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Observations of Crystallofolia in the 19th Century

by Bob Harms ()

First Half of the 19th Century

The earliest description of crystallofolia is for Helianthemum canadense (earlier Cistus canadensis) [Cistaceae / Rock-rose Family], with common names 'rock–rose, frost–plant' in Amos Eaton's 1818 A manual of Botany for the Northern and Middle States, 2nd ed.,* reporting observations made by the author in 1816:
In Nov. and Dec. of 1816, I saw hundreds of these plants sending out broad, thin ice crystals about and inch in breadth from near the roots. These were melted away by day, and renewed every morning for more than 20 days in succession.
[p. 206]
*The first edition of Eaton's Manual, 1817, was "was issued 'in a contracted form' "[Historica Botanica], and was not likely to have included his comments on Helianthemum, but the common name 'frost–plant' might well have appeared there.
Pluchea species [Asteraceae / Sunflower Family] have played a major role in treatments of crystallofolia, although none seem to have been noticed since the 19th Century until my own observations of P. odorata in Central Texas. Ice formations were first recorded for Pluchea foetida (earlier Conyza bifrons / P. bifrons) in 1824 by Stephen Elliot [Sketch of the Botany of South Carolina and Georgia]. Most noteworthy is Elliot's preliminary attempt to explain the phenomenon, seeking possible answers in the plant's anatomy. Botanists of the period seem to have been unaware of his query.

In late November 1828 the Central Texas frostweed, Verbesina virginica [Asteraceae / Sunflower Family], was first observed by Jean Luis Berlandier in the hills above the Guadalupe River (northwest of San Antonio), and described in his journal (first published in 1850 in Spanish: Diario de viage de la Comision de limites ..., with Rafael Chovell; in English from Berlandier's French version only in 1980).* An excerpt from November 28 is given below; for the entire entry for November 28.

The causes of this phenomenon are unknown, but since the stem of these plants with living roots still contained moisture, may it not be assumed that the moisture at the center of the stem is the basis for the crystallisation, and that the cold, set in opposition to the stem, forces the water out, via the longitudinal fissures, and causes it to freeze as it emerges into the air.
* The exact dates in the two published versions differ by 2 days. The 1980 translation from the French is essentially the same, but contains a few more details. A note appended to the text in 1980 (by C.H. Muller) incorrectly identifies the frostweed as a very closely related species, Verbesina microptera, perhaps based on the common name 'capitana.' V. microptera is not known from the hill country environment clearly established in the diaries. Moreover, 'capitana' is also established as a common name in N. Mexico for V. verbesina — cf. D. L. & F. A. Latorre, "Plants used by the Mexican Kickapoo Indians" (Economic Botany 3l, 1977).

In 1833 detailed observations, supported by superb drawings, of a similar frost emergence were reported in England by Sir John Herschel for thistle (Carduus sp. [Asteraceae / Sunflower Family]) and heliotrope (Heliotropium sp. [Boraginaceae / Forget-me-not Family]).*
*London and Edinburgh Philosophical Magazine, 3d series, vol. 2, pp. 110–111 & Plate II, “Notice of a remarkable Deposition of Ice round the decaying Stems of Vegetables during Frost”.

"Fig. (A), Plate II. shows the general appearance of this accumulation;"

"the mode in which it was attached to the stem, and seemed to emanate in a kind of riband– or frill–shaped wavy excrescence, — as if protruded in a soft state from the interior of the stem, from longitudinal fissures in its sides, — is exhibited at fig. (B)."

"... the stem presented the singular appearance (C) of a thick massive coating of ice interposed between the wood and its integument, which was swollen and rifted."
Additional noteworthy details from Herschel's report:

Four years later, 1837, William Darlington's Flora cestrica added Cunila origanoides (earlier Cunila mariana) 'common dittany' [Lamiaceae / Mint Family] to the list of known frost plants [p. 350]:

In the beginning of winter, after a rain, very curious and fantastic ribbands [sic] of ice may often be observed, attached to the base of stems of this plant — produced, I presume, by the moisture from the earth rising in the dead stems by capillary attraction, and then being gradually forced out horizontally, through a slit, by the process of freezing. The same phenomenon has been noticed in other plants. See obs. on Helianthemum, p. 314.

