Hans Halbwachs
Publications: Google Scholar
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.
Key publications
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:
Key publication
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.
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► 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
Key publication
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.
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► 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.
Key publications
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.
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► 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.
Key publication
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
A Cuphophyllus
pratensis
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.
Key publications
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.
Key publications
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.
Further reading
Dietl G.P., Flessa K.W., editors. 2017. Conservation Paleobiology - Science and Practice. Chicago and London: The University of Chicago Press.