1. Saltcedar (Tamarix) Physiology - a Primer Dr. Curtis E. Swift Colorado State University Cooperative Extension

2. Tamarix – uses in ancient times Charcoal from Tamarix twigs – found in caves of Natufian culture (C. 12300-10500 BC) – Mount Carmel, Israel Ley-Yadun, S., and Weinstein-Evron, M. 1994. Late Epipalaeolitic wood remains from el-Wad Cave, Mount Carmel, Israel, New Phytol. 127:391-396.

3. Tamarix – uses in ancient times Manna from Heaven - Manna scale (Trabutina mannipara) –Biblical manna - one of the food sources consumed by the Israelites during their wanderings in the wilderness of Sinai Ben-dov, Y. 1988. Manna scale, Trabutina mannipara (Hemprich & Ehrenberg) (Homoptera: Coccoidea: Pseudococcidae) Systematic Entomology 13:387-392.

4. Manna scale Trabutina mannipara

5. Saltcedar – in the United States Introduced by nurseryman in early 1800’s as an ornamental Later used as an erosion-control plant in New Mexico 1920 - 40 or 50 thousand acres over one million acres by 1965 Anderson, J.E., 1982. Factors controlling transpiration and photosynthesis in Tamarix chinensis Lour. Ecology 63(1):48-56.

6. Saltcedar – in the United States Since the early 1900’s Tamarix has rapidly invaded the ecosystem of the lower Colorado River and its tributaries –Resulted in the replacement of up to 90% of the riparian communities historically dominated by cottonwood-willow forests Sala, A, and Smith, S.D. 1996. Water use by Tamarix ramosissima and associated phreatophytes in a Mojave desert floodplain. Ecological Applications 6(3):888-898.

7. Saltcedar Genus Tamarix Native to the Mediterranean region, central Asian and north African deserts A naturalized shrub or small tree in U.S. Widely distributed phreatophyte in the southwestern United States Ginzburg, C. 1967. Organization of the adventitious root apex in Tamarix aphylla. Amer. J. Bot. 54(1):4-8.

8. Floodplain survival Variety of environmental attributes affect the mechanisms controlling populational and ecological relationships between floodplain species. Cleverly, J.R., Smith, S.D., Sala, A., and Devitt, D.A. 1997. Invasive capacity of Tamarix ramosissima in a Mojave Desert floodplain: the role of drought. Oecologia 111:12-18.

9. Floodplain survival of native species Willow is more tolerant of water and salt stress than cottonwood Responsible for the persistence of Salix vs. Populus on the Colorado River Busch, D.E., and Smith, S.D. 1995. Mechanisms associated with decline of woody species in riparian ecosystems of the Southwestern U.S. Ecological Monographs 65(3):347-370.

10. Tamarix success as an invasive plant Success in the floodplain results from: –ability to grow rapidly in wet years –ability to tolerate or avoid extreme water and heat stress in drought years Cleverly, J.R., Smith, S.D., Sala, A., and Devitt, D.A. 1997. Invasive capacity of Tamarix ramosissima in a Mojave Desert floodplain: the role of drought. Oecologia 111:12-18.

11. tolerant of desiccation of watercourses Blackburn, W.H., Knight, R.W., and Schuster, J.L. 1982. Saltceder influence on sedimentation in the Brazos River. J. Soil. Water. Conserv. 37:298-301 Tamarix success as an invasive plant

12. tolerant of salinization of surface soils Busch, D.E., and Smith, S.D. 1993. Effects of fire on water and salinity relations of riparian woody taxa. Oecologia 94:186-194. Tamarix success as an invasive plant

13. Tolerance of Floods Salt grass and dwarf willow developing on sand bars – shallow roots - swept away by floods Tamarisk is hardy enough to withstand floods, continue to grow, stabilize the underlying surface, and trap sediments Graf, W.L. 1978. Fluvial adjustments to the spread of tamarisk in the Colorado Plateau region. Bulletin Geological Society of America 89(10):1491-1501.

