Tales and mysteries of fungal fruiting: How

f u n g a l b i o l o g y r e v i e w s 3 0 ( 2 0 1 6 ) 3 6 e6 1

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Tales and mysteries of fungal fruiting: How morphological and physiological traits affect a pileate lifestyle c € Hans HALBWACHSa,*, Josef SIMMELb, Claus BASSLER a

German Mycological Society (DGfM e.V.), Danziger Str. 20, 63916 Amorbach, Germany Chair of Ecology and Conservation Biology, Institute of Plant Sciences, University of Regensburg, Germany c Bavarian Forest National Park, Freyunger Str. 2, 94481 Grafenau, Germany b

article info

abstract

Article history:

Mushroom-forming fungi exhibit a tremendous variety of morphological, physiological and

Received 1 April 2016

behavioural traits. Though science had taken up the challenge to relate these traits to func-

Received in revised form

tions in the 20th century, such deliberations became much rarer in recent decades. In the

17 April 2016

review presented here we aim at reviving this research area, particularly in regard to

Accepted 18 April 2016

ecological implications. We have therefore compiled fruit body traits with their evidenced or suggested functions. Some traits have no immediate functional meaning, but many are

Keywords:

suggestive of some ecological importance. Many traits serve more than one function, and

Basidiomycetes

traits interact in the sense of trade-offs, patterns that reflect the economy of fungal design.

Fruit bodies

In conclusion, the review comes up with well and little-known mushroom properties, and

Functional traits

the numerous gaps in attributing traits to functions.

Morphological traits

ª 2016 British Mycological Society. Published by Elsevier Ltd. All rights reserved.

Mushrooms Secondary metabolites

1.

Introduction

After having spore traits and dispersal-related mechanisms € ssler presented in a previous review (Halbwachs and Ba 2015), we now focus on the fruit bodies traits proper. This encompasses architectural, reproductive, protective, growthand phenology-related traits. Functional traits have evolved either by adaptive radiation (Gillespie, 2009) or by exaptation (Gould, 1997). These traits are intricately interrelated to ecological behaviour and fitness (Palm and Chapela, 1997; Violle et al., 2007). Or

in other words, if we want to fully understand the ecology of organisms, populations, ecosystems, and biodiversity patterns a trait-based approach is needed (Koide et al., 2014; Aguilar-Trigueros et al., 2015). In fungi such a methodology € ssler et al., 2015, has only been applied in few cases (e.g. Ba 2016a,b; Halbwachs et al., 2014). Mycological pioneers like € umann have tackled in the early 20th A.H.R. Buller or E. Ga century some of the more basic questions relating to sporocarps. Some additional answers about fruiting behaviour and fruit body ecology were supplied by e.g. R. Moser and  menc¸on during the second half of last century, and H. Cle

* Corresponding author. E-mail address: [email protected] (H. Halbwachs). http://dx.doi.org/10.1016/j.fbr.2016.04.002 1749-4613/ª 2016 British Mycological Society. Published by Elsevier Ltd. All rights reserved.

Tales and mysteries of fungal fruiting

€ ssler et al. (2014). Many aspects still remain in recently by Ba the dark, particularly about the connection between ecological strategies of fungi and traits of their fruit bodies (Pringle et al., 2015). Higher fungi display a striking variety of fruit bodies (Fig. 1). In this review, we focus on basidiomycete macrofungi that form mushrooms, i.e. agaricoid and boletoid fruit bodies of saprotrophic and ectomycorrhizal fungi. The probably first agaricoid basidiomycete appeared in the evolutionary history of life during the Cretaceous (see Fig. 2), judging by the extremely meagre fossil record (Taylor et al., 2014: 179). The number of mushroom-forming species (agarics and boletes) is presently likely to surpass 9000 world-wide (Kirk et al., 2011). This figure is conservative, because with proliferating application of molecular methods drastic rise of new species is to be expected (Hawksworth, 2001; Blackwell, 2011). Mushrooms vary in shape, size, longevity, growth habits, phenology, colour, texture, odour, taste and more. These qualities apply to the saprotrophic as well as to the ectomycorrhizal guild. As in other organisms traits and trait combinations (!) should also be adaptive in fungi (Gavrilets and Losos, 2009). There are many widely scattered direct and indirect suggestions and clues in the sense of expert opinions, but only very few that are armed with hard evidence, e.g. the antibiotic pigment in Mycena aurantiomarginata (Jaeger and Spiteller, 2010). This is in most cases understandable, because testing e.g. assumptions about the adaptive value of colour or taste is either very difficult or not feasible. For statistical investigations, fungal databases are mostly too limited, particularly with regard to abiotic and biotic circumstances associated with occurrence. We have, however, compiled all pertinent information about response traits of agaricoid and boletoid basidiomycetes accessible to us and offer either evidenced or plausible explanations whenever possible. The latter should give a kick e so we hope e towards more studies in this research area. We follow a line which starts with the question why stipitate sporocarps of basidiomycete agarics (Agaricales and Boletales) take a pivotal role in fungal biology in the first place, followed by a detailed account of what mushrooms have morphologically and physiologically developed to optimise their dispersal fitness under differing environmental regimes. We then describe how mushrooms are formed as part of the fungal lifecycle, and round off with looking at the timing of mushroom fruiting (phenology). As we try to uncover trends, all relative and absolute measures refer to averages, if not stated otherwise. Taxon names have been adopted from www.speciesfungorum.org. Authors of figures are listed in the Appendix Table A2, if not otherwise mentioned in captions. The remaining figures have been contributed by the authors.

2. Why fruit bodies?: the ecological rationale of fungal fruiting Any organism needs to propagate and to disperse. Dispersal is essential for foraging and expanding to additional habitats

37

(“bet hedging”, see e.g. Mayhew, 2006: 67f), facilitating the reduction of intraspecific competition (Mayhew, 2006: 66), alleviating predation pressure by reducing density (JanzenConnell hypothesis, see Nathan and Casagrandi, 2004) but also allopatric speciation (Giraud et al., 2010). Higher fungi, being sessile and iteroparous organisms, disperse by vegetative and sexual means. Fungal fruit bodies produce propagules (diaspores) for sexual propagation. Their haploid germ tubes merge by outcrossing and form dikaryotic mycelia (Carlile et al., 2001: 58, 248). Without sex, higher fungi would be less adaptable to environmental changes and highly variable parasites (Brown, 1999). Heterozygotic outcrossing leading to meiosis also provides means to repair DNA damage (Moore and Frazer, 2002: 68), and to resist cellular parasites through mutations (Hamilton et al., 1990). In addition, sex reduces intraspecific competition by producing genotypic variants (Brown, 1999). Moreover, the genotypic plasticity allows fungi to occupy new habitats more successfully, thus fostering speciation (Mayhew, 2006: 137e142). Obviously, benefits of recombination and investing in fruit bodies evolved because sex pays, though pay-offs are likely (cf. Bonte et al., 2012). Vegetative propagation is mainly achieved by developing hyphal structures (mycelia, rhizomorphs and sclerotia) that are often capable to bridge considerable distances. Some basidiomycetes grow rhizomorphs over several hundred meters, e.g. Armillaria bulbosa during over 1000 y (Anderson, 1992). This exemplifies the major constraint of vegetative propagation. It is slow and cannot react to short term threats, such as long-lasting water logging episodes. Propagation by diaspores overcomes space and time constraints in a far more effective way than vegetative propagation. Dispersal of spores can happen by abiotic mechanisms (mainly by air and water movement), and by biotic vectors such as insects and mammals, bridging distances of several kilometres within few € ssler, 2015). A special case is Mycena days (Halbwachs and Ba citricolor, a tiny mushroom parasitising on Citrus. Its cap acts itself as diaspore (Watling, 1996). In agaricoid and boletoid basidiomycetes, diaspores are produced in a hymenium (lamellae or tubes) which is attached to the underside of the cap of a mushroom. In other basidiomycetes the hymenium may rest inside the sporocarp as in gasteroid fungi, cover the ends of coralloid fruit bodies as in Ramaria or the whole fruit body as in the Tremellaceae, and may completely cover the surface of corticoid fungi or covers the underside of bracket fungi (cf. menc¸on et al., 2012: 291e301). As we will see in the Cle following sections, the mushroom architecture has many ecological functions and may even have advantages over other fungal blueprints.

