The Truffle-like 'Protubera canescens' Is an Early Developmental Stage of the Cage Fungus 'Ileodictyon'

2010·2 MB·English

Contributions
The truffle-like Protubera canescens is an early
developmental stage ofthe Cage Fungus Ileodictyon
W
Tom May1 Nigel Sinnott2and Alice Sinnott3
,
'RoyalBotanicGardensMelbourne,PrivateBag2000,SouthYarra,Victoria3141.Email:[email protected]
211SmartSt,SunshineWest,Victoria3020
35MoiraStreet,Sunshine,Victoria3020
Abstract
Recentcollections from a site in the Melbournesuburb ofAltona North indicate that the truffle-like fungus
Protubera canescens is the young stage ofthe Cage Fungus Ileodictyon gracile. Over several months, fruit-
bodies consistent with descriptions ofProtubera canescens were observed, but later, at the same site, lattices
emerged,typicalofIleodictyongracile.Intheunopenedfruit-bodiesradialthreadswereobservedinthegelati-
nouslayeroftheperidium. Thesestructuresmatchwithliteraturereportsofthemorphologyofbothspecies,
although theyhavebeen little discussed previously in Ileodictyongracile. Two other truffle-like species, Pro-
tubera africanaandRhizopogon rodwayi, have theradial threads and co-occurwithIleodictyongracile. Thus,
thepossibilitythattheyarealsoyoungstagesofIleodictyonshouldbeexplored.DevelopmentinIleodictyonis
unusual in combining the benefit ofan enclosed, hypogeal truffle-like stage, where sporeproduction ispro-
tectedfromdesiccation,andanepigeallattice-stage,fromwhichsporesaredispersedbyinsects.(TheVictorian
Naturalist127(2),2010,49-54)
Keywords: Phallales; Clathracae; Protophallaceae; LatticeFungus;hypogeal fungi
Introduction
Ileodictyon is the familiar Cage or Lattice Fun- hautuensis) and Protophallaceae (several spe-
gus, comprising two species, I. cibarium and cies including the type ofthe genus, P. marac-
I. gracile, both widespread in Australia (Grey uja). Hosaka et al. (2006) suggested that those
and Grey2005). Theyemerge from an egg-like Protubera species that fell within families that
structure and form a lattice with a slimy spore otherwise contained stinkhorns (Lysuraceae)
massontheinside. Incontrast,Protuberaforms andlatticestinkhorns (Clathraceae)werelikely
underground truffle-like fruit-bodies with the to be unopened stinkhorn fruiting bodies. We
spore mass (gleba) remaining enclosed (inde- reportherefieldobservations thatconfirm that
hiscent)withinanouterlayer(peridium).There Protubera canescens is an early developmental
are about a dozen species ofProtubera one of egg’stageofIleodictyon.
,
which,Protuberacanescens hasbeendescribed
, ObservationsatAltonaNorth
from Australia (Beaton and Malajczuk 1986;
While looking for fungi along a stretch ofKo-
MaIlnlcolcahssi1f9i8c9a;tiCoansstbelalsaendooanndmoBrepehvoelro1g9y9,4)b.oth roroit Creek on 21 May 2006, two of the au-
thors (AS and NS) came across a large cluster
Protubera and Ileodictyon have been placed ofwhite, spherical fungal fruit-bodies, 3-8 cm
in the Phallales (the stinkhorn fungi), but the
former genus has been considered to belongto diameter, on or half-buried in deep, rich, loose
the family Protophallaceae due to the indehis- soil near or under native trees and shrubs (Fig.
centfruit-body, while the lattergenus hasbeen la). The location was at the bottom ofa bank
placed in the Clathraceae (Hawksworth et al. south-west of (and below) John Street, near
1eg9g8’3)towfhoerrme atnheabfrouviet-gbrooduyndemferrugiets-bofdryomwiatnh HaWrhriesnRehsaenrdvleeidn,AlthteonawhNiotreths.pheres felt ge-
latinous inside, so they were not just young
arms, columns,tentaclesoralattice.
