Arbuscular Mycorrhizal Fungi (Glomeromycota) Associated with Roots of Ammophila Arenaria Growing in Maritime Dunes of Bornholm (Denmark)

Vol. 80, No. 1: 63-76 , 2011 ACTA SOCIETATIS BOTANICORUM POLONIAE 63

ARBUSCULAR MYCORRHIZAL FUNGI (GLOMEROMYCOTA) ASSOCIATED WITH ROOTS OF AMMOPHILA ARENARIA GROWING IN MARITIME DUNES OF BORNHOLM (DENMARK)

JANUSZ BŁASZKOWSKI , B EATA CZERNIAWSKA Department of Plant Protection, West Pomeranian University of Technology Słowackiego 17, 71-434 Szczecin, Poland [email protected] (Received: March 11, 2010. Accepted: January 5, 2011)

ABSTRACT 155 rhizosphere soil and root mixtures were collected from under Ammophila arenaria colonizing maritime dunes of the island Bornholm (Denmark) to determine arbuscular mycorrhizal fungi (AMF) of the phylum Glomeromycota co-existing with this plant. In the laboratory , each mixture was divided into two parts. One part was used to establish a pot culture with Plantago lanceolata as the host plant to initiate sporulation of fungi that had not produced spores in field conditions. In the second part , the numerical and species composition of the spore populations of AMF sporulating in the field was determined. Spores of AMF were found in 70 field- collected samples and 134 trap cultures. They represented 26 species and six undescribed morphotypes in six genera of the Glomeromycota. Of them , 20 species and three morphotypes in five genera occurred in the field , and 16 species and three morphotypes in five genera were found in trap cultures. The fungi most frequently revealed were members of the genus Glomus ; a total of 17 species and six morphotypes of this genus were recognized. Considering the occurrence of spores in both field samples and trap cultures , the fungi most frequently co-occurring with roots of A. arenaria growing in the dunes of Bornholm were G. irregulare (present in 73.6% of samples) , followed by Scutellospora dipurpurescens (19.4%) and Archaeospora trappei (10.3%). However , Glomus irregulare mainly sporulated in trap cultures; spores of this fungus were found in only 0.6% of field samples. Other relatively frequently found species were G. aggregatum (9.0%), G. eburneum (7.1%), Paraglomus laccatum (5.2%), and S. armeniaca (6.5%). The species most abundantly sporulating in the field were G. aggregatum (produced 28.36% of all spores isolated) , G. badium (11.00%), and S. dipurpurescens (21.55%).

KEY WORDS: arbuscular mycorrhizal fungi, Bornholm, distribution, Glomeromycota, maritime sand dunes.

