ARTICLE 229 (ghost fungus; Agaricales fungal physiology insect-fungal interactions Kangaroo Island spore dispersal ) in the temperate south of the IMA FUNGUS · 7(2): 229–234 (2016) 229–234 · 7(2): FUNGUS IMA Omphalotus nidiformis Marasmiaceae
7 " G # " 2 MATERIALS AND METHODS MATERIALS Australian temperate-zone Omphalotus nidiformis is an basidiomycete, generally found at or near the base of Eucalyptus most often in the range of 20-40 cm diam. It produces J & !K LK $ # L " !M " 'O$ Agaricales, we capitalized on the presence of continent. In this study, this fungus to test the hypothesis that ITS bioluminescence " # " # " # " incidental by-product attraction, warning signalling, and as an # " # E despite focused on the ecological role of bioluminescence, # " the widespread Omphalotus nidiformis Omphalotus et et al. 2008). G 5 G ' Neonothopanus ) and Control pairs, for 480 trap-hours on moonless nights. ) and Control pairs, for 480 trap-hours on ). Bioluminescence , Tom Wood , Tom ' O. nidiformis et al !/='+$ # Marasmiaceae
J 5 ' 7 # " ## Agaricales, Bioluminescence has been known from fungi since ancient times, but little work has been done been known from fungi since ancient times, Bioluminescence has
), a widespread Australian temperate zone species. We examined three We Australian temperate zone species. ), a widespread (Agaricales, Marasmiaceae ( ! "" # $ For bioluminescent fungi, it has been suggested that G \ # X O " O 5 # ] X J # O " J 7 5 # X " X J J # O " J 7 # G G JG +==+ G Z © 2016 International Mycological Association © 2016 International Mycological conditions: distribute and transmit the work, under the following are free to share - to copy, You Attribution: 2 ' Philip Weinstein corresponding author e-mail: [email protected] corresponding author J P /9 /='UZ G P /* J /='UZ P '' < /='U spore-dispersing insects, and we aimed to establish if this was the case for the ghost fungus, Omphalotus and we aimed to establish if this was the spore-dispersing insects, nidiformis # P # Z L # Z # " " # " \ " O " " !K LK $ 7 L (baited with fresh bioluminescent # " 7 and Control traps (mean Treatment between in mean insect abundance There was no statistical difference = ;; = +? " $ 7 # # and conclude that for some fungi, bioluminescence may competing hypotheses for fungal bioluminescence, L # # " " _ # ## " " # # " Q # " ## # G G JG +==+ G Non-commercial: No derivative works: if you get Any of the above conditions can be waived For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. # # Nothing in this license impairs or restricts the author’s moral rights. permission from the copyright holder. Bioluminescence has been known since ancient times, Bioluminescence has been known since Aristotle by with bioluminescent fungi being documented from that of differed (384-322 BC) as emitting light “which P # " !& '*+/ 5 6 INTRODUCTION 7 # # # " # ocean (Rees et al '**9$ & " !'*9;$ potential ecological roles of bioluminescence, listing defence, and communication, but did not discuss fungal offence, <# '+= === # # " # >' ?= @ # " /==' !5 6 al /='=$ the attraction of potentially spore dispersing insects can # " # " " and this is supported by the recent experimental work in D < garderni P'= ++*9Q # " /='U => =/ =' VOLUME 7 · NO. 2 et al.