In a recentphylogeneticanalysisbased on sev- puffballs, and they had white rhizomorphs
eral DNA regions, Hosaka et al. (2006) found (root-like structures) at the base. Further ex-
amination, particularly of the cross section
thatspeciespreviouslyassignedtoProtuberafell
(Fig. lb), revealedthattheyhadathree-layered
within five different families: Clathraceae (Pro- peridium. The outer layer was thin and mem-
tubera canescens), Gallaceaceae (P nothofagi), branous, and the inner layer (which bounded
Lysuraceae(P clathroidea), Phallogastraceae(P. the greenish-olive gleba) was also very thin.
Vol 127 (2) 2010 49
Contributions
Fig. 1. Ileodictyon gracile from Altona North, a. unexpanded fruit-body (each segment on the scale at left
^ cross secti°n °funexpanded fruit-body (agreeing with structure ofProtubera canescens), note
the radial threads in thegelatinous layerofthe peridium (RT) and the circularstructures (Cl) at the baseof
the threads, adjacent to thegleba (GL); c. partiallyexpanded lattice arising from ruptured peridium; d. fully
expandedlatticeandremnantsofperidium (lowerright)showingpolygonalpatternoninnersurface. Photos'
AliceSinnott.
Between the inner and outer layers there was rial was gentlycutso thata section ofthe outer
a thick gelatinous layer through which ran ra- peridiumandgelatinouslayerwaspeeledaway,
dial, white threads, dividing the middle layer the whitish radial threads (sutures, see Fig. lb,
into roughly equal compartments. This perid- RT) revealedon thesurfaceofthecentral gleba
ium structurematchescloselythatofProtubera formed a mosaic or lattice pattern very remi-
canescens, as described from Western Australia niscent ofan Ileodictyon. The arms ofthis lat-
byBeaton andMalajczuk(1986) andillustrated tice ‘in miniature’ can be seen in cross sections
byBougherand Syme (1998: p. 127). assmallcircularstructuressittingatthebaseof
Fruit-bodies ofProtubera canescens and Ileo- the radial threads in the gelatinous layer, at the
dictyon had previouslybeen observed (byTM) boundarybetween the gelatinous layerand the
at roughly the same spot in the Royal Botanic gleba (Fig. lb, Cl).
Gardens Melbourne, although at quite differ- As the Altona North site was easy to get to,
ent times. This raised the possibility that the and there were numerous fruit-bodies, it was
former might be the immature, unopened egg’ clear that an excellent opportunity had arisen
stageofthelatter. Insupportofthishypothesis, to check whether the peridium ofP canescens
when a fruit-body of the Altona North mate- really remained closed or not, and a watching
50 The Victorian Naturalist
Contributions
briefwas kept on this location. Several further
visits byNS and AS revealed most ofthe fruit-
bodies unchanged, though a numberhad been
disturbed and damaged. A likely explanation
for this was thatbirds had dug out and pecked
openfruit-bodiesin searchofinsectlarvaethat
were frequentlyobserved feedingonthe gleba.
On a visit on 25 June 2006 there were small,
almost dried-up lleodictyon lattices at the site.
These had all been disturbed, and it was not
clear whether the lattices were the result of
natural opening or ofdamage bybirds. Undis-
turbed fruit-bodies, of which there were still
plenty, remainedclosed.
The situation became clearer on 1 July when
esommeer,geatdlenaasttu,roaflltyhe(lFaitgtsicelsc.weIrde).foIunndfactto,hoanvee cFiagn.es2c.enDsi’afgorrammofofllceroodsisctsyeocntigroanciolfetfhreom‘PrBoetlugbrearvae
lattice, which had begun to emerge when the South,showing radial threads (RT) bifurcatingadja-
fruit-body was picked up, expanded in one of cent to the gleba (GL) to form circularorpolygonal
the collectors hands while the other collector structures(Cl).
was photographing it. Mostofthe fruit-bodies, Protubera canescens from Belgrave South (Fig.
however,were still closed.
A number of unopened, undamaged fruit- 2) clearly depict the radial threads, with most
bodies were removed and stored, half-covered ofthembifurcatingimmediatelyadjacenttothe
with soil from the site, in a large pot. None gleba, to form triangular orirregularlycircular
of the potted fruit-bodies opened, and by 7 structures. In the illustration in Beaton and
August all had disappeared, probably eaten Malajczuk(1986) thereisalsosomebifurcation
awayfromthe insidebythelarvaethatrelished ofthethreadsattheotherend,immediatelyun-
the gleba. A few more lattices appeared at the dertheouterlayeroftheperidium,butwehave
Altona North site in July, but most ofthe un- not observedthis inVictorian material.
damaged fruit-bodies remained unopened. Radial threads in the gelatinous layer at an
On 20 August there were no longer any fruit- early stage of fruit-body development have
bodies at the site, just white mycelium under not been highlighted for lleodictyon, but are a
thesoilanda fewfragmentsofdried peridium. characteristic ofthe Clathraceae (Dring 1980).
