Causes and Consequences of High Osmotic Potentials in Epiphytic Higher Plants

ARTICLE IN PRESS

Journal of Plant Physiology 161 (2004) 1119–1124

www.elsevier.de/jplph

Causes and consequences of high osmotic potentials in epiphytic higher plants

Craig E. Martina, T.-C. Linb,*, K.-C. Linc, C.-C. Hsuc, W.-L. Chiouc aDepartment of Ecology & Evolutionary Biology, University of Kansas, Lawrence, KS 66045, USA bDepartment of Geography, National Changhua University of Education, 1 Jin-de Road, Changhua 500, Taiwan, ROC cTaiwan Forestry Research Institute, 53 Nan-hai Road, Taipei 100, Taiwan, ROC Received 21 November 2003; accepted 28 January 2004

KEYWORDS Summary Drought stress; Past reports of the water relations of epiphytes, particularly bromeliads, indicate that Epiphytes; tissue osmotic potentials in these tropical and subtropical plants are very high (close Ferns; to zero) and are similar to values for aquatic plants. This is puzzling because several Lycophytes; ecophysiological studies have revealed a high degree of drought stress tolerance in Orchids; some of these epiphytes. The goal of this study was two-fold: (1) to increase the Osmotic potential; number of epiphytic taxa sampled for tissue osmotic potentials; and (2) to explain the Photosynthesis; apparent discrepancy in the signiﬁcance of the tissue water relations and tolerance of Stomata; drought stress in epiphytes. Tissue osmotic potentials of 30 species of epiphytic ferns, Taiwan; lycophytes, and orchids were measured in a subtropical rain forest in northeastern Transpiration; Taiwan. Nearly all values were less negative than –1.0 MPa, in line with all previous Water relations; data for epiphytes. It is argued that such high osmotic potentials, indicative of low Water-storage parench- solute concentrations, are the result of environmental constraints of the epiphytic yma habitat on productivity of these plants, and that low rates of photosynthesis and transpiration delay the onset of turgor loss in the tissues of epiphytes such that they appear to be very drought-stress tolerant. Maintenance of photosynthetic activity long into drought periods is ascribed to low rates of transpiration and, hence, delayed tissue desiccation, and hydration of the photosynthetic tissue at the expense of water from the water-storage parenchyma. & 2004 Elsevier GmbH. All rights reserved.

Introduction osmotic potentials are adaptive in two ways. First, as tissue water potential declines during a drought, A common adaptation of plants tolerant of drought a low osmotic potential allows for the maintenance stress is a highly negative tissue osmotic potential of non-zero cell turgor pressures, i.e., avoidance of (Larcher, 1995, Lambers et al., 1998). Such low plasmolysis, for a longer period into the drought,

*Corresponding author. E-mail address: [email protected] (T.-C. Lin).

