330

Phytologia (December 2011) 93(3)

REGENERATION OF LOPHOPHORA WILLIAMSII

(CACTACEAE) FOLLOWING MUMMIFICATION OF ITS
CROWN BY NATURAL FREEZING EVENTS,
AND SOME OBSERVATIONS ON MULTIPLE STEM
FORMATION
Martin Terry
Department of Biology, Sul Ross State University, Alpine, TX 79832
[email protected]
ABSTRACT
Exposure of Lophophora williamsii to environmental
temperatures that remained continuously below freezing, with lows
estimated at or below 10 to 15C for three consecutive days, resulted
in freeze-drying of the crowns of some individuals in their natural
habitat. I dug up one such plant, brought it back to the lab, planted it in
a pot, watered it weekly, and monitored it for signs of life. Eight weeks
later new growth was observed as incipient lateral branches from the
meristems at areoles on the subterranean portion of the stem. Eleven
weeks after replanting and watering, there were four such offsets on the
plant. This recovery attests to the resilience of this species in the face
of extreme environmental conditions. It also shows that prolonged
freezing under dry conditions constitutes a natural mechanism for
destruction of the apical meristem. Such meristem destruction by frost
would have the same effect on lateral branching as removal of the
apical meristem by human harvesting of the crown, and thus provides
an alternative mechanism for the formation of pseudocespitose clusters
of densely packed individuals in habitat. The concepts of cespitosity
(multiple stems on a single plant) and pseudocespitosity (multiple
individuals in a dense cluster) are discussed with examples. Phytologia
93(3): 330-340 (December 1, 2011)
KEY WORDS: Lophophora, peyote, cold tolerance, apical meristem,
subterranean areoles, lateral branching, regeneration, cespitose.
During the interval of 25 Feb 2011, the Big Bend region of
Trans-Pecos Texas experienced a hard freeze which in many areas had

Phytologia (December 2011) 93(3)

331

the longest continuous duration of sub-freezing temperatures in living

memory (A.M. Powell, pers. comm.). This freeze occurred five months
into a drought during which no biologically significant precipitation
had occurred. A population of Lophophora williamsii (Lem. ex SalmDyck) J.M. Coult. (peyote) in southern Presidio County was adversely
affected by the combination of drought and frost (pers. obs.).
Drought is a frequent phenomenon in Trans-Pecos Texas, and
the Lophophora plants respond to it by contraction of the root (and
possibly the underground portion of the stem, which may be
substantially larger in volume than the root). This contraction pulls the
crown of the plant down to, or even below, ground level, thus reducing
its exposure to the evaporative forces of sun and wind (Fig. 1), as has
been documented in Ariocarpus fissuratus, a sympatric cactus similar
in habit and habitat to L. williamsii (Garrett et al., 2010).
The hard freeze of Feb 2011, however, was no ordinary
occurrence. According to weather records for Presidio, Texas (U.S.
Border Patrol, unpublished data), beginning the night of 2 Feb, the
temperature remained at or below freezing continuously until the
afternoon of 5 Feb, and the low temperatures in this interval were 9C
on 3 Feb, 14 on 4 Feb, and 14 on 5 Feb. The altitude of Presidio is
ca. 800 m. The L. williamsii specimens that suffered frost damage were
at ca. 1300 m in the vicinity of the Chinati Mountains. That difference
in altitude virtually ensures that the temperatures experienced by the
population of L. williamsii were lower than the temperatures recorded
at Presidio. Also associated with the higher altitude would be a lower
atmospheric pressure, which would have increased the rate of
sublimation of ice to water vapor, thus enhancing the lyophilizing effect
of the cold dry air. The combination of the extreme low temperatures
and the extreme duration of those low temperatures made this the most
intense cold-weather event on record for this region.
MATERIALS AND METHODS
On 24 Apr 2011, a typical eight-ribbed adult L. williamsii
specimen measuring ca. 5 cm in diameter and growing in calcareous
soil on an exposed natural terrace near the top of a slope was carefully
dug up so as to cause minimal damage to the distal portion of the

