

    In research on aerial algae habitat distribution, it was determined that cyanophytes, such as Gloeocapsa sp. and Lyngbya sp., inhabit the Muryong Royal Tomb in Gongju (Kim et al. 2001). Additionally, studies on Chlorella attached to a stone Buddha (Klochkova and Kim 2005), and aerial algae distributed on five (Lim and Lee 2008a) and eight (Kim et al. 2010) stone cultural properties have been conducted in Korea.

    According to Hyvert (1972), 39 aerial algae species have been identified, and studies on the genus Synechococcus have reported that it lives endolithically with lichen in the church of Minas Gerais, Brazil (Allsopp et al. 2004). Five taxa including Coccomyxa are green algae that live on marble (Lamenti et al. 2000), and Chlorella has been discovered in the Maya ruins of Mexico (Videla et al. 2000). Research about microalgae in stoneworks located in Spain (Sarro et al. 2006) and a study of cyanophytes that inhabit a church wall located in Porto Alegre, Brazil (Crispim et al. 2004) has also been performed. The main objectives of this study were to identify aerial algae living in stoneworks and to record new species in Korea. In addition, ecological characteristics of the identified algae were investigated by analyzing the ecological factors related to their distribution.

    MATERIALS AND METHODS

    Collections of aerial algae were sampled at Gyeonggido, Jeolla-do, Gyeongsang-do, and Chungcheong-do on 24 stoneworks from March 2009 to October 2010 (Table 1, Fig. 1). The aerial algae samples were collected from more than one part and in every aspect of the stoneworks using a soft brush and sterilized depressor. A 5 × 5 cm2 quadrat was used for quantitative analysis. Each sample was sealed and refrigerated in a light-tight container with sterilized distilled water and transferred to the laboratory (Crispim et al. 2004). Some of the samples were stored fixed in 1% formalin. Among them, the unrecorded Korean species were cultured indoors, and maintained in the algal culture collection of Kyonggi University (ACKU).

    An analysis of physico-chemical environmental factors such as surface temperature of the stonework, light intensity, and humidity were conducted for all sampling dates. Temperature was measured with a stem thermometer, and surface temperature was measured with a Testo 830- T1 (Testo, Lenzkirch, Germany), humidity was measured with a Testo 625 (Testo), and light intensity was assessed with a LX-1108 instrument (Lutron, Taipei, Taiwan). Temperature, humidity, and light intensity have tremendous effects on algae distribution; however, these variables largely depend on the season and time of collection. Therefore, we measured plant coverage, canopy, distance to trees, and distance to water to identify relatively stable environmental factors that could replace temperature, humidity, and light intensity (Fig. 2).

    Plant coverage was considered the distribution of woods within a 10 m radius of the stoneworks as a percentage. The number of trees screening light was measured within a 1 m radius of the stoneworks as a percentage to assess the canopy. Tree distance was considered the closest distance to a tree within a 5 m radius. The water distance was the closest distance to a river or lake within a 1,000 m radius. Biological pollution coverage was calculated by measuring the bryophyte area using AutoCAD 2008 (Autodesk Inc., San Rafael, CA, USA). The taxonomic classification system was based on Hirose et al. (1977), and aerial algae were identified referring to Prescott (1973), Prescott et al. (1972, 1977, 1981, 1982), Chung (1993), John et al. (2002), and Wehr and Sheath (2003). Dominant species were analyzed by relative abundance. The collected samples were examined under

    a light microscope (400-1,000×) to determine the total number and the dominant species. Light microscopy was carried out using an Olympus BX41 microscope (Olympus, Tokyo, Japan) equipped with Nomarski differential interference optics. Species newly recorded in Korea were illustrated using a drawing attachment together with light microscope photographs. SPSS version 12.0 (SPSS Inc., Chicago, IL, USA) was used to analyze the relationships between aerial algae and the environmental factors.