3. Form follows function: the mushroom blueprint The basic architecture of agaricoid and boletoid fruit bodies aka basidiomes, basidiocarps, sporocarps or simply mushrooms has not changed probably since approximately 100 million years (Hibbett et al., 1995): stipe, cap, sporophore. This arrangement is obviously successful, and, therefore,

38

Fig. 1 e Fruit body types af various macrofungi: e.g. bracket type (1), agaricoid (2, 3, 7, 9, 10, 15), tremelloid (4, 16), coralloid (6, 14), gasteroid (11), cup fungi (5, 9) (Photography:  menc¸on et al. (2012) and Ulloa et al. (2012) for further classification. Alison Pouliotª, with permission). See also Cle

H. Halbwachs et al.

Tales and mysteries of fungal fruiting

39

Fig. 3 e Functions attributed to fruit body morphology. Fig. 2 e Reconstruction of a fruit body of Archaeomarasmius legettii, a mushroom recovered from Cretaceous amber (East Brunswick, New Jersey, USA: Hibbett et al., 1997) The cap is ca. 3.2 mm wide. (Courtesy of D.S. Hibbett).

genetically conserved as also in other organisms, e.g. the liverwort Marchantia and the green alga Acetabularia. This architecture is found e with variations in morphological details e in almost 40 genera with close to 8000 species (Kirk et al., 2011). Irrespective of the ecological guild of a mushroom (saprotrophic, parasitic or ectomycorrhizal) the main functions of the fruit body can be described as shown in Fig. 3. In the following sections, we show how these and other morphological features may or do work. Note that traits often have multiple functions (Prothero, 2013: 145).

4. David and Goliath: the meaning of fruit body size The fruit body size of basidiomycete macrofungi covers a wide range: some like Gymnopus androsaceus have caps of a few millimetre width, whereas Termitomyces titanicus sports caps with a mean diameter of 1 m, weighing 2.5 kg (Pegler and Piearce, 1980). Since fruit body (¼biomass) development is a considerable investment for a fungus, different taxa are clearly adapted to different biomass concepts in view of dispersal fitness. Depending on phylogenetic origin and growth conditions, basidiomycete macrofungi obviously use trade-offs between fruit body size and number, as was found € ssler et al. (2015). How this trade-off is related to myceby Ba leial biomass of genets is still unknown, because relevant data are hardly available to date. Results of the same study indicated that ectomycorrhizal fungi have larger fruit bodies than saprotrophs, possibly due to the more reliable carbon

supply via the host. Low productivity correlates with elevation and geographical latitude where more often small mushroom € ssler et al., species occur (Austwick, 1968; Kallio, 1982; Ba 2016a). Interestingly some ectomycorrhizal species occurring in temperate and in (sub-)arctic biomes do not differ in size, e.g. Leccinum versipelle or Lactarius trivialis (Kallio, 1982). Instead it is evident that in mountainous subarctic heathland the productivity is tenfold lower than in subarctic lowland birch for€nheimo, 1987). Whether this phenomenon is the ests (Metsa direct result of climatic differences or related to the size of host trees needs more investigation. Intraspecific variations (plasticity) in size are common. The former becomes evident when looking at the size data, e.g. in the Funga Nordica (Knudsen and Vesterhold, 2008). The cap diameter of Lepista nebularis for example, may vary between 4 and 20 cm. These variations are most likely caused by temperature variations (Austwick, 1968), and nutrient and especially water availability (cf. Buller, 1922b: 82e88; Moore, 1998a: 136). The authors observed in 2003 and 2015, two extremely dry years in the southern parts of Germany, considerable dwarfing in e.g. Macrolepiota mastoidea, Boletus edulis and Lepista nuda (data not shown). Large fruit bodies survive and sporulate for longer periods than small ones (Buller, 1909: 24, 221; Richardson, 1970; € rfelt and Go € rner, 1989: 48ff; Leusink, 1995; Kramer, 1982; Do Moore et al., 2008), having at the same time a larger spore production because of a larger hymenium. Parasola plicatilis perishes within a couple of hours (Roberts and Evans, 2011: 257), Clitocybe nebularis may be vital over almost 30 d (Moore et al., 2008). The higher longevity is mainly caused by the slower desiccation of large fruit bodies (Moser, 1993). In addition large fruit bodies possibly delay destructive action of predators by sacrificing trama. But this is only one side of the coin. Large fruit bodies may attract friendly foes e.g.

40

insects (Bunyard, 2007), and other fungivores that digest mushrooms and disperse the spores by excretion, e.g. squirrels (see Fig. 4) (Currah et al., 2000), deer, slugs and many other animals (for a comprehensive account refer to Halbwachs and € ssler, 2015). Ba A few taxa have evolved a trick to overcome the dispersal constraints connected with small fruit bodies, i.e. sensitivity to desiccation. Marasmius rotula can survive through rewetting several weeks, but also other species such as Gymnopus dryophilus, Marasmius oreades, some Lactarii and boletes show the same property (Gilliam, 1975).

5. Well capped: protective properties of the pileus The pileus is primarily a physical protection of the hymenophore against biotic and abiotic hazards (Fig. 1). Apart from biomass, which is protective in itself as lined out above, the pileus may possess properties to enhance its function. It is often covered by protective tissues, such as a felty (tomentose) or viscid (glutinous) pileipellis, by small or large scales (squamulose or squarrose), hairs (ciliate, sometimes only at the cap margin), spines (echinate), woolly tissue (lanuginose, floccose), veils etc. All these structures are assumed to reduce effects of excessive radiation, desiccation and/or deter

H. Halbwachs et al.

fungivores (for details and references see Table A1 in the Appendix, for examples see Fig. 5). Extreme cases of a viscid pileipellis are e.g. Mycena epipterygia (Fig. 5f), Crepidotus mollis, Panellus mitis, and some Psilocybe species: they have a gelatinous e rubbery skin (Michael et al., 1986: 17). Veils and cortinas have an additional advantage during maturation of the fruit boy, they keep humidity in the hymenium, which is crucial for sporulation (Ingold, 1966). Desiccation is a permanent threat for mushrooms, but excessive water can be detrimental, too. To avoid soaked hymenia some mushrooms have a hydrophobic pileipellis, such as Agaricus bisporus (De Groot et al., 1996). On the other hand, in some taxa water is accumulated in the trama so that evaporation leads to cooling and eventually to increased airflow beneath the cap, which fosters spore dispersal (Husher et al. 1999). Pigmentation is also a functional feature. A colour may signal poisonous or unpalatable qualities, or the other way round, may attract vectors. Many pigments are antibiotic, melanins fortify cell walls and resist microbial attacks, and some pigments act as filters against hazardous radiation. A more detailed account of macromycete pigments is found below in section 8. In conclusion, the pilei of the Agaricomycetes support, protect and supply the hymenophore. In addition, they may serve as bait for vectors.

6.

Fig. 4 e Red squirrel (Tamasciurus hudsonicus) carrying a bolete into a spruce tree (Jasper National Park, Alberta, Canada)

Fruit body building: keeping the head up

Already Ingold (1946) noted: “Small agarics tend to be relatively tall and have relatively thin stalks, and large agarics tend to be relatively short and have relatively thick stalks as compared with an ‘average type’. It is suggested that these tendencies for form to alter with size follow from simple mechanical and functional considerations”. The build of agaricoid mushrooms is apparently governed by architectural constraints, as we could confirm (Fig. 6). The graphs show that the larger the cap the thicker the stipe, and the slimmer the build the smaller the fruit body, which corroborates the findings of Bond (1952). It is self-evident that stipe length correlates with wind dispersal fitness, and thickness with stability, leading to a trade-off. Most species with thin or long stipes as Macrolepiota procera have a pronounced cortication and/or are hollow (Buller, 1909: 41), some have tough textures as Collybia fusipes. This leads to a similar rigidity as thick stipes, and to a flexibility enabling the cap to swing back into its original position (wind!), thus maintaining the vertical orientation of the hymenium. Mushrooms with thick or ventricose stipes are often hollow (e.g. Suillus cavipes), have stacked caverns (e.g. Russula laurocerasi) or cores with a cottony texture (e.g. Russula decolorans). All these structures combine biomass economy with physical stability, presumably as for instance in grasses (Niklas, 1992). What about those taxa, those have thick and throughout fleshy stipes, as Boletus edulis? One plausible explanation could be that compact stipe trama acts as nutrient and water repository, possibly a biomass investment into longevity. Short and stocky fruit bodies may have survival advantages in wind-prone settings (Moser, 1993), and are

Tales and mysteries of fungal fruiting

41

Fig. 5 e Protective morphological structures: a [ tomentose (Xerocomellus chrysenteron), b [ ciliate (Lactarius mairei), c [ squarrose (Strobilomyces strobilaceus), d [ echinate (Cyptotrama asprata), e [ viscid (Cortinarius vanduzerensis), f [ gelatinous (Mycena epipterygia).

Fig. 6 e Left: ratio between cap Ø and stipe Ø, right: ratio between slenderness (stipe Ø/cap Ø) and biomass of fruit bodies for 593 mycorrhizal and saprotrophic species (all values log-transformed). Data extracted from Knudsen and Vesterhold (2008).

