Distribution and Ecology of Clathrus archeri in Romania

Although Clathrus archeri is a widely spread species in the Western Europe, in Romania it is considered a rare species, identified from only eight sites. In July 2013, it was found in two new sites from Gurghiu and Bârgău Mountains, in the Romanian Eastern Carpathians. This paper presents a detailed description of the new recorded specimens and of the habitat where this fungus was found. Plant communities where Clathrus archeri was recorded belong to the “mountain hay meadows” habitat type (Festuco rubrae Agrostietum capillaris community). Taking into consideration the previous published data, the comparison with other habitats types in which this species occurs suggests that Clathrus archeri has no special preferences for certain environmental conditions.


Introduction
Clathrus archeri (Berk.)Dring [Anthurus archeri (Berk.)E. Fisch.] was introduced to Europe in 1914 in Eastern France (Vosges Mts.), probably together with wool imports from Australia (Kreisel H, 2006;Salcedo et al., 2006).It has since spread throughout the whole Europe (Desprez-Loustau, 2009).Its name derives from the Greek kleithron = grid, box, cage and archeri = named after Archer.This fungus, also named "devil's fingers", was first described as Lysurus archeri by Rev. M. J. Berkeley (1860) and later it was transferred to Anthurus because of its free arms (rather than having a cage form).After that, Dring (1980) transferred it to Clathrus, a genus that includes the so-called "cage fungi", many of them with tropical distributions or Southern Hemisphere origins.The history of its presence in Europe is interesting.The fungus spread fast throughout the northeast of France and was discovered in 1968 in Enfants Noyés region from Belgium (Piérart and Girard, 1969;Fraiture, 2010), which was for more than 20 years the only location in that country where the species was known.Later, it spread to Germany, Austria, Switzerland, Italy and the centre of France (Fourré, 1985).According to Parent et al. (2000), sporocarp abundance is high for this species.Other authors too (Parent and Thoen, 1986) regard the hypothesis that this fungus was introduced to Europe on the wool of sheep from Australia and New Zealand as plausible.According to these authors, the Australian fungus has become established in a large area of central Europe.Also, it has been recorded from the Iberian Peninsula (Sarrionandia et al., 2010).After reports of it spreading around Europe, its presence was also found in other regions such as Santa Cruz in California (North America) (Arora and Burk, 1982).
Clathrus archeri is a rare macromycetes species in Romania (Tănase and Pop, 2005) although it is one of the most recorded species of Clathrus in other European countries.It is also a red-listed species in several countries: Bulgaria (Gyosheva et al., 2006), Ukraine (Didukh, 2009) and Denmark (Vesterholt, 1998).
During a mycological survey in the Romanian Carpathians, in July 2013, two new sites for Clathrus archeri were recorded.The purpose of this paper is to provide information regarding the distribution of this species in Romania (based on both current and historical data) and to determine the environmental and habitat characteristics of the places where the samples were found.

Materials and methods
The study is based on the material collected in the Romanian Eastern Carpathians: Bârgău Mountains (47º16'57.13'' N,24º56'37.05'' E,1.052 m altitude) and Gurghiu Mountains (46º 38'29.9'' N,25º10'42.05'' E,1.195 m altitude).The occurrence of Clathrus archeri in Romania has been mentioned previously in the scientific literature (Beres, 1996;Beres, 2012).The article has been structured in two parts.The first part contains information about the species distribution in Romania and the second part contains information about the sites recorded in 2013.Sites where the species was found are shown on the map of Romania (Fig. 2).The material was identified based on macroscopic and microscopic characters analyses on the bases of the following literature: Breitenbach and Kränzlin (1986), Borgarino and Hurtado (2004), Bon (2004), Courtecuisse (2000), Consiglio and Papetti (2001) and Hans (2001).The scientific names have been updated using Index Fungorum database (http://www.indexfungorum.org/names/names.asp).One voucher specimen from the examined material was deposited in the Herbarium [I] of the "Alexandru Ioan Cuza" University from Iaşi, Faculty of Biology [voucher I 182335].The description of the species is based on the new specimens collected by us from the two areas mentioned above.At the same time, we recorded all the plants species and vegetal communities in which the species occur.

