An unusual ice type, called hair ice, grows on the surface of dead wood of
broad-leaf trees at temperatures slightly below 0
Both hair-ice-producing wood samples and those with killed fungus show essentially the same temperature variation, indicating that the heat produced by fungal metabolism is very small, that the freezing rate is not influenced by the fungus activity, and that ice segregation is the common mechanism of ice growth on the wood surface. The fungus plays the role of shaping the ice hairs and preventing them from recrystallisation. Melted hair ice indicates the presence of organic matter. Chemical analyses show a complex mixture of several thousand CHO(N,S) compounds similar to fulvic acids in dissolved organic matter (DOM). The evaluation reveals decomposed lignin as being the main constituent. Further work is needed to clarify its role in hair-ice growth and to identify the recrystallisation inhibitor.
One of the most exciting types of ice takes the shape of fine hairs (diameter
near 0.02 mm, length up to 20 cm). It can be observed in forests, on dead
wood, usually on the ground and sometimes on trees that are still standing (Fig. 1).
This so-called hair ice or ice wool grows on the surface of the unfrozen wood body of
certain moist and rotten branches of broad-leaf trees. The hairs are smooth,
often with a silky shine. They are found in bunches of beautiful structures
such as curls and waves, sometimes with clear parting or zoning, but without
ramification. Although individual hairs are mostly separate, they follow a
macroscopic order, often with surprising regularity. The hair base is rooted
at bark-free positions or where the bark is loose, but never on the bark.
The outer end is either free or in contact with an ice crust or with
surrounding material, such as bark or leaves. Sometimes hairs loop back to
the branch. Bands of parallel hairs can sinter along contacting lines
without losing the original shape until melt onset. In cold, dry air,
however, hair ice sublimates within a short time. Therefore it can be observed
under calm, humid conditions only, at air temperatures slightly below
0
Hair ice on a stem of dead beechwood (26 December 2009, Moosseedorf), hair length up to 10 cm.
Time-lapse videos of hair-ice growth support visual observations, in that the growth is controlled and synchronised over macroscopic parts of the wood. The hair curvature results from lateral gradients in the growth velocity. The primary direction is radial, the hairs being in the prolongation of wood rays (Fig. 2). Indeed, our observations indicate that the hairs are rooted at the mouths of these rays (Wagner and Mätzler, 2009). Furthermore, the hair-ice thickness (Fig. 3) corresponds to the diameter of the cells (Figs. 8 and 9 in Sect. 2) forming the channels in the wood rays (Schweingruber, 1990).
Cross section of a hair-ice-producing beech branch (
The fine hairs can keep their shape over a long time – many hours or even days. This is surprising because recrystallisation of small ice crystals to larger ones is a fast process, especially at temperatures close to melting point. The observed stability is an indication that hair ice is doped with a recrystallisation inhibitor. Examples are antifreeze proteins (AFP), also called ice-binding proteins (IBP); see Griffith and Yaish (2004).
Enlargement of hair ice on beechwood, image width 3.2 mm.
Melting hair ice, showing tiny droplets on hardly visible strings.
Reduction and suppression of hair-ice growth after fungicide treatment; durations from 0 to 120 min are indicated.
When the air temperature exceeds 0
We received many reports on the observation of hair ice, mainly at latitudes
between 45 and 55
Although the literature on hair ice is not abundant, it reaches back about one century. Wegener (1918), the founder of the theory on continental drifts, published the most relevant paper of earlier work. He observed hair ice in winter 1916/1917 in the Vosges Mountains, and in February 1918 in northern Germany at Rheinsberg in der Mark. He was able to grow hair ice again on the branches that he found. Wegener assumed a relationship between the formation of hair ice and the mycelium visible on the branch surface. His consultant, Arthur Meyer, confirmed that these branches contained fungus mycelia. He assumed a type of Ascomycota; however, he was unable to determine the species. Mühleisen and Lämmle (1975) described the reproduction of hair ice on rotten wood of broad-leaf trees in a climate chamber. They assumed that some type of osmotic pressure is acting. Lenggenhager (1986) observed hair ice in areas near Bern, Switzerland from 1979 to 1985. Being aware of these observations, Wagner (2005) supposed the involvement of a fungus activity without the knowledge of Wegener's work. Wagner found that the presence of fungus mycelia in the wood body of hair-ice-producing branches is manifested in the microscopic and macroscopic view. Fruiting bodies of fungi were observed as shown by Wagner and Mätzler (2009). They developed a method to repeatedly grow hair ice on a covered balcony during nights with freezing conditions. Their more specific hypothesis, that the metabolism of these fungi is a prerequisite for the formation of hair ice, was supported by their tests. A further hypothesis was the assumption that gas pressure, caused by fungal metabolism, ejects water through wood rays to the wood surface. Furthermore, they concluded that hair ice is formed from water stored in the wood. Dash et al. (2006) considered hair ice as a frost-heave phenomenon associated with ice segregation. In the present work we recognised signatures of this effect during hair-ice growth.