Belowaverage rainfall inwinter2006 mayhave Radial threads are not mentioned in the de-
contributed tothelackofexpansion oflattices. scriptions ofI. cibarium and I. gracile by Cun-
ningham (1944), although in the accompany-
SynonymyofProtubera canescenswithlleo- ing figure ofa cross section ofan unopened /.
dictyongracile cibarium egg (pi. XII, fig. 4), the radial threads
ProtuberacanescenswasdescribedasProtubera are visible within the thick gelatinous layer of
because the Western Australian material was the peridium, and at their inner end are many
not seen to open and yet contained apparently structures with convoluted outlines, that are
maturespores. The onlydifferencebetween the the developing arms of the lattice. Semmens
typedescriptionofProtuberacanescensandthe (1967), in an overlooked description of the
AltonaNorthmaterialisthatBeatonandMala- development of lleodictyon gracile (as Clath-
jczuk (1986) donotexplicitlynotethepresence rus gracilis), does mention the radial threads,
incrosssectionofcircularstructuresatthebase calling them ‘hyphal threads forming a series
ofthe radial threads (which they call sutures’) of membranous division-walls’. He also notes
traversingthe gelatinous layer ofthe peridium. that the tubes that will eventually form the
However, close examination ofthe original il- fruit-body are initially attached to the base of
lustrations ofProtubera canescens (Beaton and the radialthreads, adjacentto thegleba, andhe
Malajczuk 1986) shows aslight expansion ofat depicts the incipient tubes as roughly circular
least some ofthe threads where they meet the in cross-section (Semmens 1967, plate XIV-7),
gleba. Field noteswithacollection identifiedas although he does not show the tubes as occur-
Vol 127 (2) 2010 51
Contributions
ringatthebaseofeachradialthread.Theradial where joined (Cunningham 1944; Grey and
threads are also illustrated by Dring (1980: fig. Grey2005). Lattices ofthe AltonaNorth mate-
17E) for Ileodictyon gracile, who does depict rialfitwellwiththe characteristicsofI.gracile.
the developing lattice tubes as occurring at the Hosaka et al (2006) included three collec-
base ofeach thread (as observed in the Altona tions ofI.gracileand one ofI. cibarium intheir
North material). Castellano and Beever (1994) analysis ofmolecular data. It is not clear from
comment on the general similarity between the phylogenetic tree in Hosaka et al. (2006) if
Protubera and the Clathraceae, byvirtue ofthe collections of the two species fall in separate
presenceofradial threads (‘sutures’) and small, clades (monophyletic clusters), because there
smooth spores, but they do not comment fur- is very little difference in the DNA sequences
theronthegreatsimilaritybetween Ileodictyon among the collections ofboth species. The two
andspeciesofProtuberawithathickgelatinous collections ofProtubera canescens which were
middle layerto the peridium. includeddonotclusterimmediatelyadjacentto
We did not fully investigate the three-di- oneanother—oneseemsto fallwithcollections
mensional structure ofthe radial threads, but ofI. gracile, with the other closer to the collec-
Semmens (1967) shows that what appears as tion ofI. cibarium.Thereisverylittledifference
threads in cross section are thin plates that are between sequencedatafortheProtuberacanes-
embedded in thegelatinous middlelayerofthe cens collections and that ofthe two Ileodictyon
peridium. Whenthelatticehasfullydeveloped, species. Further analysis of morphology and
thelooseand separatedfragmentsoftheperid- DNA sequence data that includes multiple
iumshowapolygonalpatternonthe innersur- samples from both species ofIleodictyon is re-
face (Fig. IdandGreyand Grey2005: 99). This quiredto confirmthatI.gracileand I. cibarium
patternshowstheedgesofthosethinplatesthat are independent species, and to establish ifthe
formed the arms of the lattice and indicates unexpanded material of both species has the
wheretheyhaveseparatedfrom it.Thispolygo- formofProtuberacanescens, oriftherearesub-
nal pattern is also illustrated by‘Gaye from the tle differences in the unexpanded stage ofthe
Hunter’ (2009). two speciesofIleodictyon.