14. Plant Success When a species is competitively superior under both wet years and drought, it would be expected to persist as the sole species through successional time. Cleverly, J.R., Smith, S.D., Sala, A., and Devitt, D.A. 1997. Invasive capacity of Tamarix ramosissima in a Mojave Desert floodplain: the role of drought. Oecologia 111:12-18.

15. Tamarix invasiveness Plant spread upstream at ~ 20 km/yr (12 mile/yr). –Colorado and Green River in Utah Graf, W.L. 1978. Fluvial adjustments to the spread of tamarisk in the Colorado Plateau region. Bulletin Geological Society of America 89(10):1491-1501.

16. Tamarix invasiveness Annual production of 600,000 windborne seeds for each mature tamarisk tree Spreads rapidly by layering Robinson, T.W. 1958. Phreatophytes. US Geological Survey Water-supply paper 1423:70-75. Wilkinson, R.E. 1966. Adventitious roots on saltcedar roots. Bot. Gaz. 127(2-3):103-104.

17. Tamarix invasiveness All the aboveground portions of saltcedar will develop adventitious roots and form new shrubs if kept wet in moist soil. ~100% of stem cuttings sprout at all times of the year if kept moist and warm. Horton, J.S. 1977. The development and perpetuation of the permanent Tamarisk Type in the phreatophyte zone of the southwest. USDA, FS, General technical report RM 43:124- 127.

18. Tamarix invasiveness Fluvial Adjustments Islands have become longer and wider Channel-side bars have widened Some alluvial-fan surfaces have expanded Resulted in: –Reduction in channel widths –Flooding over the bank Graf, W.L. 1978. Fluvial adjustments to the spread of tamarisk in the Colorado Plateau region. Bulletin Geological Society of America 89(10):1491-1501.

19. Phreatophytes Plants that are tightly linked to aquifers for water uptake. –Dependent on groundwater (water table and capillary fringe) as a moisture source. Busch, D.E., Ingraham, N.L., and Smith, S.D. 1992. Water uptake in woody riparian phreatophytes of the southwestern United States: a stable isotope study. Ecological applications 2(4):450-459.

20. Phreatophytes Phreat = well; phyte = plant Waisel, Y, Eshel, A., and Kafkafi, U. 1996. Plant Roots: the hidden half. Marcel Dekker, Inc. New York, NY Can absorb water deep and release it at or near the soil surface. The soil surface is where nutrients are most available.

21. Phreatophytes Classified on type of water required – Groundwater – water table or capillary fringe – Moisture from unsaturated soils Busch, D.E., Ingraham, N.L., and Smith, S.D. 1992. Water uptake in woody riparian phreatophytes of the southwestern United States: a stable isotope study. Ecological applications 2(4):450-459.

22. Phreatophyte - Definitions Obligate - require uninterrupted access to saturated soil –Roots in water table or capillary fringe Cottonwood and willow Turner, R.M. 1974. Quantitative and historical evidence of vegetation changes along the upper Gila River, Arizona. USGS Professional Paper 655-(H):1-20.

23. Phreatophyte - Definitions Facultative – able to use water from the water table and associated capillary fringe –able to extract water and survive indefinitely in unsaturated soils. Tamarix Everitt, B.L. 1980. Ecology of saltcedar – a plea for research. Environ. Geol. 3:77-84

24. Facultative Phreatophytes Ability to use water from unsaturated soil have a greater ability to: –withstand stress tolerance –increase their nutrient uptake soil nutrients are often more abundant above the saturated zone Pinay, G., Fabre, A., Vervier, P., and Gazelle, F. 1992. Control of C, N, P, distribution in soils of riparian forests. Landscape Ecol 6:121-132.

