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Functional traits are widely recognized as a useful concept for elucidating ecological roles and systems. While, e.g., botanists have developed this field during the past few decades, mycology still needs to catch up. Only during recent years, ecological research has begun appreciating the fundamental role of fungi in virtually all ecosystems, especially regarding nutrient cycling, and thus taking part in maintaining biodiversity and resource availability.
Fungi use a wide array of resources in extremely differing habitats and need to respond accordingly in many ways, be they of morphological, physiological, or behavioral nature. To a good part, this is reflected by the amazing diversity of fungal shapes, sizes, colors, etc., which was already recognized centuries ago, as the lithograph of A.Cornillon (ca 1827) shows.
What are functional traits? Traits are the tools for survival, reproduction, and dispersal. In plants, e.g., the color of a flower attracts pollinators, winged seeds are carried by wind over long distances, and poisonous leaves deter herbivores. Analogous morphological and physiological characteristics are observed in fungi. Think of fruit body pigmentation, spore size, and poisonous taxa. Fungi show a plethora of traits. Their ecological functions are often obscure. For example, why do most species of the bolete family rely on poroid (sponge-like structure) and not more efficient, lamellate hymenophores (spore-producing tissue), or why are many fruit bodies shaped like a bell? Fungal traits apply to all compartments, the mycelium, the fruit body, and the spores. In mushrooms, a wide spectrum of characteristics can be observed (after Buller 1909):
Understanding those traits and trait combinations helps appreciate the complex interactions among fungi and with other organisms, above all plants and animals. Only then, can conservation efforts be made, particularly in view of man-made changes in our natural environment.
Halbwachs H., Bässler C. 2021. Functional Traits of Stipitate Basidiomycetes. Reference Module in Life Sciences. Elsevier.
Halbwachs H., Bässler C. 2020. No bull: Dung-dwelling mushrooms show reproductive trait syndromes different from their non-coprophilous allies. Mycological Progress 19: 817-824.
Dawson S.K., Boddy L., Halbwachs H., Bässler C., Andrew C., Crowther T.W., Heilmann‐Clausen J., Nordén J., Ovaskainen O., Jönsson M. 2018. Handbook for the measurement of macrofungal functional traits; a start with basidiomycete wood fungi. Functional Ecology 33(3): 372-387.
Halbwachs H., Simmel J., Bässler C. 2016. Tales and mysteries of fungal fruiting: How morphological and physiological traits affect a pileate lifestyle. Fungal Biology Reviews 30(2): 36-61.
Halbwachs H., C. Bässler. 2015. Gone with the wind – a review on basidiospores of lamellate agarics. Mycosphere 6: 78-112.
► Fruit body size of mushrooms: we found that ectomycorrhizal (mutualistic) species tend to have on average larger fruit bodies, probably because they receive sufficient carbon as photosynthate (sugars) in a reliable way. Conversely, saprotrophic mushrooms need to invest in costly enzymes to extract carbon from recalcitrant sources such as wood, litter, or humus.
Standardized effect size (estimate divided by standard error) of the difference between mutualistic and saprotrophic fungi for fruit body size. A negative effect size indicates that fruit body size in saprotrophs is smaller than in mutualists. Values <1.96 and >1.96 indicate signiﬁcant effect sizes. The 1.96 level of signiﬁcance is indicated by the dashed line. The vertical solid line indicates the standardized effects size from the generalized least-square models.
Large fruit bodies are associated with considerable reproductive and dispersal advantages over smaller mushrooms:
Bässler C., Heilmann-Clausen J., Karasch P., Brandl R., Halbwachs H. 2015. Ectomycorrhizal fungi have larger fruit bodies than saprotrophic fungi. Fungal Ecology 17: 205–212.
► Spore size of mushrooms: Guild differences we also found with basidiospores of mushrooms. Ectomycorrhizal spores tend to be more ornamented than the saprobic guild, possibly an adaptation for arthropod vector dispersal. The latter show more often thick and melanized walls as protection against stressful environments.
A - Warty Cortinarius spores, image Linus Kudzma; B - Spiked Inocybe peckii spores, image courtesy Ditte Bandini; C - Thick-walled and pigmented Agaricus spores, image Byrain; D - Thick-walled and melanized Coprinus spores, image TimmiT; image licences A, C, D: CC BY-SA 3.0
Halbwachs H., Brandl R., Bässler C. 2015. Spore wall traits of ectomycorrhizal and saprotrophic agarics may mirror their distinct lifestyles. Fungal ecology 17: 197–204.
► Resource availability and mushroom morphology: Resource availability affects mushroom characteristics, too. We found that reproductive morphological traits of mushroom assemblages, i.e. fruit body size and spore characteristics respond to resource availability along an altitude gradient in the Bavarian Forest. The slope of the Bohemian massif served as gradient for climate and resource availability:
The suggestion that mushroom sizes should
decrease with less resources (proxy: vegetation coverage) is plausible. The
change of spore shape with resource depletion is less intuitive. We assume that
elongate spores are better suited in patchy environments because they are
carried further than globose ones.
Bässler C., Brandl R., Müller J., Krah F.S., Reinelt A., Halbwachs H. 2021. Fruit body size of mushroom assemblages: environmental drivers on a global scale. Ecology Letters 24(4): 658-667.
Bässler C., Halbwachs H., Karasch P., Holzer H., Gminder A., Krieglsteiner L., Gonzalez R.S., Müller J., Brandl R. 2016. Mean reproductive traits of fungal assemblages are correlated with resource availability. Ecology and Evolution 6(2): 582-592.
