Photosynthetic Patterns of Sonoran Desert Lichens II. A Multivariate Laboratory Analysis

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Flora (1982) 172: 419-426

Photosynthetic Patterns of Sonoran Desert Lichens II. A Multivariate Laboratory Analysis

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THOMAS H. NASH lIP), OTTO L. LANGE 2 ) and LUDGER KAPPEN 2 )

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Summary The gas exchange performance of two Sonoran Desert lichens, Parmelia kurokawae and Acarospora schleicheri were examined over drying curves, under 4 different light regimes at 5 different temperatures varying from 4 - 31°C. Between 40 and 130 % water content relatively uniform gas exchange rates were observed for each temperature and light combination. Gas exchange rates increased with higher light intensities. At lower light intensities there was a depression in gas exchange rate at higher temperatures due to high respiratory rates. Temperature optima varied as a function of light intensity, varying from 0 -10°C at low light intensities to about 20°C at high light intensities (500-750.uE· m- 2 • S-l). The relatively low temperature optima reflect the fact that the lichens are most active in winter, particularly in early morning hours.

Introduction In the arid interior of the Sonoran Desert over 80 species of lichens have been reported (NASH 1975). Almost all of these species are either saxicolous or terricolous. NASH et al. (1977) have demonstrated that lichen cover and biomass are much higher on north-facing slopes than south-facing slopes. In the initial paper of this series (Nash et al. 1982), it was demonstrated that the winter environment is the lichens' most favorable period for photosynthesis because of greater moisture availability from atmospheric sources during this time. Initial field photosynthetic measurements showed a strong dependence on winter precipitation periods, after which favorable moisture conditions may persist for a day or longer. It is the purpose of the present paper to examine the relationship of photosynthesis in Parmelia kurokawae HALE and Acarospora schleicheri (AeH.) MASS., two of the most common epilithic, saxicolous lichen species in the Sonoran Desert, to variation in temperature, thallus water content and light intensity, all in a multivariate context. The latter three parameters are known to be of major importance in determining lichen photosynthetic patterns (LANGE 1969,1980; KERSHAW 1972,1975).

Materials and Methods Material of the two species was collected in South Mountain Park, Phoenix, Arizona (33° 25' N, 112°01' VV), in late September, 1978, and was immediately shipped airmail to Wtirzburg. Prior to running the experiments, the thalli were placed in a temperature-controlled growth chamber, where they were exposed to 12-h-periods of alternating light (ca. 230.uE . m -2 • S -1) and darkness at 17°C for 6 d. They were moistened daily by spraying. On the 5 d prior to commencement 29 Flora, Ed. 172