25. The Vascular System

26. Water Uptake of Saltcedar Waisel, Y., Liphschitz, N., and Kuller, Z. 1972. Patterns of water movement in trees and shrubs. Ecology 53(3):520-523. Straight ascent turning into ring ascent

27. Phreatophytes Have roots that extend down to the water table or other periodically stable water supply Roots can extend to a depth of 53 meters Waisel, Y, Eshel, A., and Kafkafi, U. 1996. Plant Roots: the hidden half. Marcel Dekker, Inc. New York, NY

28. Tamarix The genus is generally characterized by a deep and intensively branched root system. Adventitious roots develop from the lenticels. Ginzburg, C. 1967. Organization of the adventitious root apex in Tamarix aphylla. Amer. J. Bot 54(1):4-8.

29. Root Development Salix – root elongation rates are slow – emphasis on lateral root growth helps protect against late season flood scour Tamarix –Greater root elongation rate –Allows seedlings to persist in dry soils while Salix seedlings die Horton, J.L., and Clark, J.L. 2001. Water table decline alters growth and survival of Salix gooddingii and Tamarix chinensis seedlings. Forest Ecology and Management 140:239-247.

30. Root Development Populus seedlings – 0.6 – 1.3 cm/day – 72-162 cm by end of first season Salix seedlings – 1.0 – 2.1 cm/day Horton, J.L., and Clark, J.L. 2001. Water table decline alters growth and survival of Salix gooddingii and Tamarix chinensis seedlings. Forest Ecology and Management 140:239-247.

31. Saltcedar Reputation as the heaviest water user of all the phreatophytes Gay, L.W., Sammis, T.W., and Ben-Asher, J. 1976. An energy budget analysis of evapotranspiration from saltcedar. Hydrology and water resources in Arizona and the southwest 7:133-139.

32. Water Use by Saltcedar Able to desiccate floodplains and lower water tables Blackburn, W.H., Knight, R.W., and Schuster, J.L. 1982. Saltcedar influence on sedimentation in the Brazos River. J. Soil. Water. Conserv. 37: 298-301

33. Saltcedar T. chinensis with adequate water transpires copiously Rates are similar to other phreatophytes in same area Anderson, J.E., 1982. Factors controlling transpiration and photosynthesis in Tamarix chinensis Lour. Ecology 63(1):48-56.

34. Transpiration Exchange of water vapor between the plant canopy and the atmosphere depends upon air and leaf temperatures –atmospheric humidity –aerodynamic or boundary layer resistance –leaf diffusive (stomata) resistance Anderson, J.E., 1982. Factors controlling transpiration and photosynthesis in Tamarix chinensis Lour. Ecology 63(1):48-56.

35. Transpiration of Saltcedar Stomata respond to temperature, humidity, and light intensity * Gas exchange * Vapor release

36. Transpiration of Saltcedar 20 o C (68 o F) and 45% RH –saltcedar twigs transpire a weight of water greater than their own fresh leaf weight each hour. –Similar rate to common herbaceous plants –Not unusually high where compared with other plants with an abundant water supply. Anderson, J.E. 1977. Transpiration and Photosynthesis in saltcedar. Hydrology and water resources in Arizona and the Southwest 7:125-131.

37. Transpiration Rates At 30 C (85 F) and 45% RH –Populus fremontii and Eleagnus angustifolia practically identical to saltcedar Tamarix chinensis. Anderson, J.E., 1982. Factors controlling transpiration and photosynthesis in Tamarix chinensis Lour. Ecology 63(1):48-56.

38. Transpiration Tamarix is more drought tolerant than Salix Salix transpires more water per unit leaf surface area and is less tolerant of seasonal water stress than Tamarix Cleverly, J.R., Smith, S.D., Sala, A., and Devitt, D.A. 1997. Invasive capacity of Tamarix ramosissima in a Mojave Desert floodplain: the role of drought. Oecologia 111:12-18.

39. Saltcedar & Flooding Inundation for 36 months results in 99% plant kill whether the trees were partially or entirely submerged. Inundated trees did not foliate the third growing season – 24 months of inundation may be adequate Wiedemann, H.T., and Cross, B.T. 1978.Water inundation for control of saltcedar along the periphery of lakes. Proceedings, Southern Weed Science Society 31:229.

