fungos luminescentes

8/8/2019 fungos luminescentes

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A R T H R O P O D S A TT R A C T E D T O L U M IN O U S F U N G IBY JOHNIVINSKIDepartment of Entomology and NematologyUniversity of FloridaGainesville. Flo rida 326 11

Some fungi emit light. Luminescence may be present in mycelia[e.g. a num ber of Mycena species (Wassink 1978)l o r in b o thmycelia and fruiting bodies [e.g. North American populations ofPanellus (= Panus) stypticus, Buller 19241. Lights have beendescribed as blue, w hite, o r green d epen ding on th e species (Bu ller1924, W assink 1978). Emission intensities vary con siderably. In th eforests of Borneo Mycena (= Porom ycena) m anipularis are visibleat ca. 40 m eters (Zahl 1971). A n Austra lian species 1 "pours fo rth i tsemerald green light" with sufficient intensity to read by (Lauterer1900 in Buller 1924). N ort h Am erican form s, such as examined here,tend t o be dimm er. The eye often requires several minutes of d a rkadaptation before their glows become visible.The receiver(s) toward which fungi direct their luminous signalsare unknown. Lights have been supposed to lure spore dispersinginsects (Ewart 1906), but such an argum ent fails to accou nt fo rmycelial lights (Ramsbottom 1953). There has apparently been nocon jecture o n th e benefits mycelia accrue by glowing. Th e differen tenvironm ents of mycelia and fruiting bodies make it que stiona blewh ether th eir lights are directed at identical receivers or even servesimilar functions.Until this time any propo sed reactions of animals to fungal lightshave been speculative. I here present evidence that certain arthro-pods are more likely to be captured in traps baited with light-emitting mycelia and fruiting bodies than in controls containingfungus-free substrate or dead and dark specimens of luminousspecies. Several possible interactions between fungi and attractedarthropods are discussed.

Described as Panus incandescens, a name of doubtful taxonomic value (seeWassink 1978).Manuscript received by editor September 29, 1981.

Pu&e 88:383-390 (1981). http:llpsychecnlclub ore/SMS-M html


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384 Psyche [Vol . 88

Test tubes (10 X 75 mm) were covered with Tack Trap@,a stickytrapping compound, and capped with a cork. Luminous twigs,conifer needles and leaf fragments, covered with mycelia of aMycena sp., were put into 31 such tubes. An identical number ofcontrol tubes contained similar but nonluminous forest litter. Tubeswith glowing fungi were placed as closely as possible to the originalposition of their contents (note that mycelia are most abundant deepin litter, but traps were placed on the litter surface). Controls wereset ca. 80 mm to the side. Glass screw top vials (14 X 40 mm) werealso coated with Tack Trap@. From 3-6 fruiting bodies of theluminous mushroom Dictyopanus pusillus were put into 72 suchvials. An identical number of controls contained 3-6 D. pusillus,killed and rendered nonluminous by bathing in alcohol. Luminousand control vials were alternately placed, ca. 80 mm apart, on andby rotting logs on which D. pusillus had been found. Traps were putout at night, gathered the following morning, and arthropods stuckon their surfaces removed.

All specimens were captured during August in Alachua County,Florida.

More arthropods were captured on traps baited with glowingfungal mycelia (Mycena sp.) and luminous fruiting bodies (D.pusillus) than their respective controls (x2= 10.14, p< .001; x2=6.41, p < .01, see Table 1). Taxa significantly more abundant onluminous traps in the summed samples are Collembola (x2= 12.8 1,p < .001), and Diptera (x2 = 5.54, p< .025). It is of interest thatCollembola are not attracted to the bioluminescence of a sedentaryluminous predator, larvae of the fungus gnat Orfelia ultoni (Sivin-ski 1982). Predators, i.e. spiders, ants, earwigs occur in a luminous:dark ratio that borders on significance (x2= 3.76, p< .lo). Groupscaptured in statistically indistinguishable numbers on luminous andcontrol traps are Isopods (x2= 0.78, p> .25) and Amphipods (x 2=0.59, p > .25). An unusual set of captures is the 5 crickets,Eunemobius carolinus, taken only with luminous mycelia.