    RESULTS

    Table 2 shows the results of the physico-chemical, and ecological environmental factors of the stoneworks where the aerial algae was found. The air temperature was 10.2-29.9℃ and surface temperature was 7.5-30.0℃. Humidity was 41.4-90.0%. The light intensity values were the highest at the Yeondae small temple A-3 (39,000 lux), and the lowest were recorded at Gwang-gyo mountain 2-1 (162 lux). Due to strong wind, measuring the humidity, and light intensity at the Unjusa Temple, the stone wall at Jucksung-myeon, Danyang-gun, and the stone wall at Pyeongchang-gun was difficult. Plant coverage at the three sites including Gwang-gyo Mountain 3-2 had the highest value at 80%, whereas the Unjusa Temple A5 was not affected by plant coverage with a value of 0%. Stone wall 1 at Jucksung-myeon, Danyang-gun, which was a site where light was screened by trees, had a canopy value of 100%. Five sites, including Unjusa Temple A4, had a 0% canopy value. Tree distance ranged from 0 to 5 m, indicating that most sites were affected by trees. Water distance values were 0.1-1,000 m.

    Four phyla, 4 classes, 8 orders, 4 suborders, 13 families, 23 genera, 46 species, 3 varieties, and 1 forma were collected and identified as aerial algae (Table 3). Cyanophytes were the most dominant taxa, with 3 orders, 2 suborders, 5 families, 10 genera, 26 species, 3 varieties, and 1 forma. Only one species, Botryococus braunii, was considered a xanthophyte, and bacillariophytes had 2 orders, 2 suborders, 5 families, 9 genera, and 16 species. Chlorophytes had 2 orders, 2 families, 2 genera, and 3 species.

    Stone wall 1 at Jucksung-myeon and Danyang-gun had the most taxa among the stoneworks with 21 taxa including Aphanocapsa elachista. Gwang-gyo Mountain 3-1 had only one taxon, Chroococcus varius (CHVA). C. varius had the most varied growth range, appearing in 21 different stoneworks including Gwang-gyo Mountain 1-2. Protococcus viridis, which appeared most frequently in Lim and Lee (2008b), was found at five sites including Gwanggyo Mountain 1-1.

    The habitats of all taxa were evaluated after reviewing other studies (Table 3). Five taxa, including Synechococcus aeruginosus, were newly recorded in Korea. Among the 50 taxa, 37 taxa including Aphanocapsa elachista are known to inhabit aerial and aquatic environments. Additionally, 3 taxa, including Chroococcus bituminosus, were distributed only in aerial environments.

    Phylum Cyanophyta

    Class Cyanophyceae

    Order Chroococcales

    Family Chroococcaceae

    Synechococcus aeruginosus Nageli

    Cell long and cylindrically shaped, with a width of 6-16 μm and length of 13-30 μm. Light blue-green color, with many granules; lives in freshwater and hot springs (Hirose et al. 1977).

    Synechococcus aeruginosus (SYAE) lives in Sola lake in Taba Egypt (Badawy et al. 1999). In Korea, one species, Synechococcus lividus, was identified under the genus Synechococcus (Chung 1993). That study revealed that S. lividus lives on the surfaces of stone walls inhabited by bryophytes. The tree distance from the stoneworks was 0 m, with 50-70% plant coverage, which was probably due to its relatively high water composition.

    Sites of collection. t, u, v (Figs 3E & 4A).

    Order Nostocales

    Suborder Nostochineae

    Family Scytonemataceae

    Scytonema coactile Montagne var. thermalis Geitler

    Cell olive or purple-green in color. Main axis pseudobranched and filamentous. Sheaths have no layered structure or color. Cell is (11)-15-18 μm in diameter and becomes narrower at the tip. Trichome is cylindrical with width of 9-11 μm and length of 7-20 μm. Heterocysts are cylindrical, and it inhabits hot springs (Hirose et al. 1977).

    Scytonema coactile var. thermalis (SCTH) has been found in Japan (Hirose et al. 1977), and we found that it lives on stone. Water distance was >1,000 m, and tree distance was 0-5 m.

    Sites of collection. k, p, r, s, u (Figs 3A & 4C).

    Order Nostocales

    Suborder Nostochineae

    Family Scytonemataceae

    Scytonema coactile Montagne var. minor Wille

    Cell is thick and 1 mm in width. Pseudo-branching mostly originates from main axis. It has a yellow-brown colored sheath without a layered structure, and a diameter of 14-16 μm. Trichomes are cylindrical with no joints; width is 8-10 μm. Heterocysts are cylindrical or square shaped, and it inhabits hot springs (Hirose et al. 1977).