Prof. Eaton and Dr. Bigelow have noticed the formation, in freezing weather, of curiously curved ice–chrystals near the root of H. canadense. I have not observed them in that plant; but have seen them very beautiful in the Cunila mariana or Dittany. Mr. Elliot, also, remarked the same phenomenon in the Conyza bifrons. Vide Ell. Sk. 2. p. 322.

Darlington's reference to Dr.Jacob Bigelow in part reflects H. canadense's long standing use as an herbal medicine (as Cistus). Constantine Hering et al (1866) write:
It is an old popular medicine in this country for all kinds of so-called scrofulous diseases and had after being introduced in Great Britain in 1799, gained such a reputation that it was cultivated from seeds.
But they also note being unable to find reference to Cistus in Bigelow's publications.

In 1843 John Torrey's A flora of the state of New York : comprising full descriptions of all the indigenous and naturalized plants hitherto discovered in the state; with remarks on their economical and medicinal properties, vol. 1, p 77, gives common names for H. canadense as 'Frost–weed, Frost–wort,' with the comment:

It received its popular name from the circumstance of its shooting out, early in winter, icy crystals from the cracked bark near the root. A similar phenomenon has been noticed in several other plants but has not yet been satisfactorily accounted for.* [Torrey's note refers to Herschel's article. It is interesting that he seems unaware of Elliot and Darlington.]

Asa Gray's A manual of the botany of the northern United States (first edition, 1848) seems to follow Torrey in noting for H. canadense ('frost–weed'):

Late in autumn crystals of ice shoot from the cracked bark at the root, whence the popular name.
But he does not mention this with the second Helianthemum species listed, H. corymbosum, nor does he note it in his description of Cunila mariana (dittany, now C. origanoides) or Pluchea foetida. And later 19th Century editions do not change this. The 1908 7th edition, New Manual of Botany, revised by B. L. Robinson and M. L. Fernald, extends the frost description to a newly recognized third Helianthemum species, H. majus (now H. bicknellii), added by Fernald (author for the species). Why Gray seemed to limit his recognition of the phenomenon may at first blush seem strange, but it seems inconceivable that it was because he was unaware of the reports by Elliot and Darlington, among the most notable contemporary writers on botany. Since the early common name 'frost–plant' (later 'frost–weed', even 'iceplant' 'frost–wort') was in usage, especially among herbalists, it thus merited comment in a work that otherwise provided a terse minimalist taxonomic listing of known species with only distinctive traits indicated.

The first detailed study came only in 1848, by John Le Conte of the University of Georgia, based on Pluchea foetida and P. camphorata (published in 1850). Le Conte provides illustrations, commenting:

The root is perennial, but the stem is annual and herbaceous. [p. 21; but this seems to conflict with the unqualified statement on p. 33:
the reason why the phenomenon is manifested only in certain kinds of plants, probably arises from several peculiarities in their physical condition. ... They must be herbaceous and annual to secure medullary rays of sufficient size and openness, and, it is probable that all vital action mush have ceased in order that the fluid which is elevated from the soil may be unmixed with the proper juices of the plants; a mixture which would interfere with congelation.

The stalks thus became completely rifted by a succession of severe nights, from the height of six or seven inches down to ground. [p. 23]

The stems which had been cut off within three or four inches of the ground, exhibited the phenomenon as conspicuously as those which were left untouched. [p. 24]

They [ice formations] frequently commence two or three inches from the ground, and extend from three to four inches along the axis of the stem. (Fig. A.) It is proper to state that, at this season, the stalks are dead, and quite dry to within six inches of the earth, below which they are generally green and succulent.
[For Le Conte's explanation.]

The additional facts which my observations establish ... appear to be irreconcilable with the idea that the physiological functions of the plant have any share in the production of it. We must, therefore, look to the moist earth for the large supply of water necessary for the development of these voluminous masses of ice. [p. 24]

The phenomenon manifested on certain plants is every way analogous to that relating to the protrusion of ice from certain kinds of soil, and admits of the same explanation. The porous pith furnishes a constant supply of warm water from the earth, while the wdge-shapred medullary rays secure the mechanical conditions necessary for the development of a projectile force in the proper direction. [p. 33]

Le Conte's general descriptions, as well as one drawing (figure C), are at times presented without quotes or attribution virtually unchanged from Herschel; or if in quotes, modifications are not noted. (For a comparison.)

Second Half of the 19th Century

Le Conte's article was surveyed by Ludolph Treviranus in Botanische Zeitung already in 1850, and soon thereafter several papers on ice formations in plants were presented by German botanists.