42

Fig. 7 e A specimen of Amanita muscaria that has lain in the horizontal position over night (after Krieger, 1936: 43). In Coprinellus curtus this reaction takes only around 1 h (Buller, 1909: 70e71).

potentially able to withstand frost for a longer time than delicate ones. At the same time, mushrooms with short stipes may trap humidity under cap and hymenophore. Most stipes are cylindrical, ventricose or taper towards the tip (conical), fewer become thinner the other way round (inverted conical). Many taxa with cylindrical or conical stipes have a thickened or bulbous stipe base, some exhibit disk-shaped bases, especially in the Mycenaceae. All this again is suggestive of a trade-off between biomass economy and maintaining fruit body stability as well as geotropic orientation of the hymenium. Stipes, those are thinner at their upper part than at their base seem to have an additional advantage. They can easier bend into a vertical position than a cylindrical or ventricose stipe when e.g. growing out of crevices or after physical disturbance of the substrate (geotropism, see Fig. 7 and more details in section 9 below). Macromycetes with inverted conical or tapered bases seem to fructify from relatively deep strata, so that the stability of the fruit body is ensured by the surrounding substrate (P. Karasch, pers. obs.) as for example in Butyriboletus appendiculatus. Many taxa have lubricous stipes (e.g. in Hygrophoraceae), and may have the same properties as already described for caps. Others are pigmented, interestingly mostly towards the stipe base, which is suggestive of an antibiotic function with regard to soil-borne organisms (see section 8).

H. Halbwachs et al.

The stipe surface often shows structures, such as scales, ridges and bristles, that may at least slow down invertebrates while advancing to the nutritious hymenium. The reticulate cutis structures observable in many boletes at first glance have no obvious function. Yet, they are caused by the remnants of a palisadoderm, that completely covers and protects the stipe of young specimens. When growing and expanding this palisadoderm is stretched horizontally and fragmented, and thus causes ridges and depressions, analogous to expanded metal. In e.g. Boletus erythropus fine scales are caused by a comparable mechanism (Fig. 8). An obvious obstacle pose annuli (ring-shaped structures € rfelt and Jetschke, 2001: left by the velum partiale, see e.g. Do 337), particularly when shaped like a downward sleeve (Fig. 9). Annuli may cause as an obstacle some, albeit minor, air turbulence and thus slightly increase dispersal efficacy, as Buller (1922: 394) suggested. A number of taxa have evolved clustered (cespitose) fruit bodies as e.g. Agaricus bohusii and many wood-dwelling agarics. Some taxa have dendroid stipes with multiple caps (Fig. 10). For one, this habit traps humidity, necessary for successful sporulation (Moser, 1964). Second, it is able to adjust fruiting biomass to nutrients and water availability. Third, cespitose fruiting is predominantly seen in lignicolous fungi, which need to bend their stipes to reach a favourable position, and horizontal orientation for their caps (phototropism combined with geotropism, see section 9 for details). This degree of bendabilitiy is presumably easier to achieve with thin stipes than with thick ones. In a cluster of H. lateritium of say 12 each cap would be ca. 60 mm wide. To achieve the equivalent cap area in one, the diameter would be ca. 20 cm, which would need a stipe of ca. 2.5 cm diameter and almost 20 cm length to be able to bend by 90 (cf. Fig. 9). In the end, it seems that being cespitose is simply a question of geometry. Still, reaching a horizontal position of the pileus can be solved in a different way. In several clades of Agaricales, the stipe is more and more reduced, while the pileus itself undertakes the task of correct orientation, e.g. in Pleurotus, Claudopus, and Crepidotus. Pilei of that fruit body type can be attached to the substrate (dead wood in most cases) laterally or to their upper side, without the need to bend a stipe.

Fig. 8 e Structure of the stipe surface in Boletus reticulatus (left) and B. erythropus (right). In young stipes (top; cross section), a continuous layer of palisadoderm (black) is covering a cutis (grey); in older stipes, the palisadoderm is stretched and fragmented (centre and bottom; cross section and top view). Note that the varying distribution of palisadoderm fragments matches with ridges or depressions in the cutis layer. (Scale bar 1 mm).

Tales and mysteries of fungal fruiting

43

Fig. 9 e Various Amanitas with annuli (modified after Lindau and Ulbrich, 1928: 364).

The shape of caps and their attachment to the stipe vary greatly across the Agaricales. These cap/stipe configurations of mature fruit bodies are often suggestive of bearing an ecological meaning, though it is mostly difficult to prove. Still, some ecological interpretations are worthwhile to consider (Table 1). As it can easily be seen that fruit body statures generally combine several advantages or functions. The already mentioned trade-off between fruit body number and size while maintaining reproductive fitness seems to be the rule. The question remains, why terricolous agaricoid fungi follow different concepts of compartmentalising biomass into few large or many small fruit bodies. Spatial and temporal resource distribution is likely to play a decisive role, which generally leads to differing life history types. The latter span from ruderal (r-type) to combative (C-type) strategies (see e.g. Dix and Webster, 1995: 5e11). This is a simplistic model, though useful to illustrate fungal habits. The interplay of these strategies with substrate availability is schematically visualised in Table 2. In conclusion, the build of fruit bodies reflects multiple trade-offs among dispersal fitness, architectural stability and

environmental hardiness. The trait syndrome observed for a particular species appears to maintain its composition but changes in the dimension of individual traits to adjust to environmental fluctuations.

7. Spore factory: hymenophore

it’s

all

about

the

As lined out above the positioning of the hymenophore is vital for the reproductive fitness of mushrooms. The architecture can be categorised into lamellate, poroid and hydnoid (tooth-shaped). Lamellae and lamellulae (small lamellae filling gaps between gills with growing radius of the cap) are always radially oriented, though theoretically, they also could be arranged concentrically or spirally, which would make the hymenal area significantly be larger (Fischer and Money, 2010). But then the vertical orientation of the gills during expansion of the pileus would physiologically be more demanding, i.e. more costly, than with a radial arrangement (Buller, 1922b: 378ff). At the same time radial gills should stabilise particularly thin-fleshed caps. Contrary to intuition

Fig. 10 e Cespitose fruit bodies: left Hypholoma lateritium, a lignicolous species with cespitose fruit bodies, right Polyporus umbellatus with composite stipes.

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H. Halbwachs et al.

Table 1 e Examples of ecological interpretations of fruit body shapes. Examples

Type and function(s) Plane-convex, thick stipe: This mostly fleshy type is a good water and nutrient reservoir for spore generation and release. It poses a barrier to the hymenium for invertebrates and is a good insulation against excessive temperatures. It offers optimal space for a hymenium (the larger the circumference the more lamellae or tubes can be cramped in, cf. Fischer and Money, 2010).

Clitocybe nebularis Depressed, funnel-shaped: This mostly thin-fleshed type exposes the mainly narrow gills to a relatively broad aerial layer, thus improving wind dispersal, and finally reproductive fitness. At the same time, the investment of this type into sporocarp trama is relatively low, in spite of decurrent gills. Whether this type of cap has an advantage by being able to collect and absorb precipitation, is unknown.

Pseudoclitocybe cyathiformis Cylindrical, campanulate, conical (mostly thin-fleshed): Such cap shapes are mostly correlated with long and thin stipes. This has static reasons: the centre of gravity sits relatively low, and thus stabilises the construction. Often bell-shaped caps are only loosely attached to the stipe, and remain therefore in optimal position, regardless of any tilt of the stipe (Buller, 1909: 43). Evidently slim caps keep humidity better than expanded ones, and again this optimises spore release, despite thin trama.

Coprinellus micaceus

Tales and mysteries of fungal fruiting

45

Involute margin: Before mushrooms expand, their cap is incurved. In some species, the cap margin remains involute even when reaching maturity. This € rfelt and Go € rner, 1989: 61). reduces predator attacks (Do

Paxillus involutus

tubular (poroid) hymenia are less efficient, they offer ca. 25 % less area than gilled caps with a given diameter, hydnoid con€ der, 1983). Still, other than lamelfigurations ca. 80 % less (Po late hymenophores must have some advantage. The poroid architecture makes it more difficult for predators to reach the nutritious hymenium, and keeps humidity better than the other forms, i.e. are better suited for arid habitats. Mushrooms with hydnoid hymenophores have direct access to turbulent air for spore dispersal, and may take advantage of invertebrate vectors. Studies about such interpretations seem not to exist. Highest gill density is achieved by fungi with thick stipes and wide caps. They can accommodate more lamellae and lamellulae around than thin stipes. Dense gills or narrow pores retain humidity better than wider arrangements, though the latter may have advantages in the exposure of spores to turbulent air. At the same time, the risk for getting fungivores into the hymenium is greater. Some Marasmius species have extremely thin stipes that would only allow few gills to get attached. This constraint is overcome by forming a collarium around the stipe, thus increasing circumfer€ der, 1983). ence (Po

Mushrooms with thick gills, e.g. waxcaps, produce less hymenal area than thin ones due to the space constraint of fungal caps. Moser (1993) assumed that thick gills are, nevertheless, of advantage in dryer environments, because their relatively high biomass conserves more water to ensure full turgenscense. The profile of all hymenal configurations mentioned is wedge-shaped, which optimises the discharge of spores (Moore, 1991). The attachment, particularly of gills to the stipe, shows some variation between decurrent (continuing downwards), adnate (broadly attached) to adnexed (narrowly attached) and finally free (not attached). Whether these forms are functional is unknown. Free and  notched forms may be advantageous in species with fast unfolding caps by minimising gill ruptures near the stipe. To our knowledge, no studies have taken up this question so far. Free gills may also serve as a pseudocollarium for easier accomodation of primary gills, as in Mycena adscendens. In some taxa, e.g. the Mycenaceae, various strategies to enlarge the Hymenium can be observed. Apart from collaria, furcated, decurrent and anastomosed lamellae occur, even poroid types are encountered (Fig. 11).