332

Phytologia (December 2011) 93(3)

taproot and to the lateral roots. The individual was selected because, as
with approximately 35% of the plants in the population, its crown had
evidently been completely freeze-dried by the prolonged hard freeze of
early February. Whereas in a normal L. williamsii specimen in the same
population the crown would consist of raised, soft parenchyma tissue
covered with gray-green dermal-epidermal tissue (Fig. 1), in the case of
the frost-damaged specimen the crown had been reduced to a thin layer
of hard dry tissue of light reddish brown color and of the consistency of
solid wood (Figs. 2a, 2b, 2c). This frost-damaged specimen retained a
high density (due to high water content) in its subterranean stem and
root, which suggested that the plant could be alive. Therefore it was
brought back to the greenhouse, replanted in a pot, watered weekly, and
monitored for signs of life.
RESULTS AND DISCUSSION
On 16 Jun 2011, ca. 8 weeks after the specimen was replanted
in the greenhouse, three offsets were visible above ground level, and by
7 Jul 2011 (ca. 11 weeks after replanting) a fourth offset had appeared
above ground level (Fig. 3). Offsets are lateral branches produced by
areolar meristems on the subterranean stem in response to death or
removal of the apical meristem at the center of the crown of the cactus.
The production and development of such lateral branches as a
consequence of human harvesting of peyote is described and
photographically documented by Terry and Mauseth (2006).
Commercial peyote harvesting typically involves cutting the crown off
at such a depth as to effect the removal of the apical meristem of the
harvested plant. The lateral branches produced as a result (due to
derepression of branching as a consequence of removal of the apical
meristem, which is the source of branch-suppressant auxins) emerge
from the ground as small crowns around the perimeter of the
decapitated parent plant (Fig. 4), and eventually mature into
independent plants that ultimately detach themselves from the
degenerating body of the parent plant (Terry and Mauseth, 2006).
A problem arises in field interpretation of close clusters of
crowns of L. williamsii. By definition a cespitose individual has a
central parent stem, which has produced multiple lateral branches,
each of which bears a crown, and each of these lateral branches in turn

Phytologia (December 2011) 93(3)

333

may give rise to multiple lateral branches with their own crowns. Thus
the key criterion for a cespitose plant is that all crowns are connected
by living tissue (particularly vascular tissue) to the central parent stem;
i.e., a cespitose plant is a single plant with multiple stem branches
(Powell and Weedin, 2004). The problem lies in distinguishing a
cespitose plant from a dense cluster of unconnected but often
contiguous individual plants; such a cluster can be characterized as
pseudocespitose. The mechanisms for the development of such
pseudocespitose clusters of individual plants include the following:
(1) The plants all germinated from seeds produced by a parent
plant or plants, living or long dead. The adults that develop
from such seeds are then simply separate individual plants
that happened to germinate very close to the parent plant,
and hence very close to each other, which is a frequent
occurrence in cultivation, where L. williamsii is a copious
seed producer (pers. obs.).
(2) The crown of the original parent plant was harvested by
humans who removed the apical meristem along with the
crown (or button), whereupon lateral branching
produced new crowns which put down their own
adventitious taproots and ultimately became independent
of the parent stem, which eventually degenerated and died
(as in Fig. 4, where the harvesting occurred per the
protocol of a controlled study of the effects of harvesting:
Terry et al., unpublished data).
(3) The crown of the original plant was killed, or the apical
meristem was destroyed without necessarily killing the
crown, by some environmental insult, such as undergoing
severe frostbite and/or lyophilization as described above,
or simply being stepped on by an ungulate. The
progression of subsequent events would be essentially
identical to those caused by harvesting since the critical
event is the loss of the apical meristem, regardless of the

334

Phytologia (December 2011) 93(3)

specific cause of such loss and the end result will
likewise be the death and disappearance of the parent
plant, leaving a dense cluster of independent clonal
progeny occupying the spot where the parent plant had
been.