INTRODUCTION At present , AMF are placed in the phylum Glome- romycota C. Walker et Schuessler , comprising four orders , Arbuscular mycorrhizal fungi (AMF) occur commonly ten families , and fourteen genera (Schü βler et al. 2001; in the world and associate with 70-90% of vascular land Błaszkowski 2003; Oehl and Sieverding 2004; Sieverding plants (Smith and Read 2008). and Oehl 2006; Walker and Schüßler 2004; Walker et al. Habitats especially favoring AMF are maritime sand 2007a , b; Palenzuela et al . 2008; Walker 2008). The most dunes (Koske 1987; Dalpé 1989; Tadych and Błaszkowski numerous group of fungi in the Glomeromycota is the 2000a ), mainly because of their low nutrient content and genus Glomus Tul. et C. Tul. , including ca. 53% of all organic components (Koske 1988; Nicolson and Johnston AMF described to date , i.e. , ca. 210 species (Błaszkowski 1979). The association of AMF with maritime dune plants 2003). However , Morton (2000) hypothesized , when 154 may be of considerable ecological significance for their species were known in the literature , that the number of establishment and growth , because these fungi enhance existing species of AMF may be at least 2-fold higher. The plant nutrient uptake , increase plant tolerance to drought hypothesis agrees with the results of recent molecular and salt stress , and protect against soil pathogens (Koske et investigations of diversity of AMF indicating that many al. 2004). At least 32 newly described species of AMF revealed sequence types cannot be assigned to named fungi have originally been associated with roots of dune plants (e.g. Hijri et al . 2006). and many others have occurred in maritime dunes (Sridhar The reasons of omissions of these unknown species and Beena 2001; Błaszkowski 2003). functioning in different ecosystems around the world may 64 GLOMEROMYCOTA IN SAND DUNES OF BORNHOLM Błaszkowski J. et al. be (1) lack or rare sampling of AMF in most regions of the annual temperature is 7.9 °C; it is highest in August Earth , (2) the few specialized and experienced mycologists (16.7 °C) , and lowest in January (0.1 °C). dealing with morphology of members of the Glomeromy- cota , and (3) seasonal , rare or no sporulation of many AMF Soil chemical analyses in the field conditions (Gemma et al . 1989; Stürmer and The contents of total N and organic C were determined Bellei 1994 ; Stutz and Morton 1996). according to Kjeldahl , P and K after Egner-Riehm , and Mg An effective method forcing production of spores of after Schachtschabe (Ostrowska et al. 1991). AMF hidden inside roots of their host plants is cultivation of field-collected mixtures of rhizosphere soils and root Collection of soil and root samples, establishment fragments of these plants in successive (Stutz and Morton of trap and single-species cultures, and extraction of spores of AMF 1996) or long-term (Oehl et al . 2004) pot trap cultures. Bornholm is one of the 443 islands and the easternmost 155 rhizosphere soils and roots of sampled plants were located administrative district of Denmark (officially the collected on 2-3 October 2004 from a depth of 5-30 cm Kingdom of Denmark ) of the geographical coordinates of using a small garden shovel. About 100-200 cm 3 samples 55 °5’N and 14 °56’E. It occupies an area of ca. 600 km 2 were placed in plastic bags. After their transfer to a and the length of its coastal line is ca. 141 km. Because of laboratory in Poland , they were first stored at 4 °C for ca. the favourable climate , the plants growing on the island one month and then used to establish trap cultures. Trap are , e.g. orchids , anemone , and many species of the cultures were established to initiate sporulation of AM Mediterranean Sea region. Therefore , Bornholm is named a fungal species rarely sporulating in the field and species green island , and its flag is a modified flag of Denmark , in that did not produce spores at the time of collection of the which the white cross is replaced with a green one. Lawes- field samples. The growing substrate of the trap cultures son and Skov (2002) found that the highest plant diversity was the field-collected material mixed with an autoclaved in Denmark occurs on its major islands , including coarse-grained sand coming from maritime dunes adjacent Bornholm. to Świnoujście (pH 6.7; 12 and 26 mg L-1 P and K , The eastern , northern , and western coasts of Bornholm respectively; Błaszkowski 1995). The mixtures were pla- generally are rocky with only small sandy areas , whereas ced into 9 ×12.5-cm plastic pots (500 cm 3) and densely the southern coast is represented by extensive and wide (up seeded with Plantago lanceolata L. Plants were grown in a to 1 km) beaches and mobile dunes colonized mainly by greenhouse at 15-30 °C with supplemental 8-16-h lighting Ammophila arenaria (L. ) Link . provided by one SON-T AGRO sodium lamp (Philips In the literature , there is only one report of fungi found in Lighting Poland S.A.) placed 1 m above pots. The Bornholm. It regards the newly described species , Glomus maximum light intensity was 180 µE m-2 s-1 at pot level. irregulare Błaszk. et. al. , and co-occurring other AMF Plants were watered 2-3 times a week. No fertilizer was (Błaszkowski et al. 2008a). applied during the growing period. Trap cultures were for The aim of this paper is to show the results of investi- the first time harvested four months after plant emergence gations of the occurrence of AMF associated with roots of and then every ca. 6 months until 2008 . After each harvest , Am. arenaria colonizing maritime dunes of Bornholm. The the cultures were reseeded with P. lanceolata . Spores were presence of AMF was determined based on both spores extracted by wet sieving and decanting (Gerdemann and isolated from field-collected mixtures of the rhizosphere Nicolson 1963). soil and root fragments of Am. arenaria and pot trap Spores of identical morphological characters were used cultures established from part of each field mixture. The to establish single-species cultures. Single-species cultures spore populations of AMF revealed were analyzed using were established and grown as given in Błaszkowski et al . different statistical methods. Additionally , the known (2006), with two exceptions. First , instead of marine sand distribution of the revealed species and undescribed their growing medium was an autoclaved commercially morphotypes in maritime dunes of other regions of the available coarse-grained sand (grains 1.0-10.0 mm diam. – world is presented and discussed. 80.50%; grains 0.1-1.0 mm diam. – 17.28%; grains <0.1 mm diam. – 2.22%) mixed (5:1 , v/v) with clinopthilolite (Zeocem , Bystré , Slovakia) of grains 2.5-5 mm. Clino- MATERIALS AND METHODS pthilolite is a crystaline hydrated alumosilicate of alkali metals and alkaline earth metals having , e.g. , a high ion Study sites exchange capability and selectivity , as well as a reversible The study sites were maritime sand dunes located along hydration and dehydration. pH of the sand-clinopthilolite the bank of the Baltic Sea surrounding the Bornholm island mixture was 7.3. Second , the cultures were kept in belonging to Denmark . Mixtures of rhizosphere soils and transparent plastic bags , 15 cm wide and 22 cm high as root fragments were collected from eight dune sites located suggested by Walker and Vestberg (1994) , rather than open near Balka (site 1 ; 55° 02’N , 15° 06’E; Tab. 1 ), Boderne (2 ; pot cultures (Gilmore 1968). To prevent contamination of 55° 01’N , 14° 54’E ), Dueodde (3 , 6, and 7 ; 54° 59’N , the cultures with other AMF but still to allow exchange of 15° 04’E ), Hasle (4 and 8 ; 55° 10’N , 14° 42’E ), and gases , we left an opening , about 1 cm wide , in the centre of Snogebæk (5 ; 55° 01’N , 15° 07’E ). Most samples were the upper part of each bag , while the edges on both sides taken from sites 2 , 3, 6, and 7. were closed with small plastic clips. The cultures were Based on data from 1961-1990 (www.dmi.dk/dmi/index/ watered with tap water once a week , harvested after five danmark/klimanormaler.htm) , the mean annual sum of months when spores were extracted for study. To reveal rainfall in Bornholm is 604 mm; it is highest in November mycorrhizal root structures , root fragments located ca. 1-5 (76 mm) , and lowest in February (32 mm). The mean cm below the upper level of the growing medium were cut Vol. 80, No. 1: 63-76 , 2011 ACTA SOCIETATIS BOTANICORUM POLONIAE 65 off with a scalpel. The host plant of single-species cultures coefficient expresses the proportion of the number of was also P. lanceolata . spores of a particular species in all spores of AMF recovered. The total spore volume was calculated by Microscopy survey multiplying the total number of spores of a given species Morphological properties of spores and their wall by the average volume of a spore of this species. The structures were determined based on observation of at least average volume of a spore was calculated from its average 100 spores mounted in polyvinyl alcohol/lactic acid/ diameter and equation of a sphere. glycerol (PVLG; Omar et al. 1979) and a mixture of PVLG and Melzer’s reagent (1:1 , v/v). Spores were crushed to varying degrees by applying pressure to the cover slip and RESULTS AND DISCUSSION then stored at 65 °C for 24 h to clear their contents from oil droplets. These were examined under an Olympus BX 50 General data compound microscope equipped with Nomarski differen- The soil chemical properties of the sites sampled are tial interference contrast optics. Microphotographs were shown in Table 1. pH in 1M KCl ranged from slightly acid recorded on a Sony 3CDD color video camera coupled to to neutral. The contents of total N was very low , and the microscope. organic C low. The concentration of available Mg was Terminology of spore structure is that suggested by Stür - medium. The availability of K and P was very low to low. mer and Morton (1997) and Walker (1983). Spore colour Spores of AMF were found in only 70 of the 155 field- was examined under a dissecting microscope on fresh spe - collected samples , but they occurred in 134 trap cultures cimens immersed in water. Nomenclature of fungi and with each field sample , i.e. , in 87% of all the trap cultures plants is that of Walker and Trappe (1993) and Mirek et al. established. (info.botany.pl/czek/check.htm ), respectively. The authors The spores isolated from both the field samples and trap of the fungal names are those presented at the URL web cultures represented 2 6 species and 6 undescribed page http://www.indexfungorum.org/AuthorsOfFungal morphotypes in 6 genera of the Glomeromycota (Table 2). Names.htm. Specimens were mounted in PVLG on slides In the field samples , 20 species and three undescribed and deposited in the Department of Plant Protection , morphotypes in five genera were found , and 1 6 species and West Pomeranian University of Technology , Szczecin three morphotypes in five genera were isolated from trap Poland. cultures. Colour microphotographs of spores and mycorrhizae of Ten species and three undescribed morphotypes in four the formally described species can be viewed at the URL genera were found only in the field samples , and six http://www.agro.ar.szczecin.pl/~jblaszkowski/ . species and three morphotypes in two genera were revealed only in trap cultures. Ten species in four genera sporulated Statistical analysis in both the field and trap cultures. Differences in the structure of arbuscular fungal The low percent of the field-collected root-soil mixtures communities were investigated by determining the with the exceptionally low numbers of spores , the frequency of occurrence of species , spore abundance and disclosure in trap cultures of six species and three undes- species richness , and by calculating dominance coefficients cribed morphotypes not sporulating in the field , and the (Górny and Gruma 1981) and total spore volumes. Spore frequent occurrence of spores of species found in this study abundance , coefficients of dominance , and the total volume in the field of other dune sites of Poland and the world of spores of each species were determined based on spores indicate that the Bornholm dunes do not favour sporulation isolated only from field-collected samples. Frequency of of AMF. occurrence and species richness were calculated based on The high predominance of members of the genus Glomus spores isolated from both field-collected samples and trap in the communities of AMF of dunes of Bornholm agrees cultures. Frequency of occurrence was calculated by with the species composition of these fungi recovered from determining the percentage of field-collected samples and dunes of the Baltic Sea (Błaszkowski 1993a ,b), the Hel trap cultures from which spores of a particular species were Peninsula (Błaszkowski 1994a ), Italy (Giovannetti and recovered. Spore abundance and species richness were Nicolson 1983; Puppi and Riess 1987) , Scotland (Nicolson defined by determining the number of spores and species , and Johnston 1979) , Madras , India (Mohankumar et al. respectively , occurring in 100 g dry soil. Dominance 1988) , Canada (Dalpé 1989) , Florida (Sylvia 1986; Sylvia

TABLE 1. Chemical properties of soils of the eight examined maritime sand dune sites of Bornholm .

No. of site* pH in 1 M KCl Contents in Available forms in mg/100 g of soil

Total N org. C Mg K P

1 6.50 0.18 1.77 3.17 2.16 0.84 2 6.70 0.19 1.86 3.47 2.66 1.06 3 6.75 0.22 2.14 3.40 2.57 1.67 4 6.40 0.25 2.41 3.14 2.60 2.55 5 6.55 0.23 2.25 2.95 2.74 2.02 6 6.61 0.24 2.32 2.84 2.99 1.10 7 6.59 0.20 1.95 3.24 2.57 1.27 8 6.62 0.22 2.15 3.02 2.32 2.30 * see Materials and methods 66 GLOMEROMYCOTA IN SAND DUNES OF BORNHOLM Błaszkowski J. et al.

