BIOLOGIJA. 2018. Vol. 64. No. 3. P. 181–190 © Lietuvos mokslų akademija, 2018

Reported and potential bioluminescent species in Lithuania

Asta Malakauskienė Bioluminescent species are those producing and emitting light by chemical reactions and using it for a wide range of functions Kaunas Botanical Garden, important for survival, hunting, camouflage, mating, recognition, Vytautas Magnus University, and communication. Studies on Lithuanian bioluminescent spe- Ž. E. Žilibero St. 6,

Kaunas 46324, Lithuania cies biodiversity are scarce. The aim of this study was to review available information about reported and potential (found near the borders of the neighbouring countries) bioluminescent (fire- flies, fungi, centipedes, springtails), and luminescent (mosses) species in Lithuania. Available sources of literature on the diver- sity of Lithuanian, Latvian, Polish, and Belarusian bioluminescent species were studied, and folklore and verbal evidence of seen bio- luminescent species were analysed as well. All collected informa- tion was generalized and presented as a list of Lithuanian biolu- minescent species. The results showed that representatives of 26 different bioluminescent and one luminescent species may glow in the dark in Lithuania depending on the season, temperature, humidity, pH and oxygen presence in their environment: two re- ported and one potential (immigrating from Poland and Belarus) species of ; recently reported one species of bioluminescent centipedes from the family of Geophilus; one potential species of bioluminescent springtail (reported in Latvia and Poland); 21 re- ported species of bioluminescent fungi; one reported species of lu- minescent moss. Glowing must be confirmed for two fungi species mentioned in folklore, also one species is found that does not glow in Lithuania but is bioluminescent in North America. Specimens of Chlorociboria sp. and Xylaria hypoxylon found in the Botanical Garden of Vytautas Magnus University did not glow, while Armil- laria mellea glowed brightly emitting green light.

Keywords: bioluminescent, , centipede, springtail, , moss

INTRODUCTION click-beetles, most of other examples are in the sea (McCapra, 1976). In general, is Although the best known terrestrial luminescent produced through chemical reactions in which organisms are firefly, glow-worm, and certain substrates, called , and , called , are involved in the production of light (Shimomura, 2006). Luminescence provides a se- * Corresponding author. Email: [email protected] lective advantage mediated through its detection 182 Asta Malakauskienė and responses by other organisms; its functions public is usually aware only of the glowing firefly may be classed as defensive, offensive, or com- (Lampyris nocticula and Phosphaenus hemipter- municative (Woodland Hastings, 2011). While us) and sometimes fungi (mostly Armillaria mel- in nature plants do not use chemical reactions lea) species. The aim of this study was to review to produce light, scientists have already tried the available information about reported and to reconstruct complex metabolic pathways of potential (found near the border of the neigh- prokaryotes and force them to function in plant bouring countries and having the potential of chloroplasts, leading to emission of light visible migrating to Lithuania) bioluminescent (fire- to the naked eye in the dark (Krichevsky et al., flies, fungi, centipedes, springtails), and lumi- 2010). nescent (mosses) species in Lithuania. Recent research on the behaviour and the ecology of European bioluminescent species MATERIALS AND METHODS seems to lag behind compared to other con- tinents (De Cock, 2009). There may be several This paper is an overview of available informa- reasons for European fireflies being less studied: tion about all the bioluminescent species found, European fireflies are less eye-catching and of seen, and reported in scientific works or the me- lower biodiversity of species compared to other dia, mentioned in Lithuanian folklore, or hav- continents. Firefly displays are only seen late at ing the potential of migrating to Lithuania from night, but the high degree of urbanisation, in- the neighbouring countries (Latvia, Poland, Ka- dustrialisation and intensive agriculture disturb liningrad region, or Belarus). Verbal confirma- their observation (De Cock, 2009). New studies tion of seen bioluminescent species, which had on the application of bioluminescence give hope not been reported before, were also collected that this natural phenomenon will be a great tool if possible. Usually the Lithuanian public are for creating more sustainable urban spaces in not aware of other bioluminescent species, ex- future: with glowing street trees (Dr. Alexander cept the firefliesLampyris ( nocticula and Phos- Krichevsky’s research group at the State Uni- phaenus hemipterus) and, in rare cases, fungi versity of New York, later at “Gleaux” or former (mostly Armillaria mellea). It is hard to confirm “Bioglow”, US), plants shining as desk lamps for if the species reported or mentioned in folklore reading books (Prof. Michael Strano’s research actually glow in Lithuania during a certain group at Massachusetts Institute of Technology), season and under environmental conditions as and glowing facades of buildings (Sandra Rey’s there is very little photographic evidence pub- research group at “Glowee” in France). lished. All collected information was general- Studies on the biodiversity of Lithuanian bio- ized, concentrated, and presented as a list (in luminescent species are scarce, while the general Table 1).

