Fungal behaviour: a new frontier in behavioural ecology

While there is increasing acceptance that non-neural organisms such as plants, slime moulds, and bacteria can perform behaviours, the vast kingdom of fungi usually forgotten.We argue also be studied through theoretical framework behavioural ecology. This would benefit both fungal biologists – yielding a better understanding lives ecologists, providing access to model help explain evolution primary senses potentially discover behaviours new science.Fungi have analogous those other organisms, they exhibit behaviour, memory. suggests multitude questions paths could taken broaden our this forgotten underestimated branch in tree life. As human beings, make up everyday lives. What we do from moment wake go back sleep at night all classified concepts The same applies vertebrates and, some extent, invertebrates. Fungi are, most people’s eyes perhaps, eukaryotic multicellular with which humans share least commonalities. However, still express obtain their although are very different ours lens Moreover, insights behaviour may drive ecology general. All prokaryotic or eukaryotic, macroorganisms microorganisms, solve similar set basic problems survive: how energy nutrients, avoid being eaten killed, spread offspring partition resources between these activities [1.Dusenbery David Life small scale behavior microbes. Scientific American Library, 1996Google Scholar]. To address problems, evolved sets solutions (Figure 1 Table 1).Table 1Comparison key features abilities important for major phyla, comparable vertebratesaThe classification considerable flux genome sequencing increasing. number phyla currently ranges five 12 depending on author. Here consider JGI Mycocosm Fungal Genomics Resource (https://mycocosm.jgi.doe.gov/mycocosm/home). Numbers approximate details often uncertain. Only used comparison has largely been developed based them.ChytridiomycotaZoopagomycota MucoromycotaAscomycotaBasidiomycotaVertebratesProportion species Kingdom (approximate)<10<154525NAMain habitatAquatic/moisture filmsSoil plants animalsAllTerrestrialTerrestrial/aquaticSpread sporesSwimmingPassivePassivePassiveNAReproductionAsexual/sexualAsexual/sexualAsexualbSome predominantly asexual./sexualAsexual/sexualSexualGrowth pattern: determinate, d; indeterminate, icBody form hyphal, but yeasts.d/iiiidSpecialised hyphaedMorphology hyphae specialised specific function.nyyyNAYeast body formna fewyeSubphylum Saccharomycotina contains about 1000 species, yeasts.a fewNAMorphological switchingfMorphological switching includes ability change hyphal yeast vice versa or, some, production hyphal/mycelial forms associated differing physiological activities.nyynCross walls hyphaenngCross-walls produced delimit reproductive structures block following damage.yyNANetwork formationnn/yhSome, example, Mortierella, anastomoses.yyinternalComplex multicellulariSimple multicellular: cells direct contact environment, while not complex [62]., c; simple multicellular, sA few sss/cccMaximum size<1 cm<1 m?Usually <1 m? Occasionally several metresA few: many ha; >150 000 kg150 kgMaximum age1 week?<1 year<50 yearsA >1000 years200 yearsMovement water/nutrients over long distances within bodynnjNutrient movement does occur hyphae, mycelia relatively small.yyyAbility use extremely molecules (e.g., lignin)nnA fewSomenTropic/taxic responsesyyyyya them.b Some asexual.c Body yeasts.d Morphology function.e Subphylum yeasts.f Morphological activities.g Cross-walls damage.h Some, anastomoses.i Simple [62.Nagy L.G. et al.Fungi took unique evolutionary route multicellularity: seven challenges life.Fungal Biol. Rev. 2020; 34: 151-169Crossref Scopus (3) Google Scholar].j Nutrient small. Open table tab constitute 2–6 million more [2.Hawksworth D.L. Lücking R. diversity revisited: 2.2 3.8 species.in: kingdom. ASM Press, 2017: 79-95Crossref (92) Scholar,3.Baldrian P. al.High-throughput view magnitude global diversity.Fungal Divers. 2021; (Published online February 19, 2021. https://doi.org/10.1007/s13225-021-00472-y)Crossref (18) Scholar] (Box 1), despite rapidly genetics, biochemistry, cell biology physiology, surprisingly large gaps behaviours. We believe greatly under ecology, turn, will including fungi.Box 1Fungal characteristics relevant behaviourFungi one main lineages Like animals possess traits cell–cell communication, adhesion, long-range transport, programmed death, developmental program [40.Watkinson S.C. al.The fungi.3rd edn. Academic 2015Google fewer types (>12 compared >100 ~30 plants) origins Although unicellular yeasts), mycelial, comprising fine filaments [hyphae I)]. Hyphae grow by apical extension explore environment I), feeding extracellular digestion (secreting enzymes break down smaller ones absorbed). Tip growth, direction, controlled multicomponent organizing centre Spitzenkörper near tip fractal, tree-like system [63.Boddy L. Donnelly D.P. Fractal geometry microorganisms environment.in: Biophysical chemistry fractal processes environmental systems. John Wiley & Sons, 2008: 239-272Crossref (19) Scholar], lateral branches join adjacent resulting adaptive networks [7.Boddy Saprotrophic cord-forming fungi: meeting challenge heterogeneous environments.Mycologia. 