    Scytonema coactile var. minor (SCMI) is known to inhabit Japan and China; however, only S. crispum and S. myochorus has been identified locally (Chung 1993). In this study, S. coactile var. minor appeared at 10 sites including Gwang-gyo Mountain 1-1 and seemed to be affected by trees.

    Sites of collection. a, b, e, i, k, l, m, o, v, w (Figs 3C & 4D).

    Order Stigonematales

    Family Stigonemataceae

    Stigonema ocellatum (Dillwyne) Thuret f. ocellatum

    Cell shaped like grass or a thread; 25-50 μm wide with irregular branching. Usually exists as a single filament, but occasionally can be found as double filaments. Branches are slightly slimmer than the main axis. Sheath is relatively thick, and may have yellow, yellow-brown, or no color. Trichomes are elliptical or square-shaped, and it inhabits humid dirt, rocks, and grass (Hirose et al. 1977).

    Stigonema ocellatum f. ocellatum has been studied on rocks exposed to natural light in Venezuela (Lakatos et al. 2001). In particular, it was found in places far away from water in the Australian study; however, we found it on stoneworks exposed to aerial algae without any relationship to water distance.

    Sites of collection. c, e, g, h, I, j, l, m, r, s, t, u, v, w (Figs 3B & 4E).

    Order Nostocales

    Suborder Oscillatoriineae

    Family Oscillatoriaceae

    Oscillatoria boryana Kutzing

    Cell dark colored; trichomes are flexible in the shape of a wave. The cell continuously folds, and length is less than or equal to half the width. Width of the cell is 6-8 μm, and length is 4-6 μm. The apical cell is circular or a sharp circular cone, and has no calyptra (Hirose et al. 1977).

    Oscillatoria boryana has been found in India (Kalavathi et al. 2001), and some studies have reported it in Japan, China, and North America (Hirose et al. 1977). We found it at one site, the Yeondae small temple A-3, with a tree distance of 0 m, and a water distance of >1,000 m. These results indicates that it maintains humidity using trees.

    Site of collection. r (Figs 3D & 4B).

    Cyanophytes were dominant at 22 sites among the aerial algae (Table 4). In particular, cyanophytes dominated by >50% at 15 sites, including Gwang-gyo mountain 1-1 (Kim et al. 2010). Hantzschia amphioxys (HAAM) and Cymbella delicatula, which are bacillariophytes were dominant at the Yeondae small temples A-1 and A-2. HAAM is known to be found at high humidity sites with bryophytes (Lim and Lee 2008a, Kim et al. 2010). Filamentous cyanophytes of Scytonema, Stigonema, Oscillatoria, and Nostoc were dominant at 15 sites including Gwang-gyo Mountain 1-1. Coccoid-shaped cyanophytes such as Chroococcus and Aphanocapsa were dominant at seven sites including Gwang-gyo Mountain 1-2.

    A principal component analysis was conducted to identify the relationships between the aerial algae and ecological factors. The varimax method (Kim et al. 2007) was used to obtain the results (Fig. 5).

    All species were divided into ecological groups according to the correlation coefficients. The identified species were divided into biological pollution coverage of bryophyte (Br), high humidity (Hu), and dry (Dry) groups with

    a negative correlation with humidity and canopy (Fig. 5). Species in the Br group were cyanophytes and bacillariophytes such as Nostoc commune (NOCO), Oscillatoria geminata var. subphurea (OSGE), Orthoceira roeseana (ORRO) and Navicula crytocephala (NACR). These species showed high correlation coefficients with bryophyte biological pollution coverage ranging from 0.68 to 0.84. The Dry included Chroococcus pallidus, HAAM, SCMI among others. The Hu group included CHVA, SCTH, Pinnularia borealis (PIBO), Navicula goeppertiana (NAGO), and SYAE.