40. Photosynthesis in Saltcedar Photosynthetic tissue –Cladophylls Cylindrical leaf-like photosynthetic stems Bear two sizes of whorled clasping leaves –scale-like – 3 mm in length –Cauline leaves – 8 – 9 mm long –Covered with a white salt “bloom” Wilkinson, R.E. 1966. Seasonal development of anatomical structures of saltcedar foliage. Bot. Gaz. 127(4):231-234.

41. Saltcedar leaf surface has a waxy covering Composition and quantity varies seasonal differences in temperature and rainfall Quantity and composition of waxes on leaves of salt cedar is thought to be the basis for differences in sensitivity to herbicides Mayeux, J.S., Jr., Jordan, W.R. 1984. Variation in amounts of epicuticular wax on leaves of Prosopis gladulosa. Bot. Gaz. 145(1):26-32.

42. Tamarix Cuticle development Wilkinson, R.E. 1966. Seasonal development of anatomical structures of saltcedar foliage. Bot. Gaz. 127(4):231-234

43. Tamarix Cuticle development Wilkinson, R.E. 1966. Seasonal development of anatomical structures of saltcedar foliage. Bot. Gaz. 127(4):231-234

44. Tamarix Cuticle development Wilkinson, R.E. 1966. Seasonal development of anatomical structures of saltcedar foliage. Bot. Gaz. 127(4):231-234 In addition, the quantity and composition of wax on leaf surfaces of tamarisk varies during the season

45. Tamarix Cuticle development Wilkinson, R.E. 1966. Seasonal development of anatomical structures of saltcedar foliage. Bot. Gaz. 127(4):231-234

46. Photosynthesis optimum leaf temperatures for photosynthesis between 23 and 28 C (73 – 82 F) at 35 C (95 F) photosynthesis reduced about 20% Anderson, J.E. 1977. Transpiration and Photosynthesis in saltcedar. Hydrology and water resources in Arizona and the Southwest 7:125-131.

47. Photosynthesis Anderson, J.E. 1977. Transpiration and Photosynthesis in saltcedar. Hydrology and water resources in Arizona and the Southwest 7:125-131.  net photosythetic rate transpiration rate

48. Photosynthesis Optimum temperature 23 - 28 C (73 – 82 F) Photosynthesis is optimum in early part of day Time with lower evaporation and transpiration demands Anderson, J.E., 1982. Factors controlling transpiration and photosynthesis in Tamarix chinensis Lour. Ecology 63(1):48-56.

49. Photosynthesis Observed optimum temperature 23 - 28 C (73 – 82 F) To maximize photosynthesis during hottest part of the day would result in much higher transpiration losses relative to carbon gains Anderson, J.E., 1982. Factors controlling transpiration and photosynthesis in Tamarix chinensis Lour. Ecology 63(1):48-56.

50. Stomata Close in response to increasing temperature Saltcedar –insures seedling survival until the root system taps water table –enables plant to invade and succeed in areas subjected to periodic drought. Anderson, J.E. 1977. Transpiration and Photosynthesis in saltcedar. Hydrology and water resources in Arizona and the Southwest 7:125-131.

51. Photosynthesis & Saltcedar Light saturated at 44% of full sunlight –1100 nEinstein m -2 s -1 at 400 to700 nm Rate of photosynthesis is considerably lower than the rates for herbaceous plants. Anderson, J.E. 1977. Transpiration and Photosynthesis in saltcedar. Hydrology and water resources in Arizona and the Southwest 7:125-131.

52. Photosynthesis Light cloud cover reduces irradiation below saturation, reducing photosynthesis Stomata close to conserve moisture when light is limiting to photosynthesis Anderson, J.E., 1982. Factors controlling transpiration and photosynthesis in Tamarix chinensis Lour. Ecology 63(1):48-56.