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of the experiments, photosynthetic measurements on the lichen material were made under stand· ard conditions (17 ac, 230,uE . m- a • S-l) and almost exactly the same photosynthetic rate mea· surements were obtained each day, a fact indicating uniformity of response through time. Experi· ments were terminated in mid·December, two months after their initiation. Photosynthetic and dark respiratory measurements were made with a flow· through infrared gal analyzer system, which has been described in detail by LANGE (1980). Measurements were made almost simultaneously on lichen material in four cuvettes, which were submerged in a water bath for temperature control (± 0.1 ac accuracy). Outside air, averaging 330 ppm CO a and flowing at a controlled rate of 30 1· h- 1 , was passed through a water trap prior to flowing through the cuvettes. The differential in CO a concentration between measuring and reference airstreams was measured with an infrared gas analyzer (URAS, Hartmann and Braun) with a full scale sensitivity of +25···0···-25 ppm CO a. The difference between the differential signal and a zero signal (reference gas stream) was used to calculate net CO 2 exchange for the enclosed thalli. The cuvettes were illuminated with mercury high pressure lamps and the photosynthetically active irradiance was measured with a quantum sensor (Lieor). The lichen thalli (ca. 0.5 g dry weight per cuvette) and their associated rock substrates were 'loosely fastened with metal thread to plexiglass frames that fit into the cuvettes. Prior to experimentation the lichens were sprayed intermittently with deionized water over 5 min period until soakerl and then blotted to remove excess water. (Extensive soaking is as.sumed to occur rarely in the field.) Both prior and after each experimental run (ca. 50 min), the lichen and associated rock fragments were weighed. At the termination of the whole experiment, the lichen material was carefully scraped from the rock and oven·dry weight (60 ac for 24 h) measurements were separately obtained for both lichen and rock material. Both were then resprayed and a series of lichen: rock weight proportions were obtained 8:s drying occurred. These proportions were used to convert the combined lichen plus rock weight measurements during the experiment to estimates of lichen water content. Thus, the lichen water content values discussed hereafter are approximate, calculated values and not directly measured values. For each temperature gas exchange measurements were made over drying curves at light intensities of 0, 40, 125, 230, 500 and 750 ,uE . m -a . s-1, as measured within a cuvette. Light intensities below 500 ,uE . m- 2 • S-l are common values experienced by lichens on shaded north· facing exposures during winter months (NASH et al. 1982 and unpublished data). Complete replica· tion of the measurements described above were made at temperatures of 4, 10, 17, 24, and 31 ac and preliminary measurements were made at 38 ac. All of these temperatures lie within the annual temperature variation at Phoenix, which frequently ranges from -5 to +50 ac. Early daylight hoUt· temperatures during the winter months, a time of probable maximal photosynthetic activity, commonly vary between 0 and 15 ac. Prior to making measurements at any particular temperature, the lichens were always incubated at that temperature for at least 12 h in growth chambers. The experiments were run in the sequence 17, 10, 4, 24, 31 and 38 ac. After running the lower sequence of temperatures, reincubation at 17 ac lead to gas exchange measurements which essentially duplicated earlier obtained measurements at that temperature. In contrast, repeated measurements at 17 ac after the 38 ac measurements gave values of approximately 60 % of those obtained initially. Whether this decrease in gas exchange capacity reflected a real high temperature effect (MACF ARLANE & KERSHAW 1978) or simply a deterioration of the lichen material through time was not ascertained. Four replicates of each species were run for the entire experiment. Fig. 1. Gas exchange (CO a uptake and output) of Parmelia kurokawae and Acarospora 8chleicheri as a function of photosynthetically active radiation (0, 40, 125 and 230,uE . m-2 • s-l), of thallus temperature, and of thallus water content, expressed as percent of dry weight. Each value plotted represents a mean equilibrium value as measured over approximately 50 min. The 4 different symbols for each species correspond to 4 different thalli. In the case of Acarospora one specimen (open squares) exhibited higher net photosynthetic values than the other three specimens.

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Results and Discussion The magnitude of the gas exchange rates in the Parmelia species were consistently higher than those for the Acarospora species for all temperature and light intensity combinations (Fig. 1). For example, maximal net photosynthetic rates in the Parmelia for the 10-24 DC range and 230,uE . m -2 • S-1 were 4-5 mg CO 2 ' g-1 . h -1; whereas, the corresponding values in the Acarospora were 1.5-2.5 mg CO 2 ' g-1 . h- l . Likewise maximal respiratory rates in the Parmelia generally exceeded the Acarospora by a factor of two. These differences may well reflect the fact that the Parmelia has a much thinner thallus than the Acarospora and consequently the diffusion resistance to CO 2 through the thallus (see electrical analogue model of LANGE 1980) is predictably lower in the Parmelia. In addition, photosynthetic rates in the Parmelia may be high because of a relatively high algal to fungal ratio. The threshold water content for gas exchange activity is approximately 20 % (Fig. 1), a value which corresponds closely to those reported by LANGE (1969, 1980) for the Negev Desert lichen, Ramalina rnaciformis (DEL.) BORY. No measureable gas exchange activity was detected at 15 % water content or less. With the current data set, it is impossible to define precisely a moisture compensation point as done by LANGE (1980), although it occurs at approximately the same water content value. As water content increases above 20 %, gas exchange rates increase rapidly until maximal values were obtained in the range of 40-60% water content (Fig. 1). In general, the maximal values were sustained up to 120-135 % water content, the maximal water content values at which gas excha;nge measurements were made. A linear regression through the gas exchange values for this water content range generally yielded regression lines with slopes not significantly different from zero except for 17 DC where slight reductions in net photosynthesis at higher water contents were observed in the Parmelia. The water content-dependent dark respiration of these lichens clearly follows a saturation type curve, similar to that reported by LANGE (1969, 1980) for Ramalina maciformis. Addition of water to air-dried lichen material initiates dark respiratory activity. This activity increases with increasing thallus water content, a fact undoubtably resulting from the increasing gradient in CO 2 concentration from internal lichen CO 2 concentration to the outside air. The gradient increases as respiratory activity increases until saturation of the biochemical reactions in terms of hydration is reached. Thereafter the outflow of CO 2 equals internal CO 2 production and the rate of CO 2 release becomes independent of increasing water content. Other investigators, primarily using the closed cuvette system of LARSON & KERSHAW (1975) to measure gas exchange, have reported a variety of respiratory responses. In some cases a sa.turation or near saturation type curve was found, as in Stereocaulon paschale (L.) HOFFM. (KERSHAW & SMITH 1978) and in Peltigera dolichorhiza (NYL.) NYL., Pseudocyphellaria billardierii (DEL.) RAS. and Sticta caperata BORY in NYL. (SNELGAR et 301. 1980). However, in other cases continually increasing respiratory rates with increasing water content values have been reported, i.e. Cladonia spp. (LECHOWICZ & ADAMS 1974), other Pseudocyphellaria spp. and an Usnea sp. (SNELGAR et 301. 1980) and at least

