Cactus frost-hardiness physiology

Meaning of resistance measured in an experiment

Frost survival depends on which tissues remain functional and whether the plant can regenerate organs after warming. Cell frost hardiness, absence of segment necrosis and renewed whole-cactus growth are different outcomes. Winter hardiness additionally includes the whole season, root-zone conditions and plant state after thawing. Excised-tissue experiments compare physiology, while field trials reveal combined effects of weather and site. [Nobel and De la Barrera 2003] [Ishikawa and Gusta 1996] [Guevara et al. 2000]

In many papers, LT₅₀ is the temperature at which cellular neutral-red uptake falls to half the control value. The dye accumulates in living cells, and the result assesses tissue damage. In Ishikawa and Gusta's study, LT₀ meant the lowest tested temperature without visible damage in all assessed segments, while LT₅₀ related to damage to half the tissue. Interpret each abbreviation from the individual paper's methods. [Loik and Nobel 1993b, pp. 1724–1725] [Ishikawa and Gusta 1996, pp. 1891–1892]

Cooling rates may vary, ice may be initiated or arise spontaneously, and exposure may last an hour or many nights. Thawing method and assessment time are equally important. In Nobel's 1990 paper, some temperatures were determined for complete loss of cell staining, and tabulated results for 5/−5°C were extrapolated. They cannot be treated as equivalent to experimental LT₅₀ from other papers. [Nobel 1990, pp. 315–318] [Ishikawa and Gusta 1996]

Extracellular ice and protoplast dehydration

Tissue may remain supercooled, containing liquid water below its equilibrium freezing temperature. Initial crystal formation causes an exotherm, a brief temperature rise from release of freezing heat. In the examined Coryphantha vivipara material, supercooling to about −6°C was followed by a recorded rise to about −2°C. Initial ice formation outside the protoplast did not mean immediate tissue death. [Nobel 1981, pp. 195–197] [Nobel 1982]

Ice in extracellular spaces lowers water potential and draws water from cells. The protoplast, the living cellular contents surrounded by a membrane, shrinks. Dissolved-substance concentration rises, and membranes and proteins must remain functional despite water loss. These changes need reversing after thawing. Tolerance of extracellular freezing therefore also depends on dehydration tolerance. [Goldstein and Nobel 1994] [Loik and Nobel 1991]

Acclimatization does not always increase deep-supercooling capacity. After keeping three opuntias at day/night temperatures of 10/0°C, Goldstein and Nobel found ice initiation at a higher temperature than in plants kept at 30/20°C. In the photosynthetic parenchyma of O. ficus-indica, the mean changed from −4.9 to −2.1°C, and in material identified as O. humifusa from −3.6 to −2.8°C. Measurements included four plants per species. Earlier, gradual ice formation may allow more orderly water loss from cells. This interpretation explains how greater resistance may coexist with less supercooling. [Goldstein and Nobel 1994, p. 679, Table V]

Nuclear magnetic resonance measurements indicated that at −15°C, at least about 10% of water remained liquid in winter O. humifusa material. In two more sensitive opuntias, liquid water fell below 10% at about −10°C. Assigning some signals to intracellular and extracellular compartments interprets water relaxation properties rather than directly imaging ice distribution. [Goldstein and Nobel 1994, pp. 679–680]

Water loss, sugars and mannitol

Autumn hydration loss reduces shoot volume and increases solution concentrations. In Loik and Nobel's experiment, material from Bald Knob, Virginia, identified as O. humifusa, lost water after transfer from 25/15°C to 5/−5°C despite a moist substrate. After seven weeks, photosynthetic and water-storage parenchyma thickness decreased by 61% and 65%, respectively. Each measurement series included five segments. Increased osmotic pressure did not demonstrate synthesis of new osmolytes here because pressure was lower when tissues were compared at full water saturation. [Loik and Nobel 1991, pp. 342–344]

Another protocol revealed increased soluble sugars and mannitol. The 1994 paper compared four plants per species after 3–4 weeks at 30/20°C or 10/0°C. In O. humifusa, photosynthetic-parenchyma fructose rose from 15.3 to 69.0 mmol/kg fresh mass, glucose from 18.9 to 54.1 and sucrose from 8.4 to 19.7. The contributions of concentration through water loss and solute synthesis therefore depend on species, tissues and acclimatization course. [Goldstein and Nobel 1994, pp. 677–679, Table II–IV] [Loik and Nobel 1991]

Means ± standard error, n = 4 plants per species. Transcribed from table II. Positive osmotic pressure is a different expression of an osmotic quantity from negative osmotic potential. Results concern material described by the authors, including the historical concept of O. humifusa. [Goldstein and Nobel 1994, p. 677, Table II]