53. Stomata close to conserve moisture when light is limiting –Similar conclusion in other studies Populus spp. Picea engelmanii Kaufman, M.R. 1976. Stomatal response of Engelmann spruce to humidity, light, and water stress. Plant Science Letters 3:898-901. Pallardy, S.G., and Kozlowski, T.T. 1979. Stomata response of Populus clones to light intensity and vapor pressure deficit. Plant Physi90logy 64:112-114..

54. Stomata and light intensity With most plants –Drop in light intensity Stomata close slowly –Increase in light intensity Stomata open rapidly Woods, D.B., and Turner, N.C. 1971. Stomatal response to changing light by four tree species of varying shade tolerance. New Phytologist 70:77-84.

55. Stomata and light intensity Saltcedar –Drop in light intensity Stomata close rapidly –Increase in light intensity Stomata open slowly A mechanism to reduce water loss Anderson, J.E., 1982. Factors controlling transpiration and photosynthesis in Tamarix chinensis Lour. Ecology 63(1):48-56.

56. Water use efficiency Photosynthesis vs. water uptake Tamarix has the highest water use efficiency of the woody riparian taxa investigated – Populus, Salix –Based on carbon isotope research Busch, D.E., and Smith, S.D. 1995. Mechanisms associated with decline of woody species in riparian ecosystems of the southwestern U.S. Ecological Monographs. 65(3):347-370.

57. Water use efficiency Photosynthesis vs. transpiration Tamarix chinensis –4.3 mg water/g dry weight of tissue (dwt) Populus fremontii –6.8 mg/g dwt Eleagnus angustifolia –6.7 mg/g dwt Anderson, J.E. 1982. Factors controlling transpiration and photosynthesis in Tamarix chinensis Lour. Ecology 63:48-56.

58. Water use efficiency Photosynthesis vs. transpiration Salix and Tamarix - comparable rates - Mojave desert Cleverly, J.R., Smith, S.D., Sala, A., and Devitt, D.A. 1997. Invasive capacity of Tamarix ramosissima in a Mojave Desert floodplain: the role of drought. Oecologia 111:12-18.

59. Salt effect on Photosynthesis and Transpiration Rates of photosynthetic carbon fixation and transpirational water loss changed very little with increasing salt treatment Reduction in growth with increased salt levels were due to increased respiration and/or salt pumping Kleinkopf, G.E., and Wallace, A. 1974. Physiological basis for salt tolerance in Tamarix ramosissima. Plant Sci. Ltr. 3:157- 163.

60. Salts and plant growth Excess soluble salts in the soil –Decrease absorption of essential nutrients –May have a direct toxic effect –May increase osmotic gradient and prevent adequate water uptake Hayward, H.E., and Berstein, L. 1958. Plant-growth relationships on salt-affected soils. Bot. Rev. 24:584-635.

61. Salts and plant growth Osmotic effects of soluble salts are the most detrimental single factor to vegetation in saline areas. Hayward, H.E., and Wadleigh, C.H. 1949. Plant-growth relationships on salt-affected soils. Advances in Agron. 1:1-38.

62. Salt uptake Trees capable of accumulating salts can maintain turgor and high leaf conductance as tissue water potential declines; other plants are required to close their stomates to maintain turgor. Osonubi, O., and Davies, W.J. 1978. Solute accumulation in leaves and roots of woody plants subjected to water stress. Oecologia 32:3223-332.

63. Tamarix survival on saline soils maintain high uptake of ions a. salt extrusion by salt glands b. cellular compartmentation c. utilization for osmoregulation Greenway, H., and Munns, R. 1980. Mechanisms of salt tolearance in nonhalophytes. Annual Review of Plant Physiology. 31:149-190.