TABLE 2. Arbuscular mycorrhizal fungi associated with roots of Ammophila arenaria colonizing maritime dunes of Bornholm .

Fungi Frequency Dominance Total spore of occurrence (%) (%) volume µm 3×10 6 Field soils Trap cultures

Acaulospora lacunosa J.B. Morton 0.6 – 0.73 44.56 Acaulospora mellea Spain et N.C. Schenck 4.5 0.6 7.27 522.40 Ambispora gerdemannii (S.L. Rose, B.A. Daniels et Trappe) C. Walker, Vestberg et Schuessler 0.6 – 0.27 77.54 Archaeospora trappei (Ames et Linderman) Morton et Redecker 0.6 10.3 0.003 2.10 Glomus aggregatum Schenck et Smith emend. Koske 7.1 9.0 28.36 829.92 Glomus badium Oehl, Redecker et Sieverd. 0.6 – 11.0 84.70 Glomus claroideum Schenck et Smith 0.6 – 0.09 10.30 Glomus constrictum Trappe 0.6 2.6 0.09 17.15 Glomus drummondii Błaszk. et Renker – 1.3 – – Glomus eburneum L.J. Kenn., J.C. Stutz et J.B. Morton – 7.1 – – Glomus etunicatum W.N. Becker et Gerd. 0.6 – 0.18 7.18 Glomus fasciculatum (Thaxter) Gerd. et Trappe emend. Walker et Koske 0.6 1.9 10.0 552.90 Glomus geosporum (T.H. Nicolson et Gerd.) C. Walker 1.3 – 0.91 224.30 Glomus gibbosum Błaszk. 1.3 – 1.36 70.65 Glomus intraradices N.C. Schenck et G.S. Sm. 0.6 0.6 0.91 32.60 Glomus irregulare Błaszk., Wubet, Renker et Buscot 0.6 73.6 0.18 4.78 Glomus lamellosum Dalpé, Koske et Tews – 0.6 – – Glomus mosseae (T.H. Nicolson et Gerd.) Gerd. et Trappe 0.6 0.6 0.18 53.02 Glomus pustulatum Koske, Friese, C. Walker et Dalpé 3.9 2.6 4.91 226.26 Glomus versiforme (P. Karsten) S.M. Berch – 1.9 – – Glomus walkeri Błaszk. et Renker – 0.6 0.18 – Glomus 130 0.6 – 1.45 2.71 Glomus 149 – 3.2 – – Glomus 178 – 7.1 – – Glomus 194 0.6 – 0.82 1.12 Glomus 202 – 0.6 – – Glomus 206 0.6 – 0.27 0.54 Paraglomus laccatum (Błaszk.) Renker, Błaszk. et Buscot – 5.2 – – Scutellospora armeniaca Błaszk. 6.5 – 8.64 882.56 Scutellospora dipurpurescens Morton et Koske 19.4 5.8 21.55 13006.51 Scutellospora pellucida (Nicol. et Schenck) Walker et Sanders 1.3 – 0.18 62.08 Scutellospora persica (Koske et C. Walker) C. Walker et F.E. Sanders 0.6 – 0.009 137.19 and Will 1988) , Wisconsin (Koske and Tews 1987) , San The main reasons of the lack of sporulation in trap Miguel , California (Koske and Halvorson 1989; Koske , cultures of nine species and three morphotypes revealed only pers. comm.) , and Hawaii (Koske 1988; Koske and in the field-collected samples probably were (1) expulsion or Gemma 1996). In contrast , maritime dunes of Massachus- suppression of these fungi by species more competitive or sets (Bergen and Koske 1984; Gemma and Koske 1988; faster adjusting to the conditions of trap cultures and (2) Gemma et al. 1989), Rhode Island (Friese and Koske 1991; incompatibility of the above- and underground conditions Koske and Halvorson 1981) , the Atlantic coast from New and the plant host of these cultures with the ecological Jersey to Virginia (Koske 1987) , northern California (Rose requirements of these fungal species. Then , the lack of 1988) , and New South Wales , Australia (Koske 1975) were findings of six species and three morphotypes in the field dominated by Gigaspora and Scutellospora spores. samples , which later produced spores in trap cultures , may The high predominance and diversity of members of the have resulted from either the lack of sporulation of these genus Glomus in dunes of Bornholm supports earlier species at the time of sampling of the field root-soil mixtures reports of a good adaptation of these fungi to a wide range or too low level of colonization of roots of A. arenaria by of physical and chemical soil conditions (Anderson et al. these fungi. Many species of AMF sporulate seasonally or 1984; Grey 1991; Haas and Menge 1990; Porter et al. not at all in the field (Gemma and Koske 1988; Gemma et 1987). Daniels and Trappe (1980) found that the optimal al. 1989) and the beginning of sporulation requires attaining temperature for germination of spores of Glomus spp. was a minimum threshold level of root colonization , which is 14-22 °C, i.e. , a temperature range of a vegetative period of regulated by the fungal genotype alone or in combination Bornholm (www.dmi.dk/dmi/index/danmark/klimano- with host factors (Franke and Morton 1994; Gazey et al. rmaler.htm). In contrast , species of Gigaspora and 1992 ; Stutz and Morton 1996 ). Scutellospora prefer warmer soils (Koske 1981; Schenck et Frequency of occurrence al. 1975). Koske (1987) proved statistically that temperature was the main abiotic factor determining the structure The fungi most frequently identified were members of of AMF community in dunes extending from New Jersey the genus Glomus (Table 2) . A total of 1 7 species and six to Virginia. Acaulospora and Archaeospora spp. rarely morphotypes of Glomus were revealed. Other fungi dominate in AMF communities (Błaszkowski 1991 , 1993 a, relatively frequently occurring in the dunes of Bornholm b, 1994 a; Gerdemann and Trappe 1974). were Scutellospora species : four species were recognized. Vol. 80, No. 1: 63-76 , 2011 ACTA SOCIETATIS BOTANICORUM POLONIAE 67

