Geouitrobiology htunøl, Volume 13, pp I l7-127

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Discovery of Ca Oxalate Crystals Associated withFungi in Moss Tfavertines (Bryoherms, Freshwater

Heterogeneous Stromatolites)

PIERRE FREYTET

University of ParisParis, France

ERIC VERRECCHIA

URA 157 CNRSUniversity of BourgogneDijon, France

Buffered tlecalcification of live moss and liverwort (Hepaticae) travertines resul¡ed inthe release of a large number of organisms (bacteria, cyanobacteria, fungi, eukaryotical.gae, and sm¿ll animals), which constitute an "organic mat" (also called an algalmat or biofilm), This mat is calcified and commanly has laminations, allowing mnsstravertines to be considered as stromatolitic structures. After decalcification of 300samples of lravertines (using dilute acetic ucid), only 9 released Ca oxalate crystals inthe form of needle bundles, spherulites, and tetragonal bipyramidal prisms. These

crystall.ine forms are identical 1o those found in some phanerophytes and soils.Mycelian flaments also exist in lravertines mostly composed of algae, and it is possi-ble that Ca omlate crystals can be formed. However, being metastable, these crystalstransformvery quickly into calcite by diagenesis, in the same way as aragonite in tlrcst ronuto Iile s of sah *^ater etnironments.

Keywords aquatic fungi, biomineralization, Ca oxalate, freshwater stromatolites,moss tufa

In freshwater environments, numerous organisms are susceptible to encrustation by calciumca¡bonates. Altbough this process has been documented in Pia's (1934) compilation of older re-

search a¡ld in numerous more recent publications (Golubic, 1976; Pentecost & Riding, 1986;

Riding, 1991), nowhere has reference been made to the occurrence of Ca oxalate in travertines.

The mechanism of carbonate precipitation, whether it be purely physicochemical, re-

lated to photosynthesis, or associated with both these processes in variable proportions, is

not discussed here in detail. Numerous organisms are coated with crystals or epiphytic or-ganisms, which a¡e themselves encrusted. The difficulty in estimating which of the crys-

Received 19 December 1994; accepted 24 April 1995.We wish to thank Dr. P. Blanc (Université Pierre et Marie Curie, Paris) for his help in operat-

ing the scanning electron microscope and microprobe, K. Verrecchia for translating the text fromFrench, and the two anonymous reviewers for their constructive comments. This work was fundedin part by European Economic Comnrunity grant ERB400lGT93l740 (E.Verrecchia).

Address correspondence to Dr. Eric Verrecchia, URA 157 CNRS, Centre des Sciences de laTerre, Université de Bourgogne, 6 Bd. Gabriel, 21000 Dijon, France.

117

II8 P. Frq,tet and E. Verrecchia

tals are related to which organism has already been discussed by Davis (1901, p. 495) inrelation to Characeae covered with Rivularia and Schizotåru.r in marls.

Microorganisms cover all types of subst¡ates, both mineral and organic. They constitutethe "algal mat," recognized for the hrst time by Müller (17'77; in Gerdes & Krumbein, 1987)

in an intefidal zone of the North Sea, and also described in calcareous travertines (Cohn,

1862; Meunier, 1898), and in fluviatile and lacustrine oncolites (Munay, 1895). The algal

mat in its noncalcif,red form has been described in the lacustrine environment by Forel (1901,

p.234), under the name "organic felt," a concept that has been employed by numerous other

authors (e.g., Symoens, 1957; Duvignaud, 1970; Burne & Moore, 198'l;Pedley,1992).Mosses commonly act as supports for the agal mat, resulting in the "moss travertines"

described by Unger (1861; in Pia,1934), Cohn (1864), Emig (1917), Van Oye (7937,p.243 and 246), Symoens (1957), Grüninger (1965, in Golubic, 1973), Freytet and Plet(1991), and Geurts etal. (1992). These are the "phytoherms" of Cipriani etaJ. (1977),aterm also employed by Pedley (1990,1992), synonymous with "bryoherms."

Early diagenesis of these calcihed mats results in numerous recrystallizations, leadingseveral authors to minimize or negate the role of organisms in favor of purely physicochem-ical crystallizations in moss travertines (Irion & Müller, 1968; Emeis et al., 1987), as wellas in other types of freshwater stromatolites (Braithwute, 1979; Risacher & Eugster, 1979).

In accordance with other authors (e.g., Golubic, 1976), moss travertines ale consid-ered here to be stromatolitic structures, because they have laminations and they are the

result of microorganism activity. In this case, the initial form of the structure takes that ofthe living substrate, resulting in a heterogeneous stromatolite, as opposed to homoge-neous stromatolites in which the morphology is related only to sporadic algal growth(studied by Logan et aI.,1964; Hofmann, 1969).