64. Salt glands and epidermal salt hairs Function in ion regulation salt hairs accumulate ions and excrete them from leaves, regulating cellular ionic content Karimi, S.H., and Ungar, I.A. 1989. Development of epidermal salt hairs in Atriplex triangularis willd. in response to salinity, light intensity, and aeration. Bot. Gaz. 150(1):68-71.

65. Salt Hairs & Glands of Halophytes Form in early stages of development Critical for the salt tolerance of young developing halophytes Karimi, S.H., and Ungar, I.A. 1989. Development of epidermal salt hairs in Atriplex triangularis willd. in response to salinity, light intensity, and aeration. Bot. Gaz. 150(1):68-71.

66. Salt hairs – secondary functions Reduction of intense illumination Insulation against excessive heat to reduce transpiration Water storage Water absorption Ehleringer, J., and Bjorkman, C.J. 1978. Leaf hairs: effects on physiological activity and adaptive value to a desert shrub. Oecologia 37:183-200.

67. Tamarix Salt Gland Collecting Cell Secretory Cells Pore Cuticle Fahn, A. 1988. Tansley Review No. 14. Secretory tissues in vascular plants. New Phytol 108:229-257.

68. Tamarix Salt Gland Salts (chlorides) move through the apoplast from the xylem to the salt glands Cuticle almost completely separates salt glands from the mesophyll tissue A subcuticular space (collecting chamber/cell) between the cuticle and the gland Campbell, N., and Thomson, W.W. 1975. Chloride localization in the leaf of Tamarix. Protoplasma 83:1-14.

69. Tamarix Salt Gland Numerous mitochrondria Nuclei Fahn, A. 1988. Tansley Review No. 14. Secretory tissues in vascular plants. New Phytol 108:229-257. Requires energy

70. Tamarix Salt Glands Young and mature stems and leaves possess numerous salt glands Bosabilidis, A.M., and Thomson, W.W. 1984. Ultrastructural differentiation of an unusual structure lining the anticlinal walls of the inner secretory cells in Tamarix salt glands. Bot. Gaz. 145(4):427-435.

71. Salt Glands Assumed salt glands secrete sodium chloride in large quantities Sodium chloride secretion has been used synonymously with salt secretion Arisz, W.H. Camphuis, J., Heikens, H. and van Tooren, A.J. 1955. The secretion of the salt glands of Imonium latifolium. Acta Bot. Nerr. 4:322-338.

72. Sodium in Halophytes The level of sodium in halophytes is low –cytoplasm is largely by-passed by sodium perhaps by transport in small vesicles Hall, J.L. and Flowers, T.J.1973. The effect of of salt on protein synthesis in the haloophyte Suaeda maritina. Planta. 110:361.

73. Sodium transport in Tamarix Most of Na transported to leaves is excreted by salt glands Na accumulates in large quantities when present in high concentration in the nutrient solution Na concentration in roots and stems is much lower than in leaves Kleinkopf, G.E., and Wallace, A. 1974. Physiological basis for salt tolerance in Tamarisd ramosissima. Plant Sci. Ltr. 3:157- 163.

74. Tamarix survival on saline soils Ions detected in high concentration in leaf tissue are also found at high concentrations in soil and water Secreted ions represent ions in the soil and solution Berry, W.L. 1970. Characteristics of salt secreted by Tamarix aphylla. American Journal of Botany 57:1226-1230.

75. Salt Secretion Bicarbonates are excreted in large amounts (60%) even when not in the soil solution –metabolically produced; requires energy Tamarix secretes actively even under low salt conditions Berry, W.L. 1970. Characteristics of salt secreted by Tamarix aphylla. American Journal of Botany 57:1226-1230.

76. Physiology a branch of biology that deals with the functions and activities of life or of living matter (as organs, tissues, or cells) and of the physical and chemical phenomena involved the organic processes and phenomena of an organism or any of its parts or of a particular bodily process Merriam-Webster Collegiate Dictionary: http://m-w.com/cgi-bin/dictionary

77. Tamarix Physiology An effective invader of riparian areas Successful competitor with native species Thank you!