Table 1. List of reported and potential bioluminescent species in Lithuania Potential of migrat- Bioluminescent species Reported in Lithuania Bioluminescent features ing to Lithuania Firefly Females glow (underside of Lampyris nocticula Yes their last three abdominal seg- ments) and do not fly Both females and males are feebly bioluminescent (glowing Phosphaenus hemipterus Yes underside of their last two ab- dominal segments in response to disturbance) and do not fly Bioluminescent species in Lithuania 183

Table 1. (continued)

Verbal confirmation by six Phausis splendidula or different unrelated persons. Reported in Poland Females glow, but do not fly, syn. Flying fireflies, glow in green, and Belarus males fly and glow Lamprohiza splendidula spotted in the western and southern regions of Lithuania Centipedes (Geophilus) Yes. Reported in 2012 in the residential area of An- takalnis, Vilnius; another The underside of its body verbal confirmation received glowed, leaving green slime in 2018, to the effect that it when touched. The glowing was spotted in the residential specimen from Vilnius Bel- Geophilus sp. area of Karoliniškės, Vilnius. montas district was described In September 2018, one glow- by Ingrida Šatkauskienė (Assoc. ing specimen was caught in Prof., VMU) as one of the two Vilnius Belmontas district and possible species: Geophilus ea- was brought for analysis to soni or Geophilus carpohagus Vytautas Magnus University (VMU) Springtails (Collembola) A species wide- spread in the North- Anurida granaria ern hemisphere. Whole body emits light Reported in Latvia and Poland Fungi Yes. Research on more de- Armillaria cepistipes Glowing young tailed identification is needed Yes. Research on more de- Armillaria gallica Glowing young mycelium tailed identification is needed Armillaria mellea Yes Glowing young mycelium Yes. Research on more de- Armillaria ostoyae Glowing young mycelium tailed identification is needed Reported in Estonia Armillaria tabescens Glowing young mycelium and Germany Chlorociboria aerugina- Yes. Reported in some re- Glowing young mycelium scens ferences Glowing fruiting bodies? In folklore it was called Clavaria botrytis or syn. Bioluminescence of this spe- “naktižibas, naktižibis”, mean- Ramaria botrytis? cies is not confirmed by visual ing “shining at night” evidence Collybia tuberosa Yes Glowing young mycelium Collybia radicata or syn. Yes Glowing young mycelium Xerula radicata epipterygia Yes Glowing young mycelium 184 Asta Malakauskienė

Table 1. (continued)

Glowing young mycelium and Mycena haematopus Yes fruiting bodies Mycena inclinata Yes Glowing young mycelium Mycena maculata Yes Glowing young mycelium Mycena polygramma Yes Glowing young mycelium Mycena pura Yes Glowing young mycelium Mycena rosea Yes Glowing young mycelium Mycena sanquinolenta Yes Glowing young mycelium Mycena stylobates Yes Glowing young mycelium Mycena zephirus Yes Glowing young mycelium Omphalotus olearius Yes. Very rare, only one habi- Glowing mycelium and fruiting tat known body stipticus The species is found in Lithu- Does not glow in Lithuania, ania, but it is not biolumines- but is bioluminescent in North cent here America Suillus bovinus? Yes. In folklore it was called Glowing fruiting bodies? “nakcižieda”, meaning “bloom- Bioluminescence of this spe- ing at night”, naktižibas, cies is not confirmed by visual naktižibis, žibanaktis, meaning evidence “shining at night” Tricholoma sciodes Yes Glowing young mycelium Xylaria hypoxylon The species is found in Lithu- Glowing reported in Euro- ania, although there is no pean countries, though not yet confirmation about its biolu- confirmed by visual evidence in minescence Lithuania Mosses Not bioluminescent Yes. Very rare. One habitat Tiny clear spherical protone- (does not use chemical registered in Biržai in 1998 mal cells reflect light to give off reaction for glowing), but (on spruce tree windfall roots a greenish-golden color luminous (reflects light) in a dense fir grove) moss, capable of glowing in the dark Schistostega pennata Note: the luminescence of species not in bold type is not confirmed by visual evidence or it does not glow in Lithuania.