Taking into account the frequency of occurrence of the Glomus aggregatum has been the only AMF found in AMF identified in both the field soils and trap cultures , the maritime sand dunes of Scotland (Nicolson and Johnston fungus most frequently occurring in dunes of Bornholm 1979; Koske pers. comm.). It has also dominated in mari- was G. irregulare , which sporulated very infrequently in time sand dunes and shores of Quebec , New Brunswick the field , but was the most frequently found fungus in trap and Nova Scotia , Canada (Dalpé 1989). cultures (Table 2). Another frequently occurring AMF was Scutellospora dipurpurescens has dominated in dunes of S. dipurpurescens , which , however , markedly more frequ- SNP (Błaszkowski 1993b; Tadych and Błaszkowski ently sporulated in the field conditions. Additionally , 2000a ). relatively frequently revealed fungi also were Ar. trappei , In contrast , the dunes of the Szczecin coast have been G. eburneum , S. armeniaca , and P. laccatum . Of them , S. dominated by G. corymbiforme , G. pustulatum and S. armeniaca was found only in field-collected samples , and dipurpurescens , and those of the Gdańsk coast by G. spores of G. eburneum and P. laccatum were revealed only constrictum and G. ? heterosporum Smith et Schenck in trap cultures. Archaeospora trappei spores also were (Błaszkowski 1993b ). Glomus microcarpum , S. dipur- extracted mainly from trap cultures. purescens and G. constrictum have predominated in the Hel Peninsula dunes (Błaszkowski 1994a). The dominant Spore abundance AMF of Italian dunes have been G. mosseae (Nicol. et S. calospora The overall average ( ±S.D.) spore abundance of AMF in Gerd.) Gerd. et Trappe , (Nicol. et Gerd.) G. macrocarpum G. microcarpum the field-collected soil-root mixtures was 7.36 ±22.10 and Walker et Sanders , and ranged from 0 to 153 spores in 100 g dry soil. (Giovannetti and Nicolson 1983; Puppi and Riess 1987). In Such a low spore abundance of AMF has been recorded the Lake Huron dunes , Canada , the dominating AMF have G. caledonium only in dunes of Cape Cod , Massachusetts (0.2-16.2 spores been (Nicol. et Gerd.) Trappe et Gerd. and a in 100 g dry soil; Bergen and Koske 1984) , Santa Catarina , species forming yellow brown spores (Koske et al. 1975). Brasil (0-69; Stürmer and Bellei 1994) , and Pakistan (1-29; The populations of AMF of dunes of the eastern coast of A. scrobiculata Khan 1974). the U.S.A. have been dominated by Trappe , G. gigantea G. deserticola G. fasciculatum Scute- In Poland , the average abundances of spores in 100 g dry , , , and llospora weresubiae soil of the Baltic Sea coastal dunes located in the former Koske et Walker (Bergen and Koske Gdańsk and Szczecin districts were 96.7 and 72.0 , 1984; Koske 1987; Koske and Halvorson 1981; Sylvia respectively (Błaszkowski 1993b ), the Hel Peninsula 99.8 1986; Sylvia and Will 1988). The most abundantly sporu- (Błaszkowski 1994a ), and the Słowiński National Park lating fungus in the Wisconsin Great Lake dunes has been G. etunicatum Scutellospora cora- (SPN) 75.9 (Tadych and Błaszkowski 2000a ). (Koske and Tews 1987). lloidea S. In maritime dunes of other regions of the world , the (Trappe , Gerd. et Ho) Walker et Sanders , heterogama S. spore abundance of AMF has also generally been markedly (Nicol. et Gerd.) Walker et Sanders and calospora higher than that in dunes of Bornholm: Florida (0-677; (Nicol. et Gerd.) Walker et Sanders have Sylvia 1986; Sylvia and Will 1988) , Lake Huron (0-632; predominated in the Lanphere-Christensen sand dunes of Scutellospora hawaiien- Koske et al. 1975) , Rhode Island (101-336; Koske and the Pacific Coastline (Rose 1988). sis G. microaggregatum Halvorson 1981) , Italy (0-250; Puppi and Riess 1987) , and Koske et Gemma , Koske , Gemma G. sinuosum New South Wales (0-110; Koske 1975). et Olexia , (Gerd. et Bashi) Almeida et Schenck , Glomus 807, G. intraradices and Diversispora Species richness spurca (C.M. Pfeiff. , C. Walker et Bloss) C. Walker et Schuessler have belonged to the most abundant species in Taking into account the spores isolated from both the the root zone of plants of Hawaiian dunes (Koske 1988; field-collected samples and trap cultures , the overall Koske and Gemma 1996). In dunes of San Miguel Island , average ( ±S.D.) species richness of AMF in dunes of the species most frequently occurring have been G. Bornholm was 1.83 ±1.26 and ranged from 0 to 6. etunicatum , G. pansihalos , and G. trimurales (Koske , pers. Similar overall average species richness data were comm.). Most spores isolated from sand dunes of Santa recorded from dunes of the Cape Cod , Massachusetts (av. Catarina , Brazil , have belonged to A. scrobiculata (Stürmer 1.7; Bergen and Koske 1984) , SNP (av. 2.4) and the and Bellei 1994). The dune plants of the west coast of Szczecin coast (av. 2.2) examined by Błaszkowski (1993b ), India have most frequently hosted G. albidum , G. clarum , New South Wales (av. 1.5-2.4; Koske 1975) , and Hawaii G. fasciculatum (Kulkarni et al. 1997), Gigaspora marga- (av. 2.0 and 2.4; Koske 1988 , Koske and Gemma 1996 , rita , G. sinuosum , S. calospora , and S. pellucida (D’Cunha respectively). Higher richness values were noted in dunes and Sridhar 2009). The coastal sand dunes of New South of the Gdańsk coast (av. 3.6; Błaszkowski 1993b ), the Hel Wales have been predominated by A. scrobiculata and a Peninsula (av. 3.9; Błaszkowski 1994a ), Rhode Island (av. red-brown-spored species (Koske 1975). 3.1; Koske and Halvorson 1981) , New Jersey to Virginia (av. 4.9; Koske 1987) , and Santa Catarina , Brazil (av. 5.9; Total spore volume Stürmer and Bellei 1994). The species of AMF of dunes of Bornholm forming spores of the markedly greatest total spore volume was S. Dominance dipurpurescens (Table 2). Other species yielding high The eudominants (of a coefficient of dominance of spore volumes were S. armeniaca , G. aggregatum , G. D>10.0% ) of dune soils of Bornholm were G. aggregatum , fasciculatum and A. mellea , as well as G. pustulatum and S. dipurpurescens , and G. badium (Table 2) . The domi- G. geosporum . nants (D=5.1-10.0%) were G. fasciculatum , S. armeniaca , Scutellospora dipurpurescens and S. armeniaca have and A. mellea . also ranked first in production of the greatest total spore 68 GLOMEROMYCOTA IN SAND DUNES OF BORNHOLM Błaszkowski J. et al. volume in maritime dunes of the Vistula Bar in north- NOTES ON MORPHOLOGY AND DISTRIBUTION western Poland (Błaszkowski et al. 2002a ). Another large OF UNDESCRIBED MORPHOTYPES biovolume was by G. fasciculatum . In maritime dunes OF AMF FOUND IN DUNES OF BORNHOLM extending from northern New Jersey to Virginia , the species of AMF forming spores of the greatest total spore Glomus 130 volume have been Gigaspora gigantea (T.H. Nicolson et The description and illustrations of morphological pro- Gerd.) Gerd. et Trappe , G. globiferum Koske et C. Walker , perties of Glomus 130 spores have been presented by G. tortuosum N.C. Schenck et G.S. Sm. , S. dipapillosa (C. Błaszkowski et al. (2001). Walker et Koske) C. Walker