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19811 Sivinski - rthropods and Luminous Fungi 385Table 1. The numbers of Arthropods captured on traps containing luminous

mycelia (Mycena sp.), luminous fruiting bodies (Dictyopanus pusillus), and the irrespective controls.

Mycena D . Summed Summedsp. Control pusillus Control Fungi Co nt ro l

CollembolaIsotomidae /

EntomobryidaeSminthuridae

DipteraPhoridaeSphaeroceridaeCecidomyiidaeCeratopogonidaePsychodidaeMycetophilidae

PredatorsAraneidaFormicidaeCarabidaeDermaptera

HymenopteraIsopodsAmphipodsAcariOrthoptera

GryllidaeBlattellidae

CicadellidaeThysanopteraUnidentifiedAll Arthropods


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386 Psyche [Vol . 88

Attraction of insects to fungal lights does not demonstrate thatluring arthropods is the function of the bioluminescence. With thiscaveat in mind, note that an acceleration in the rate of certainfungus/insect interactions even as an effect of a bioluminescentsignal is apt to influence the evolution of luminous fungi. Inparticular, the argument that fungal lights are functionless, and byimplication harmless by-products of metabolism, loses force (seealso Lloyd 1977). Bearing a light near arthropods is unlikely to beselectively neutral (for counterviews, see Duller 1924; Prosser andBrown 1961).Some possible functions of fungal glows become more plausiblewith, or fail to find support in, the presented data. Both arediscussed below.2Attraction of spore dispersers: Stinkhorn fungi (Phallales) useodor, and perhaps color, to attract spore dispersing insects. Diptera ,in particular, consume a sweet malodorous spore-containing mu-cous smeared on the fungal surface. Spores develop after beingdischarged in the insect feces (discussed in Ramsbottom 1953). Anearly conjecture on the function of fruiting body luminescence wasthat lights, like odor and color in stinkhorns, lure spore dispersers(Ewart 1906; see also Lloyd 1974, 1977).3A large proportion of the animals attracted to luminous fungi arepotential consumers of its spores. Many Collembola feed on fungalspores, mycelia, and fruiting bodies. Some members of capturedDiptera families breed in fungi. The phorid Megaselia halterata, forinstance, is a pest of cultivated mushrooms (Oldroyd 1964). Whetherspores of D. pusillus pass unharmed through the insect gut is

*The following functions concern heterospecific receivers; however, biolumines-cence is often intimately associated with m ating (see Lloyd 1977). Sex ual co ng re ss inrelevant Basidiomycetes co nsists of exchange of nuclei between haploid m ycelia . Is itpossible that glows might direct the growth of photo-sensitive hyphae at this stageand so serve as mating signals? Such an explanation fails to account for lum ino sity indiploid mycelia or the fruiting body.

in se ct s m ay evolve an affinity for fungal lights due to "rewards," in food, she lter,etc., the fungus provides. An alternative is that attraction is due to fungalexploitation of arthro pod "phototropisms." Th e function of "photot ropisms" a reoften obscure. S om e are apparently effects of orientation systems based o n therelative position of celestial objects (see Lloyd 1977).