Table 2 e Relations among an upper soil profile (in this example a cambisol of temperate forests), spatial and temporal resource availability (stability), fruit body traits and life history type continuum (expressed as ruderality). The visualisation is an interpretation of life history strategies (Grime, 1977) in relation with evidence about the fruit body size-number trade€ ssler et al., 2014), and with common field observation. The wedges represent effect or trait gradients. off (Ba Horizon Litter (L) Organic layer (O) Topsoil (A)

Depth (cm) 2e6 2e10 10e30

Resource stability

Fruit body number

Fruit body size

Longevity

Ruderality

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H. Halbwachs et al.

Fig. 11 e From left to right: Mycena ascendens with Pseudocollarium, Hemimycena ignobilis with descendent and some forked gills, Mycena rapiolens with anastomosed gills, Favolaschia calocera with poroid hymenium.

A few basidiomycetes produce conidia for asexual reproduction, such as Dendrocollybia racemosa on the stipe (Fig. 12). Conidiospores are able to survive in adverse conditions menc¸on et al., 2012: 122). (Cle

The hymenal surface and/or edge often produce cystidia or similar protrusions. These elements have multiple functions: they can keep gills at an appropriate distance, act as spacers to keep basidia sufficiently apart and act as air traps to keep up humidity (Largent et al., 1978: 71; Moore et al., 1998). Finally, they seem to fend off predators such as spring tails (Nakamori and Suzuki, 2007). Differing trade-offs between hymenal area, predator protection and dispersal efficacy have probably evolved due to biotic and abiotic constraints at differing biomes. The intricate trait patterns and mechanisms of ballistic spore discharge, dispersal by various means, germination and establishment add to the complexity of fungal lifestyles, and are decisive for reproductive competence. Details on this dimension of fungal fitness have been € ssler covered by the authors previously (Halbwachs and Ba 2015).

8.

Fig. 12 e Dendrocollybia racemosa.

Inner values: physiological traits

Not only a large biomass increases longevity, but also certain hyphal structures (Moser, 1993). Caps and/or stipes may be soft or tough, depending on the nature of the plectenchyma (hyphal context). The latter may be composed of one, two or three (sometimes even more) different hyphal types, the mitic systems. Most Agaricales develop monomitic plectenchyma consisting only of generative hyphae (the hyphae of the growing mushroom that partially develop into hymenal tissue). Dimitic systems combine generative and mainly fibre or binding hyphae. Examples are Hydropus, menc¸on et al., 2012: 304). TriMegacollybia and Clitocybula (Cle mitic systems are rarely found in the Agaricales (only in some polypores). Mitic systems and stiffness of the fruit body are directly related: the more mitic components the tougher the texture. A tough stipe can also be formed by generative hyphae that are tightly packed (thigmoplect) or by hyphae that are firmly glued together e.g. to horny stipes menc¸on et al., 2012: 306). A as in Marasmius (colloplect) (Cle detailed description of mitic systems is found in menc¸on et al. (2012: 302e306). Cle

Tales and mysteries of fungal fruiting

Mushrooms, as all fungi, are chemical factories. They produce a wide spectrum of secondary metabolites that are not required for housekeeping (growth, development or reproduction). Whether odourous volatiles, taste compounds, exudations or pigments, many of these constituents are essential in keeping hazards at bay such as extreme environmental conditions and predators. The chemical defence and chemical communication is based on a plethora of compounds that are mostly highly complex, and their ecological roles are in most cases still obscure (Spiteller and Spiteller, 2008; Spiteller, 2015). The most obvious products are pigments that are visible as colouration of fruit bodies. Sometimes pigments are also embedded in the trama, e.g. in Lactarius indigo (see Table 3). Fungal pigments are generally costly to synthesise. Complicated chemical pathways involving various enzymes and co-enzymes require a high energy input (cf. Gill and Steglich, 1987). This implies that pigments have important functions for mushrooms. These functions include antioxidative, free radical scavenging, anticarcinogenic, immunomodulatory, antiviral, and antibacterial qualities (Velısek and Cejpek, 2011). Some fungal pigments are toxic, such as the orellines in Cortinarius orellanus (Gill and Steglich, 1987: 230f) and anthrachinones in Dermocybe (M. Stadler, pers. comm.). Not all mushrooms are colourful, many are drab in colour like Lactarius turpis, the Ugly Milkcap (sic!). This mushroom is dirty olive-brown, and one could assume that this serves as camouflage so that it is overlooked by important fungivores. This is not likely because mushrooms generally develop conspicuous odours, a much more telltale signal for animals than colours. On the contrary, mushrooms more than often show bright colours that probably have a warning function with regard to repugnant tastes or toxic properties (aposematism), as in the toxic and pungent tasting Russula emetica with its bright-red cap. Interestingly one finds other, harmless and mild-tasting species that use the same warning signal, e.g. Russula paludosa, possibly a (Batesian) mimicry (cf. Larson, 2009). Aposematism and mimicry in mushrooms, both phenomena should not be overrated, because evidence is still scanty (Guevara and Dirzo, 1999). Generally, conclusive hypotheses or even theories about fruit body pigmentation have not been presented to date. This may be due to diverse factors that lead to pigmentation, e.g. with regard to phylogenetic roots, optical effects on predators, radiation protection, thermal effects, and the fact that fungal pigments are mostly reactive or protective chemicals with antibiotic qualities. It is a general observation in ecology that traits may serve several functions, as for instance feathers of birds serve as thermal protection, as flight apparatus and as sexual attractors. Also in plants, overlapping responses to single traits are common (Lavorel and Garnier 2002). White or whitish mushrooms may have an advantage because of their high albedo, which may lead to less desiccation. At the same time, it could be a trade-off for other potent secondary metabolites. This interpretation is as speculative as the attributions shown in Table 4. There is considerable information about the chemistry of fungal pigments, but very little about their autecological functions. This is understandable,

47

because designing evidential experiments is a great challenge (cf. Guevara and Dirzo, 1999). A rather spectacular phenomenon is bioluminescence (luminosity) in ca. 70 mushroom species belonging to e.g. Armillaria, Omphalotus and especially Mycena (for an example see Fig. 13). Bioluminescence is also known in insects and particularly marine organisms for which the biological functions are well known, namely to attract mates, for defence, for luring or confusing prey and more (Haddock et al., 2010). In fungi the underlying mechanism, the luciferineluciferase reaction, is known for more than a century, but the ecological meaning remained e paradoxically e in the dark, until recently. At least for the Brazilian Neonothopanus gardneri (Marasmiaceae) it has been shown that the green light, emitted only(!) during night, attracts insect vectors (Desjardin et al., 2008; Oliveira et al., 2015). From Australia it has been reported that Omphalotus nidiformis (ghost fungus) may attracts slugs by odour and luminescence (Young and Smith, 2005: 16). Whether bioluminescence in fungi has always a functional bearing is not known. Another colour phenomenon is staining when lesions occur (“bruising”), and trama is exposed to oxygen. Some illustrative examples are described in Table 4, including the compounds involved and their properties. Producing secondary metabolites with antibiotic properties upon injury are not confined to coloured compounds. We have already touched upon mushroom exudates, which are produced by lactifers when the trama becomes exposed to oxygen. Such latex or milk occurs in Lactarius, Lactifluus (see Table 4) and Mycena. E.g. Mycena galopus produces white milk, which becomes antifungal when reacting with oxygen (Spiteller, 2015). Whether fungal latex becomes a physical barrier when drying up as in certain plants is unknown, albeit plausible. Another or additional explanation: latex may be produced to gum up the mouthparts of predatory insects (Wicklow, 1988). Many mushrooms have an unpleasant taste as in Russulales, which can be excruciating pungent for humans and presumably for mammals in general. Bitter taste is also repugnant, but at least in deer only when they have experienced gastrointestinal distress with a certain mushroom (Nolte, 1998). Some taxa are hardly attacked by slugs, e.g. Lactarius quietus or Inocybe geophylla (Buller, 1922a). Volatile secondary metabolites (odour) can have deterring qualities. The typical “mushroom smell” (1-Octen-3-ol and up to 70 other components, Guthmann et al., 2011: 72) is a response activated by injury of trama (Spiteller, 2015) and deters slugs, to some extent (Wood et al., 2001). Probably the same and other odours attract fungivores that serve as vectors as it is known from truffles (Kirk et al., 2011: 640). The multifariousness of fungal odorants is perplexing. Mushrooms produce smells that resemble smells from other sources such as flour, marzipan, radish, coconut, rotting cab€ rfelt and Jetschke, 2001: bage, carrion, fruits, stink bugs etc (Do 135). If some of these smells possess biological functions is largely unknown. Most mushrooms rely on, for humans sensorically inconspicous substances, that deter or kill predators. Toxic secondary metabolites are produced by almost all mushrooms, even the priced bolete is slightly poisonous when ingested

Table 3 e Pigments of some macromycetes and their assumed functions. Species

Pigment(s) Violet: Cortiferrin, an iron(III)-complex which contains DOPA (Spiteller and von Nussbaum, 2005: 65), a neurotransmitter (Misu and Goshima, 2006). The biological function in fungi is unknown.