et F.E. Sanders , S. fulgida Earlier found associated with Am. arenaria growing in Koske et C. Walker , and S. verrucosa (Koske et C. Walker) maritime dunes adjacent to Tel-Aviv , Israel (Błaszkowski C. Walker et F.E. Sanders (Koske 1987). and Czerniawska 2006; Błaszkowski et al. 2001). Glomus 149 THE OCCURRENCE OF AMF FOUND IN MARITIME DUNES Spores single in the soil; hyaline; globose to subglobose; OF BORNHOLM IN OTHER DUNE SITES OF THE WORLD (71-)91(-122) µ m diam (Fig. 1). Spore wall with three hyaline layers (layers 1 -3 ; Fig. 2). Layer 1 evanescent , at Most of the species of AMF found in dunes of Bornholm first smooth , then roughened , (0.5-)1.3(-2.0) µ m thick , were earlier revealed in many other dune sites located in dif - rarely present in mature spores. Layer 2 laminate , smooth , ferent regions of the world (Table 3). Apart from the Born - (2.5-)3.7(-5.5) µ m thick. Layer 3 flexible to semi-flexible , holm dunes , in the literature there is no other report of the (0.8-)1.2(-1.6) µ m thick. Layers 1 -3 not reacting in finding Am. gerdemannii in dune soils. Other species of AMF Melzer’s reagent. Subtending hypha funnel-shaped , (10.0-) found in the study presented here , but so far rarely reported 12.3(-16.0) µ m wide at the spore base , occluded by a cur- from dunes are G. walkeri and Pa. laccatum . The former spe - ved septum continuous with spore wall layer 3. cies has originally been described from spores isolated from a Apart from Glomus 149, only G. achrum Błaszk. et al. pot culture derived from a mixture of the rhizosphere soil and and G. diaphanum J.B. Morton & C. Walker form spores roots of Oenothera drummondii Hook. colonizing maritime remaining hyaline throughout their entire life cycle , whose dunes adjacent to Tel-Aviv (Błaszkowski et al. 2006). The spore wall is 3-layered and the innermost layer is flexible finding of the fungus in northern Europe suggests it to be to semi-flexible. adapted to a wide range of temperature. Thus , it may be Compared with Glomus 149 spores , those of G. achrum widely distributed in the world , at least in sand dunes. are much smaller [(25-)43(-55) µm diam when globose vs. Paraglomus laccatum has originally been described (as (71-)91(-122) µm diam] , their spore wall layers 1 and 3 G. laccatum Błaszk.) from field-collected spores extracted stain intensively in Melzer’s reagent (vs. none of the spore from under Festuca sp. growing in a forest at Jastrzębia wall layers reacts in this reagent) , and have a much Góra in northern Poland (Błaszkowski 1988). The fungus narrower subtending hypha [(2.9-)4.3(-5.1) µm wide at the has also relatively frequently been isolated from trap spore base vs. (10.0-)12.3(-16.0) µm wide at the spore cultures with soils of different cultivated and non-dune base; Błaszkowski et al. 2009) . uncultivated sites of northern Poland (Błaszkowski et al . The main property separating Glomus 149 and G. 2002a; Tadych and Błaszkowski 2000b; Iwaniuk and diaphanum is the reactivity of spore wall layer 1 of the Błaszkowski 2004a , b). Dr. C. Walker found it in the latter species (Błaszkowski 2003; Morton 2002; vs. no United Kingdom (pers. comm.). Thus , this species reactivity). probably is widely distributed in the world. The infrequent disclosures of Pa. laccatum in field-collected soil samples Glomus 178 may result from the lack or irregular sporulation of this Spores formed singly in the soil (Fig. 3); sometimes also fungus in field conditions and a low persistency of its produced inside spores of other arbuscular fungi. Spores spores. In the field , a great part of AMF either do not hyaline; globose to subglobose; (35)63(78) µm diam; sporulate at all or their sporulation is infrequent and sometimes egg-shaped; 50-70 × 65-90 µ m; with one seasonal (Stürmer and Bellei 1994; Stutz and Morton subtending hypha (Fig. 3). Spore wall comprising three 1996). Paraglomus laccatum forms small , hyaline spores hyaline layers (layers 1-3; Fig. 4). Layer 1 , forming the with a delicate spore wall that may easily be decomposed spore surface , evanescent , usually slightly roughened on its by soil microorganisms. Many soil microorganisms are upper surface , (0.5)0.7(1.0) µ m thick , almost always highly parasites of AMF (Lee and Koske 1994). deteriorated or completely sloughed in mature spores. Still another interesting AMF found in the study Layer 2 laminate , smooth , (2.5)3.5(4.4) µ m thick , frequ- discusses here is G. irregulare , a species recently described ently stratifying into groups of laminae (sublayers) in from spores coming from under Am. arenaria colonizing vigorously crushed spores. Layer 3 flexible , smooth , ca. sand dunes of Bornholm (Błaszkowski et al. 2008a). 0.5 µ m thick , usually tightly adherent to the lower surface Glomus irregulare is probably widely distributed in the of layer 2 in slightly crushed spores (Fig. 4) , but frequently world , although rather rarely recorded to date , probably separated from this layer in vigorously crushed spores. because of the tendency to hide its spores inside roots and None of these layers stains in Melzer’s reagent. Subtending the exceptionally rare production of extraradical spores hypha hyaline; straight or curved; cylindrical to flared; (Błaszkowski et al. 2008a). It has probably earlier many (3.2)4.6(5.9) µm wide at the spore base. times erroneously been identified as G. intraradices based For the first time found in a pot trap culture with a mixture on both spore morphology and results of molecular of the rhizosphere soil and roots of Zea mays L. cultivated environmental analyses (Stockinger et al. 2009). near Faro , Portugal , in December 2000. Later isolated from Vol. 80, No. 1: 63-76 , 2011 ACTA SOCIETATIS BOTANICORUM POLONIAE 69 ; a t a 8 d 8 ; . 9 ; s l s 1 9 b e l 8 u r l 9 i p p a 1 n 6 6 8 6 ; W n u i 0 0 0 0 n 3 , d , 0 0 0 0 o 8 . a s n 2 2 2 2 l 9 r 4 a a . . . . 1 o l l l l 9 t a a a a a v 9 i n e l t t t t 1 v o i a l e e e e s , k l y H i i i i b s o s S k k k k , s d c w s s s s ; i a e 6 n o r 6 3 w w w w a 9 8 N k p 8 9 o o o o 9 8 z e 9 d 9 k k k k 1 9 s n k 1 n i 1 z z z z a 1 s a ł s s s s a , , a a o t e a a a a i i 6 2 B m ł ł ł ł t s a v K 0 t 9 ; l o d B B B B m e ; 0 9 b y . ; ; ; e ; ; c R n 7 2 l 1 , S a a a a a a a , ; n 8 , b a , t t t t t t t G ; b a 6 9 6 9 a a a a a a a u 3 1 6 d 2 v 8 1 0 9 d d d d d d d p 9 9 5 8 n 0 o 9 0 9 ...... n 9 9 i e a 9 l l l l l l l 9 0 2 1 2 1 u 1 1 k 9 b b b b b b b 1 2 G 0 7 e . . r , , , s 1 l l u u u u u u u . r 0 9 ; k e 0 0 0 o l a a 6 p p p p p p p e s 2 9 5 a k 9 9 9 a t t l 8 n n n n n n n K k o . 1 8 y 9 9 9 t l l e e a 9 u u u u u u u . 