1120 C.E. Martin et al. relative to a plant with a high (less negative) found in aquatic plants (Larcher, 1995; Lambers osmotic potential. Second, a highly negative water et al., 1998) and are difficult to reconcile with the potential allows a plant to harvest water from soils results of the above studies on epiphyte responses with low water potentials. Of course, these two to drought (also see discussions in Benzing (1990) adaptive features are closely interrelated. and Zotz and Hietz (2001)). On the other hand, this Epiphytic higher plants are typically found in potential discrepancy might reflect an artifact of subtropical and tropical forests (Benzing, 1990). sampling, as osmotic potentials have been mea- Despite the generally moist nature of these sured in relatively few epiphytic species. environments, the microsites occupied by epi- Thus, there were two goals of this study: (1) to phytes are frequently subjected to localized determine if high tissue osmotic potentials are droughts between rainfall events (Richards, 1952, characteristic of most epiphytes or if such high Gessner, 1956, Withner, 1959). Because many values are limited to those taxa previously epiphytes typically lack soil or another external sampled; and (2) to explain the apparent discre- source of water, drought stress is reportedly quite pancy between the reported drought stress resis- common in spite of high annual precipitation in the tance and high osmotic potentials in at least some habitats of these plants (Sinclair, 1983, Kluge et al., epiphytic taxa. To address the first goal, tissue 1989a, b, Benzing, 1990). Potentially exacerbating osmotic potentials were measured in 30 species of this problem, many epiphytes, e.g., most orchids, epiphytes in a subtropical rain forest in north- ferns, and ‘‘atmospheric’’ species of Tillandsia, eastern Taiwan. Included were four species of lack morphological features that trap or store lycophytes, 17 species of ferns, and nine species water for use during drought periods (Benzing, of orchids. 1990; Martin, 1994). Therefore, it is not surprising that many epiphytes are thought to be considerably tolerant of drought stress. As an example, two investigations (Benzing and Dahle, 1971; Nowak Materials and methods and Martin, 1997) of the morphological and physiological responses to drought in the epiphytic Study site and plants bromeliad Tillandsia ionantha reported positive rates of photosynthesis after months of desicca- The study site was a subtropical forest at 600 m tion. Benzing and Dahle (1971) even referred to this elevation in the Fushan Experimental Forest in epiphyte as nearly poikilohydric in light of their northeastern Taiwan (longitude 1211340 E, latitude findings. In another study of an epiphytic bromeliad 241460 N). Plants (see Table 1 for list of species) with Crassulacean acid metabolism, withholding were selected in a partially disturbed section of the water for a month reduced but did not eliminate forest to allow easy accessibility for collection of nocturnal CO2 uptake in Tillandsia utriculata (Stiles leaves. The study site included several walking and Martin, 1996). Similar findings have been trails and was several hundred meters from the reported for other epiphytic bromeliads (Kluge laboratory building. Species of dominant trees at et al., 1973; Martin and Siedow, 1981; Adams and this site were numerous, primarily in the families Martin, 1986; Martin and Adams, 1987; Griffiths Fagaceae and Lauraceae; examples include Litsea et al., 1989; Martin and Schmitt, 1989) and orchids acuminata (Bl.) Kurata (Lauraceae), Machilus zui- (Sinclair, 1983, Goh and Kluge, 1989). In contrast, hoensis Hayata (Lauraceae), Castanopsis cuspidata some epiphytes, including three ferns in the genus (Thunb. ex Murray) Schottky var. carlesii (Hemsl.) Pyrrosia (Sinclair, 1983; Kluge et al., 1989a, b; Yamazaki (Fagaceae), and Pasania hancei (Benth.) noteFthe genus Drymoglossum is now considered Schottky (Fagaceae). Climatic conditions at the the same as Pyrrosia (Hovenkamp, 1986)) and three Fushan site are subtropical, with monthly average orchids (Sinclair, 1983), are reportedly much less air temperatures ranging from 101Cto251C and resistant to drought stress. monthly rainfall ranging from less than 10 cm to In spite of the drought-tolerant nature of many over 50 cm, with maxima occurring in the summer epiphytes, especially bromeliads, several studies months. During the time of measurements in this indicate that tissue osmotic potentials in these study (16–23 June 2001), local environmental plants are surprisingly high, usually less negative conditions were: average air temperature of than –1.0 MPa (Harris, 1918; Gessner, 1956; Biebl, 23.41C (minimum 20.51C, maximum 27.91C), aver- 1964; Sinclair, 1983; Smith and Luttge,. 1985; age air relative humidities over 80%, and average Griffiths et al., 1986; Luttge. et al., 1986; Smith daily wind speeds from 1.3 to 3.5 m sÀ1 (maxima et al., 1986; Martin, 1994; Zotz and Andrade, ranged from 5.4 to 12.3 m sÀ1). Most days were 1998). Such high osmotic potentials are typically intermittently cloudy without precipitation, ARTICLE IN PRESS

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Table 1. Mean (standard deviations in parentheses; N ¼ although 4.6 cm of rain fell during the month of 5 plants for individual species, unless otherwise noted) June 2001. osmotic potentials (Cp) of leaves of epiphytic lycophytes, ferns, and orchids collected in a subtropical rain forest in northeastern Taiwan. Tissue osmotic potential