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The Australian ghost fungus Omphalotus nidiformis in natural daylight and B. " E " " D " # C. The Kangaroo Island study site consisting of sclerophyll woodland dominated by Eucalyptus fasciculosa, and D. G # # # " _ " G \ 5 O # G Qj {
Fresh, glowing specimens were located in Flinders Chase 7 # National Park, Kangaroo Island, South Australia, in open confounding or dilution from other light sources, but at the E ' DX # same time limited the number of catch nights possible. # G M J j j q " ! E + Nocturnal trapping was undertaken on clear nights $ " " ! $ # # " (intermittent light cloud, no rain) with no wind, and with '= E'> L !G U oC. Traps were deployed and X " J \ " # X*+'='GZ E ' # ' L L " # # L " # Z M " '5$ \ " 5 " The site was deliberately chosen to be free from any " " " " '/ oC. Traps were " !'* /= K /='+$ " E '
230 IMA FUNGUS
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# # # " # " L\ " G in the abundance counts and used a log link function. Model " " lme4 package (Bates et al. /='?$ R-; / = !7 /='+$ ! 5 7 \ We checked basidiomes for bioluminescence regularly in the sticky traps at night, we summed the abundances across " the two sampling nights for analysis; exploratory analysis # " Q " ## R 7 " K " 7 " corroborating records of winter basidiome production from catch abundances between sites or between trap-pairs within J & # J G ! \ Z pers com.). to zero in the analysis. Consequently, model estimates were 7 # \ " equal to those from a generalised linear model (Poisson # E += G " $ ## site, three types of traps were deployed: sticky (see below), 7 # E L !'$ !'=$ 7 ! $ " RESULTS number of trap hours by trap type. 7 # " " \ " " # L " # pairs of sticky traps were used at each of the four sites, with attachment to mycelium (which did not glow). Flying insects " # were, as expected, not abundant at this time of year, with attached. All traps were separated by approximately 2 m and # " !7 '$ # " # " " ! U @ '= @ / @ # any potential interference. A total of 24 traps were deployed diurnal catch numbers per trap-hour for sticky, malaise, and # '= # " " " ?9 L " $ D E nights. The total catch for each trap was counted for each " !7 '$ Diptera !\ $ night, and all insects were included in the analysis as potential and their hymenopteran parasitoids (Diapriidae, Braconidae; L 5 ## # data not shown) dominating the fauna. between Treatment and Control traps were examined using J " /' '; \ generalized linear mixed models. Site and Trap-pair within 9 7 " ## # ?9= L Site were included as random effects to account for the two 7 # ##
VOLUME 7 · NO. 2 231 et al. ARTICLE
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in mean insect abundance between Treatment and Control again suggesting that the attraction of spore dispersing 2 !0 ' ' '> P = 0.28). Mean insect abundance in the # O. nidiformis. \ = +? " !*+ @ < # M # = ;> = 9=$ = ;; !\_ = /= = +?$ insect abundance at the time of basidiome production, and the Treatment (Fig. 2). ## # M # " M " # DISCUSSION fungi in the complete absence of competing light sources " " < # " # " suggesting that bioluminescence in Omphalotus nidiformis To explain the presence of bioluminescence in O. does not attract potential spore dispersing insects. Firstly, nidiformis, it is therefore necessary to explore competing " " " "" # L # # " \ ## # " " # !< et al. /='+$ That O. nidiformis glows continuously suggests that there is 5 L ## " " Bermudes et al. !'**/$ "" attraction of potential spore dispersing insects in this species. " # Secondly, the abundance of potential spore-dispersing insects bioluminescent species glow more strongly than other parts E L 7 ! " Omphalotus nidiformis$ J particularly the case at night, because nocturnal sticky, malaise !'*9'$ " M # \ " L " '= @ # # test-tubes and found that more arthropods were attracted to L !7 '$ M luminous forest litter containing mycelia of a Mycena species # " L L " " # L # \ "" " = ;; # " _ \ " # < et al. !/='+$ # " " " models of the Neotropical Neonothopanus garderni 7 ## L " " qX5 " +;= 7 Treatment (bioluminescent) and Control sticky traps. For compared catches with lights on and off, and found that # " " " " under conditions of low insect abundance would require a _ # " " # \ " # " " " the spore-carrying basidiomes, and one would expect that # ;==MU+= !K O " /==?$ " the strength of such an attraction would swamp any potential " E # " " # " possible that a trade-off operates between basidiome damage fungi (Faldt et al '***$ D and spore dispersal (cf. pollen consumption v. pollination