9 u 1 1 1 e d a K a l i i 1 , , , , , , , s 1 n W i i i i i i i i i i i ; a t t k k . W i a l k k k k k k k k k k k a e 8 s s t t d s s s s s s s s s s s s a t 8 e d n K e n w w n e t 9 i n w w w w w w w w w w w o c a o o o n e d 1 a n s o o o o o o o o o o o s n k k e r n r i n s k k k k k k k k k k k e z z e e a a k o a p r z z z z z z z z z z z p s s k k s k v i e v p s s s s s s s s s s s a a l e s s l f o e ł ł o a a a a a a a a a a a u u b i r o o a e ł ł ł ł ł ł ł ł ł ł ł B P B K R B B B K B B B A G G B K B K B H B B s n e , c s e e . m r r d u l o r p f m i r o , u s u t r w m p a e i u c e t v d c h a . t . , a c l S f i G m . , o n , u a a u t s m t c P c e e i u t a , t i r i . e t s a n s l a G e e n u e , t s n i o m s i s r u c u d o a d . p n . r m G . o S e . , G , m h t G m , m m o , e u e u u e e a t n r r a i e d a a e d i s l l s s . s o u u s e t r o G g o n s a a l e , m u u m c r c . i d p r m . . s i . u G e r G . t G , s e G c , m , e G i p , i m t r c m , e . a m i t i a u r u a S s d s u d d m i s t a e i , n o a u c i i s o l a c o r s i l m r s u b g u c a l o e d e a l o l e b r l . k b n i d r m t e m l e m i l b o g g G n p a a i c p . o i l . g , . m g u . h . w . G l a S G . S m l n . m , . G , r G , e , u u G i s i , s G s o , p m G i r , e e d , e n . u , d m d B c r c i e a e s m i S i n u . a e e c b o u d r , l d o m a m l s p G h r . s r a o l u a t d e u p m , o r e i e r o p t r g G f a c c p n a s a a e u m i m , i i m r s r l u r r o s t p u t u d l t a r o u r m e t d l r r l . i n t a n e r e u i g a e n u i d . s r . t l v g . . p A u p . . u a a u G i . . G . , r o p G G c g G G t , d f , i S a G G . e , , s , , n . i c e i i , r , , i m e l i i s G S g l m m g c . u m d d m m a , , i n e r u u g f u n n e u t t u G a d u o a t . e m r c c f o o a c , a p i i c . d . o e r l a i G s r r i m m m i s t t p r a a G A , o o t s u n s s s r z m m , , r t e s t i o e m n n o a u u a a a a g n n h e u c o o l r r s m i e m c r i i . o l c c g c i d d r r o . . s l c d . . . . n G . . r o a n e . a G G u e c , . u G G G G G b G t , m , G p y c S , , , , e m , . , . , s . a , m m s . u m l m m m m m e m m G A S t u u e m m r c t t e i u u u u u G a u u , , , a a i t t t t t u r t t l u a c c a a , a a a r a t l e d l l a a a a a c i c i a e u a s s s i i o d l a u d a e e i u u g g g g g c i p r r o o o i p i c c u r c c e e e e e p p t t n s c i i n n n s s o c c r r r r r g a s s e p p l u r c c s u u u o u r a e g g g g g l n n a a a l s t s l a l r m c c c a b g g g g g r r o l o f g u a n e r a r . r t t a a a a c c f i c i a a f a a l l l . n a a p a a ...... r c r u . . f G P G A G A G G G A S A G G G F A G G S A G G o s e i d c n e a , p l a s i o f n P r o , a e ) t e d o s d c m e a i r n n w t J r i a e o l , r u r a l r a c o w c e u i c a P r m ł c d o H , f y s e c f n a , k s e i y c o A a o y r d e l k n ) d n , i a p n r t n o n s a a a c d u P ( a ł u r p o u P e ł l w n e i l y T F a h t t , p o a o a W . t i i t l g , s , h i y r P n s s n , a e l o A E e s , l k C t L n o a o . a e . . t s P ( , i a z t u e c , p t S a e l n e r i I o r t , d . u i v A A a l a i t a h u . . i ó n , p l n d D s a T p U g M ź d e g y T a u N S S - a c n G . . l , S a u s u i n . I k e o t a s C s d a k a n h o 3 r U U a , I i c d n K o i , i n s r h p c a o , , a n n a a , n b n g b i i k E c a r l a i u k d w a P i c a ę i e r s n n r t o a n d p b n L o a a z , m n h i P i g f ń u a o r a n a d a i n r t a o y G B r t r a l o w l r r m l l l r w f r ę d o p s e u e i a e a a a u d ł a a a a a a l A n a a J c t n T G a i B G H H K I K I J K J L L K C C F F G 70 GLOMEROMYCOTA IN SAND DUNES OF BORNHOLM Błaszkowski J. et al. ; ; a 7 6 6 1 t 9 0 0 8 a ; 9 . 0 0 9 d 1 2 2 1 . m l . . a n l l b m a a o u m o s 6 6 t t p c r 8 m e e 8 n . o e 9 9 i i s u v 1 r 1 k k l G , s s e i . a , l d p k 5 w w a H s n , 8 o o t a e d 9 w k k e k n 1 e o z z s e a s s k k r a o k a a s z e e ł ł 0 s s o K k k 0 o l a B B s ; ł K 9 0 a ; ; K o 7 8 ; 2 B a a a ; 8 t t t W 9 9 K i ; 6 9 a a a 8 4 1 8 k ; 4 5 d 6 8 1 d d d 8 s 9 9 1 8 8 n 0 n 9 . . . 9 9 1 e 9 a 9 l l l w 9 0 o 1 1 1 k 9 s 1 b b b o 1 e 2 e r s . r i 1 u u u k k . l r k e e e o o l s z p p p a e s l e k k a v l s o l n n n K t k o s l k e a t l a e u u u s a ł o K e d a K B , , , o r B n H W i i i i K ; d a W a d K k k k k 7 n 9 9 9 d d d d s s s s s n m 8 a d n d 8 8 8 n e n n n a u 9 n w w w w a o c a a n 9 9 9 a a r k 1 a s o o o o a n 1 1 1 e e e r h n n m k k k k e e e e c k k o é é é e a r z z z z m k k s s s m y v p p p e g h s s s s r s s e l l l l r f o o e d a a a a i o ű a a a o a o ł ł e ł e ł t r a K K G T S H F D B B D K D B K B M R B , , m , e i u r t r a a e l l k u l u t g a s e r w u r . p i . m . G u , G t G e , a , l e s m u a e a a r t a c c c e o s i i i s c f s u s i i d s r r s s p a o r r e e r . e e p p m a v G p . . . r t . , . S S G e n S , , G i , a , a a , . s e a d d e e s i i G d c a s i c c i , e o c u u d s l l a m u s l m l a l c u r l e e o i . t e s a p p a m G r r l p . . t . e , u . S S n s p c i S G , , e i . s . , , c c m m S i n e s G m u u r , e d t a t , u f c a a a t a a l s l r . d m l m a u i e l u a u u u r G c t g t t r t u s t u , s t e u a a l r l s u n l p u l m i r r u u p u p e i t u . u c p . . p . s e i p . G . u c i n G G G , s S r p G d , , , a , u s . , . s m f m e b e S u m G . m c t u e c , i t u , i u a . G t t a d e l a d c l , c a a G a u i a l u a r r e c r , m i u t i c s a a i u s c n c m s r t r i c s t n e t u o c s c t i a n o n s m f i a r i m a c f t r a . . . . g f . s . a e . G G n G G . G r G , , o , , S G , g , i c s , i , m m g m e . m m e d u u a m c u r t t u u a i n G a . t t e u c c a d t d o , i i d , l a a d i G i r r i a a c u c c m t t m c , m i r i c o i g s s u u u u n r c a n m l t e e l t n n l r l u a a r u u a p c t t o l o l e t r e i r g p i e c c c n e . p r p i d e t a ...... a . . r . . s r t S P G S G G G G g G n G G . , , , , , , , , g , o i r , , s m i s c a m m m m m m m e m m A u e d m m . . c t i u u u u u u u u u , a i n t t t t t t t u u t t m c a G G a d e e d o l a a a a a a a c c i e u s a i , , l i i d d e a u g g g g g g s a p c c r m r o i i a a u r c i e e e e e e p t t s c o t u i n e e o o i r r r r r r s a s s m s l p l l l b r r c s u r l r l l g g g g g g n n u u a a b t s a a r c e e e e g g g g r i g g r o l l o p g e n a t a p p c c c a a c a a d g a a i f m l m . n p ...... r . u . S G S F G G G S A G A G G G G G G A G G G G A e d n i m e d i r a n t r i p a r u l S a c A o , c S . . P a m d o , v U A f n A a s . . k a , a o d r e r l S . S ) a i a . . l a i o n s . B i c n A ( P n o U . P U z e a i a A e i a l a . , t , t , t p S d g i t r i . a C s . s a r d d S a s s a c i . n , d o n B . n n i U n A n o d i t . o r k n e . V a a , a U l , C i t e a p l l n n c a n t a s S i , s o A i , l s v o n C o t a . l o . i a r u r i n I a t t i d o a a , i P w a d a S d g C e p U l d n r N . c a P s y C , s i e i . , a a C a n S i a d e , n t M l t i , o U u I h u 3 d , s k s n o a u o n n k n , h , h r p g e a n I s r r a c n i a c s c y E c e a n l C c a d i ń e r i e r e a l J B S a r ż i o n n L n t e h r a M h s i d g b e y o t a t g e o w d j s r B r e z o o w w w ł r m e w n n d r a a a a o e e e o e m r u s h o ł a a o A n n G T a N N N S N O O Q R S S O P i L M M M M M Vol. 80, No. 1: 63-76 , 2011 ACTA SOCIETATIS BOTANICORUM POLONIAE 71