Although the existence of calcite-encrusted aquatic fungi has been known for a longtime (e.g., Tilden, 1897), it has rarely been documented in the literature. However, the

mycelian filaments, abundant in soils, commonly have been observed covered with calciteand Ca oxalate crystals (Cromack et al., 1919; Graustein et al., l9ll; Klappa, 1979;

Phillips et al., 1987). The latter are frequently associated with terrestrial lichen (Wadsten

& Moberg, 1985). The aim of this a¡ticle is to describe Ca oxalate crystals associated withfungi that develop into an algal mat, also composed of bacteria, cyanobacteria, eukaryoticalgae, and animals, all epiphytic on bryophytes (mosses and liverwort, Hepaticae).

Materials and Methods

Three hundred aquatic mosses were sampled from diverse ecological sites (runningwater, stream and river banks, falls, slope runoff, springs) in westem and northern Europeand in Morocco. Pa¡t of the sample was fixed in the field in a solution of l07o formalde-hyde and another pa-rt was preserved in a dry state, after rapid desiccation (in the sun). Incertain favorable cases, it was possible to bring back living organisms to the laboratoryand keep them for several days to several weeks, which allowed the mobile microfauna(Protozoa, Rotiferae, insect la¡vae, crustaceans) to be observed.

Some samples were preserved in formol and divided up for various purposes: (1) forthin sections used in petrologic studies, (2) to observe the relationship between the crys-tals and organisms, under an optical microscope, after crushing/dilaceration, (3) in orderto determine the organisms present and to observe their mutual relationships, under opti-cal microscope, after slow decalcification with 507o acetic acid, (4) for observation underscanning electronic microscope, after coating the sample with gold or carbon, and (5) forelementary chemical zuralyses, using a microprobe.

Ca Oxalate Crystals in Moss Travertines 119

Algae have been identified using the classic works of Geitler (1930-1932), Bourrelly(1966, 1968, 1970, 1988), Heering (1914, l92I), Printz (1964), and studies by Golubic(1967) and Kahn (1978). Mosses and hepatics have been identified using Augier (1966)and volume 14 of the flora of Pascher, by Vy'arnstorf et al. (1914). Insofar as the fungiwere concerned, the absence of fruitifications made a precise identification impossible.

Results

General Distribution of Orgønisms in the Mut Associ.ated with Mosses

A moss travertine is composed of three basic parts in cross section (Figure 1):

o An upper green part, 0.5-1 cm thick, where the leaves may be covered at mostwith a few diatoms.

¡ A middle parf, l-2 cm thick, white (due to calcite) and friable. After crushing anddecalcif,rcation, this part was seen to be composed of live stems and leaves (green

chloroplasts) and covered with a large quantity of epiphytes: colonies of bacteria,coccoid and filamentous cyanobacteria, hlamentous and unicellular eukaryoticalgae (desmids), diatoms, fungal filaments (siphomycetes), and animals living onthe leaves (either mobile or tube-forming).

o A lower white part, much harder than the upper two parts, formed by calcite sur-rounding the debris of dead stems and leaves (still identif,rable), brown to brown-red, and containing only mycelian filaments and clusters of bacteria.

@

o

Figure 1, Schematic cross section of a calcified biological mat on a moss travertine: (A) Uppergreen part, having only epiphytic diatoms. (B) Middle part, weakly encrusted (calcite and oxalates),

having a mat very rich in species of bacteria, fungi, cyanobacteria, eukaryotic algae, animals. (C)

Lower part, strongly calcified (effects of early diagenesis), having only fungi and bacteria. a, Epi-phytìc diatoms; b, stalked diatoms (C)'mbella); c, mycelium filament; d, bacterial cluster; e, coccoidcyanobacteria; i desmid; g, Phormidiunt incrustatum; h, Sc¡,tsn¿rn6' i, Gongrosira; j, Schizothrix(Irructis); k, Oocardium; l, Vorticella (Protozoa).

120 P. Freytet and E. Verrecchia

Hepaticae travertines have another composition, related to the particular mode of thal-lus (PeLlia Jnbbroniontt) superpositioning. ln the case of moss travertines, Figure I showsseveral variations, mainly in the composition of the biological population, which is rarelya single species of algae or mycelian filament. Generally, in travertines where bothmycelian frlaments and algae are present, there is no preferential organization that wouldindicate a lichen biocoenosis.

Mosses, Hepalicae, and Fungi with Crystals

Details of algal populations will be the subject of future publications. For the purposeof this article, only observations of bryophytes that have mycelian filaments bearingCa oxalate crystals are discussed. More than 300 moss and Hepaticae samples con-tained mycelian filaments, but only 9 of these were associated with Ca oxalate crystals(Table 1).