Cortinarius violaceu Yellow: b-Carotene and carotenoids (Gill and Steglich, 1987: 196), substances that are known to scavenge hazardous oxygen radicals (El-Agamey et al., 2004).

Cantharellus cibarius Red: Russupteridine derivates (Gill and Steglich, 1987: 212f). The fungus has a pungent taste and is toxic (Guthmann et al., 2011: 290), the colouration presumably serves as a warning signal.

Russula emetica Blue: Azulene derivate (Gill and Steglich, 1987: 186), which may have antibacterial effects induced by light (Baptista et al., 2011).

Lactarius atroviridis

Tales and mysteries of fungal fruiting

49

Green: Necatorone is a mutagenic alkaloid (Gill and Steglich, 1987: 227; Spiteller, 2015). Real green fungal pigments are rare. Green tints may often be composed of blue and yellow pigments.

Imleria badia Brown: Badione A (Gill and Steglich, 1987: 55), which is formed by the yellow trama pigment norbadion A by oxidation (Guthmann et al., 2011: 89), perhaps a protective mechanism.

Boletus aereus Black: Possibly melanins formed by oxidation (see Table 4: Reddening/ blackening).

Boletus aereus

raw (Guthmann et al., 2011: 73) (see also Box 1). Most toxins seem not to be effective across all groups of predators (Guevara and Dirzo, 1999), though humans and many other mammals share an aversion to pungent and bitter substances (Spiteller, 2015). Psychotropic substances such as psilocybin seem to affect not only humans, but e.g. also dogs (Kirwan, 1990). Field mycologists know, for example, well that mushrooms poisonous for humans are devoured by slugs without showing any irritation. It is e at first glance e hard to understand, why some mushrooms have evolved poisons lethal for mammals. One possible explanation is that, for instance, wild boars are obviously sensitive enough to avoid such mushrooms, when members of their sounder suffer from poisoning. Still, most mushroom toxins lead to

reversible irritations (indigestion, sensorial glitches etc.), which may provoke a learning effect and avoidance, mainly in vertebrates. Toxins, antifeedants and antibiotic active substances are either constitutive or activated upon injury (Spiteller, 2015). Stadler and Sterner (1998) found chemical changes due to injury in more than 50 % of 121 macrofungi investigated. Secondary metabolites include a wide spectrum of compounds, mainly phenolics and other aromatic compounds, terpenoids, alkaloids, hydrogen cyanide releasing substances and amino acids and peptides (Spiteller, 2015). How many different metabolites exist is virtually unknown, not even rough estimates can be found in the literature, the more so as the regulation of their synthesis seems to be very complex,

50

H. Halbwachs et al.

Table 4 e Some colour changes in mushrooms when bruised. Reaction Bluing

Reddening /blackening

Yellowing

Greening

Example Caloboletus calopus The fungus contains xerocomic acid which in the presence of oxygen undergoes an enzymatic transformation to blue quinone methide derivates (Nelsen, 2010), which have antibacterial properties (Zhou, 2009). Russula nigricans This species shows intense reddening when bruised, turning to black. The amino acid tyrosine is enzymatically oxidised to a red intermediate and further to melanin (Gill and Steglich, 1987), a potent bioactive agent against aggressive substances and microbes (Kuo and Alexander, 1967; Bell and Wheeler, 1986). Agaricus xanthoderma When bruised this species develops bright chrome-yellow stains. This is caused by xanthodermin, a compound that is active at least against Bacillus subtilis and B. brevis (Gill and Steglich, 1987: 239). Lactarius deterrimus The mushroom exudes ample quantities of an orange latex, which turns green after exposure. The fluid contains lactarofulvenol which oxidises to a mixture of coloured sesquiterpen and azulen derivates (Guthmann et al., 2011: 269), which may have antibiotic properties (Steglich et al., 1997: 587).

including epigenetic mechanisms (Brakhage, 2013). Regulator crosstalk between relevant gene clusters adds another level of complexity: several gene clusters may be simultaneously activated, and open a possibility of combinatorial biosynthesis, leading to the production of novel compounds (Brakhage, 2013). The intraspecific chemical armament of mushrooms appears to constantly change, which makes it difficult for predators to develop resistance, a classical Red Queen effect (Kempken and Rohlfs, 2010; Rosindell et al., 2015). The Red Queen, a literary character of a fantasy story by Lewis Carroll, had to keep up running to stay in the same place. Not only substances are produced, that fight or attract predators such as sequiterpenoids (Hanson, 2008), but also some, which protect against environmental hazards, such as extreme temperatures. It is well known that mycelia of mushrooms survive frost below 10  C up to several weeks (Moser, 1958). Field mycologists have come across many examples of the fruit bodies withstanding some frost, too. The authors observed e.g. sporocarps of Cuphophyllus virgineus covered in hoarfrost in the morning, and visibly growing towards noon after the sun had come up. It may well be

Fig. 13 e Mycena singeri, a bioluminescent mushroom from the New World tropical belt.

Box 1 Edible mushrooms

Fruit bodies of wild fungi are part of the human diet in all cultures since ancient times. Presently, over 1000 species are collected for food in more than 80 countries all over the world. In Siberia, almost half of the population collects huge quantities of mushrooms. With only few exceptions wild fungi must be cooked before consumption to avoid gastric irritations or poisoning. Then they are nutritious and a valuable food supplement. Moreover, edible, and also medicinal mushrooms can be a considerable part of income, especially in developing countries. From Scandinavian countries, it has been reported that cattle and reindeer consume sporocarps of Boletaceae. Sources: Ramsbottom, 1953; Palm and Chapela, 1997; Boa, 2007.

Tales and mysteries of fungal fruiting

assumed that this is due to the same substances which have been found in mycelia and spores, namely antifreeze proteins (which also protect against heat), sugars and beta€ ssler, 2015). laines (Blunden, 2001; Halbwachs and Ba Mushrooms often absorb or contain considerable amounts of metals. Cortinarius violaceus fruit bodies appear to have the highest content of iron of all mushrooms (7.5 mg per 1 g fungal dry weight, Roth, 2015). (Radioactive) Caesium is accumulated by a number of species, e.g. Cortinarius caperatus, an edible mushroom (Guthmann et al., 2011: 425). Other metals include cadmium, lead, mercury, silver and arsenic, which have toxic properties. Some trace metals such as copper, cobalt or molybdenum are essential co-factors of enzymatic pathways (Mendel et al., 2007). In addition, many rare-earth elements occur in relatively low concentrations, preferentially in the pileipellis and the lamellae (Falandysz and ka, 2013; Grawunder and Gube, 2015). Whether and Borovic in which way most of these metals serve a biological purpose is unknown. One phenomenon waits for explanation, the exudation of liquids as droplets (Guttation). Various mushrooms are guttulate, such as Chamaemyces fracidus, Hebeloma crustiliniforme, Hydnellum peckii, Lacrymaria lacrymabunda, Lactarius chrysorrheus, Limacella guttata, Paneolus guttulatus, Russula sardonia, Sarcodon lundelli, Suillus granulatus and Tricholoma pessundatum. Whether guttation can be attributed to a common function is questionable. In conclusion, the physiological properties of mushrooms are overwhelming, and eclipse the diversity of morphological traits. Particularly the secondary metabolites offer an unsurpassed functional spectrum, which to date is only deciphered to a minor extent. This challenge is mainly taken up by pharmacologically oriented research. Though evidence is still scarce, medicinal mushroom industry is thriving already nowadays (Watkinson et al., 2016: 403f), particularly in Asian countries (Smith et al., 2002). The fact that synthesising secondary metabolites is generally energy-consuming should lead to trade-offs, e.g. a lower growth rate (Shaw, 1992). Trade-offs connected with defence syndromes are subject of some ecological hypotheses in plant ecology (Stamp, 2003). The resource availability hypothesis has gained some support recently. It predicts that species adapted to resource-poor environments grow inherently more slowly, invest more in constitutive defences and support lower herbivory than species from more productive habitats (Endara and Coley, 2011). This is likely to be similar in mushrooms.