trap cultures containing rhizosphere soils and roots of (1) Am. arenaria growing in mobile dunes of the 6 0

0 Mediterranean Sea adjacent to Cape Salinas , ; 2 7 . l 9

a Majorca , Spain , in August 2001 (one culture) , (2) ; 9 t b 1 e

8 Am. arenaria h

i colonizing dunes of the Medi- 0 c k 0 s y 2

d terranean Sea near Karabucak-Tuzla , Turkey , in w . a l o T a k June 2001 (one culture) , and (3) Am. arenaria t z d e s n a i a 7 ł colonizing dunes of the Baltic Sea overlaying k i 8 s B k 9 ; s w 1 Bornholm , in October 2004 (10 cultures) . 6 b o w s 0 , k o 0 a z w The distinctive morphological properties of k s 2 4 3 e b z a 0 0 T s a ł 7

0 Glomus 0 a k

9 178 are its small spores produced singly d B ł 2 2 s 9 n ; , i B 1 a w a b k ; t in the soil and remaining hyaline throughout their a a s e h i 7 2 a 7 6 2 c k n 9 0 d 9 w r 8 s 0 y 9 0 . 9 entire life cycle , their 3-layered wall structure in o e l 9 o 0 d 1 2 1 k z b 1 a 2 . , K z a l u C . T r s which layer 3 is flexible , and the unusually 8 ; l a p e a m 8 a 2 d d ł t n k 9 9 t n n l e m u B narrow subtending hypha (Figs 3 and 4). Addi- e a a 1 a 9 e i , i i i i i 1 d k G W k k k k k . n s Glomus l s tionally , the unique property of spores of s s s s s a d d a e w n n w w w w w c k t o a a o o o o o n e u

k 178 is that they do not sink in water. i k k k k k e z e e é r n z z z z z s k k e p a s s s s s a s s

l Results of preliminary molecular-phylogenetic f ł a a a a a a o o w e ł ł ł ł ł I B R D B B B K B B K analyses of the SSU rDNA sequences of spores of Glomus 178 (data not presented here) indicated it a d , i Paraglomus s

c to be most closely related to spp. , i.e. e u l c l i P. brasilianum , P. laccatum , and P. occultum , e d , p a a r .

d fungi also producing glomoid spores. Of them , a S i r , c t s u n only the former two species produce only hyaline l n i l e . e c p G s spores (Błaszkowski 1988; Błaszkowski pers. . e , r S m

u P. , observ.; Renker et al. 2007). Mature spores of u p s m r o u u occultum

t are slightly yellow (Morton and Redec- b p a i b l i d u

g ker 2001). . t . s S a u , c

G Glomus P.

i Although the spore wall of 178 and p a , s . c e r m a a e brasilianum G i consists of three layers , the innermost u e p , n r s . e e o s

S Glomus a p o component of this wall in 178 is a thin (ca. m , e s r s m a o a s

. P. brasilianum d e 0.5 µ m thick) flexible layer , and in it . i o g G c S m . , u , l . is a laminate layer , 1.0-2.2 µ m thick (Błaszkowski , e G l m e G , u m i p , s r i pers. observ.). Additionally , the upper surface of e s . o o d l e f S m n l i c r , s

e P. brasilianum i o

i spore wall layer 2 of is ornamented r o d r f m m e i a e a v s r m l k with minute ridges (Błaszkowski , pers. observ.; r . l a u . e a r r G t v G d w ,

n Morton and Redecker 2001; Spain and Miranda . , i . . m . G m G G u , u 1996) , whereas all spore wall layers of the fungus G s , , r , m o m o l m u l m u p u

s discussed here are smooth. e t t s u o c a s o l m i l l e

o Paraglomus laccatum r a forms spores with only a u e t l g b t s . s . b m n i u a

G 2-layered spore wall (Błaszkowski 1988; Renker o G g l p , c , . . . . m m G G et al. 2007) , not differentiating layer 3 of the G u G u , , , t e , e e a m d r spore wall of Glomus 178 . Moreover , the laminate i m a c u a i t e o l u a r n s a e u c P. laccatum s a i a u c spore wall layer 2 of consists of easily d g l t i s i o e e l c e r n o r l m e . . r u r e separating , thick (0.5-2.2 µm thick) laminae. The t . i p a G G l e . m . G , , c . .

S Glomus , G

s laminae of the spore wall layer 2 of 178 . m m , A G e , m e r e i u u G , , u t t r m c a , a a s a are thin (<0.5 µm thick) and always tightly adhere l a a i a e u s s a o d l e u g g s l i p c o o u l i e e p g s o c n n r e r s g to each other. e p l b u u u r r e g g l a a b m l r c c r e i g g r i g e r a t a a p g i a l a Apart from the differences listed above , the l l . n p ...... r . . u . G S F S A A G G G A G G species compared here also differ in size of their

. spores and subtending hyphae. Spores of Glomus a A . d S a .

d 178 generally are markedly smaller [(35-)63(-78) n o a U , C C d

s µm diam when globose vs. (52-)80-85(-131-140) e , t e n d t k a p m e e r

l P. brasilianum i r a s µm diam in and (50)87(130) µm in t a r o i u C P r u P h a c f l P. laccatum ,

c ] and have a narrower subtending t c a o a m c o n s i a f s r o s e hypha [(3.2-)4.6(-5.9) µm wide at the spore base t i o a . r e s c ) i i n s A n A c M . d ( P. brasilianum i o

e vs. (4.0-)6.2(-8.3) µm wide in and d s , e i S v a t t p d . e . n d i i i o s r n a n r s s P. laccatum n U A l

o (7.4-)9.7(-12.9) µm wide in ; Błasz- . a a . n o a P t l , o e l h r e S p L a n e o s e n . P e h v l c n o a a P u i e kowski 1988 , pers. observ.; Morton and Redecker c , i U r a e e m l , c a e d g C s c e r , i o S o e n I i . r a c a r d i n l P 2001; Renker et al. 2007]. , h i 3 B ś a n v G B a j v s h p n a i o , a C n u E c n a l r a r Glomus i v r o g l o o Another unique property of 178 is that its o e n L h P i h t a i g k u A c t n t i t s s i - B s o e a u r w l d s i e a e i e h spores float in water. Morton and Redecker (2001) o w e A n N n G T a i S Ś T T V V W W W reported that Archaeospora trappei spores also tend 72 GLOMEROMYCOTA IN SAND DUNES OF BORNHOLM Błaszkowski J. et al. to float in water. Indeed , spores of this fungus sometimes do their empty or almost empty sporiferous saccules that then not sink in water , but only when they are associated with function as a “buoy” (Błaszkowski , pers. observ .).