Hair ice grows on porous substrates containing liquid water. We call this ice type a “basicryogen”, in order to distinguish it from ice that grows from atmospheric water. Different basicryogens grow on different substrates and with different ingredients. The co-existence of liquid water, ice, and the porous substrate at the ice front are common to all basicryogens. This general phenomenon is called ice segregation. The thermodynamic phenomenon of frost heave (Vignes and Dijkema, 1974; Dash, 1989; Ozawa, 1997; Dash et al., 2006) is a common driver for these ice types.
Hair ice grows on the wood surface while a connected network of water
inside the wood remains in the liquid state. Due to molecular interactions
at the large specific interface area between wood cells and the water,
the melting point inside the wood is reduced to below 0
How can we understand this process? The large dipole moment of the water
molecule causes charges on the surface of liquid water and ice. Energy is
needed to set up the associated electric field. Surface energy can be
reduced if a liquid-water film remains between the wood and the ice surface
due to the flexibility of the liquid to neutralise the local charges. Under
freezing conditions, suction forces are set up, caused by the interface
energy of the wood–water–ice sandwich, to attract liquid water from the
pores of the wood toward the freezing front. In this way the liquid-water
film is maintained. Frost-heave processes in fine-grained soil also act in
this way (Ozawa, 1997; Dash et al., 1995, 2006). Although the theory of ice
segregation is still incomplete (Dash et al., 2006), empirical insight in the
behaviour was found by experimental studies. Ozawa and Kinosita (1989)
investigated ice growing on the surface of a microporous filter. The thin
liquid film, separating the ice from the filter material, was confirmed. The
authors observed that the growth rate of ice increases proportionally with
the depression
Advancing the understanding of the hair-ice phenomenon was the objective of this work. In Sect. 2, we will confirm that a winter-active fungus is needed for hair-ice formation. We will identify the acting fungus. In the physical analysis of Sect. 3 we will study the temperature variation of wood during ice formation. Wood samples with and without the acting fungus will be studied. The results point us to the search for a recrystallisation inhibitor produced by the fungus and thus also to the chemical analysis, detailed in Sect. 4. Final discussions and conclusions will be given in Sect. 5.
In winter 2010/2011 Gerhart Wagner refined the hair-ice experiments of
Wagner and Mätzler (2009). A hair-ice-active branch was cut into five
pieces (length 35 cm, diameter 2 cm) and exposed to a commercial fungicide
(a Miocolor “Schimmelentferner”, sodium hypochlorite, conc. 4.4 %): piece
no. 0 remained untreated, no. 1 was exposed for 15 min, no. 2 for 30 min, no. 3
for 60 min, and no. 4 for 120 min. On the first evening (18 December 2010), the
air temperature was close to
The following morning all pieces melted at room temperature before they were
exposed to the cold again. The air temperature rose from
A hair-ice branch of about 20 cm in length and 2 cm in diameter was cut into
four similar pieces on 03 January 2011. Three of them were exposed to hot (90 to
95
Treating the branches with alcohol (70 %) or with the weak fungicide,
Imaverol – an imidazole, also called Enilconazole
(C
Heat treatment showed the most radical hindrance to hair-ice growth. 1 min in hot water was sufficient for a complete suppression. For
fungicides, the type and duration of the treatment played a role. Whereas our weak
fungicide did not have any effect, complete suppression was achieved with
the stronger fungicide after treatment lasting 2 h. The results are plausible in
view of the fungus hypothesis. At a temperature of at least 90
From January to March 2012, from December 2012 to April 2013, and from November 2013 to March 2014, a total of 78 hair-ice-bearing twigs and branches were collected in the forests near Brachbach/Sieg in Germany (northern slope of “Windhahn”). Some of them were kept on a moss-covered shadowy area or temporarily on a wet towel in a closed plastic box in the garden of one of the authors (G. Preuss) to simulate forest-floor conditions. Additionally, 41 hair-ice-bearing trees, boles, and branches were observed in their natural location in the forest. Most of the species, or at least the genus of the dead branches, were identified by species-specific characteristics visible in the microscopic wood anatomy (Schoch et al., 2004, and Richter and Dallwitz, 2000). Fungi growing on the examined branches and logs were identified if necessary by microscopic characteristics with the help of Gminder (2008), Haller and Probst (1983), Jülich (1984), Krieglsteiner (2000), Laux (2010), Moser (1963), and Rothmaler (1994). Samples of the fruiting bodies were prepared as squash mounts and sometimes coloured by Phloxine B to stain the basidia. Hand-cut sections of hair-ice-bearing wood samples were prepared as wet mounts and afterwards coloured by the dye “Cotton Blue”, following the instructions of Bavendamm (1936) according to the description of Riggenbach (1959). This is an approved method to make fungal hyphae visible within wood cells.