9. The making of fruit bodies: mechanisms of fungal fruiting Fruiting is not a spontaneous process, it requires the combination of suitable circumstances as precondition. First of all, the mycelium needs to develop and acquire nutrients and water from a quantitatively and qualitatively adequate substrate to become competent for fruiting (Moore, 1998a: 176f). Second, the environmental conditions must be within specific ranges, above all (substrate) temperature, the above- and belowground water regime, light and CO2 concentration re, 1980). (Manache

51

These conditions set, what is the kick-off for fruiting? The underlying reason is an arrest in mycelial growth, which seems to be triggered by disturbance: light exposure, temperature shock, nutritional crisis, injury and edge encounter (Moore, 1998a: 398). The latter can frequently be observed in hollow-ways, gullies and on ravines (cf. Lysek, 1984: 338), and as the authors did, at cross-sectional surfaces of decaying boles. Temperature drops are often fruiting elicitors (Pinna et al., 2010), e.g. a drop of 5  C over a few days in Boletus edulis (Olivier et al., 1997). That nutrition depletion commonly provokes fruiting is well known since the beginning of the 20th century (Hawker, 1950). In some cases, also bacteria are involved in fruiting initiation (De Groot et al., 1998). Even some quite exotic triggers have been found. Log banging is routinely used in shiitake cultivation (Royse, 2009), and electricity is known to induce fructification (Takaki et al., 2014). The latter may explain the alleged increased mushroom fruiting after thunderstorms (Wasson et al. 1986: 83e94). All these effects set off a chain of endogenous signalling and regulation events, in which cAMP (cyclic adenosine monophosphate) and € es and Liu, 2000; protein kinase A play important roles (Ku Rassow et al., 2008). The morphogenesis of mushrooms is indeed genetically controlled, but does not follow a tightly pre-programmed protocol. The regulation of fruit body development is highly complex, endogenous and exogenous constraints and factors may alter the fruiting process, partially by epigenetic mechanisms € es and (Moore, 1998a: 392e404; Busch and Braus, 2007; Ku  lez, 2015). Still, some blueprints govern the Navarro-Gonza way, how fruit bodies develop. These development types go back to the seminal work of Reijnders (1963). For basidiomycete mushrooms, two basic types are relevant. In hemiangiocarpic basidiocarp development through the development stages, starting with the primordium, the fruit body is enclosed by a velum. It rips apart when the cap unfolds, forming veils, annuli and sheaths. The gymnocarpic type does not show a protective velum. In any case, mushrooms grow in a way that keeps the cap in a horizontal position. We have already mentioned geotropism (or gravitropism), the ability to adjust the fruit body to allow for optimal spore shedding (vertical orientation of the hymenal surface). The bending of the stipe is basically achieved by developing longer cells in the lower part of the bending zone, and by restricted growth of the upper part (Moore, 1998b). The sensing mechanism seems to be statolithic: the nuclei in the cells are suspended in a mesh of actin filaments, which are attached to the cell wall, thus exerting a “tugging” stimulus by gravity, causing the cell to elongate (Moore et al., 1996). After the development of a cap the signalling for adjustment to gravity predominantly originates from the hymenium (Badham, 1982). The strictly vertical orientation of gills and tubes are maintained by the coarser stipe reactions. Finetuning is achieved by adjusting the hymenal elements themselves (Cooke and Whipps, 1993: 213) (Fig. 14). The gravitropic response is often suppressed by phototropism, the reaction to light (Griffin, 1996: 210f). Though fungi are not autotrophic, which would imply the use of light and CO2 to produce sugars as nutrient (photosynthesis), they are sensitive, especially to blue light during initiation and

52

H. Halbwachs et al.

Fig. 14 e Sideways folded gills after the cap had been turned upside down for 12 h (Lepista nuda). Often the gills are virtually flattened after such treatment and look like a closed old-fashioned iris diaphragm. The black line indicates the position of the cross-section shown on the right (Scales: mm).

growth of fruit bodies (Kendrick, 1985: 148). Certain species would form aberrant fruit bodies when growing in the dark (cf. Figs 16 and 6). Sensing light is achieved by opsins, basically the same receptor structures as in light sensing organs of e.g. animals (Bahn et al., 2007). In mushrooms, the lightsensitive receptors sit in the stipe and control sideway growth towards the highest light intensity, when growth is e.g. initiated in a crevice of a log (e.g. in Neolentinus lepideus, Buller, 1909: 48). When the stipe tip reaches open air and the light becomes sufficiently intense, geotropism takes over, the stipe bends upwards and develops a cap which shades the stipe uniformly (Carlile, 1965; Moore, 1991). The

Fig. 15 e Fruit bodies of Hygrocybe coccinea and Cuphophyllus virgineus after wriggling their way through turf and densely growing plant stems.

bending mechanism is probably based on enzymes and hormonal control analogous to plants, leading to a unilateral expansion of stipe cells (Bunyard, 2012). Another interplay can take place between geotropism and thigmotropism, a growth reaction to obstacles. Mushrooms have basically three options to overcome obstacles, (1) by enveloping the object with their fruit bodies (Werner, 2003), (2) by forcefully pushing the obstacle away by turgor (see Box 2), or (3) by an avoidance reaction upon contact (Werner, 2003; Halbwachs € ssler, 2012). and Ba The avoidance reaction can be quite sensitive, as experienced by the authors in course of a growth experiment with Stropharia rugosoannulata when applying a weight of only 8 g upon the cap (not shown). The very moment contact with the obstacle is lost, geotropism takes over again (Fig. 15). The sensing mechanism could be triggered by an unbalanced stress on the stipe when elongation is mechanically obstructed. The receptors proper are probably similar to other eucaryotic organisms, such as higher plants. When a cell membrane is deformed a system of microstructures and enzymes causes calcium ion channels to open, which induces an electro-chemical signal in the cell, eventually triggering a cell inflation (Jaffe et al., 2002; Bahn et al., 2007). Mushrooms may also react to wind (anemotropism) in an at first glance counterintuitive way. When exposed to low wind speeds (ca. 10 cm/s) fructifying Psilocybe cubensis turns into the wind, until gravitropism takes over again once the cap opens (Badham, 1982; Moore, 1991), giving the stipe a form of a tilde: w. The mechanism behind anemotropism is the asymmetrical desiccation of the stipe. It slows down hyphal growth on the windward and water-deprived side of the stipe, whereas the opposing cells grow normally, and hence cause the stipe to bend into the wind (Badham and Kincaid, 1984).

Tales and mysteries of fungal fruiting

53

Fig. 16 e Examples of aberrant sporocarps: 1 cup-shaped proliferation in Laccaria laccata; 2 morchelloid form in Clitocybe odora; 3 fasciation in Amanita citrina; 4/5/7 fruit body concrescence in Russula fragilis, Boletus edulis, Lepista nuda; 6 sterile antlered fruit bodies due to lack of light in Lentinus squamosus (Modified after Lindau and Ulbrich, 1928: 43).

Whether this is an adaptation is doubtful. It is more likely a straightforward biophysical response. Not only tropisms can cause sometimes quite strange forms. Intraspecific shape variations (teratological forms) are common, too. This has intrigued mycologists since the 19th century (e.g. Phillips, 1881e1882; Magnus, 1906), obviously because of the bizarre manifestations (Fig. 16). Some of these aberrations are induced by environmental factors, such as light deprivation, air pollution (Michael et al., 1983: 26e34) or mineral oil fumes (Kearney and Kearney, 2009). Others appear after infection with viruses or fungi, and often such anomalies are caused by genetical or epigenetical mechanisms (Watling and Moore, 1994). Though the occurrence of stipitate fungi implies a terrestrial lifestyle, the design is evidently also suitable for an aquatic environment. There are a few taxa, that habitually fruit submerged in fresh or sea water. Recently a new Psathyrella species, which lives in clear, cold waters of a river in Oregon (USA), has been identified (Frank et al., 2010). The spores are dispersed by sticking together and forming rafts. This

Box 2 Force of growing mushrooms

The force exerted by mushrooms can be astonishingly high. In Agaricus bisporus one fruit body of average size pushes with ca. 88 N when growing, enough to lift 17 € ssler, 2012). In this way tarpounds (cf. Halbwachs and Ba mac and heavy stones can be moved (Moore et al., 2011: 328ff). The biomechanical mechanism of fruit body elongation is no mystery, it is rather the simple sum of parts, fuelled by turgor (Money and Ravishankar 2005).

mushroom shows exactly the same features as any other Psathyrella (Fig. 17), an astounding example of the versatility of the mushroom architecture. In conclusion, the fruiting of mushrooms is a complex endogenous process, though primarily initiated by external factors, that stimulates among others the production of endogenous signalling and regulatory compounds. Other regulatory mechanisms are responsible for several tropisms to ensure the vertical exposure of the hymenophore.