In addition, samples of three species of biolu- feature was tested every hour after the specimens minescent fungi (Armillaria mellea, Chlorocibo- were brought to room temperature. ria sp., and Xylaria hypoxylon) growing in the Bo- tanical Garden of Vytautas Magnus University RESULTS AND DISCUSSION were collected to test and prove their glowing features in Lithuania. Infected wood specimens Fireflies were taken from growing trees and were trans- Two species of fireflies have long been known ported to a room where the temperature was in Lithuania (Pileckis, Monsevičius, 1995; Fer- around 21°C. The specimens were moistened enca, 2004; Tamutis et al., 2011; Kazantsev, with tap water and left in the dark. The glowing 2012): Lampyris nocticula and Phosphaenus Bioluminescent species in Lithuania 185 hemipterus. Female individuals of both spe- each segment of its body; the source of light is cies glow but do not fly, males fly but do not beneath the body of the insect and can be made glow (Lampyris nocticula) or do not fly but out through its exterior. It is also capable of se- glow (Phosphaenus hemipterus) (Telnov 2004; creting bioluminescent slime, and the emission Novak, 2008; Majka, MacIvor, 2009; Hop- spectrum of this luminescence was found to kins et al., 2015). Verbal confirmation of at have the maximum of about 510 and 480 nm least 6 different unrelated persons, that glow- (Anderson, 2008). Another verbal confirma- ing flying fireflies have been already spotted tion of glowing centipedes was received in 2018, in western and southern Lithuanian regions, the finder claimed he had seen a spotted glowing indicate that probably the third species of fire- centipedes in the residential area of Karoliniškės flies is already migrating from Poland (Novak, in Vilnius. In September of 2018 one glow- 2018; Kubisz et al., 2000; De Cock, 2009) and ing specimen was caught in Vilnius Belmontas Belarus (Aleksandrovich et al., 1996). Phau- district by Kristina Girčytė and was brought to sis splendidula or Lamprohiza splendidula is Vytautas Magnus University for identification. found in those countries. The male individuals Assoc. Prof. Ingrida Šatkauskienė identified of the species fly and glow in the dark (females the specimen (Fig. 1) as Geophilus carpopha- glow, but do not fly). gus or G. easoni (further research is planned to identify the species finally). Centipede Glowing centipedes (Geophilus sp.) were re- Springtail ported to be found in the residential area of Bioluminescent springtails (Collembola) are re- Antakalnis in Vilnius in October 2012 (in an ported to be found in soils all around the globe: urban tree forest), but exact species for example, Anurida granaria and Onychi- was not identified. The finder (Liudas Aidietis) urus sp. are widespread, while Lobella sp. is sent some two individuals to the Lithuanian In- present in Japan (Oba, Branham, 2011; Her- stitute of Ecology of the Nature Research Centre ring, 1987). In Lithuania, around 120 species for species recognition, but the species was not of springtails are found, although their biolu- identified (http://kauno.diena.lt/<...>, 2012). minescent features have not been traced yet Centipedes left green slime on a palm when (Sukackienė, 2015). The bioluminescent species a closer look was taken. Centipede Orphaneus Anurida granaria has been reported in Latvia brevilabiatus, common in tropical forests in (Grinbergs, 1956; 1960) and Poland (Skarzyn- Asia and Africa, produces light from the secre- ski, 2001), which strongly implies that probably tions of two luminous patches near the ends of they live in Lithuania as well.

Fig. 1. Specimen of Geophilus, which was caught in Vilnius Belmontas district in 2018 by Kristina Girčytė and identified as G. carpophagus or G. easoni by Ingrida Šatkauskienė, Assoc. Prof. at Vytautas Magnus University 186 Asta Malakauskienė