The presence of radial threads in the thick- Within other families of the Basidiomycota,
ened, gelatinous mid-layer of the peridium is regionssuchasthe InternalTranscribedSpacer
remarkablysimilarinbothProtubera canescens (ITS)oftheribosomalDNAhavebeenfoundto
andtheunopenedstagesofIleodictyon.Inother vary slightlywithin species, but differ between
respects, apart from the maturity ofthe lattice most pairs of species, such as in Cortinarius
itself, Protubera canescens and Ileodictyon are (Froslevetal 2007).TheITSwasnotoneofthe
also very similar, including sharing abundant regions included by Hosaka et al (2006) and
white rhizomorphs (although these are not analysis ofsequences from this region for Ile-
unusual in the Phallales). odictyon wouldbeofinterest.
ObservationofthedevelopmentoftheAltona FormalsynonymyofProtuberacanescenswith
North material from unexpanded fruit-bodies Ileodictyongracile is not warranted until unex-
tothoseproducingalatticeshowsthatthemor- pandedfruit-bodiesofIleodictyon cibariumcan
phology of the young stage of an Ileodictyon be compared to those ofI.gracileto determine
matches that of the description for Protubera if there are any distinguishing characters be-
canescens. This conforms to the finding ofHo- tweenthetwospeciesatan earlystageofdevel-
saka et al. (2006) that collections identified as opment.
Protubera canescens, Ileodictyon gracile and I. SynonymyofothertaxawithIleodictyon
cibarium were all extremelycloselyrelated in a
phylogeneticanalysis ofDNA sequencedata. gracile
In the type species of Protubera (P. maracu-
If Protubera canescens is an Ileodictyon, to ja Moller) fruit-bodies remain closed in all
whichspeciesdoesitbelong?Thetwospeciesof stages of development from initiation to final
Ileodictyon, I.gracileandI. cibarium,aredistin- dissolution (Moller 1895 as cited by Malloch
guished in the lattice stage by the former hav-
ingsinuouslyfolded arms,which are expanded s1p9e8c9i)e.sNoefvePrrtohteulbeesrsa, mitayis bpeossiimbmlaetuthraet sottahgeers
wherejoined, andthe latter having concertina-
ofstinkhorns, especially given the range ofre-
like folding ofthe arms, which do not expand lationships uncovered by Hosaka et al (2006).
52 The Victorian Naturalist
Contributions
Most species ofProtubera (Malloch 1989) have expanded fruit-bodies, but are produced once
the glebadivided into several discrete sections, theprimordial fruit-bodies haveexpanded sig-
and hence ifthey do turn out to be immature nificantly. In truffle-like fungi, where the fruit-
forms, they will be unrelated to Ileodictyon. body remains wholly or partially buried, the
Thereare,however,twospeciesthathaveasin- fruit-body never expands and mature spores
gle, central, gleba surroundedbya thickgelati- remain within the un-ruptured peridium. Dis-
nous layer which is traversed by radial threads persal oftruffle-like fungi is usually the result
(sometimes described as sutures’), and that ofingestionbymammals. In contrast, the Cage
also have well-developed rhizomorphs. These Fungus has an enclosed, truffle-like fruit-body,
areProtuberaafricana Lloydfrom SouthAfrica initially in which to produce spores, with the
(Malloch 1989) and P. parvispora Castellano benefitofprotectionfromdesiccation,butthen
and R.Beever from New Zealand (Castellano switches to an epigeal fruit-body, which gives
and Beever 1994). In addition, Rhizopogon access to insects (such as flies) which are pre-
rodwayi McAlpine from Tasmania shares a sumed to disperse the spores. Insects are at-
verysimilar morphology, with a gelatinous pe- tracted to the foetid-smelling spore masses ad-
ridium traversed by radial ‘fibres’ (McAlpine heringto the innersurface ofthe lattice, which
1895). The illustration accompanying the type explodes to its full size on rupturing ofthe pe-
description ofRhizopogon rodwayi also shows ridium (Bougherand Syme 1998).