10. Fruit body timing: the phenology of fungal fruiting € rfelt and Mushrooms may appear within hours or days (Do € rner, 1989: 48). The speed of fruit body development is not Go constant. Several phases can be observed (Fig. 18). The phases in fruit body development shown in Fig. 18 generally follow a sigmoid curve that is based on the logistic function, a derivate of the Gompertz curve (Winsor, 1932). However, here are exceptions, for instance in Lactarius necator: the elongation of the stipe is delayed and the cap already expanded when breaking the soil surface, thus delaying airborne insect attacks (Hanski, 1989). In ectomycorrhizal taxa a diurnal rhythm might occur, because fruit body growth de€ gberg et al., 2001). This pends on current photosynthate (Ho € ssler would be in line with a finding of Halbwachs and Ba (2012), who recorded the growth of an Amanita phalloides fruit body during several days. The curve showed weak diurnal oscillation of growth speed. Stamets (1993) described the cultivation demands for a number of edible and medicinal fungi. Under controlled conditions, he found that mycelial development, primordia formation and fruit body development showed different requirements (Table 5).

54

H. Halbwachs et al.

Table 5 e In most cases the three development phases showed similar optimum patterns. Temperature range 7e27  C, humidity range 80e100 %, CO2 concentration range 20,000 ppm.

Temperature Humidity CO2

Fig. 17 e Psathyrella aquatica growing underwater in the Rogue River (Oregon) (Frank et al., 2010), reprinted with permission from Mycologia. ªThe Mycological Society of America.

Mycelial development

Primordia formation

Fruit body development

High High High

Low High Low

Intermediate Low Low e intermediate

Illuminance was generally needed for primordia formation and fruit body development, but varied between 50 and 1000 lux among the different species. Substrate moisture was uniformly 75 %. An example (Coprinus comatus) is given in Table 6. How the physiological and environmental factors translate into the phenology of wild mushrooms is not clear in every detail, though temperature and moisture seem to play temporal key roles (Dix and Webster, 1995: 394e397; Moore et al., 2008; Pinna et al., 2010). Sufficient substrate moisture may not only be generated by precipitation, but also by condensation of soil-borne water vapour, when air temperature drops (Halbwachs, 2007). Intuitively one would assume that saprotrophic and ectomycorrhizal fungi behave differently, because the carbon supply is tied to the host trees with a seasonally changing photosynthate production. Evidence at present points at abiotic environmental (Straatsma et al., 2001; Halbwachs, 2007), climatic (Boddy et al., 2014) and genetic (Selosse et al., 2001) factors. On the other hand, ectomycorrhizal fungi show a trend of having more compressed fruiting seasons, which is probably linked to the phenology of the hosts (Boddy et al., 2014). A more direct effect of photosynthate supply on fruiting of the ectomycorrhizal guild was found to € gberg et al., 2001). This is be on the number of sporocarps (Ho reflected in the change of productivity and phenology of ectomycorrhizal mushrooms due to climate change: in a Swiss fungus reserve production doubled since 1975, the fruiting € ntgen et al., 2011). The fruitperiod was delayed by ca. 10 d (Bu ing season of the mycorrhizal guild in a Japanese deciduous forest is connected to increased net photosynthesis rates in host plants, leading to unimodal fruiting (Sato et al., 2012). In boreal coniferous forests the fruiting season is apparently extended, probably due to continuing photosynthesis of the evergreen hosts until the first enduring snowfall (Fortin and Lamhamedi, 2009). Phenology seems not only being driven by direct environmental effects, but also by indirect ones. It is highly probable that the phenologies of fungivores,

Table 6 e Growth parametres for Coprinus comatus. Mycelium Fig. 18 e Schematic of fruit body development. Legend: a“embryonic” stage (primordium); b- button stage; c-stipe elongation; d-final expansion of cap, start of sporulation. Continuous line: fruit body growth; dotted line: cap diam€ rfelt and Jetschke, 2001: eter (Redrawn and modified from Do 342).

Temperature Humidity CO2 Light



21e27 C 95e100 % 5e20 & ./.

Source: Stamets (1993: 225).

Primordia 

16e21 C 95e100 % 0.5e1 & 500e1000 l

Fruit bodies 18e24  C 80e90 % 0.5e1 & 500e1000 l

Tales and mysteries of fungal fruiting

especially insects, and mushrooms interact (Hanski, 1989: 43ff). On the one hand, seasonal constraints limit fungal fruiting and peak seasons of fungivorous insects. If they coincide, perhaps by coevolution, mushroom species had to develop effective defences, such as deterrents (see section on secondary metabolites) and/or large (long-lasting) fruit bodies (Hanski, 1989: 58f). On the other hand some fungi may have evolved phenologies which evade fungivore seasons (Boddy and Jones, 2008), probably also following the Red Queen principle. Invertebrates acting as vectors and mushrooms may have synchronised their phenologies. To our knowledge, the interaction of such phenologies has never been subject of rigorous studies. Fungal fruiting phenologies are changing in many countries. They coincide with the extension of the growing season due to climate change, especially in the ectomycorrhizal guild (Kauserud et al., 2008, 2012; Gange et al., 2013). Frequently one encounters claims about the influence of the moon on fruiting. This has been subject to some scientific evaluations (Halbwachs, 2008; Egli et al., 2006). All these authors conclude that there is no evidence suggesting such a relationship. Moreover, it was pointed out that plausible physical and physiological mechanisms could not be identified. In conclusion, it becomes clear that the timing of fruiting is crucial for development, function and survival of mushrooms, and finally for reproductive fitness.

11.

The bottom line: fit for fearsome habitats

Trait-based approaches have some tradition in plant and animal ecology (Violle et al., 2007; Gagic et al., 2015). In this respect, mycology is lagging behind though fungi are important components of most ecosystems (cf. Crowther et al., 2014). Mushrooms inhabit almost all terrestrial biomes, even at polar regions and deserts. As the example of some Hygrophoraceae shows, mushrooms may have extremely wide ecological amplitudes. Hygrocybe conica, for instance, have been found from low to high latitudes, from tropical rainforests up to arctic biomes (Halbwachs et al., 2013). Still, there are specialists. E.g. Entoloma alpicola exclusively occurs in arctic (alpine) or subarctic (subalpine) habitats, though its morphological traits do not much differ from those of mushrooms found in warmer biomes. Secondary metabolites, particularly antifreeze substances, could be the crucial factor. In addition, the cap is dark brown, a coating which absorbs infrared radiation, potentially leading to increased temperature in the trama. Perhaps the explanation is more tied to behavioural traits, such as low competitive qualities, which prevent this species to gain a foothold in warmer regions with higher fungal diversity. However it may be, it seems that morphological and physiological toolboxes are the basis of mushroom adaptability (cf. Box 3). We see numerous trade-offs as part of the enormous trait repertoire. Most traits come at a cost. Most Hygrocybe species invest in bright colours, moisture absorbing pileipellis and in toxins, but not in individual fruit body size. They, nevertheless, may survive

55

Box 3 Some fruit body traits in Chlorophyllum rachodes

 Large fluffy scales: insulate against heat, bar UV radiation, reduce desiccation, deter fungivores  Long stipe: sporulation into turbulent air  Stipe hollow: stability (large cap!)  Stipe base bulbous: fixation to substrate  Partial veil: protects the hymenium  Annulum: deters soil-borne fungivores  Reddening/browning when bruised: antibiotic precursor is activated  Toxic (haemolysins and agglutinins): deters fungivores (Guthmann et al., 2011)

for more than one week (authors’ observation), as large mushrooms do. Fruit body traits or trait combinations appear in species with distant phylogeny, hence they are not automatically markers of relatedness. The existence of a taxon-specific trait inventory does not necessarily lead to stereotypical patterns. In fact, the considerable plasticity of species in configuring fruit bodies is an adaptive motor mainly fuelled by environ€ es and mental cues and physiological conditions (Ku  lez, 2015), thus eventually leading to epigeNavarro-Gonza netic processes. It is evident that most mushrooms are armoured with a number of physiological and morphological defence mechanisms at the same time. At first glance, this may look like an overkill, but it probably isn’t. The combination of defence traits may act a filter against various predators allowing some taxa to act as vectors (cf. Wicklow, 1988). An analogeuous illustrative case is blackthorn (Prunus spinosa). This bush develops black berries with an astringent taste that abates after first frost, having reached maturity. Birds eat the berries and disperse the seeds. The bush itself is effectively protected against herbivores by extremely spiny branches.

56

H. Halbwachs et al.

Table 7 e Taxa with convergent traits. Hydrogen cyanide production

Spikes, cilia etc.