Halbwachs H., Heilmann-Clausen J., Bässler C. 2017. Mean spore size and shape in ectomycorrhizal and saprotrophic assemblages show strong responses under resource constraints. Fungal Ecology 26: 59-64.
► Mushrooms and environmental stress: Fungi have conquered almost every nook and cranny of planet Earth, thus contributing to ecosystem processes. Tropical and arctic biomes are extremely contrasting biomes, particularly in terms of temperature. Still mushrooms cope with such conditions, using a "toolbox" containing physiological and morphological instruments:
Mushrooms employ, by and large, similar physiological and morphological toolkits. They make them ﬁt for extreme environmental conditions by expressing traits according to biome characteristics. This way, fungal assemblages are formed and both pheno- and genotypic plasticity is capitalized.
Halbwachs H., Simmel J. 2018. Some like it hot, some not – Tropical and arctic mushrooms. Fungal Biology Reviews 32(3): 143-155.
Waxcap fungi are conspicuous mushrooms colonizing undisturbed and oligotrophic habitats. For this reason, these fungi are used as indicators of near to nature grassland.
Examples of waxcap fungi
B Hygrocybe calyptriformis, image Len Worthington
C Hygrocybe astatogala, image Michael Wallace
D Hygrocybe cantharellus, image Dan Molter
E Gliophorus psittacinus, image Dan Molter
F Hygrocybe punicea
Licences B-E CC BY-SA 3.0
Follow-up research found DNA of Hygrocybe coccinea in roots of the ribwort plantain and hyphae of several waxcaps in rootlets of associated plants. All these findings point to waxcap fungi receiving photosynthate (sugars) from their hosts. Unclear remained why the 15N signatures were extraordinarily high as if waxcaps received their nitrogen from sources high in the food chain.
It still remains unclear whether the fungus swaps nitrogen for plant carbon (photosynthate). For improving our understanding, Cuphophyllus virgineus is being sequenced to identify genes involved in relevant enzyme production, such as proteases (M. Thines Lab, Frankfurt). Another project is planned to explore the enzyme profiles expressed by waxcaps.
Halbwachs H., Easton G.L., Bol R., Hobbie E.A., Garnett M.H., Peršoh D., Dixon L., Ostle N., Karasch P., Griffith G.W. 2018. Isotopic evidence of biotrophy and unusual nitrogen nutrition in soil-dwelling Hygrophoraceae. Environmental Microbiology 20(10): 3573-3588.
Halbwachs H., Dentinger B.T.M., Detheridge A.P., Karasch P., Griffith G.W. 2013. Hyphae of waxcap fungi colonise plant roots. Fungal Ecology 6(6): 487-492.
Tello S.A., Silva-Flores P., Agerer R., Halbwachs H., Beck A., Peršoh D. 2013. Hygrocybe virginea is a systemic endophyte of Plantago lanceolata. Mycological Progress 13(3): 471-475.
Surprisingly, fungal functional traits and paleoemycology show meaningful relations regarding present ecological questions. Paleoecology provides insight into past ecosystems and, thus, delivers clues on how biodiversity and ecosystems were affected by climate shifts. Fossilized fungal remains may, therefore, serve as ecological indicators. If, for example, a fossilized secotoid mushroom (puffball with stipe) would be found, it would be probable that this fungus occurred in a relatively dry, semidesert climate. Due to the ephemeral character of most fungi, fossils of fruit bodies are extremely rare. The best-preserved fungal fossils are found in amber, like the mushroom similar to the extant genus Marasmius (image to the right); Myanmar, Middle Cretaceous (ca. 100 Ma) (after Cai et al. 2017, licence CC BY 4.0; bar 1 mm).
Amberized fossils are often difficult to detect. Elaborate methods, such as embedding in resin for producing sections, followed by electron, confocal as well as differential interference contrast microscopy or phase contrast X-ray synchrotron imaging, are often needed. As an alternative approach, I developed a method that isolates microfossils, such as spores with organic solvents. This method revealed in the meantime hundreds of microfossils (palynomorphs), mainly including fungal spores and plant pollen:
Examples of fungal microfossils and pollen; A Melanized hyphae, B-F Ascospores, G Ascospore aff. Cladosporium, H Ascospore aff. Altenaria, I Melanized basidiospores aff. Psathyrellaceae?, J Pollen aff. Betulaceae
Cladosporium and Altenaria are mold fungi, thriving on moist, decaying plant matter as it occurs in humid, temperate biomes. Betulaceae are index plants for warm-temperate to boreal settings.
Halbwachs H., Grímsson F., Potapova M., Dolezych M., LePage B. 2022. Microfossils in resin from the middle Eocene Buchanan Lake Formation, Napartulik, Axel Heiberg Island, Nunavut, Canada. Palynology: 1-13, DOI 10.1080/01916122.01912022.02127956.
Halbwachs H., Harper C.J., Krings M. 2021. Fossil Ascomycota and Basidiomycota, With Notes on Fossil Lichens and Nematophytes. Reference Module in Life Sciences. Elsevier.
Halbwachs H., Bässler C., Worobiec E. 2020. Palynomorphs in Baltic, Bitterfeld and Ukrainian ambers: a comparison. Palynology DOI 0.1080/01916122.2020.1863274 online
Halbwachs H. 2019. Detecting fungal spores and other palynomorphs in amber and copal by solvent treatment. Palynology 44(3): 521-528.
Halbwachs H. 2019. Fungi trapped in amber – a fossil legacy frozen in time. Mycological Progress 18(7): 879-893.
Dietl G.P., Flessa K.W., editors. 2017. Conservation Paleobiology - Science and Practice. Chicago and London: The University of Chicago Press.