The first of these was by Robert Caspary, 1854, who had observed the same formations on 11 exotic species in a German botanical garden. Unlike the natives in natural environments thus far observed, Caspary's plants had been caught by a hard frost in a fresh green state, "even in bloom," and perished. These included annuals (2) as well as perennials (9). He refers to the formations of the type in Figs. 1 & 3 below as Eisblätter [ice leaves]; those of the type in Fig. 2 as fasrige Eislage [fibrous ice layers] — a distinction he maintains throughout the article, implying an essential difference. [Note: Our Verbesina virginica exhibits both types on the same stem, depending upon the extent of the epidermis rupture, the ice formations being identical in structure but not in scope.]

Fig. 2. Lantana aculeata [Verbenaceae / Vervain Family] Figs. 1 & 3. Cuphea cordata [Lythraceae], Transverse section on right. (Fig. 1 was slightly edited & colorized by Bob)
a = stem ('greenish'); b = ice (blue); c = torn loose epidermis (grey).
Caspary's 1854 images.  

Caspary examined the ice forms and the structure of the plants in great detail, perhaps focussing on features discussed by Le Conte, e.g. the distance above the stem base and significance of the medullary rays as a prerequisite condition.
The ice formations occurred not only at the base of the stems of the plants, but everywhere; also the most remote, highest and thinnest twigs, which were elevated roughly 3 feet above the soil ....
And he argues [pp. 672-3] that by his measurements the medullary rays [Markstrahlen] cannot account for the dimensions of the observed ice lamellae, additionally claiming that two of the seven species he studied in detail even lacked medullary rays.

The fact that these were all exotics subjected to freezing temperatures at a stage of growth not matched by plants in their native environment leaves open the possibility that Caspary's findings may only indirectly shed light on the biophysical mechanisms of crystallofolia as a natural phenomenon. But his work must stand as one of the most significant contributions to the general process of ice crystal formation in plants.

In 1860 a second German plant physiologist, Julius Sachs, published a lengthy article on ice formation in plants in the broadest possible sense. In general he added relatively little to the previous studies of crystallofolia in the narrow sense, relying primarily on Caspary's survey for earlier work, and quotes only a couple of paragraphs from Caspary. Worth noting among his observations are:

The quantity and manner of formation of the crystals shows in any case that the water in their formation does not arise either through the contraction of the base/substratum [Unterlage] alone nor through the expansion of the water. [p. 16, page refs. to the 1890 reprint of the article]

It is clear that the mode of explanation that I have given applies equally well to the soil as to plant tissues. I thus agree completely with v. Mohl's view, when he claims no essential difference between the ice formation in the soil and in plants. [p. 17; this essentially echoes Le Conte's view]

Prof. H. Hoffmann in his Grundzügen der Pflanzenklimatologie 1857 pp. 327–329 has given measurements in order to identify the contraction of succulent plant tissues during freezing using volumetric means. The contractions which he achieves in this way amount to 21 to over 30 percent of the original volume in the leaves. This quite incredibly large contraction prompted me to conduct new experiments on this subject, all the more so since I considered the method used by Herr Hoffmann to be unfeasible. [p. 18; Sachs' new experiments [pp. 18–20] do not support Hoffmann's views on contraction.]

Sachs alone recognizes the significance of freezing phenomena for issues of plant distribution and natural selection.
Unfortunately the necessary conditions for the data given here are still too little known; but they merit the greatest attention not only from a physiological point of view, but are also of decided importance for plant geography and evolutionary history, as A. De Condolle repeatedly notes. [p. 41]

Gray 1868 (Gray's lessons in botany and vegetable physiology... glossary, or, dictionary of botanical terms; (also) Manual of the botany of the Northern United States) lists three species of Helianthemum, and gave the genus common name as FROSTWEED, associating ice formation at the genus level.

Two short papers from the last quarter of the century advanced our knowledge of crystallofolia with Cunila origanoides. In the first of these Pennsylvania naturalist Jacob Stauffer noted, 1877, that the root was not dormant:

... I took up a number of the plants, and always found a vigorous scaly root bud, undergoing development at this early season under ground, to produce a new stem the following spring. I came to the conclusion that, as the temperature was below freezing and snow was on the ground, the expanding bud, in close proximity to the surface, gave out sufficient caloric or warmth to generate vapor from the moist soil.