a lattice-shaped pattern on the surface of the The Altona North material was initially half-
peridium. Despite the close morphological buried and the ‘Protubera canescens collection
similarityofPparvispora to P canescens, DNA from Belgrave South was hypogeal. Bougher
sequence data place the former species in the and Malajczuk (1986) note that Western Aus-
Protophallaceae, along with P maracuja and tralian material of Protubera canescens was
severalotherspeciesofProtubera (Hosakaetal. mostly hypogeal and decayed in situ. Further
2006). Therefore,caremustbetaken inmaking observations are required on the proportion of
judgements aboutrelationshipsbasedsolelyon fruit-bodiesthatremainburiedandunexpand-
morphology ed, and whether this is due to unfavourable
The closesimilaritybetween Protuberacanes- weather conditions or other factors. The role
cens and P africana and Rhizopogon rodwayi ofinsectlarvaeobservedto devourthegleba in
suggests that these two species could well be unopened fruit-bodies also needs investigation
immatureIleodictyon. ItisalsorelevantthatIle- as to whether this provides the fungus with an
odictyon gracile is known from Tasmania and alternativemethodofsporedispersal.
South Africa (Cunningham 1944; Dring 1980), Initially, in the ‘Protubera’ stage, we observed
which is where Protubera africana and Rhizo- alattice‘inminiature’surroundingtherelative-
pogon rodwayi occur. Cunningham (1944) al- ly firm gleba. However, just before expanding,
readysuggested thatRhizopogon rodwayiwasa the lattice occupies the whole interior of the
phalloidstinkhornegg,andChangandKantvi- fruit-body, with the arms tightly folded within
las (1993) note that the type ofthe species has the peridium (Semmens 1967). Growth in the
been annotated as being theyoung state ofIle- lengthofthelatticearmsapparentlypushesthe
odictyon gracile (as Clathrus gracilis). As with lattice into the area initially occupied by the
Protubera canescens, until developmental dif- gleba. The gelatinous middle layer of the pe-
ferences between I. gracile and I. cibarium are ridium becomes a little thinner before the pe-
known, it is not possible to definitelylinkPro- ridiumruptures(Semmens 1967),whichwould
tubera africana or Rhizopogon rodwayi to par- also create some extra room for expansion of
ticularspecies ofIleodictyon. the lattice. Thus, production of spores within
DevelopmentinIleodictyon the unopened Cage Fungus fruit-body forms a
Connection of the two ‘phases’ of the Cage slimymasswhichadherestothearmsofthelat-
Fungus, Protubera canescens and Ileodictyon tice as it expands before bursting from the pe-
ridium. Presumably, spores are mature before
gracile, indicates an unusual strategy for the
thelatticebursts fromwithin theperidium.
btiomdiyngexopfansspioorne.production in relation to fruit- Comparison of spore dimensions for Ile-
odictyon gracile and the various Protubera and
In the fruit-bodies of epigeal fungi, such as
Rhizopogon discussed above shows onlyminor
agarics, mature spores are not present in un-
Vol 127 (2) 2010 53
5 5
Contributions
Table 1.SporedimensionsreportedintheliteratureforspeciesofIleodictyonandselectedspeciesofProtubera
Species Sp6o-relengthxwidth (pm) Reference
4.5-
Ileodictyongracile 5-6.5(-7.5) x2-2.5 BougherandSyme(1998)
Ileodictyongracile 6x 1.5-2. Cunningham(1944)
Ileodictyoncibarium 4-6x 1.8-2. Cunningham(1944)
Protuberacanescens 4-5.5 x2-2.5 BeatonandMalajczuk(1986)
Protuberacanescens 4-5(-5.5) x 2-2.5 BougherandSyme(1998)
Protuberaafricana 4. 6.2x 2-2.8 Malloch(1989)
differences (Table 1), which could well be due References
to spores in theglebaofunopened fruit-bodies BeatonGandMalajczukN(1986)NewspeciesofGelopellis
notbeingfully mature (such as ata stagewhen andProtuberafromWesternAustralia. Transactionsofthe
the lattice arms were at a very early stage of BoBurgithiesrhMNyLcoalnodgiScaylmSeocKie(t1y98978,)4F7u8n-g4i8o2f.SouthernAustralia.