The type of examined hair-ice wood varied from fallen twigs, attached and fallen branches, to dead standing trees and fallen or felled boles, except for one case: a hazel tree, which was still living, bore hair ice several times on a dead part of the wood.
In the majority of cases the consistency of the dead wood was “rather hard” – indicating an initial stage of decay – but four samples had a “distinctly softened” texture, adopting the terms of Heilmann-Clausen and Christensen (2003). The integrity of the bark differed from almost intact to completely lost. If it still existed at all, the bark peeled off from the hair-ice-producing wood surface and often got lost during the observation period.
Hair ice was observed on ten different broad-leaf tree species belonging to five different plant families (Table 1).
Hair-ice-bearing wood species, range of diameters and identified
fungal species D is
Eleven different fungal fruiting bodies were identified on the wood samples
– in some cases up to three species on the same piece of wood. The list is
certainly not complete. One of these fungi,
Three wood samples, first with hair ice, later with the fruiting body of
Microscopic views of a hair-ice wood sample (
Microscopic characteristics of the Ee fruiting body (scale bar:
10
Microscopic view of hair-ice wood showing fungal hyphae coloured by
“Cotton Blue” within the wood tissue. The varying thickness of the fungus
hyphae was caused by the colouring procedure (scale bar: 10
Under humid conditions (in nature or in a closed plastic box containing a
wet towel) and at temperatures above freezing, small water droplets
often appeared on the surface of the Ee fruiting body overnight (Fig. 6f).
This might be a case of guttation, which is the active exudation of
an aqueous solution. The phenomenon is well-known related to different vascular
plants, but also related to some fungi (Knoll, 1912; Thielke, 1983). The observation
of Sprecher (1959), who describes a reinforcing effect at temperatures near
Cross sections of the fruiting body were 30 to 100
Beneath the fruiting body, the superficial wood cells are almost filled by hyphae (Fig. 7a, b). The fungus seems to grow along the wood vessels (Fig. 9a) and intrude into the deeper wood tissue along the wood rays (Figs. 7c and 9b).
Some hair-ice wood samples found in November were examined by microscope, too. At that time of the year, there was no macroscopic sign of a fungal fruiting body on the wood surface. But when microscopic mounts were coloured by the dye “Cotton Blue”, they showed, that the wood tissue was pervaded by fungal hyphae running along the wood vessels and rays (Fig. 9b). Except for the density of the hyphae, the findings looked exactly like those from the wood samples with an Ee fruiting body.
As our main result, we unravelled the mystery about the whitish covering described by Wegener (1918) and Wagner (2005) by the identification of Ee. The opinion of Wegener's consultant, A. Meyer, who did not expect the appearance of a fruiting body and thought that the determination of the species would be impossible, has been disproved. Furthermore, the result specifies the fungus hypothesis of Wagner and Mätzler (2009).
Insight in the physics of hair ice is found from thermal signatures of hair-ice wood, i.e. the temperature enhancements caused by heat sources associated with the ongoing processes. These include (1) heat generated by fungal metabolism, (2) latent heat of fusion when water freezes in contact with the wood, and (3) heat used or generated by recrystallisation.