There are two principal types of mycelian filaments without cell walls(Siphomycetes,'Figures 2,3,and 4): (l) very thin f,rlaments (0.5-1 ¡.tm), straight, some-what branching, cylindrical and smooth, colorless, and (2) larger fìlaments, from 5 to 20

¡lm in diameter, very irregularly cylindrical, wavy, ramihed, sometimes with lipidic in-clusions. No fruitifications were observed.

Crystals Associated with the Biological Møt

The middle part of the travertine contains a small quantity of oxalate crystals, in associ-ation with calcite. Only one observation was made of an oxalate crystal protrudingfrom a calcitic mass (Figure 3). The other observations were made on residues of decal-cification using dilute acetic acid. By chance, the oxalates are not soluble under theseconditions.

Table IExample of Bryophyta associated with fungal filaments and calcium oxalate crystals

Genus Location Environment

P e I I i a fab b ron i an a R ADDIGymno sto mu m calcareum NEESDid¡, ¡n6¿o, top hac e us (BRID. ) JUR.Eucladium v e rticillatum (SMITH) B.eHymeno stylium c urv i ro s t re (EHRH. )

LINDB.C ra t o ne u rum c ommutat um (HEDW. )

ROTH.Hy g ro amb ly s t e g ium t e nax (HEDW .)

JENN.Lep t o d¡, ct i u m r ip ari um (HEDW. )

V/ARNST.B rcc h¡tt he c ium riv u La re B.e.

DordogneDordogneEssonne

Dordogne

Lot

Hautes-Alpes

Dordogne

Saône et LoireSaône et Loire

Vy'eeping rocksVy'eeping rocksIntermittent streamWeeping rocks

Weeping rocks

Weeping rocks

Stream

Small riverSmall river

Note. Examples taken from France.

Ca Oxclate Crystals in Moss TraverÍines 121

A

Figure 2. Hymenost¡*lium curvirostre travertine on weeping rocks, southwestern France. (A) De-calcified sample showing several mycelian filaments and rare coccoid cyanabacteria. (B) Thin sec-tion, polarized light. The biological crust is highly impregnated with micrite, microsparite, and nee-dle bundles. Scale bar: 10 ¡,rm.

Crystallizations (photographed using optical and electronic microscopes) take theform of hbers in bundles or radial arrangements (Figures 44, B, and 5A) and tetragonalprisms, commonly terminated by pyramids (Figure 5C). Detailed study of the crystal faces(Figure 6) allowed the identihcation of the mineral type. The body is composed of a prismcrystal form { 100}, a¡rd the termination is pyramidal crystal forms { 101 }. These faces can

Figure 3. Scanning electron micrograph of a Hymenost¡,lium curvirostr¿ travertine (same sampleas Figure 2), showing randomly distributed clusters of micrite and microsparite, covered to variousextents with organic matter and hlaments (f) and the termination of a prismatic Ca oxalate crystalwith a pyramid (Ox). Scale bar: 10 pm.

122 P. Freytet and E. Venecchia

B

Figure 4. Oxalate crystals and fibers seen under optical miroscope. Samples decalcified using diluteacetic acid. (A) Needles and rods (arrow) on a mycelin filament (Hygroamblystegium tenax traver-tine, with clusters of bacteria, diatoms, Vorticelles; permanent stream, southwestem France). Scale

bar: 50 pm. (B) Same sample, needles and rods grouped into bundles and radiating clusters. Scale

bar: 50 ¡.rm. (C) Biological mar on Eucladium verticillatunt with Gloeocapsa alpina, Schizothrix caL-

cicola, and mycelian filaments bearing prismatic oxalate crystals (anow). Permanent stream, south-

westem France. Scale bar: 100 pm. (D) Prismatic crystals (anow) on a mat of mycelian filamentscovering a Leptodyctium riparium travertine, associated with clusters of bacteria, diatoms, and sev-

eral Gongrosira incrustans filaments. Permanent stream, east-central France. Scale bar: 100 pm.

be truncated or incomplete, which lead to irregular pyramidal faces. The angle formed be-

tween the faces (100) and (101) is 60'. This value corresponds to the measurements made

by Frey-Wyssling (1981) of 59.8', indicating polyhydrated Ca oxalate (weddellite,CaCrO.). The tetragonal prismatic crystal habit is characteristic of oxalates, and micro-probe measurements of the C and O peak ratios (following the method of Verrecchia et al.,

1993) verihed that the hbers, like the prisms, were oxalates and not a particular form ofcalcite (Figure 7). Like the tetragonal crystals, the fiber clusters adhere to the surface ofthe hlaments. One observation was made of a prism partially enclosing a filament, whichis common to calcite crystals associated with algae (Zygnema, Batrachospernxwn mono-liferum), certain diatom stalks, and cyanobacteria (Rivularia haematites).In all cases, the

crystals a¡e external to the organisms, and not skeletal, intercellula¡, or within their tissues.