Sugars and polyols, including mannitol, lower solution freezing temperature. This effect is too small to explain deep-frost tolerance alone. In the 1991 paper, a 0.56 MPa osmotic-pressure increase corresponded to a freezing-temperature reduction of only about 0.43°C. The authors considered additional membrane and protein protection and changed water properties. These mechanisms must be distinguished from directly measured compound concentrations. [Loik and Nobel 1991, p. 345] [Goldstein and Nobel 1994]

Mucilage in water management

Cactus mucilage includes hydrophilic polysaccharides that bind water. Its presence in the apoplast, the network of cell walls and spaces outside protoplasts, affects water partitioning between tissue compartments. In O. ficus-indica after 13 days at 10/0°C, mucilage quantity and extracellular water proportion increased. Ice initiation also shifted to a higher temperature in experiments with isolated mucilage. [Goldstein and Nobel 1991, pp. 956–960]

Water initially bound outside cells may supply growing ice and limit abrupt water loss from protoplasts. This is a functional hypothesis consistent with water-relations results. Mucilage quantity does not provide a universal resistance measure. In an experiment on O. humifusa, it increased per unit area, while in twenty O. fragilis populations it decreased on average. This shows differences in species responses and experimental conditions. [Loik and Nobel 1991, pp. 343–345] [Loik and Nobel 1993b, pp. 1728–1730]

Abscisic acid and acclimatization signalling

Abscisic acid, ABA, is a hormone involved in plant responses to changed water relations and temperature. Loik and Nobel compared Ferocactus viridescens, Opuntia ficus-indica and O. fragilis. After 14 days of transition from 30/20°C to 10/0°C, LT₅₀ improved by 1.7, 2.2 and 14.6°C, respectively. Response magnitude therefore strongly depended on species. [Loik and Nobel 1993a, pp. 872–874]

Applying ABA at 30/20°C partly reproduced the cold response. After four days of spraying with 7.5 × 10⁻⁵ mol/l solution, tolerance increased by 0.5, 4.1 and 23.4°C, respectively. These series included five plants each, assessed through neutral-red uptake after one-hour sample exposure at the test temperature. Response differences also indicate different tissue sensitivities to the hormonal signal. [Loik and Nobel 1993a, pp. 872–875]

Experimental injection of water into stems restricted ABA accumulation and removed much of the hardening. In O. fragilis after 14 days, LT₅₀ was −3.5°C with water injection and −20.6°C without it. Injecting water into tissues is not equivalent to ordinary watering. Results support roles for hydration and ABA signalling, but do not provide a tested method of hardening cacti with a hormone product. [Loik and Nobel 1993a, pp. 874–875]

Seasonal resistance on the Canadian prairie

In opuntias near Pike Lake, Saskatchewan, high winter resistance coexisted with very low resistance of new growth. Ishikawa and Gusta collected material from September 1985 to September 1986. Detached segments were placed in moist sand. They were held at −3.5°C for 12 hours to initiate ice, then cooled at 2°C per hour to −12°C and 5°C per hour to lower temperatures. Thawing occurred overnight at 4°C. [Ishikawa and Gusta 1996, p. 1891]

At least five segments were used per temperature, and tests were repeated three times. Necrosis was assessed after four weeks at 22°C. Root and new-shoot formation were additionally monitored for 2–3 months in two replicates of the regeneration experiment. These conditions are essential to interpreting the table below. [Ishikawa and Gusta 1996, pp. 1891–1893]

Data from table 2. LT₀ is the lowest tested temperature at which all assessed segments remained without visible damage. The June-growth result describes death after freezing initiation, not a determined LT₅₀. Distinguishing these criteria prevents apparently comparing identical quantities. [Ishikawa and Gusta 1996, p. 1893, Table 2]

Some winter O. fragilis segments survived immersion in liquid nitrogen only after preliminary freezing to −40°C. This caused severe dehydration before further cooling. Preliminary freezing only to −20 or −30°C did not provide this result. The experiment concerns cryotolerance of detached material, not garden overwintering. [Ishikawa and Gusta 1996, pp. 1892–1894]

Twenty populations of Opuntia fragilis

Loik and Nobel compared material from twenty locations after a shared cultivation period. Plants were then transferred from day/night temperatures of 25/15°C to 5/−5°C for 14 days, with twelve-hour lighting and watering. Five segments were examined per population. Samples were cooled at 8–10°C per hour, held at the test temperature for an hour and warmed at 5°C per hour. LT₅₀ was determined from reduced cellular staining relative to the 0°C control. [Loik and Nobel 1993b, pp. 1723–1725]