78 Vol. 80, No. 1: 63-76 , 2011 ACTA SOCIETATIS BOTANICORUM POLONIAE 73

Glomus 194 In Melzer’s reagent , only spore wall layer 1 stains Spores formed singly in the soil; pale yellow; globose to purplish-red. Subtending hypha straight or slightly recur- subglobose; (52-)62(-68) µ m dim; rarely ovoid; 49-69 × ved; cylindrical to funnel-shaped; ( 8.0-)11.1(-17.5) µ m 58-84 µ m; with one subtending hypha (Fig. 5) . Spore wall wide at the spore base; open or occluded by a curved consists of three layers (layers 1-3; Fig. 6). Layer 1 semi- septum continuous with spore wall layer 3. permanent , hyaline , (1.0-)1.7(-2.1) µ m thick , usually Similarly to Glomus 202 spores (Figs 7 and 8) , those of present as more or less deteriorated structure in mature G. fasciculatum occur in aggregates and singly in the soil , spores. Layer 2 laminate , pale yellow , (2.3-)4.3(-5.8) µ m are pale yellow in colour , and their spore wall comprises thick. Layer 3 flexible to semi-flexible , (0.5-)0.8(-1.0) µ m three layers of which layer 3 is flexible to semi-flexible thick. In Melzer’s reagent , only spore wall layer 2 stains (Błaszkowski 2003). However , G. fasciculatum spores purplish red (Fig. 6) . Subtending hypha cylindrical to generally are markedly larger [(50-)105(-130) µm diam funnel-shaped , 2.8-4.0 µ m wide at the spore base , occluded when globose vs. (38-)67(-84) µm diam when globose in by some innermost laminae of spore wall layer 2 and a cur- Glomus 202], their spore wall layer 1 is a permanent ved septum continuous with spore wall layer 3. structure remaining intact in even older spores (vs. short- Morphologically , the described species of the Glomero- lived , frequently highly decomposed or completely sloug- mycota most resembling Glomus 194 are G. drummondii hed at maturity) , and have a subtending hypha of a more and G. walkeri , fungi also producing spores singly in the regular shape (cylindrical vs. cylindrical to funnel-shaped). soil whose spore wall consists of three layers of similar Most importantly , in Glomus 202 only spore wall layer 1 phenotypic properties (Błaszkowski et al. 2006). Moreover , stains in Melzer’s reagent , whereas in G. fasciculatum the G. drummondii spores overlap in size with those of the spore wall components reacting in this reagent are layers 1 species discussed here. The main differences separating and 2. Glomus 194 from G. drummondii and G. walkeri hide in Glomus 206 the biochemical properties of the components of their spore wall. In Glomus 194, spore wall layer 2 stains in Melzer’s Spores formed in loose aggregates , more rarely singly in reagent (Fig. 6) . In G. drummondii , the reactive component the soil; pale yellow; globose to subglobose; (45-)70(-90) of its spore wall in this reagent is layer 3 , and in G. walkeri µm diam; with one subtending hypha (Fig. 9) . Spore wall layer 1. Additionally , even the lower limits of the range of with two layers (layers 1 and 2; Fig. 10). Layer 1 muci- width of the subtending hypha of spores of G. drummondii laginous , rather short-lived , hyaline , (0.4-)0.6(-0.8) µ m [(4.1-)6.2(-9.3) µ m wide at the spore base] and G. walkeri thick. Layer 2 laminate , smooth , pale yellow , (2.1-)3.8(-5.8) [(7.4-)9.1(-12.7) µ m wide at the spore base] exceed the thick. In Melzer’s reagent , only spore wall layer 1 stains upper limit of that of Glomus 194 spores. purplish-red (Fig. 10). Subtending hypha straight or slightly recurved; cylindrical to funnel-shaped; (4.0-)7.5(-10.0) µm wide at the spore base; pore open. Glomus 202 Of the known species of the Glomeromycota forming Spores formed singly and in loose aggregates in the soil; glomoid spores of a 2-layered spore wall in which layer 2 pale yellow; globose to subglobose; (3 8-)67(-84) µ m diam; is laminate , Glomus 206 is most closely related in morph- with one subtending hypha (Fig. 7) . Spore wall with three ology to G. antarcticum , G. aureum , G. deserticola , and G. layers (layers 1-3; Fig. 8). Layer 1 mucilaginous , rather pallidum . Spores of all these fungi form mainly in conglo- short-lived , hyaline , (0.8-)2.2(-3.5) µ m thick. Layer 2 merates , are yellow-coloured , and more or less overlap in laminate , smooth , pale yellow , (3.3-)4.5(-10.0) µ m thick. size (Błaszkowski , pers. observ.; Cabello et al. 1994; Hall Layer 3 flexible to semi-flexible , (0.5-)0.8(-1.5) µ m thick. 1977; Oehl et al. 2003 ).

9 10

Figs 1 and 2. Glomus 149. 1. Intact spores. 2. Spore wall layers (swl) 1-3. Figs 3 and 4. Glomus 178. 3. Intact spores. 4. Spore wall layers 1-3. Figs 5 and 6. Glomus 194. 5. Intact spore. 6. Spore wall layers 1-3.; note swl 2 stained intensively in Melzer’s reagent. Figs 7 and 8. Glomus 202. 7. Spores in a loose aggregate. 8. Spore wall layers 1-3. Figs 9 and 10. Glomus 206. 9. Spores in a loose aggregate. 10. Spore wall layers 1 and 2; layer 1 stained in Melzer’s reagent. Figs 1, 2, 8 and 9. Spores in PVLG. Figs 3, 5 and 7. Spores in lactic acid. Figs 4, 6 and 10. Spores in PVLG + Melzer’s reagent. Bars: Figs 4-6, 8 and 10 = 10 µ m; Figs 1-3, 7 and 9 = 20 µ m. 74 GLOMEROMYCOTA IN SAND DUNES OF BORNHOLM Błaszkowski J. et al.

The most evident difference readily separating Glomus rhizal fungal species new for Poland and Europe. Mycotaxon 206 from most of the species listed above is the reactivity 81: 281-292. of their spore wall layer 1 in Melzer’s reagent. Apart from BŁASZKOWSKI J. , ADAMSKA I. , CZERNIAWSKA B. 2003. Acaulospora scrobiculata Glomus versiforme Glomus 206, spore wall layer 1 of only G. aureum stains in and (Glome- this reagent (Błaszkowski , pers. observ.; Oehl et al. 2003). romycota) , arbuscular fungi newly and second time , respectively , found in Poland. Acta Mycol. 3 8 (1/2): 31-42. However , compared with Glomus 206 spores , those of G. aureum BŁASZKOWSKI J. , CZERNIAWSKA B. 2006. The occurrence are produced in sporocarps (vs. in loose aggregates of arbuscular mycorrhizal fungi of the phylum Glomeromyco - in Glomus 206 ; Fig. 9) , usually are ovoid (vs. globose) , and ta in Israeli soils. Acta Soc. Bot. Pol. 75: 33 9-350. slightly smaller [(27-)40-60 µm diam when globose vs. BŁASZKOWSKI J. , CZERNIAWSKA B. , KOWALCZYK S. , (45-)70(-90) µm diam when globose]. TURNAU K. , ZUBEK S. Ambispora gerdemannii and Glo - mus badium , two species of arbuscular fungi (Glomeromyco - ta) new for Europe and Poland , respectively. Acta Mycol. (in ACKNOWLEDGMENTS press). BŁASZKOWSKI J. , CZERNIAWSKA B. , WUBET T. , This study was partly supported by the Ministry of SCHÄFER T. , BUSCOT F. , RENKER C. 2008a. Glomus irre- Science and Higher Education , grant no. 164/N- gulare , a new arbuscular mycorrhizal fungus in the Glome- COST/2008/0. romycota . Mycotaxon 106: 247-267. BŁASZKOWSKI J. , CZERNIAWSKA B. , ZUBEK SZ. , TURNAU K. 2008b. Glomus intraradices and Pacispora LITERATURE CITED robiginia , species of arbuscular mycorrhizal fungi (Glome- romycota) new for Poland. Acta Mycol. 43: 121-132. ABE J .-I.P. , KATSUYA K. 1995. Vesicular-arbuscular mycorrhi - BŁASZKOWSKI J. , RENKER C. , BUSCOT F. 2006. 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