Note the quadrangular stem typical for mints. (Edited by Bob)
The second, by Lester Ward, 1893, who was unaware of previous descriptions of Cunila crystallofolia, provided excellent details of the formations on the quadrangular–stemmed mint — which are quite unlike those in the round–stemmed species — the corners seemingly providing structural support. [But see also Coblentz's 1914 study below.]
There were always several of these, usually three, four, or five, all attached to the same vertical portion of the stem but at regular intervals around it like the paddles of a flutter-wheel, but all curving in the same direction after the manner of a turbine wheel. Thus, where there four they stood with each pair opposite, as in the accompanying cuts....
Two very general surveys of the phenomenon appeared in the 1890s. Plant physiologist Daniel T. MacDougal, in a short but detailed two page Science 1893 article, presented a number of claims, some of which would seem to indicate limited knowledge of previous work in this area, Le Conte as well, including:
The century closes with a report on the state of ice crystal research (in the broadest sense) by J. Christian Bay, Botanical Gazette, 1894. Bay's listing of "Plants on which ice-crystals have been observed," might seem to be a useful resource, but it goes beyond natural crystallofolia and includes arboreal needle ice as well as freezing of exotic species in cultivation in cold climates, and unverifiable identifications (and dates).* Species are presented in assumed chronological order of published presentation with no indication of crystalization type. (Bay was unaware of Eaton 1818.)
*E.g., "(?) Vernonia> sp. [Asteraceae; Atkinson, 1885–6]." This is from a brief 1894 article in which George F. Atkinson describes his field observations of Cunila in 1885–6. At the end of the article he notes having "discovered also one other plant [we are not told when] which produced these frost freaks ... From the observations I made at the time I can safely say that it was either some species of Eupatorium or Vernonia, more likely the latter. I regret now that I did not acurately determine the species".

New to Bay is the dubius claim that contraction of tissue plays a significant role in the ice formation (based on the work of German Botanists, especially Hermann Hoffmann (Witterung Und Wachsthum Oder Grundzüge Der Pflanzenklimatologie, 1857). Bay presents the following speculation [p. 325; contrast, however, the view of Sachs given above]:

The cold causes a contraction of the tissues all over the plant, and consequently the turgescence is very much diminished, as well as the permeability of the cell-walls to water. As the contents of the peripheral ends of the medullary rays freeze, expand, and are pressed forward, the stem splits in the place where it affords the least resistance, and the ice forms a layer covering the whole surface of the wound. The pressure from inside supplies water, the latter being drawn up by capillary forces.

Early Twentieth Century

In 1914 physicist William Coblentz presented the results of numerous ingenious experiments designed to test the validity of various claims concerning frost formations of Cunila in Washington, D. C. He seemed to know very little of the 19th Century literature on the subject beyond Le Conte (Hershel) and Ward, but since some of his tests refute views not held by earlier scholars — e.g., that it is not the result of accretion, "the deposition of moisture from the surrounding air" — these must reflect the "many diverse opinions [that] were received as to the cause of the ice formation."

Perhaps his most significant contribution lies in his detailed analysis of the structure of Cunila stems and the manner in which that quadrangular–stemmed mint projects its frost. The following images, colorized and slightly edited from his originals, show that:

As shown in figures 1 and 12 the stem is somewhat rectangular in outline, the pith having a similar shape, but the "corners" are rotated 45°.* At these "corners" of the pith [outlined in red below] there is but little wood between the pith and the bark, and it is along this line that the stem often cracks. ... in figures 11 and 12. The numerous holes in the wood are the "sap tubes" [in blue in Fig. 12] which form an easy path for the moisture to rise within the stem, by capillary attraction. [p. 492]
*Contrast my own sections of related mint Salvia coccinea for which the pith corners are aligned with those of the stem.