    DISCUSSION

    Physico-chemical environmental factors vary greatly due to seasonal differences and the weather conditions on the date of collection. This seems to affect changes in aerial algae groups inhabiting stoneworks (Lim and Lee 2008a). Korean aerial algae now include total 108 taxa by adding 5 taxa from the present study. We found the following ten species which are aquatic species found in aerial conditions: Aphanocapsa rivularis, SCMI, SCTH, Oscillatoria boryana, OSGE, O. iwanoffiana, Gompho-

    nema acuminatum, Navicula subminuscula, Achnanthes convergens, and Cymbella delicatula (Table 3). Species in the Br group were cyanophytes and bacillariophytes such as NOCO, OSGE, ORRO, and NACR. Algae in the genus Nostoc live mainly in terrestrial habitats and appear to be attached to lichen, fungi, bryophytes, and vascular plants (Rai et al. 2002). The Br group plays an important role in habits of aerial algae by providing humid conditions. PIBO, NAGO, HAAM of the Dry and Hu groups were classified as aerial diatoms and are found under conditions with 80% humidity (Uher 2008), and also in conditions of 40% humidity and high light (Kim et al. 2011); therefore, it was thought that these aerial algae live in a wide range of conditions.

    Correlations among other environmental factors were tested to identify other environmental factors that could substitute for humidity and light intensity (Table 5). As a result, tree distance, water distance, and plant coverage were replaceable environmental factors.