Heat generated by these processes diffuses into its environment by
radiation, heat conduction, air turbulence, evaporation, and sublimation and
therefore exact measurements are difficult to achieve. However, by careful
design of the experiments, the main heat loss can be reduced to black-body
radiation. For heat sources that change rapidly with time, the temperature
changes are damped according to the heat capacity of the wood. On the other
hand, under stationary conditions the heat power
For the combustion of nutrients by fungal metabolism, we assume a heat of
combustion Qb
Now, assuming the same branch geometry, latent heat is generated by
freezing 1 g of water per hour. The generated heating power follows from the
latent heat of fusion of ice,
Branches of beechwood with hair ice were collected in a forest in
Moosseedorf, Switzerland. The samples were thoroughly wetted in rainwater.
Then they were arranged on a plastic socket put on wet snow to stabilise
temperature and to keep the humidity at saturation to avoid evaporation and
sublimation. The entire stack was put in a plastic tub that was covered and
further insulated with a towel to reduce vapour fluxes and heat conduction
inside the tub. The tub was put in a garden hut from mid January to early
March 2011, and again in January 2012. Hair ice formed on wood samples
during cool nights. From time to time wetting was repeated. With this setup
we realised conditions for precise temperature measurements and we therefore
approached the assumption that the net heat flux can be represented by Eq. (1). For
temperature measurements we used Pt-100 sensors (length 10 mm, diameter 2.6 mm).
After calibration with an ice–water mixture at 0.00
Situation in the morning of 15 January 2012: heat-treated piece (1, bottom right), piece (2, top) with abundant hair ice, air temperature sensor (3, bottom left) with red insulation.
First measurements were taken in January 2011. During the first night, 18–19 January,
the temperature stayed above 0
First hair-ice growth was monitored from 19 to 20 January 2011 with temperature
variations shown in Fig. 11. Before midnight all temperatures decreased
linearly with time, including the passive tracer. At midnight, sudden
increases occurred for all hair-ice branches, indicating ice nucleation and
the start of latent-heat release by hair-ice growth. The start is almost
simultaneous in all branches, with slightly different nucleation temperature
(
Temperature variation during the first experiment: beechwood samples (1, 3, 4, 5, 6, and 7) with growing hair ice, and dry hazel wood (8) as a passive tracer of ambient temperature.
In the second year we tried to find out if the fungus activity is a
prerequisite of the observed temperature jumps, in other words, if the jumps
are signatures for hair-ice formation. We selected a beechwood sample with
abundant hair-ice growth. After wetting it and cutting it in half, both pieces
still showed abundant hair-ice growth during the night from 13 to 14 January
2012, with jumps similar to Fig. 11. Then one piece (1) was held in hot water
for 5 min to kill the fungus. Both pieces were exposed to the cold again
during the following night. As shown in Fig. 10, the untreated sample (2)
produced dense hair ice again, but no hair ice was found on the heat-treated
sample (1); instead, a thin ice crust covered this wood. The temperature
variations are presented in Fig. 12. All sensors started slightly above
0
Temperature variation during the second experiment: heat-treated piece (1), untreated piece (2) with hair ice, air temperature close to wood samples (3), and further away (4).
Before the onset of freezing, the temperature of hair-ice branches cannot be
distinguished from the environmental temperature. The small difference
(0.01
Before freezing begins, the wood temperatures, shown in Fig. 11 and 12, decrease to
supercooled conditions below 0
During the phase of ice growth, the wood temperature (
The temperature difference between the pieces with and without hair-ice
production is small, indicating that the freezing rates are similar. The
result means that the fungus activity hardly plays a role for the rate of
ice formation. This finding may appear as a surprise when looking at the
difference between the branches (1, 2) of Fig. 10. But, note that hair ice
is extremely fine, its density being extremely small. On the other hand the
ice crust on the heat-treated piece (1) mainly consists of bulk ice. To show
that its mass is indeed similar to the hair-ice mass, we compare two
situations with the same ice volume, one consisting of
To get an estimate of
With regard to Fig. 12, minor differences between Curves (1) and (2) can be noted. Firstly, after freeze onset, Curve (1) shows small oscillations, possibly due to recrystallisation. On the other hand, the temperature variation of Curve (2) is very smooth. Secondly, towards the end, when the strongest cooling occurs, the temperature decrease is slower for Curve (2) with hair ice than in Curve (1) due to thermal insulation by the ice wool.