This is not to imply that true cespitose Lophophora plants do

not exist. On the contrary, in the early stages of the progression of
events following loss of the apical meristem, every damaged parent
plant undergoing the transition to a pseudocespitose cluster of
independent clonal progeny plants must first go through a true cespitose
phase, where the new crowns borne on lateral branches are not yet
independent of the parent plant that lost its apical meristem. And if we
broaden the taxonomic and geographic scope beyond L. williamsii in
U.S. populations and consider, for instance, the clump-forming habit
of L. fricii growing in the Laguna de Viesca in Coahuila (Fig. 5; Terry,
2008a), L. diffusa in Quertaro (Fig. 6; Terry, 2008b), and indeed L.
williamsii at Miquihuana, Tamaulipas (Fig. 7), and El Huizache, San
Luis Potos, Mexico (Fig. 8), as documented by Anderson (1969) and
Terry (2008c and 2008b, respectively) then we see what appear to be
clear and impressive instances of cespitosity. However, the only way to
be certain as to whether a multi-crowned Lophophora specimen (such
as the specimen(s) from Terrell County, Texas, in Fig. 9) is cespitose or
pseudocespitose, is to dig it up and look at the subterranean architecture
of the plant(s) to see if the densely growing crowns are interdependent
or if some are independent of the others. The destructiveness of such
excavation, particularly in the case of what we infer to be very old
clumps of cacti of vulnerable taxa, may be deemed too high a price to
pay for scientific knowledge.
ACKNOWLEDGEMENTS
I thank A. Michael Powell for valuable comments in his
review of the manuscript. Root Gorelick provided a good excuse to get
into the field to observe the effects of the hard freeze on the local cactus
flora. Funding for this work was provided by a grant from the Alvin A.
and Roberta E.Klein Foundation and a Research Enhancement grant
from Sul Ross State University.

Phytologia (December 2011) 93(3)

335

LITERATURE CITED
Anderson, E.F. 1969. The biogeography, ecology, and taxonomy of
Lophophora, (Cactaceae). Brittonia 21: 299310.
Garrett, T. Y., Huynh, C.-V., and North, G. B. 2010. Root contraction
helps protect the livng rock cactus from lethal high temperatures
when growing in rocky soil. Amer. J. Bot. 97: 19511960.
Powell, A. M. and Weedin, J. F. 2004. Cacti of the Trans-Pecos and
Adjacent Areas. Texas Tech University Press, Lubbock.
Terry, M. 2008a. Stalking the wild Lophophora. Part 1. Chihuahua and
Coahuila. Cact. Succ. J. (U.S.) 80: 181186.
Terry, M. 2008b. Stalking the Wild Lophophora. Part 3. San Luis
Potos (central), Quertaro, and Mexico City. Cact. Succ. J. (U.S.)
80: 310317.
Terry, M. 2008c. Stalking the Wild Lophophora. Part 2. Zacatecas, San
Luis Potos, Nuevo Len, and Tamaulipas. Cact. Succ. J. (U.S.) 80:
222228.
Terry, M., Mauseth, J. D. 2006. Root-shoot anatomy and post-harvest
vegetative clonal development in Lophophora williamsii
(Cactaceae: Cacteae): Implications for conservation. Sida 22:
565592.

Fig. 1. Typical healthy specimens of Lophophora williamsii in habitat

in Presidio County, Texas.

336

Phytologia (December 2011) 93(3)

Fig. 2a.

Fig. 2b.

Fig. 2c.

Figs. 2a, 2b, and 2c. Specimen of L. williamsii whose crown underwent
natural lyophilization in the cold, dry, somewhat high-altitude
environment of the Big Bend region during the prolonged hard freeze
of 25 Feb 2011.

Phytologia (December 2011) 93(3)

337

Fig. 3. Four new offsets (pups) that emerged after transplanting the
specimen shown in Fig. 1 to a pot in the greenhouse and providing
water for 11 weeks. The emergence of offsets indicates that the plant is
alive but its apical meristem is dead.

Fig. 4. Four offsets from a decapitated subterranean stem of a L.

williamsii plant harvested in habitat three years previously in Jim Hogg
County, Texas. Such regrowth in the form of lateral branches represents
the typical response to harvesting in this species.

338

Phytologia (December 2011) 93(3)

Fig. 5. A large clump of L. fricii growing in the Laguna de Viesca in

Coahuila, Mexico.

Fig. 6. A typical clump of L. diffusa growing near a dry creekbed in

Quertaro, Mexico.

Phytologia (December 2011) 93(3)

Fig. 7. A clump of L. williamsii growing west of Miquihuana in

southern Tamaulipas, Mexico.

Fig. 8. A relatively small clump of L. williamsii growing at El

Huizache, in San Luis Potos, Mexico.

339

340

Phytologia (December 2011) 93(3)

Fig. 9. A clump of L. williamsii growing in Terrell County, Texas. The

question goes begging as to whether it is a cespitose individual or a
pseudocespitose cluster of individuals.
Note: The photographs for Figures 1-9 can be viewed in color at:
http://www.cactusconservation.org/CCI/Lwfreezedry.html