Discussion

Comparison with Oxulate Crystals of Other Environments ønd Origins

Very little is known about tbe nucleation mechanism of calcite crystals and the rea-sons that lead to a particular form of crystallization (micrite, needles, rhombohedra,

Ca Oxalate Crystals in Moss Travertines 123

Figure 5. Scanning electron micrograph of oxalate crystals, from decalcification residue. (A) Clus-ter of fibers, same sample as Figure 4A,B (Hygroamblystegium). Scale bar: l0 ¡um. (B, c,) crystalon I'eptodyctiun (same sample as Figure 4D). (B) Crystal developed around a mycelian hlament;M, cluster of organic material; C, moss cells. Scale bar20 pm.(C) Prismatic tetragonal bipyrami-dal crystals; D, diatoms; C, cells of a moss leaf. Scale bar 40 ¡tm.

\

Figure 6. Closeup of Ca oxalate (weddellite) crystal terminations and crystallographic planes.Scale bar: l0 ¡^rm.

124 P. Freytet and E. Verrecchia

- CaQQ'xH"O

----- CaCO"c

o

si Au

0

0 KeV

Figure 7, Microprobe spectra showing the C, O, and Ca contents in oxalate and carbonate crystals.

The difference between the element ratios allows identification of the minerals. The oxalate spec-

trum was obtained on a bipyramidal crystal associated with fungi. The calcium carbonate spectrum

was recorded from analysis on calcite associated with moss travertine'

more complex crystals). This is true for both freshwater (Cailleau etal.,l97l; Pente-

cost & Riding, 1986; Freytet, 1992) and saltwater environments (Chafetz & Buczyn-

ski, 1992; Castanier et al., 1989; Defarge et al., 1994). V/ith regard to oxalates, the

bibliography is not very large, although these minerals have been known of since 1825

(Bracconot).In soils, most oxalates a¡e inherited from phytolites or related to fungal activity.

Fungi excrete large quantities of oxalic acid that react with carbonate in the soil. This

leads to a complex oxalate-ca¡bonate cycle (Cromack et al., 1977; Verrecchia et al.,

1990) that results in the fixation of the oxalate ion. Oxalate is transformed into calcite by

early diagenesis (Verrecchia et al., 1993).

In many plants (lichens, phanerophytes), Ca oxalate forms within cells, although ex-

tracellular crystals also have been reported (Wadsten & Moberg, 1985). Crystal forma-

tion is usually associated with membranes, chambers, or inclusions found within the cell

vacuoles (Francheschi & Horner, 1980). The Ca oxalate found in plants is either

whewellite or weddellite, the crystal shape perhaps being molded by crystal chamber

membranes. Formation of oxalate crystals can be a means of removing oxalate from the

cell medium, which may otherwise accumulate in toxic quantities.

Insofa¡ as moss travertines are concerned, it is probable that when the appropriate

physicochemical conditions for precipitation a¡e attained, particular and very localized

contexts determine the mineralogic nature (calcite, aragonite, dolomite, magnesite, ox-

alates) and crystal forms. These contexts include membrane glucides in plant or

cyanobacteria sheaths and the variable concentration of certain ions and specific mole-

cules (such as oxalic acid or aspartic acid; see for example Cailleau eL al., 19'77; Emeis et

al., 1987), present in the environment or secreted by the organisms.

Conclusions

Moss travertines result from calcification of a biological mat in which bacteria, fungi,

cyanobacteria, eukaryotic algae, and very small animals are found. Nevertheless, the effect

Éo

0-

Ca Oxalate Crystals in Moss Travertines I2s

of diagenesis results in the rapid disappearance of organic traces, making it seem asthough only physicochemical processes a¡e involved in crystallization (sinters). In thiscomplex biocoenosis, Ca carbonate (micrite and sparite) and more rarely Ca oxalate (wed-dellite) crystals a¡e formed, the latter being strongly related to mycelian hlaments. Thehabits ofoxalate crystals are both fibrous (bundles or spherulites) and prismatic (tetragonalbipyramids). These crystalline forms are analogous to those found in soils (Graustein etal.,1977) and plant tissues (Pobeguin, 1943; Frey-v/yssling, 1981). Ir is probable thatthere is a biological control of the mineralogy and the crystal habits, exerted by (for exam-ple) the glucides of sheaths and membranes or molecules excreted by organisms. Futureresearch may reveal the oxalate crystals themselves in thin sections made from recenttravertines and their replacement by calcite, a process well known in soils (Verrecchia,1990). Decalciltcation of other travertine samples, devoid of mosses, has resulted (rarely)in the release of mycelian filaments. It is probable that the filaments themselves also se-crete oxalates, which a¡e transformed rapidly into ca¡bonates. Therefore, it is possible thatfreshwater stromatolites can contain secondary calcite that has replaced oxalates, in thesame way that saltwater stromatolites can contain secondary calcite resulting from arago-nite recrystallization.

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