Arrhenia, Clitocybe, Cortinarius (caperatus), Gymnopus, Grifola, Lentinellus, Lentinus, Lepista, Leucopaxillus, Lyophyllum, Marasmiellus, Marasmius, Melanoleuca, Meripilus, Phaeolepiota, Pleurotus, Polyporus, Pseudoclitocybe, Tricholoma

Agaricus crocopeplus, Amanita echinocephala, Amparoina spinosissima, Cyptotrama asprata, Cystoagaricus trisulphuratus, Cystoderma luteohemisphericum, Echinoderma jacobi, Favolus tenuiculus, Inocybe calamistrata, Lentinus crinitus, Marasmius hudsoni, Oudemansiella canarii, Phaeomarasmius erinaceus, Pholiota flammans, Psathyrella hirta, Ripartites tricholoma, Strobilomyces strobilaceus

Similar or identical defence mechanisms have been developed several times in mushrooms, often even in phylogenetically distant groups, such as hydrogen cyanide production € ttl, 1976) or protective structures like spikes or cilia (Table (Go 7). This underscores the relevance of such traits. Though most fruit body traits make ecological sense, they are not necessarily adaptions in a Darwinian sense. Who knows what came first, when lubricous fruit body coatings were “invented”, selective pressure of predators or changing climate? It is not a rare case that adaptive properties have turned out to be useful for other purposes. The probably most famous example is the insulating plumage of some dinosaurs that in course of further evolution became expedient for the development of avian flight (exaptation: Gould and Vrba, 1982). We said that form follows function, well, mostly. Whether fruit body properties, such as an umbonate cap or an undulate cap margin serve adaptive or ecological purposes is questionable. The same applies to habitually angled stipe bases (e.g. Agaricus abruptibulbus), serrated and eroded gills (e.g. Neolentinus lepideus), smooth hymenium (e.g. Caripia montagnei), heavily reticulated caps (e.g. Rhodotus palmatus), deeply and coarsely reticulate stipes (e.g. Heimioporus betula), and stacked caps in Podoserpula pusio (“Pagoda fungus”), and probably more. Certain characteristics exist because of morphological and physiological constraints (Prothero, 2013: 133e157). This review contains numerous suggestions and ideas about the functional relevance of mushroom response traits. This is a wide, albeit difficult field for further investigation. For one, the possibilities of experimental approaches

are limited, though feeding experiments are feasible. Field surveys on attacks of selected fungivores across species could supply additional data. The second difficulty is the lack in sufficient and reliable trait data (Aguilar-Trigueros et al., 2015). We assume that a wealth of fungal trait data does already exist, albeit widely scattered across mycological institutions and individual mycologists, and accessible only to a limited extent. An existing biological database such as Enzyclopedia of Life (EOL.org) could become the basis for an open access database that includes fungal traits. In any case, to compile comprehensive trait data, considerable funds would have to be mobilised for creating a project, which (1) provides a data structure accepted by the mycological community, (2) motivates the mycological community to share their data, (3) extracts additional data from literature, and (4) creates an online interface for feeding the database, including a quality assurance system. Apart from these somewhat “old-fashioned” approaches, modern genomic and transcriptomic techniques could shed more light on fungal adaptive traits, as it is already realised especially in plant ecology (Shaffer and Purugganan, 2013).

Acknowledgements We thank Andreas Gminder, Peter Karasch and Marc Stadler for valuable inputs.

Appendix.

Table A1 e Functions of the cap and stipe Trait

Function(s)

Umbrella-like shape of cap

   

Bell-shaped cap

    

Hydrophobic coating of cap Scales, velum remainders and tomentose surface of cap

Prevents precipitation from wetting the hymenium Prevents falling debris from contaminating the hymenium Provides shade to hymenium to reduce transpiration Underlies static constraints

Optimises humidity in the hymenium Allows for long and thin stipes (centre of gravity!) Often loosely attached to stipe > “gravitational suspension” Prevents water from soaking the trama Reduces insolation and desiccation of trama, but may also help to evaporate excessive moisture  Insulation against low temperatures  Reduces predator attacks

Sources         

Buller (1909: 24) dto. Authors’ suggestion Halbwachs and € ssler (2014) Ba Buller (1909: 43) Authors’ suggestion Buller (1909: 43) De Groot et al. (1996) Authors’ suggestion

 dto.  dto.

Table A1 (continued) Trait

Function(s)

Involute cap margin

 Reduces predator attacks

Gelatinous pileipellis

 Enables cap to absorb moisture, e.g. dew > prevents desiccation  Reduces desiccation when dried  May repel fungivores  Is an ecologically relevant trait because the synthesis of pigments, even if they are only byproducts, is highly energyconsuming  May absorb preferential wavelengths > phototropism (e.g. carotins)?  May attract or repel fungivores

Cap pigmentation

 May eliminate oxygen radicals  May have antibiotic qualities

Cap size/biomass

Built of fruit body

Trama texture

 Correlates with longevity, also by delaying destructive fungivores and desiccation

 Correlates with desiccation resistance  Dwarfing correlates with latitude, though sporocarps of common species are not smaller in high latitudes  Correlates with dispersal fitness  May correlate with attractiveness for mammalian vectors, also because of a larger surface area to emanate scents more effectively  Small size correlates with fruit body number  Tall fruit bodies may favour dispersal by wind  Sturdy fruit bodies may better survive in wind-prone habitats  Small, cespitose mushrooms may adjust total fruit body biomass to available resources. It also may enhance the ability to grow on tough woody surfaces (weight of cap!).  This type may also be able react to growth dysfunctions  Cespitose fruit bodies may retain humidity  Correlates with longevity

Velum, Cortina

 Tough textures may better withstand environmental hazards and fungivores  Protects the hymenium against biotic and abiotic hazards, especially during maturing, keeps humidity in the hymenium

Annulus Milk, Latex

 Obstacle for predators (see Fig. 3)  May have antibiotic properties

Stipe shape variations

Internal architecture of stipe Stipe texture

Stipe surface Stipe pigmentation

 May play a role in physically protecting lacerations against infection when dried  May deter fungivores  Length correlates with wind dispersal fitness  Thickness correlates with stability  Thickened base > stability, but vertical adjustability in upper part  Curved stipe > result of geotropism (see “Physiological functions”)  Hollow or stipes with pronounced cortication correlate negatively with their diameter > rigidity  Toughness and flexibility correlates negatively with diameter > rigidity  Flexibility may be advantageous in wind-prone habitats  Scales and similar scabrous structures may delay destructive arthropod fungivores  See “Cap pigmentation”

Sources € rfelt and  Do (1989: 61)  Moser (1964)

€ rner Go

 dto.  Buller (1922b: 159f)  cf. Gill and Steglich (1987)  Kendrick (1985: 148)  cf. Guevara and Dirzo (1999)  Griffin (1996: 268)  Weber (1993: 94); Velısek and Cejpek (2011)  Buller (1909: 24, 221); € rfelt and Go € rner Do (1989: 48ff); Leusink (1995); Moore et al. (2008)  Moser (1993)  Kallio (1982) € ssler et al. (2014)  Ba  Authors’ suggestion

 Buller (1909: 41)  Moser (1993)  Authors’ suggestion € rfelt and  Do (2014:70)  Moser (1964) menc¸on  Cle 597f)  Moser (1993)

Ruske

(1997:

 Buller (1922b: 394); € rfelt and Go € rner Do (1989: 61); Hanski (1989)  Authors’ suggestion  Jaeger and Spiteller (2010)  Authors’ suggestion    

Hanski (1989) Self-evident Self-evident Authors’ suggestion

 Buller (1909: 41)  Self-evident  Authors’ suggestion  Authors’ suggestion

58

H. Halbwachs et al.

Table A2 e Image sources Taxon Boletus aereus Cantharellus cibarius Chlorophyllum rachodes Clitocybe nebularis Coprinellus micaceus Cortinarius vanduzerensis Cortinarius violaceus Cyptotrama asprata Dendrocollybia racemosa Favolaschia calocera Hemimycena ignobilis Hypholoma lateritium Lactarius atroviridis Lactarius indigo Lactarius mairei Mycena adscendens Mycena epipterygia Mycena rapiolens Mycena singeri Paxillus involutus Polyporus umbellatus Pseudoclitocybe cyathiformis Russula emetica Strobilomyces strobilaceus Xerocomellus badius Xerocomellus chrysenteron

Author

Permission

Achim Bollmann Andreas Kunze Madjack74 Stu’s Images Stu’s Images John Kirkpatrick Dan Molter JJ Harrison Richard Sullivan Michael H. Lotz-Winter Dan Molter Eva Skific Dan Molter Irene Andersson Boleslaw Kuznik Wolfgang Bachmeier F. Kasparek Alan Rockefeller Quartl Lebrac H. Krisp Eric Smith Patrick Harvey Pdreijnders H. Krisp

Public domain cc license cc license cc license cc license cc license cc license cc license cc license cc license By mail 28.02.16 cc license cc license cc license cc license cc license By mail 14.11.15 By mail 24.02.16 cc license cc license cc license cc license cc license cc license cc license cc license

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