Values from table 2, p. 1727. Positive improvement means a shift of LT₅₀ towards a lower temperature. The final range is −15.6°C for Princeton to −48.9°C for Virden, averaging about −29°C. The publication's text identifies Hornby Island as least hardy after acclimatization, but the table contains a higher value for Princeton. The atlas retains all table values and explicitly states this discrepancy. [Loik and Nobel 1993b, pp. 1726–1727, Table 2]

Resistance was more strongly associated with climatic minimum temperatures of provenance than elevation alone. Water-loss magnitude, osmotic-pressure change and mucilage quantity did not explain LT₅₀ differences between populations through a simple linear relationship. A more wrinkled specimen need not be hardier. Provenance matters, but the experiment covers particular material, not every plant labelled with that locality. [Loik and Nobel 1993b, pp. 1727–1730]

Shoots, roots, fruits and meristems respond differently

Nobel and De la Barrera studied clone 1279 of O. ficus-indica. Young segments and fruits were compared after two weeks at 20/10°C or 30/20°C, and rooted one-year segments and young roots after seven weeks. Tissues were kept at the test temperature for 60 minutes. Each mean was based on 5–7 plants. Shoot acclimatization was clearer than fruit and root responses. [Nobel and De la Barrera 2003, pp. 272–275]

Means ± standard error from table 1. Regime differences were significant for segments, but not for fruits and roots. Thermal protection by soil and root tissue's physiological hardening capacity are separate properties. The cultivation implication is separate root-zone monitoring, especially when transferring ground observations to containers. [Nobel and De la Barrera 2003, pp. 275–278]

A meristem is tissue capable of division and new-structure formation. Zutta and co-authors sampled it from areole axillary buds, not the main shoot apex. After 100 days at 10/5°C, they compared its viability with photosynthetic parenchyma. Each series included five plants, with one-hour sample exposure. The meristems studied were more resistant than neighbouring photosynthetic tissue. [Zutta et al. 2011, pp. 2–4]

Means ± standard error, n = 5. Greater bud tolerance may permit regeneration of part of the shoot after damage. It does not mean whole-plant survival at LT₅₀. The name Nopalea cochenillifera in the paper is a synonym of POWO's accepted Opuntia cochenillifera. Nomenclatural record [2-WWW]. [Zutta et al. 2011, pp. 4–5]

Pelecyphora vivipara and assessing regeneration

The material studied by Nobel in 1981 came from Mercury Valley, Nevada, and now belongs to Pelecyphora vivipara (Coryphantha vivipara var. deserti in the paper). Survival trials used five plants per temperature. The night lasted nine hours, and shoot temperature remained close to target for the final four hours. Successive trials used decreasing temperatures at approximately weekly intervals. The −12°C result was obtained later. Positive night-time CO₂ uptake was confirmed before each exposure. [Nobel 1981, p. 195, Fig. 2]

A plant was considered surviving if it regained a positive night-time CO₂ balance within two months after exposure. Five plants met this criterion after −12°C, three after −15°C and none after −20°C. Results concern the material described, exposure duration and physiological survival definition. [Nobel 1981, pp. 195–196, Fig. 2]

A separate measurement series on one plant showed recovery after a night at −10°C. Maximum night-time CO₂ uptake fell by about 70% the following night, and the temperature of its maximum shifted from 10 to 6°C. By the fourth night, the gas-exchange curve had approximately returned to baseline. In the three plants surviving −15°C, night-time balance remained negative for ten nights. On the fourteenth night, uptake averaged 23% of the initial value and after two months about half. Regeneration assessment therefore included gas exchange over many days. [Nobel 1981, pp. 195–197, Fig. 1–2]

Winter carbon balance and chilling injury

Frost survival capacity coexists with seasonal photosynthesis reduction. Koch and Kennedy studied Iowa material identified as O. humifusa. Night-time CO₂ uptake was typical from April to September, while winter acidity changes were small. In March and October, they recorded late-day uptake and night-time CO₂ release. Gas measurements were taken on collected stems under conditions reproducing the field, not by continuous year-round measurement of the same plant in its habitat. [Koch and Kennedy 1980, pp. 391–394]

Night-time acidity increase does not always mean incoming atmospheric carbon. Some CO₂ may arise from respiration and be refixed. In a separate Nobel experiment, CO₂ uptake in a selected opuntia continued at a subzero tissue temperature, but the tissue was supercooled and had not frozen. Freezing resistance, photosynthesis in cold conditions and recycling of respiratory carbon require separate measurements. [Koch and Kennedy 1980] [Nobel 1990, pp. 319–321]