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198 11 Sivinski - rthropods and Luminous Fungi 3 8 7unknown. Nor is it known if attracted flies, such as phorids a n dcecidomyiids, would be useful agents of dispersal. Vagile adults m a ynot feed on fungal materials. Protein consumption by ce c i d o m y i i d sis particularly rare (see Sivinski and Stowe 1981). Spores m a y bemoved, however, by attachment to the surface of a passing i n s e c t .The topography and timing of luminous displays are o f t e nsuggestive of guiding dispersers. In Mycena pruinosa-viscida a n dM . rorida from the Far Eastern tropics only the spores emit l i g h t(Haneda 1955). Most fruiting body lights are restricted to, o rbrighter in, the spore bearing hymenium (Wassink 1978) a n dPanellus stypticus glows most strongly at the time of spore m a t u r a -tion (Buller 1924). Conscription of dispersal agents is less l i k e l y toaccount for light-emitting mycelia, unless mycelial cells pass s a f e l ythrough the gut or can be carried to new locations on an a r t h r o p o d ' sexoskeleton.Attraction of carnivores: Predaceous arthropods were f o u n d onglowing traps in numbers that border on significance, and f u n g u s /predator interactions can be imagined as important in the e v o l u t i o nof bioluminescence. Luminous fungi might concentrate c a r n i v o r e sabout them by exploiting their "phototropisms." If predators a r r i v eat rates effectively greater than lured fungivores, the r e s u l t i n gpredatorzprey ratio may favor the fungus (an argument similar tobut more evolutionarily feasible than the "burglar alarm" t h e o r y ofDinoflagellate luminescence; Burkenroad 1943; see Buck 1 9 7 ) .Such an advantageous ratio is not obvious in my sample. A l t e r n a -tively, carnivores could seek out luminous fungi as locales of h i ghprey density. Glowing mushrooms might be mistaken for l u m i n e s -cent animal prey.Attraction of fungivores: If luminous mycelia are unpalatable, o rotherwise difficult to ingest, then fungivores attracted to l i g h t smight consume adjacent competitors.Attr acti on of fertilizers: Lloyd (1974) suggests that a r t h r o p o d slured by luminescent fungus might excrete beneficial materials a n dso aid growth. Any nutritional gain must be balanced by t h emetabolic expense of the signal.Repulsion of negatively phototro pic fungivores: Bioluminescencemight repel an organism's negatively phototropic enemies or c om -petitors (Nicol 1962; see also Sivinski 1981 and citations). R e p u l s i o nis particularly plausible in explaining luminous mycelia, s o m e of


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388 Psyche [VO~ .8which occur buried in litter, inside rotting logs, or on roots deepunderground where the opacity of the environment precludesattraction as a function of light.Among surface dwelling arthropods, there is no indication of alight-avoiding taxon. This does not preclude repulsion. A rare, butdangerous, enemy could keep fungal lights burning but escapeinclusion in the present sample, especially since mycelia baited trapswere not placed in the area of greatest mycelial abundance, deep inthe leaf litter. The intended receiver may not be an arthropod oreven macroscopic. Protozoa sometimes respond to lights. A glowcould repel certain pathogens and keep the fungus free of par ticu lardiseases.Light as a warning signal: Lights emitted by unpalatable fungimight serve as warning signals directed towards nocturnal fungi-vores (a similar function has been hypothesized for ancestralflowers, Hinton 1973). Of North American fungi with luminousfruiting bodies, one, P. stypticus, is a bitter tasting purgative, whileanother, Omphalotus olearius, is a toxic hallucinogen (Miller 1979;the palatability of D. pusillus is unknown). Pleuro tus jap on icus , aluminescent Japanese species, is deadly poisonous (Buller 1924).However, the luminous fruiting bodies of Malaysian M y c e n amanipularis are quickly attacked by fungus gnats (Corner 1954;gnats could be specialists, immune to toxins). Again there is noevidence of arthropods avoiding fungal lights. My traps, of course,would fail to quantify the discouragement of deer or other largefungivores.Like aposematic insects, luminous mushrooms often occur inclumps (kin groups?) (see illustrations in Buller 1924, Harvey 1957;also descriptions in Wassink 1978). Aggregations might intensifywarning signals (Cott 1957) and be instrumental in the evolu tion ofconspicuousness (Fisher 1930, for arguments concerning the kinselection of aposematism). Several tropical light emitters, however,apparently occur singly (see Wassink 1978).White fungi can reflect enough celestial light to be surprisinglyobvious at night (noticed at twilight by Lloyd 1977). An assumptionof similar receivers for the bright white and luminous signals offruiting bodies allows the nocturnal aposematic signal hypothesis tobe tested with a larger sample. Mushrooms that appear to me to belmiformly bright white include 6 toxic species, 13 edible an d 5 whose


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19811 Sivinski - rthropods and Luminous Fungi 389palatabi l ity is unk now n (color and palatabi li ties f ro m pho tos a n dtex t of M iller 1979). This distribution does no t su pp ort the ap os em -at ism argu m ent ( in comparison with a ran dom sample of 41 n o n -poisonous and 9 poisonous species x 2 = 0.80 p > - 25 ) .