The similarity of the temperature and thus of the rate of ice growth means that ice segregation is the common mechanism for ice production on the wood surface. The role of the fungus is in shaping the ice as hairs and to prevent it from recrystallisation. This is the main result from the physics of hair ice. Furthermore it indicates that temperature and pressure enhancements associated with fungal metabolism in hair-ice wood (Wagner and Mätzler, 2009) do not appear to be noticeable.
First investigations of non-filtrated and filtrated meltwater samples from
hair ice, by means of a total organic carbon analyser (TOC-VCPH, Shimadzu,
Japan), show similar and significant amounts of organic carbon (> 200 mg L
For the elucidation of the unknown components we applied mass spectrometry (MS) aiming at a complete spectrum of organics with regard to molecular size and polarity. Representative screening was achieved by various ionisation techniques in combination with appropriate separation techniques. First, we performed gas chromatography, coupled with electron-impact mass spectrometry (GC–EIMS) of filtrated aqueous solutions according to Turska et al. (1997), followed by the more sensitive headspace-GC–EIMS (Seto, 1994, Snow and Slack, 2002). For small carboxylic acids (known as e.g., plant exudates) and peptides/proteins (possible degradation products and/or anti-freeze proteins), we used capillary electrophoresis and electrospray Fourier-transform ion cyclotron resonance mass spectrometry (ESI-FTICR-MS, Marshall et al., 1998). None of these methods yielded any significant peak.
In the second step, we applied our most sensitive mass spectrometer equipped with an electrospray source coupled to ultra performance liquid chromatography (UPLC-ESI-MS, Swartz, 2005; Guillarme et al., 2010), resulting in first (non-resolved) chromatograms. The electrospray full-scan spectra in positive and negative ionization mode and different retention times are highly complex – ranging over the whole mass range, but similar among themselves. Such spectra – Gaussian in shape with emerging odd-numbered peaks – look similar to fulvic/humic acids in dissolved organic matter (DOM) of terrestrial/marine water, soil/sediments, peat bog, kerogen, and eventually crude oil (Kujawinski, 2002; Sleighter and Hatcher, 2007; Hertkorn et al., 2008).
Therefore, in the third step, we simultaneously desalted and concentrated
hair-ice samples by solid-phase extraction (SPE). The methanolic eluates,
mixed with 20 % water for better ionisation yield, were introduced again
by flow injection in the ultrahigh-resolving ESI-FTICR-MS. In contrast to
our former investigation, we arranged the measuring conditions towards
complex samples (averaging seven spectra of 50 transients each) to improve
the statistics. The high-resolution spectrum in the mass range 200–1000 Da
[1 Dalton (Da)
Detail of a high-resolution mass spectrum of melted hair ice.
Van Krevelen plot of the CHO compounds of hair ice (for peak intensities > 600 counts), with ellipses indicating typical ranges of selected biopolymer components, adapted from Sleighter and Hatcher (2007).
In Fig. 13, ions with the mass space of 0.0364 Da (blue arrows) were derived
from the mass difference between CH
We developed a post-processing to formula assignment of all compounds based
on Scilab routines. The resulting mass lists are transformed to Excel tables
for sorting and/or preparation of graphical figures describing the
characteristics of DOM. The van Krevelen diagram – H
Mass spectrometry has shown that hair-ice water contains fragments of lignin and tannin. Lignin is a main component (20 to 30 % of dry mass) of wood, stabilising the cells against compression. In contrast to cellulose, it is more difficult to decompose. Lignin is indigestible by animal enzymes; only some fungi (causing white rot) and bacteria are able to secrete lignase and thus biodegrade the polymer. Lignin is an irregular biopolymer with molecular mass in excess of 10 000 Da, consisting of various types of substructure, that are repeated in a haphazard manner. Tannins are similarly irregular, with molecular weights between 500 and 3000 Da and up to 20 000 Da (proanthocyanidins). Lignin and tannin consist of hydrophobic skeletal structures with numerous polar functional groups. The hydrophobic lignin/tannin macromolecules may act as crystallisation nuclei.