Fungi toyae, A. gallica and A. cepistipes) are still de- Several fungi species found in Lithuania have scribed as one (Armillaria mellea) in Lithuania been mentioned as bioluminescent by differ- (Urbonas, 1997b). A. tabescens should grow in ent sources (Urbonas, 1997a; Urbonas, 1997b; Lithuania too as it is found in Estonia and Ger- Liubienė, 2015; Isokas, 2016): Armillaria mellea, many (Urbonas, 1997b). Mycelium of A. gal- Collybia tuberosa, Collybia radicata, Chlorocibo- lica, A. tabescens (Mihail, Bruhn, 2007), A. os- ria aeruginascens, Tricholoma sciodes (glowing toyae (Rishbeth, 1986), and A. cepistipes (Mihail, mycelium), and some species of the My- 2015) are also bioluminescent. cena (glowing fruiting bodies). Marasmius, My- Fungi of Mycena genus, which grow in Lithu- cena, and Collybia are surface forest litter (small ania (Urbonas, 1997b), are reported as biolumi- branches, leaves, cones, needles, and other) nescent in other countries: Mycena epipterygia, decomposing fungi, while Tricholoma decom- M. sanquinolenta, M. stylobates, (Bothe, 1931), pose the middle (deeper) layer of forest litter M. haematopus, M. zephirus, M. polygramma (Urbonas, 1997a). Some species are mentioned (Treu, Agerer, 1990; Bermudes et al., 1992), in folklore as glowing: nakcižibiai, žibanakčiai, M. pura, M. rosea, M. maculata (Treu, Agerer, naktižieda meaning “shining at night” (Liubienė, 1990), M. inclinata (Wassink, 1948), M. tintin- 2015): Suillus bovinus, Clavaria botrytis or Ra- nabulum (Bothe, 1930). maria botrytis. According to the meaning, Bioluminescent Tricholoma margarita (pre- the fruiting bodies should glow, but there is no viously known as Mycena margarita) (Desjar- written or photographed evidence; moreover, din, 2010), which emits yellowish green light these species are not included in the global list in all parts of the basidiome or nonluminescent of bioluminescent fungi species (biolumines- fruiting body in some populations, does not cence of these species must be proved). Some glow in Lithuania, but there are some reports bioluminescent fungi species that have been that mycelium of T. sciodes (Urbonas, 1997a) reported in other countries (mostly in north- glows at night. There is one habitat of Ompha- eastern America and some European countries) lotus olearius known in Lithuania (Urbonas, are also found in Lithuania: Xylaria hypoxylon 1997b), while glowing features of its mycelium (until now no evidence of glowing in Lithuania and fruiting body have been reported in other has been reported), Panellus stipticus (not glow- countries (Wassink, 1948). ing in Lithuania). Specimens of wood infected with Armil- Armillaria mellea is a parasitic fungus at- laria mellea found in the Botanical Garden of tacking around 200 different species of plants Vytautas Magnus University (Kaunas district) (Urbonas, 1997a). Six species of Armillaria are started glowing four hours after the specimens found in Northern European countries (Fin- were brought into room temperature and oxi- land, Sweden, Norway, Denmark, Holand), dation of started. The infected pieces while four species (Armillaria borealis, A. os- of wood emitted bright green light (Fig. 2) for

Fig. 2. Specimen of wood infected with Armillaria mellea, found at the Botanical Garden of Vytautas Magnus University Bioluminescent species in Lithuania 187 two nights, later the glowing gradually reduced. colour and chloroplasts move within the spher- A new cutting of the same sample wood ini- ical cells to maximize their ability to collect tiated glowing after four hours. Irrigation and the reflected light (Harpel, Helliwell, 2005). cutting new layers let the same piece of wood The plants are not contorted when dry. glow for one and a half months until it became Results showed that representatives of 26 infected with mould, which killed the biolumi- different bioluminescent and one luminescent nescent fungus inside. species may glow in the dark in Lithuania de- Xylaria hypoxylon is attributed to biolu- pending on the season, temperature, humidity, minescent species, although its luminescence pH, and the presence of oxygen in their envi- might require association with photogenic bac- ronment. Two reported and one potential of teria or other light-emitting microorganisms immigrating (from Poland and Belarus) spe- (Murrill, 1915). Evidence on the glowing of cies of fireflies; recently reported one unidenti- Chlorociboria aeruginascens is scarce, but there fied species of bioluminescent centipedes from are some reports even in Lithuania (Isokas, the family of Geophilus (in 2018 one caught 2016). Speciments of Xylaria hypoxylon (Fig. 3) specimen was described as Geophilus easoni or and Chlorociboria sp. (Fig. 4) found in the Bo- G. carpophagus); one potential species of bio- tanical Garden of Vytautas Magnus University luminescent springtail (reported in Latvia and did not glow even after two days in a humid Poland); reported 21 species (confirmation of and warm environment. glowing features still needed for some species) of bioluminescent fungi; and one reported spe- Luminescent moss cies of luminescent moss. Bioluminescent fea- A rare species of luminescent moss Schis- tures of Suillus bovinus and Clavaria botrytis tostega pennata was reported to be found in Lithuania in Biržai in 1998 (it was found on spruce tree windfall roots in a dense fir grove) (Lie­tuvos Raudonoji knyga, 2007). It was in- cluded in the Red Book of Lithuania in 2000. This moss does not use chemicals to emit light. The ephemeral protonemal mat is composed of filamentous strands of tiny clear spherical cells that reflect light to give off a greenish-golden

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