Warm-growing cacti may suffer chilling injury even without demonstrated tissue freezing. Kondo and co-authors compared transfer dates of the Maya cultivar, described as Nopalea cochenillifera, from a heated greenhouse to outdoor conditions in Nagoya. Early transfer, with the first two weeks averaging about 15–16°C, favoured acclimatization. Later treatments with lower initial temperatures suffered more damage. Results depended on season, timing and accompanying light. [Kondo et al. 2023, pp. 213–218]

Plants tolerating later cold showed different chloroplast positions and contacts with other organelles, while damaged plants showed swelling and disorganization of thylakoids, the photosynthetic-system membranes. Superoxide dismutase activity, involving an enzyme that helps remove reactive oxygen species, returned more effectively to its previous level in acclimatized plants. Enzyme assessment used three plants per treatment. Association of these traits with survival does not demonstrate that increased activity of one enzyme alone is sufficient to cause resistance. [Kondo et al. 2023, pp. 216–223]

The hardier plants in this experiment did not have the thickest cuticles. Surface wax coverage also differed. Cold tolerance therefore cannot be assessed solely from shoot-covering thickness or bloom appearance. The paper describes chilling acclimatization in a particular cultivar, without establishing a safe overwintering temperature in a Polish garden. [Kondo et al. 2023, pp. 217–223]

Field studies and a real winter

Minimum temperature does not describe stress duration. In Russell and Felker's Kingsville, Texas trial, 49 opuntia materials experienced seven frost episodes in winter 1984/1985, totalling 129 hours. The minimum was −9°C, measured outside plant tissues. The plan specified 15 plants per material, but some samples were smaller because of transplant losses or plant unavailability. Materials had different planting dates, with some arriving only in autumn and early winter. The assessed proportion of dead above-ground tissue did not exclude later regrowth from the base. [Russell and Felker 1987, pp. 546–549]

In Mendoza in August 1999, two successive nights recorded −16 and −17°C, with temperatures below −10°C for many hours. Guevara and co-authors compared six clones with 15 three-year-old plants per material and site. Age was important context. In a separate trial of nine-month-old plants, the four central plants in each six-plant plot were assessed. Mean damage to young O. ficus-indica segments was 98.1%, while three-year-old material of this species suffered much less damage. [Guevara et al. 2000, pp. 200–204]

Data from table 3. Assessment occurred 15 days after frost, excluding mother segments. This is not the percentage of entire dead plants. Clone differences were significant, but plain-versus-dune comparisons within individual clones were not. Material names follow the authors' treatment. One episode cannot establish winter hardiness in Poland. [Guevara et al. 2000, pp. 202–204]

The Bozeni, Romania trial published in 2022 compared ten taxa, with ten plants each covered and uncovered. The lowest reported temperature was −21.9°C. All uncovered plants identified as Echinocereus coccineus wilted and died, and damage also occurred under cover. Some opuntias and cylindropuntias suffered little damage. The trial used one divided rock garden, without describing individual provenance or cover construction sufficiently for faithful reproduction. Its result cautions against assigning equal winter hardiness to all cacti sold as “frost-hardy”. [Szekely-Varga et al. 2022, pp. 739–743]

Plant temperature and cultivation implications

Night-time heat balance depends on radiation exchange, air movement, shoot shape, spines and hairs. Plant surface temperature may differ from air temperature. Snow further alters near-ground conditions. In the Canadian study, an air minimum of about −38°C accompanied about −17°C near opuntias beneath snow. Microsite protection acts alongside internal tissue tolerance. [Nobel 1980, pp. 10–14] [Ishikawa and Gusta 1996, p. 1892]

The cultivation implication of the entire set of studies concerns documenting provenance and developmental stage, gradual acclimatization and separate shoot and root assessment. Summer opuntia growth requires different assessment from a hardened winter segment. Record sensor position, frost and thaw duration, snow presence and rain protection. Spring results should include necrosis, root formation and subsequent growth. [Ishikawa and Gusta 1996] [Loik and Nobel 1993b] [Nobel and De la Barrera 2003] [Guevara et al. 2000]

Moist soil did not prevent physiological dehydration in chamber experiments, but field trials indicate the importance of site and winter conditions. Laboratory hardening in watered substrate should therefore not become advice to keep a bed wet. In Polish cultivation, effective drainage, ventilated cover appropriate to the material and root-zone monitoring require assessment alongside temperature. [Loik and Nobel 1991] [Koch and Kennedy 1980] [Fleischer and Schütz 1978]

Further site guidance appears in frost hardiness and winter hardiness in collector practice. The overwintering section compares ground, containers and protected cultivation. This article's tables retain experimental conditions and do not establish recommended temperatures for whole species. [Nobel and De la Barrera 2003] [Ishikawa and Gusta 1996] [Loik and Nobel 1993b]