(p. 492)

Fig. 12 — Cross section of stem of Cunila mariana (p. 498; much reduced;
blue area shown enlarged on the right;
the bark and cortex seem to have been stripped)

Top right corner of Fig. 12;
selected xylem vessels in blue; xylem rays clearly visible in area identified as 'wood' by Coblentz
Coblentz presents arguments that do indeed seem reasonable, although sometimes difficult to follow. But since his knowledge of stem anatomy and water transport was limited, he actually fails to understand just how the water passes from the internal vessels ('sap tubes') to the wood surface — a function of the xylem rays (Le Conte's 'medullary rays') so clearly visible in his cross sections. The larger vessels (colored blue) at the stem corners are not likely to be the source of the water in ice formation at the stem midpoint — movement from the vessels would be directly via the rays radially to the exposed surface (within the areas outlined with red), and not transversely across adjacent rays. The role of 'pith' is a pseudo–issue stemming from Le Conte's unfortunate use of terminology, referring to the secondary xylem as 'pith' (Coblentz's 'wood').
It was found that the ice fringes rarely start from the side of the stem where the pith is closest to the bark. This eliminates, to some extent, the question whether the pith is instrumental in forming the ice fringes. In the splinters and in the rifted stems of Cunila, at no time was ice found to have formed along the line of separation of the stem. This seemed puzzling at first, for it appeared to contradict the idea that the moisture comes from the sap tubes within the stem, in which case one would expect to find the formation of ice fringes facilitated upon the surface laid bare by splitting. ...

The microsections of the Cunila stems show in a very unexpected manner why no ice fringes are formed upon the rifted surface of the stem. As already stated, the rift always occurs at the "corners" of the pith where the woody part of the stem is the thinnest. It may be noticed in figures 11 and 12 that at the four points where the wood is the thinnest there are usually but few, if any, sap tubes. Hence one need not expect to find ice formations upon the surfaces formed by splitting. [p. 492]

Coblentz is left to wonder why his artificially generated ice crystals are not fibrous like those in nature.
The main difficulty in this explanation of the cause of ice fringes lies in the fact that the second stage in their formation is an apparently solid wedge of ice (see, however, fig. 3B), whereas the mature fringe is fibrous in structure, very friable, and often separates into a series of wide ribbons as thin as tissue paper. The fibrous structure, however, may be the result of reformation by variations in air temperature, by evaporation, etc., which produces the white fringe shown in the photographs. [p. 497]
Had Coblentz had a broader and better understanding of the 19th Century scholarship in this area, his arguments and speculations surely would have been different. One issue worth noting in Coblentz are his claims regarding root pressure.
The roots are not necessary for the production of the ice fringes. As a matter of fact the stalk and the near-by roots are dead, although the rest of the plant (new growth) is perennial. [p. 495]

They [photographs] show that the ice may be formed upon stems without the roots. Hence the ice is not formed as result of hydrostatic pressure excerted by the roots, which are perennial. [p. 499]

No one has claimed (in the published literature) that root pressure alone causes these formations, but he fails, however, to show that root pressure does not play a significant role in naturally occurring ice formations — but note his tests with cut stems below. Whether he considers the roots to be dead or perennial is not clear.

Finally, one interesting experiment with rootless stems is presented (p. 493). Laboratory test A showed that stems that had been drying for nine weeks very rapidly absorbed moisture after being placed in water. The next morning two of four stems were 'thorougly soaked.' Then for test B, the two most active samples of test A were

"thoroughly dried and covered with cement, K [blue], and placed in water containing a red dye. Sample a was covered at the top, K, so that the water would have to come out at the sides. The sides of the immersed part of this stem were covered with cement, so that the water would have to traverse the sap tubes in order to reach the top. the immersed end of sample b was covered with cement, so that the water would have to soak in through the sides in order to traverse the stem. The next morning...(uncolored), moisture was observed on the sides of a, and the top of b showed the red dye."

Experiment B. K & dark blue = cement; red = red dye; light blue = uncolored moisture
A nice demonstration of capillary action, but somehow Coblentz doesn't seem to realize that it produced results in both stems, but different results. Why only moisture and no red dye emerged from the sides of a and by what route the red dye entered the sides of b both beg explanation apart from the seemingly stronger capillary force obtained with the open stem top of b. Apart from the fact that hydrophilic xylem vessels, lignified and dead at maturity, serve as capillary tubes, the experiment doesn't actually enlighten us on the physics of crystallofolia.

Subsequent similar tests for capillary force with cut stems were made to see how high the water would rise (p. 493):

... the stems were more than 6 cm. in length, and it was found that the water rose to a height of 5 cm. However, when uncovered and exposed to the wind the moisture did not rise higher than 1 cm. to 2 cm.
In comparison with known crystallofolia significantly higher on the stem (over 4 feet), Coblentz seems to have demonstrated that capillary forces alone can't account for the data — perhaps the tests also support a significant role for root pressure in naturally occurring formations.