Species Wp; (MPa) Leaves of epiphytes low in the canopy were Lycophytes collected by hand or by using extensible clippers Lycopodium fordii Baker À1.06 (0.07)a for plants higher in the canopy. Within 15 min of Lycopodium serratum Thunb. –1.02 (0.18) detachment, four 1.2-cm diameter disks were Selaginella delicatula (Desv.) Alston –0.99 (0.23) punched from the middle of a mature leaf of Selaginella doederleinii Hieron . –1.05 (0.18) average length and frozen at –101C in a refrigerator All lycophytes (4 species; 19 –1.03 (0.17) freezer. After at least 24 h, the disks were thawed, individuals) then pressed in a vice until a filter paper disk was saturated with the expressed liquid. The osmotic Ferns potential of this liquid was then measured with a Asplenium antiquum Makino –0.94 (0.12) Wescor (Logan, UT) Model 5500 Vapor Pressure Asplenium cuneatiforme H. Christ –1.01 (0.17) Asplenium neolaserpitiifolium –0.81 (0.16) Osmometer, using standards of known osmotic Tardieu et Ching potentials for calibration. Davallia mariesii T. Moore ex Baker –1.49 (0.16) Elaphoglossum yoshinagae (Yatabe) –1.10 (0.12) Statistical analysis Makino Lemmaphyllum microphyllum C. Presl –0.58 (0.05) Osmotic potential means of all taxa, including Lepisorus monilisorus (Hayata) –0.96 (0.14) the overall means of the three plant groups Tagawa (lycophytes, ferns, and orchids), were compared Loxogramme salicifolia (Makino) –1.14 (0.18) Makino using a nested analysis of variance (Sokal and Rohlf, Microsorium buergerianum (Miq.) –1.08 (0.21) 1981). Statistically significant differences were Ching inferred when Pp0:05: Ophioderma pendula (L.) C. Presl –0.72 (0.09) Polypodium formosanum Baker –1.15 (0.27) Pseudodrynaria coronans (Wall. ex –1.00 (0.22) Mett.) Ching Results and discussion Psilotum nudum (L.) Beauv. –1.11 (0.21) Pyrrosia lingua (Thunb.) Farw. –0.83 (0.11) The addition of 30 species of ferns, lycophytes, and Vittaria anguste-elongata Hayata –0.84 (0.07) orchids (Table 1) to previous data strengthens the Vittaria flexuosa Fee –0.98 (0.15) generalization that the tissue osmotic potentials of Vittaria zosterifolia Willd. –0.74 (0.06) epiphytes in general are very high (close to zero). All ferns (17 species; 85 individuals) –0.97 (0.25) Furthermore, small differences exist among the different groups of epiphytes, with highest values Orchids a in the orchids, also found by Harris (1918). A study Bulbophyllum japonicum (Makino) –0.52 (0.03) of particular interest includes a comparison of the Makino water relations of the epiphytic and terrestrial Bulbophyllum melanoglossum Hayata –0.53 (0.05)a Bulbophyllum retusiusculum Rchb. f. –0.45 (0.04) forms of five hemiepiphytic species by Holbrook Dendrobium chameleon Ames –0.90 (0.33) and Putz (1996). The osmotic potentials of epiphy- Eria ovata Lindl. –0.50 (0.02) tic plants were higher than those of terrestrial Eria tomentosiflora Hayata –0.54 (0.03) plants of the same species. The high tissue osmotic Haraella retrocalla (Hayata) Kudo –0.55b potentials characteristic of epiphytes are com- Liparis bootanensis Griff. –0.56 (0.06) monly found in hydrophytic, not xerophytic, plants Pholidota cantonensis Rolfe –0.94 (0.12) (Larcher, 1995; Lambers et al., 1998). As is the case All orchids (9 species; 39 individuals) –0.62 (0.21) with many aquatics, epiphytes are, therefore, The group means are significantly different (P ¼ 0:0005), as are incapable of sustaining tissue water potentials many of the means of individual species. much below –1.0 MPa without cell plasmolysis and aN ¼ 4: probable death of the plants. Based solely on this b N ¼ 1: finding, one would predict that epiphytes are incapable of tolerating even low levels of drought stress. Although it is feasible that osmotic adjustment, resulting in lower osmotic potentials during ARTICLE IN PRESS