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  • [Fig. 1.] Photographs the algae habitats sampled in Korea at the 24 stoneworks sites from 2009 to 2010. (A & B) Unjusa temple (lichen and aerial algae). (C & D) Jucksung-myeon stone wall (bryophyte). (E & F) Yeondae small temple (lichen and aerial algae).
    Photographs the algae habitats sampled in Korea at the 24 stoneworks sites from 2009 to 2010. (A & B) Unjusa temple (lichen and aerial algae). (C & D) Jucksung-myeon stone wall (bryophyte). (E & F) Yeondae small temple (lichen and aerial algae).
  • [Table 1.] Information on the 24 stoneworks from which algae were collected from March 2009 to October 2010
    Information on the 24 stoneworks from which algae were collected from March 2009 to October 2010
  • [Fig. 2.] Diagram of the method for measuring the environmental factors.
    Diagram of the method for measuring the environmental factors.
  • [Table 2.] The physico-chemical and ecological environmental factors at 24 stoneworks from March 2009 to October 2010
    The physico-chemical and ecological environmental factors at 24 stoneworks from March 2009 to October 2010
  • [Table 3.] A list of aerial algae and their habitats collected at 24 stoneworks from March 2009 to October 2010
    A list of aerial algae and their habitats collected at 24 stoneworks from March 2009 to October 2010
  • [Table 3-1.] Continued
    Continued
  • [Table 3-2.] Continued
    Continued
  • [Fig. 3.] Microscopic photographs of newly recorded species in Korea found at 24 stoneworks from 2009 to 2010. (A) Scytonema coactile var. thermalis. (B) Stigonema ocellatum f. ocellatum. (C) Scytonema coactile var. minor. (D) Oscillatoria boryana. (E) Synechococcus aeruginosus. Scale bar represents: A-E, 10 μm.
    Microscopic photographs of newly recorded species in Korea found at 24 stoneworks from 2009 to 2010. (A) Scytonema coactile var. thermalis. (B) Stigonema ocellatum f. ocellatum. (C) Scytonema coactile var. minor. (D) Oscillatoria boryana. (E) Synechococcus aeruginosus. Scale bar represents: A-E, 10 μm.
  • [Fig. 4.] Illustrations of newly recorded species in Korea found at 24 stoneworks from 2009 to 2010. (A) Synechococcus aerugonosus. (B) Oscillatoria boryana. (C) Scytonema coactile var. thermalis. (D) Scytonema coactile var. minor. (E) Stigonema ocellatum f. ocellatum. Scale bars represents: A-E, 10 μm.
    Illustrations of newly recorded species in Korea found at 24 stoneworks from 2009 to 2010. (A) Synechococcus aerugonosus. (B) Oscillatoria boryana. (C) Scytonema coactile var. thermalis. (D) Scytonema coactile var. minor. (E) Stigonema ocellatum f. ocellatum. Scale bars represents: A-E, 10 μm.
  • [Fig. 5.] Principal component analysis plot of aerial algae from 24 stoneworks in Korea during 2009 to 2010. Br, bryophyte coverage; Hu, humidity; Dry, negative correlation between humidity and canopy. ACIN, Achnanthes inflata; APEA, Aphanocapsa eachista; ANCI, Anabaena circinalis; APEL, Aphanocapsa elachista var. plantorica; APNA, Aphanothece naegelii; APPU, Aphanocapsa pulchra; APRI, Aphanocapsa rivularis; CHBI, Chroococcus bituminosus; CHMI, Chroococcus minutus; CHPA, Chroococcus pallidus; CHVA, Chroococcus varius; CYDE, Cymbella delicatula; CYSI, Cymbella sillesiaca; GOAC, Gomphonema acuminatum; HAAM, Hantzschia amphioxys; KLDI, Klebsormidium dissectum; LYAE, Lyngbya aerugineocoerulea; LYBI, Lyngbya birgei; NACO, Navicula contenta; NACR, Navicula crytocephala; NAGO, Navicula goeppertiana; NASU, Navicula subminuscula; NOCO, Nostoc commune; NOMI, Nostoc microscopicum; ORRO, Orthoceira roeseana; OSBO, Oscillatoria boryana; OSCH, Oscillatoria chlorina; OSGE, Oscillatoria geminata var. subphurea; OSOK, Oscillatoria okeni; OSTE, Oscillatoria terebriformis; OSUN, Oscillatoria uncinata; PIBO, Pinnularia borealis; PRVI, Protococcus viridis; SCCR, Scytonema crispum; SCMI, Scytonema coactile var. minor; SCTH, Scytonema coactile var. thermalis; STMA, Stigonema mamillosum; STOC, Stigonema ocellatum; SYAE, Synechococcus aeruginosus; SYAQ, Synechocystis aquatilis.
    Principal component analysis plot of aerial algae from 24 stoneworks in Korea during 2009 to 2010. Br, bryophyte coverage; Hu, humidity; Dry, negative correlation between humidity and canopy. ACIN, Achnanthes inflata; APEA, Aphanocapsa eachista; ANCI, Anabaena circinalis; APEL, Aphanocapsa elachista var. plantorica; APNA, Aphanothece naegelii; APPU, Aphanocapsa pulchra; APRI, Aphanocapsa rivularis; CHBI, Chroococcus bituminosus; CHMI, Chroococcus minutus; CHPA, Chroococcus pallidus; CHVA, Chroococcus varius; CYDE, Cymbella delicatula; CYSI, Cymbella sillesiaca; GOAC, Gomphonema acuminatum; HAAM, Hantzschia amphioxys; KLDI, Klebsormidium dissectum; LYAE, Lyngbya aerugineocoerulea; LYBI, Lyngbya birgei; NACO, Navicula contenta; NACR, Navicula crytocephala; NAGO, Navicula goeppertiana; NASU, Navicula subminuscula; NOCO, Nostoc commune; NOMI, Nostoc microscopicum; ORRO, Orthoceira roeseana; OSBO, Oscillatoria boryana; OSCH, Oscillatoria chlorina; OSGE, Oscillatoria geminata var. subphurea; OSOK, Oscillatoria okeni; OSTE, Oscillatoria terebriformis; OSUN, Oscillatoria uncinata; PIBO, Pinnularia borealis; PRVI, Protococcus viridis; SCCR, Scytonema crispum; SCMI, Scytonema coactile var. minor; SCTH, Scytonema coactile var. thermalis; STMA, Stigonema mamillosum; STOC, Stigonema ocellatum; SYAE, Synechococcus aeruginosus; SYAQ, Synechocystis aquatilis.
  • [Table 4.] Dominant species at 24 stoneworks in Korea during March 2009 to October 2010
    Dominant species at 24 stoneworks in Korea during March 2009 to October 2010
  • [Table 5.] Analysis of the correlations between environmental factors in the 24 stoneworks in Korea collected during March 2009 to October 2010
    Analysis of the correlations between environmental factors in the 24 stoneworks in Korea collected during March 2009 to October 2010