Results and discussion
Clathrus archeri is easily recognized by its characteristic appearance, with 4-8 red radial branches.It can be confused with Aseroe rubra Labill.(Starfish fungus), but this species has a broad disk at the apex of the pseudostipe and numerous bifid arms.In past, this species was recorded as extremely rare species, known only from The Royal Botanical Garden Kew and from the Surrey region of England (Pegler et al., 1995), but in the last period Aseroe rubra is more extended in England.
In the early stage, the sporocarp is a white gelatinous 'egg', 2-4 cm in diameter, up to 6 cm tall, often smaller though, with a spherical to ovoid shape and a white rhizomorph at the base.It has a thick white to ochre peridium with a squamous surface and is furrowed due to the folded arms within the 'egg'.The thin, gelatinous endoperidium is green-brown colored.The 'egg' bursts open at maturity with its 4-7 long slender arms (ca.6-10 cm in length and 1.5-2 cm width) narrowing from the base to the apex, pale pink or red-orange, white at the base, and irregularly covered with the greenish brown gleba, fragile and spongy, slightly trapped inside the volva (remains of the 'egg').The gleba has an odor of rotting meat, which attracts flies and other insects.Usually, the red, transversely rugged arms are horizontally broken and spread around (Photo 1).Description of our specimens is in full agreement with the descriptions of Clathrus archeri provided in several other papers (Breitenbach and Kränzlin, 1986;Kreisel, 2001;Tănase et al., 2009;Pegler et al., 1995;Jülich, 1989;Calonge, 1998).
Although some authors consider this species as inedible (Gerhardt, 1999;Consiglio and Papetti, 2001;Borgarino and Hurtado, 2004), others say that it is edible in its young stage despite its disagreeable smell and taste (Hans, 2001).Beres (1996Beres ( , 2012) )   and Gurghiu Mountains.Interestingly, we found this species in the most southern part of its Romanian areal (Poiana Repaş) and at the highest altitudes (approximately 1,200 m).This is its highest known location in Romania.Until now, it was found at altitudes ranging between 300 and 900 m.This confirms that this species has a broad altitudinal range.
The absence of any kind of ordinary maintenance, fertilization and the overgrazing by sheep, can create unfavourable conditions for growth and development of valuable autotrophic plants.Also, these processes create optimal conditions for the establishment and spreading of Nardus stricta.The areas with Nardus stricta, through overgrazing, depending on its intensity, will evolve either towards meadows of Agrostis capillaris, Festuca rubra and Festuca nigrescens by reducing the abundance of Nardus stricta, or to tall herb nitrophilous communities with Rumex alpinus and Urtica dioica through the complete removal of Nardus stricta.Therefore, these conditions offer few explanations for the connection between sheep grazing and the spreading of the fungus.This species of Australian origin prefers places with high intensity of grazing by sheep, or areas that are situated near these places.
The sporocarps were found inside the grass layer (20 cm height) dominated by Nardus stricta and obviously affected by overgrazing (Photo 2).Also, we identified two associated fungi species (Bovista nigrescens and Annelaria semiovata) which occur frequently in the over-grazed areas.In addition, Macrolepiota procera and Lycoperdon perlatum were found, species occurring from summer to autumn during wet periods.
A comparison with other habitats types in which this species have been identified suggests that Clathrus archeri has no special habitat preferences.It was identified within a wide altitudinal range and in a variety of habitat types.It has been found in Germany, in the Alps Mts., at 1,200 m altitude (Jülich, 1989).In the Ukraine it was found in the Ukrainian Carpathians in deciduous forests situated on areas with large quantities of organic matter (Zykova, 2007).In Poland, this species is commonly recorded in oak forests and meadows adjoining forests (Halama et al., 2010;Szczepkowski and Obidziński, 2012).Also, Clathrus archeri is established in different man-made habitats such as cemeteries, parks, recreational forests that are close to cities, etc.In some European countries, this species is considered as invasive (Desprez-Loustau et al., 2007;Wojewoda and Karasiński, 2010).The only factor influencing the expansion of this species could be the calcium content of soil, as Clathrus archeri does not thrive on calcareous soils (Parent et al., 2000;Kreisel 2006).

Conclusions
The article presents two new (for Romania) sites in which Clathrus archeri has been identified.These sites are situated at the highest elevations in Romania, known for their alien species and are located in mountain hay meadows overgrazed by sheep, in Bârgău and Gurghiu Mountains.Taking into consideration the previous published data, the species does not prefer a certain habitat type.The only aspect linking the habitats where Clathrus archeri occurs is the strong impact of human activity.