Arth ropo ds, principally Collembola and Diptera, are at t racted tothe l ights of luminous fungal mycel ia (Mycena sp.) and frui t ingbodies (Dictyopanus pusi llus) . Such at t ract ion does n ot prove t h a tbioluminescence has evolved to lure insects but does affect t h eplausibili ty of hypotheses concerning the function of fungal glows.T h e possibili ties of lights being used to lure spor e dispersers, at tr a c tconsumers of fungivores and competing fungi, repel negativelyph oto trop ic fungivores, and serve as warning signals, are discus sed.

Comm ent s by J . E. Lloyd, T. J. Walker , T. Forrest , S. Wing, a n dP. Sivinski improved the paper . B. Hollien professionally preparedthe manuscr ip t. D r . J. W. K imbrough identified D . pusillus a nd J.Sivinski helped gather specimens. Florida Agricultural JournalSeries No. 3280.

B U C K , .1978. Functions and evolutions of bioluminescence. Pages 419-460 in P. J.Herring (ed.). Bioluminescence in action. Academic Press, New York.

BULLER , . H .1924. Th e bioluminescence of Panus stypticus. R esearches on fungi. Vol. 3. pp.357-43 I .B U R K E N R O A D ,. D.

1943. A possible function of bioluminescence. J. Mar. Res. 5: 161-164.C O R N E R , . J. H .1974. Further descriptions of luminous agarics. Trans. Br. Mycol. SOC.37:256-27 1.COT T, H. B.

1957. Adaptive coloration in animals. Methuen and Co., Inc., London.E W A R T , . J.1906. Note on the phosphorescence of Agaricus (Pleurotus) candenscens. B ull.

Vict. Nat. 23: 174.FISHER,R. A.1930. The genetical theory of natural selection. Oxford Univ. Press, London.


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390 Psyche m V 0 1 . 88H A N E D A , .

1955. L um in ou s o rga nism s of J a p an a nd th e F a r E ast. P ag es 3 3 5 - 3 2 3 6 in F. HJohnson (ed.). The luminescence of biological systems. Am. A s s c . AdvSci., Wash., D. C.

HAR VEY, . N .1952. Bioluminescence. Academic Press, New Y ork.

H I N T O N ,H. E.1973. Na tural dece ption. Pages 96-159 in R. L. Gregory and E - H. H.G o m br ic h (e ds.). I llu sio n in n a tu r e a n d a rt . C ha rle s S c r i b n e r - s S o ns ,New York.

LLOYD , . E .1974. Bioluminescent com mu nica tion between fung i and insects. Fl-. Ento-mol. 57: 901977. Bioluminescence an d com mu nica tion. Pages 164- 183 in T. A - Sebeok(ed.). H o w an im al s c om m unic ate . I nd . U niv. P re ss, B l o o m i n g c e n , nd.

MILLER, . K., J R .1979. Mu shroom s of No rth America. E. P. Dutton, New York, N - Y.NICOL,J. A. C.

1962. Animal luminescence. Adv. Comp. Physiol. Biochem. 1: 2 17- 2 7 3 .OLDROYD, .1964. T he natura l history of flies. W. W. Norton and Co., Inc., N e w ork.PROSSER, . L., A N D F. A. BROWN, R .1961. Compa rative animal physiology. W. B. Saunders Co. , P h il a d e l- h i a , Pa.

RAMSBOTTOM,.1953. Mushrooms and toadstools. Coll ins, London.S IVINSKI ,.1981. The nature and possible functions of bioluminescence in C- x e o p t e r alarvae. Coleopts. Bull. (in press)1982. Prey attraction by luminous larvae of the fungus gnat O r f e Z i a ~ u l t o n i .(submitted)

S IVINSKI ,., A N D M. STOWE.I98 1. A kleptoparasitic cecidomyiid and other flies associated w i t h sp iders .Psyche. 87: 337-348.

W A S S I N K ,. C.1978. Luminescence in fungi. Pages 171-197 in P. J. Herring (ed.). B io u m i n e s -cence in action. Academic Press, New York.

Z A H L ,P. A.1971. The secrets of nature's night lights. Natl. Geogr. 140: 4 5 - 7 0 -

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