development). Further comparison of spore (UniversityofWesternAustraliaPress:Nedlands)
fduilmleynospieonnsfriunitt-hbeodsieeqsuewnocueldfrboemoufnionpteernesetd, atso CalosotmbeyalctloaatnaionnadMoAPfroNtaeunbwderZBaee.aelNvaeenrdw:RZGEeaalll(aa1c9ne9da4,)JoHuTyrrsnutfaeflrleao-nflgiBikouetma,BnaPyshiad3li2-,-
wouldtestsofmaturity(suchaswhetherspores 305-328.
can germinate). Chang YS and Kantvilas G (1993) A catalogue ofLeonard
Rodway’scollectionoffungi. I. HymenomycetesandGas-
Conclusion teromycetes.TasmanianHerbariumOccasionalPublication
4, 11-52.
Protuberacanescensisconsideredtobeanearly CunninghamGH(1944)TheGasteromycetesofAustraliaand
Id.evgrealcoiplem.enCtoanlsesqtuaegentolfy,Iletohdeicntyaomne, moPrsottulibkeerlay DrmNieenngwtDZoefa(lt1ah9ne8d0C.)la(tCPhournbatlcrieisabheeu.dtiKboeynwsthBteuolawluaettrhidonsr3)5a,r1a-ti9o6n.al arrange-
canescens should only be applied in terms ofit Froslev TG, Jeppesen TS, Lasssoe T and Kjoller R (2007)
being astage ofIleodictyon. Unexpanded fruit- Molecular phylogenetics and delimitation of species in
Cortinariussection Calochroi(Basidiomycota,Agaricales)
bodies ofIleodictyon shouldbe observedto see in Europe. Molecular Phylogenetics and Evolution 44,
what is the shape ofthe lattice that eventually 217-227.
emerges,inordertoidentifytheparticularspe- GreyPandGreyE(2005)FungiDown Under:theFungimap
GuidetoAustralianFungi.(Fungimap:SouthYarra)
cies. Fresh collections of Ileodictyon cibarium ‘Gaye from the Hunter’ (2009) Australian fungi - a blog:
needtobeexaminedcarefullytoseewhatisthe #32 Ileodictyon gracile. <http://australianfungi.blogspot.
form ofthe unexpanded fruit-body, and howit Hacwokms/w20o0r9t/h06D/L3,2-SiultetoodnicBtyCona-ngdraAciinlsew.ohrtmtlh>GC(1983)Dic-
mightdifferfrom thatofIleodictyongracile. tionary ofthe Fungi, 7 ed (Commonwealth Mycological
TheoriginaldescriptionsofIleodictyongracile Institute:Kew)
haenndceI.,ciifbianrdieuemdbaontyhodrataellforfoPmrotthuebe1r8a40csanaensd- HoDSsRoa,mkSiainmgK,puseBozantLeNSsB,,SNTS,opuaBhteraefavoerEraR,JR,WGCeaamnsldteTlJ,rlaaGnipoapceMhJiAnM,i(CA2,o0l0Kg6e)annMnoWe-,y
cens P. africana and Rhizopogon rodwayi are lecularphylogeneticsofthegomphoid-phalloidfungiwith
conf,irmed as synonyms of particular species, atnwoesnteawbloirsdhemresn.tMoyfcotlhoegniaew98s,ub9c4l9a-s9s59P.hallomycetidaeand
they do not threaten the priority of the two MallochD(1989)NotesonthegenusProtubera.Mycotaxon
long-establishednamesinIleodictyon. Mc3A4l,p1i3n3e-1D51(.1895)Australianfungi.AgriculturalGazetteof
SpecimensExamined NewSouth Wales6,752-758.
SemmensEJ(1967)Notesonthedevelopmentandstructure
Material ofIleodictyongracile (including the P. ofthe‘BasketFungus’,Clathrusgracilis(Berk.)Schlechten-
canescens stage) from Altona North has been dal.Muelleria1,219-221.
lodged at the National Flerbarium of Victo-
ria (MEL) and the Herbarium, Royal Botanic
Gardens Kew(K) (N. Sinnott3535,3548, 3566,
3631 and 3642). The collection from Belgrave
South is lodged at MEL (H. Weatherhead s.n., Received17April2008;accepted13August2009
=T.W. MayB534).
Acknowledgements
We thank Teresa Lebel, Sara Maroske and Frank
Udovicicforusefulcomments.
54 TheVictorianNaturalist