1122 C.E. Martin et al. drought stress, could increase the resistance of facilitating water absorption from rainwater/stem- these plants to drought stress, past reports of flow/throughfall (see also Zotz and Hietz (2001)). osmotic adjustment indicate that drought-induced The other adaptive feature of low osmotic poten- decreases in osmotic potentials in epiphytic bro- tials discussed in the introduction, that of main- meliads amount to only several tenths of a MPa taining high turgor pressures long into a drought (Griffiths et al., 1986; Smith, 1989; Martin, 1994; period, is obviously lacking in epiphytes. This Stiles and Martin, 1996; Nowak and Martin, 1997). problem is addressed below. Thus, even after substantial levels of osmotic The apparent contradiction between the xero- adjustment, the osmotic potentials of epiphytes phytic nature of epiphytes based on their photo- remain near À1.0 MPa. synthetic responses to drought (see above) and The results of this study raise two intriguing their hydrophytic nature based on their high questions. One, why are the osmotic potentials of osmotic potentials can be resolved by consideration epiphytes so high, similar to those of aquatic of their low gas exchange rates (Adams and Martin, plants, yet these plants grow in drought-prone 1986; Martin, 1994; Stuntz and Zotz, 2001) and microenvironments, unlike aquatic plants? Two, some common morphological features that main- how can these plants tolerate droughts, even tain hydration of the photosynthetic tissue during severe tissue desiccation in some cases, with such droughts (also see discussions in Benzing (1990) and high osmotic potentials? Zotz and Hietz (2001)). One likely explanation for The low solute content of epiphytic tissues may the low gas exchange rates, besides a potentially simply reflect their low productivity. Most, but not reduced photosynthetic capacity, is a low leaf all, of the solutes that effect plant osmotic conductance resulting from very low stomatal potentials are presumably carbon-based com- densities of the leaf epidermis (Holbrook and Putz, pounds. Because the photosynthetic productivity 1996; Martin, 1994). Thus, although epiphytes have of most epiphytes is low (Martin, 1994; Stuntz and a very limited range of water potentials over which Zotz, 2001), it is not surprising that their solute non-zero turgor can be maintained during a drought content is also low. Another possible explanation (approximately 0 to –1.0 MPa), their low transpira- for the low solute content of epiphytes, as tion rates ensure that tissue desiccation proceeds suggested by Benzing (1990), is low tissue elemen- slowly and, thus, that cell turgor is maintained for tal concentrations resulting from limited elemental long periods of drought. Another adaptive feature availability in the epiphytic habitat. Although the of many epiphytes that prolongs the maintenance data are scarce, this explanation is supported in of physiological activity during droughts is an part by comparisons of tissue elemental concentra- abundance of water-storage parenchyma (‘‘hy- tions in the epiphytic bromeliad Tillandsia pauci- drenchyma’’) in the leaf tissues (Tomlinson, 1969; folia and those in terrestrial plants (Benzing and Kaul, 1977; Benzing, 1990; Loeschen et al., 1993). Davidson, 1979; Benzing, 1990). On the other hand, Water from the hydrenchyma appears to be either elemental concentrations in tissues of Tillandsia preferentially lost during droughts or is ‘‘translo- usneoides were similar to those of terrestrial taxa cated’’ to the photosynthetic tissue (‘‘chlorenchy- (compare data in Shacklette and Connor (1973) ma’’), keeping it hydrated, during long periods of with data in Salisbury and Ross (1992)). Clearly, drought (Schmidt and Kaiser, 1987; Nowak and more data are needed before generalizations about Martin, 1997). In addition, other morphological elemental nutrient concentrations in epiphytes can features (see Benzing, 1990), including highly be made. elastic cell walls (Stiles and Martin, 1996), may be Given the reported frequency of potential important in maintaining metabolic activity as drought stress in the microenvironment of epi- water is lost during periods of drought. phytes, their high osmotic potentials should be Benzing (1990) has suggested that one potential maladaptive. As stated in the introduction, low advantage of high osmotic potentials in epiphytes osmotic potentials prove adaptive for plants in arid might be water conservation resulting in stomatal environments by allowing the extraction of water closure early in a drought, as a result of a rapid from soils having low water potentials. In contrast decline in tissue water potential. Although this with terrestrial plants, epiphytes obtain their explanation might apply to some epiphytes, e.g., water solely from rainfall, or actually stemflow those that exhibit rapid decreases in photosyn- and throughfall, both of which are very dilute in thetic activity when droughted (Sinclair, 1983; solute content, with water potentials close to zero Kluge et al., 1989a, b), it does not apply to many (calculated from data in Benzing and Renfrow epiphytes that appear resistant to drought stress (1980) and Junk and Furch (1985)). Thus, high (Benzing and Dahle, 1971; Kluge et al., 1973; osmotic potentials in epiphytes are still effective in Martin and Siedow, 1981; Sinclair, 1983; Martin and ARTICLE IN PRESS

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