The lignin and tannin classification was obtained by atomic ratios, shown in Fig. 14. By the application of electrospray, the most gentle mass spectrometric ionisation technique, covalent bonds stay intact whereas the weaker ones (van der Waals bonds and electrostatic bonds) are destroyed. Consequently, molecules in the mass range between 200 and 800 Da result, in general, as fulvic acids do. This means that we are unable to distinguish between the original lignin/tannin macromolecules and their (partial) degradation products.
We also detected sulphur- and nitrogen-containing compounds, but with very small intensities in contrast to the CHO peaks and in accordance with our TOC and TN measurements. We assume that we detected marginal leftovers from the total degradation of more easily degradable (and nutritious) wood compounds, like proteins, which had already begun the process of mineralisation. This would explain the significant ammonium concentration in melted hair ice.
Our investigations shed light on the mystery of hair ice that can grow on certain branches of dead wood. The formation is related to a winter-active fungus. Comparatively dense mycelium was observed in the superficial wood cells of hair-ice-bearing sections of the investigated branches. If the fungus activity is stopped, either by a fungicide or by hot water, the production of hair ice ceases as well.
Hair-ice shape and direction are influenced by the geometry at the mouth of the wood rays where the hairs are formed when the water is freezing. The extreme ratio of hair diameter to hair length with an order of 1 : 10 000 is most surprising. In spite of the fact that surface tension tries to reduce this ratio, the shape is maintained over many hours, and sometimes several days at temperatures close to melting point. A recrystallisation inhibitor must be responsible for stabilising the hairs. It may be contained in the thread-forming fibre that appears when hair ice starts to melt, and it could be related to lignin, the main organic component that we found.
With respect to the origin of water, hair ice is a basicryogen, meaning that the ice originates from water in a porous substrate, in our case, the wood. Inside the substrate, melting point is lowered by intermolecular forces in the interface between ice and the substrate, called premelting. When the external temperature is sufficiently low, water freezes on suitable nuclei on the substrate surface and transfers latent heat of fusion to the substrate. Once ice nuclei have formed, ice segregation starts to extract additional water from the substrate, leading to the growth of ice and to the dehydration of the substrate. We found that this effect occurs under the same conditions with similar freezing rates in wood with and without hair-ice production.
The fungus provides decomposed lignin and tannin as organic materials. The notion that they may act as recrystallisation inhibitors is indicated by properties of lignosulfonate (waste of cellulose production) found in Sandermann and Dehn (1951), namely that it delays the hardening of cement.
The fungus activity plays a minor role with regard to the rate and amount of ice formation. Hair-ice branches with active and with killed fungus undergo similar temperature curves, indicating that the freezing rates are very similar and that fungal metabolism is too weak to cause a measurable temperature enhancement. The difference must be in shaping the ice. Whereas the untreated branches produce hair ice, the heat-treated ones produce crusty ice sticking to the wood surface. Although the fungus effect is still a mystery, it must be directly related to the hair-ice shape because the suppression of hair-ice growth acts immediately after the fungus activity is stopped.
Our findings not only confirm Wegener's hypothesis that fungal activity
plays an important role, but they unravel the mystery about the whitish
covering on hair-ice-producing wood, described by Wegener (1918)
and Wagner (2005). There is clear evidence to suggest a causal relationship
between the fungus,
For several years, C. Mätzer has been working (in collaboration with Gerhart Wagner) on hair ice, its observation in nature, reproduction, and the test of a fungus hypothesis. In the presented paper he is mainly responsible for the physical measurements and interpretations, described in Sect. 3. G. Preuss investigated the fungi and the wood samples by microscopic techniques, described in Sect. 2.2, leading to the identification of Ee. D. Hofmann performed and interpreted the chemical analyses presented in Sect. 4. The paper is a strong collaboration of scientists from different fields with one object of collective discussion.
We thank Gerhart Wagner for contributing Sect. 2.1 including Fig. 5. We regret his wish not to act as a co-author. We thank the Institute of Applied Physics, University of Bern for support with the temperature measurements. Niklaus Kämpfer and Andreas Hasler first indicated possible relationships between hair ice and ice-segregation processes to us. Bernhard Steffen, JSC, Forschungszentrum Jülich, developed the Scilab-based evaluation program.
The article processing charges for this open-access publication were covered by a Research Centre of the Helmholtz Association. Edited by: J. Kesselmeier