1999; 91: 13Crossref (208) Scholar,12.Fricker M.D. mycelium network.in: Society Microbiology, 335-367Crossref (8) Scholar,64.Read N.D. al.Hyphal fusion.in: Borkovich K.A. Ebbole D.J. Cellular molecular filamentous fungi. 2010: 260-273Crossref I).In Dikarya (ascomycetes basidiomycetes), divided into compartments/cells transverse partitions (septa), extend wall inwards, leaving small, central opening allowing cytoplasmic continuity passage organelles. Compartments commonly two nuclei extent co-ordination/competition unclear [65.Mela A.P. al.Syncytia fungi.Cells. 9: 2255Crossref (7) Septal openings blocked off. prevents loss cytoplasm if hypha damaged allows differentiation morphology activity, gene expression formation tissue-like structures, dramatic responses.Fungi heterotrophs food dead organic matter, killing organisms/tissues/cells, living either parasites mutualists (lichen mycorrhizal fungi), combination methods. live environments where sources microclimatic spatially everchanging temporally They space time spores, single cells. cord- rhizomorph-forming soil search resources, operating foraging strategies [21.Boddy Jones T.H. Mycelial responses environments: parallels macroorganisms.in: Gadd G. environment. Cambridge University 2007: 112-140Crossref (21) extensive persistent biological characterised date Scholar,11.Heaton al.Analysis networks.Fungal 2012; 26: 12-29Crossref (72) Scholar,20.Fricker al.Mycelial networks: structure dynamics.in: Boddy Ecology saprotrophic basidiomycetes. 3-18Crossref (38) I). In responses. Behaviour well defined literature, broadly covers an organism’s movements, interactions, cognition (see Glossary), learning. Tinbergen introduced four classic ways asking why animal performs certain act. How improve survival reproduction? changed time? factors lead seen instance? individual it matures internal external affect this? [4.Tinbergen N. On aims methods ethology.Z. Tierpsychol. 1963; 20: 410-433Crossref (2279) These equally appropriate them gain context forage interact respond abiotic There reasons less understood than animals. microscopic opaque environments, matrix plant tissues, making difficult observe real time. Movement considered aspect frequently sessile [5.Andrews J.H. growth form.Can. J. Bot. 1995; 73: 1206-1212Crossref ‘any translocation biomass sustained own steered (navigated) response cues stimuli’ [6.Bielčik M. role active community assembly.Mov. Ecol. 2019; 7: 36Crossref PubMed Scholar]; thus, actually dynamic responsive, changing locations reallocation mycelial Scholar,8.Boddy al.Fungal network grazing.Fungal Genet. 2010; 47: 522-530Crossref (23) Figure II Box 2), clearly movement. A further hindrance understudied pivotal roles ecosystems, decomposers recyclers matter mutualistic mycorrhizas, overlooked [9.Boddy Fungi: unsung heroes planet.PAN Philos. Act. Nat. 2013; 10: 112-118Google this, (changes its patterns, architecture, spatial relationships, function) decision gained, microcosm studies Scholar,10.Fukasawa Y. al.Ecological memory relocation decisions quantity location resources.ISME 14: 380-388Crossref (11) Scholar, 11.Heaton 12.Fricker now tools study range scales 2).Box 2Methods examples varying scalesThe operates, must therefore studied, micrometres metres. Experimental setups microfluidic chips scale, laboratory microcosms trays, field present three case directional various II).Microfluidic chipsMicrofluidic chips, fabricated computer design, soft lithography, plasma bonding, contain microstructured enclosed channels chambers transparent breathable material designed researcher IIA) [66.Aleklett K. al.Build your soil: exploring microfluidics create microbial habitat structures.ISME 2018; 12: 312-319Crossref (64) techniques allow us mimic microscale (soil, cells, etc.) monitor precision [32.Aleklett exploration micro-structured Soil Chips.ISME 15: 1782-1793https://doi.org/10.1038/s41396-020-00886-7Crossref (12) Scholar,33.Held al.Intracellular mechanisms searching microenvironments.Proc. Natl. Acad. Sci. U. S. A. 116: 13543-13552Crossref (20) For was shown tips basidiomycete Psilocybe cf. subviscida when were growing labyrinths, sometimes lost confused forced navigate ’roundabouts’ IIA).Soil microcosmsSoil microcosms, compressed, non-sterile sieved soil, situation provide heterogeneity larger of, wood-decay IIB). Studies using systems revealed involving encountered ‘decisions’ out resource abandon favour [10.Fukasawa ‘memory’ direction relative original, original severed placed fresh might simply achieved development part wood elsewhere.Field systemsMycelial mapped manipulated directly adding relocating sections IIC). fairy-ring-forming fungus Clitocybe nebularis provides example field-scale directionality. It grows forest floor ever-increasing circle 30–40-cm-wide annulus When turves containing width cut reoriented, continued only approximately 90° annulus, any [31.Dowson C.G. al.Spatial dynamics interactions woodland fairy ring fungus, nebularis.New Phytol. 1989; 111: 699-705Crossref (41) Mycelia thus seem highly polar. II). Microfluidic IIA). elsewhere. Field One obstacles discussion lies fact neurons brain classical sense. concept what constitutes beyond vertebrate paradigm expanding [13.Pagán O.R. brain: flux.Philos. Trans. Soc. Lond. B 37420180383Crossref Scholar,14.Solé al.Liquid brains, solid brains.Philos. 37420190040Crossref (15) Solé al.