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$ _# Omphalotus nidiformis displays none of these characteristics: ARTICLE L # " Z strategy would be most successful in fungi that grow in occurs in open eucalypt woodland where wind dispersal of L ! " # " $ M at a time of year when the abundance of potential spore- L !5 6 et al, 2008), possibly dispersing insects is low. \ " ## \ _ ## " between catches from control traps and those baited with # " " " # " # or insect abundance, and although more bioluminescent attraction of spore-dispersing insects and the incidental species occur in tropical rainforests, it is unclear if their by-product of metabolism hypotheses for bioluminescence # ! # " # ## " $ "" lineages of fungi and possibly also differing growth that an examination of potential relationships of this nature < E # # # would be that bioluminescence in fungi arose as an incidental by-product of metabolism, and that some fungi such as O. 5 nidiformis remained in this condition. Others, such as N. G # " garderni " # L # E " E " M E potentially spore-dispersing insects. It would be a worthwhile (2004) suggests that light is emitted instead of heat as an exercise to map the ecological correlates of fungal energy by-product of enzyme-mediated oxidation reactions, " # as is the case in some bioluminescent bacteria (where # bioluminescence is continuously produced as a by-product of respiration). In O. nidiformis, bioluminescence is continuous (supporting this hypothesis), but in species of other lineages, ACKNOWLEDGEMENTS bioluminescence is regulated by a circadian clock so as to produce light only at night (which would be more consistent \ 5 5 \ with expectation if the attraction of spore-dispersers was 7 q # " " N. garderni !< et al. /='+$ 7 Z G" # Z & # metabolic by-product hypothesis could also be consistent J G Z ] ## G " # L J # Z of Adelaide for funding our work. Trapping was carried out under a " " " 5 # X D j !X/U?'>L'$ Fungal bioluminescence uses an enzymatic pathway Q # R E # Q # R !G M '*U/ 5 6 et al. 2008). This process has REFERENCES E L E !5 6 et al. /==9$ < et al !/='/$ E " E # G j M ]X !'*U/$ 7 # " # ## required for cell-free fungal bioluminescence. Archives of lineages of luminescent fungi share similar luciferin-luciferase Biochemistry and Biophysic, 97P +U>M+>; mechanisms of bioluminescence. All fungi that are known O 5 O O J !/='?$ lme4: Linear mixed- E !& " effects models using Eigen and S4 j " ' 'L>P '**? et al. /==U$ " PQQ\jGD jL 6 "Q " ? lineages; the Omphalotus-, Armillaria- and the mycenoid O 5 j& D {& !'**/$ q L L " !5 6 et al. 2008). Thus, it is possible that luminescence detected in Mycena haematopus basidiocarps. ## " ## Mycologia 84: >**M9=/ " " 5 6 5X < G] J \ !/==9$ M " Photochemical and Photobiological Science 7P '>=M '9/ CONCLUSION 5 6 5X OG q " 5K J \ D " X !/='=$ q Mycena: new and noteworthy species. Mycologia From the experiments of < et al. !/='+$ 102P ?+*M?>> M K K D " ] O "L{ GL{ !'***$ insects to at least some species of fungi, and that these fungi of bracket fungi Fomitopsis pinicola and Fomes fomentarius and " # their functions as insect attractants. Journal of Chemical Ecology Characteristics of such fungi may include the emission of 25P +U>M+*= a bright light with a nocturnal circadian rhythm, a growth & XD !'*+/$ Bioluminescence. New York: Academic Press. # & " K !'*9;$ O " # \ " J " " # Journal of
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ARTICLE O \ K & # G \ KL et turning oxygen defence mechanisms into deep-sea al. ! /==U$ 6 # Agaricales: a multilocus phylogenetic communication tools. Journal of Experimental Biology 201: Mycologia 98P *9/M**+ '/''M'//' KL " j j JG K KX K 7 J K !'*9'$ G # " Psyche: a et al. !/==/$ < # " Journal of Entomology 88P ;9;M;*= Molecular Phylogenetics and Evolution 23P ;+>M?== 7 j\ !/='+$ R: A language and environment for statistical < G] 5 6 5X OG J \ !/='/$ computing. P M # J \ "Z PQQ X " jL 6 "Q. known bioluminescent fungal lineages. Photochemical and &K !/==?$ D # " Mycologist 18: Photobiological Sciences 11P 9?9M9+/ ?M+
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