Photosynthetic Patterns of Sonoran Desert Lichens. II.

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at higher temperatures of Cetraria nivalis (L.) AeH. (LARSON & KERSHAW 1975) and Peltigera spp. (KERSHAW 1977 a, b). At the present time it is not known whether the latter response had some physiological or anatomical basis (none has been suggested) or if it was simply an artifact of the procedures employed. Between 4 and 38°C the magnitude of the respiratory response generally increased with increasing temperature (Figs. 1 and 2). This pattern of increasing respiratory rates at higher temperatures is well-known and is also apparent in the data of LANGE (1980) for Ramalina maciformis, in the data of KERSHAW & SMITH (1978) for Stereocaulon tomentosum and in the data of KERSHAW (1977 a, b) for Peltigera spp. The rapid increase in net photosynthesis with increase in thallus water content (Fig. 1) at water content values above the threshold activity value is a phenomenon generally observed by all investigators, although the rapidity of this net photosynthetic increase apparently varies among species and in relation to experimental conditions. This increase also reflects a lack of saturation of the biochemical reactions with respect to hydration (LANGE 1980). Because the CO 2 gradient between the air and the phycobiont is small (LANGE 1980) net photosynthetic rates are strongly influenced by changes in inward CO 2 diffusion resistance. On the basis of a series of CO 2 concentration curves for constant water content values, SNELGAR et al. (1981) have calculated inward CO 2 diffusion resitances which correspond almost exactly to this phenomenon. Thus, their calculations show that the resistance is high at low water contents and that the resistance decreases as water content increases. Photosynthesis is, of course, known to vary nversely with resistance to inward CO 2 diffusion (see also discussion by LANGE & TENHUNEN 1981). The relative stability of net photosynthesis at values above 40-60 % water content (Fig. 1) is in general agreement with previous studies if one considers that the present study was only conducted over a limited water content range of up to 135 %. Full saturation is closer to 200 % water content (NASH unpublished), a value observed in many species, although some blue-green algae containing species do not reach saturation until 500-600 % water content is reached (AHMADJIAN 1967). It is assumed that for the water content range of 60-135 % the inward diffusion resistance to CO 2 remains essentially constant. Recent calculations of this resistance by SNELGAR et al. (1981) support this assumption in principle. At higher water contents, especially those approaching saturation, diffusion resistance is calculated to increase and. concomitantly measured net photosynthesis decreases. For some species where apparently a water film may be held over the thallus surface, the inferred resistance may be so high that net photosynthesis is reduced to zero. Slight differences in blotting procedures may lead to vastly different net photosynthetic measurements at "saturated" conditions because the resistance to CO 2 diffusion through water is far greater than through air (SNELGAR et a1. 1981). Under nonsaturated conditions inward diffusion is assumed to be primarily gaseous diffusion through intercellular spaces, but as saturation is approached these spaces become restricted and diffusion resistance increases. Calculations of SNELGAR et a1. (1981) mply that inward diffusion resistance to CO 2 varies markedly near "saturated"

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conditions among lichen species so that some species exhibit no change in net photosynthesis with increase in thallus water content beyond conditions yielding initial maximal values and other species exhibit a sharp reduction in net photosynthesis at higher water contents because of high inward diffusion resistance to 002' As temperatures increase there is an apparent depression in the net photosynthesis at low light intensities (Fig. 1). In the case of 40 pE . m- 2 • s-1 there is a relatively high, positive rate of net photosynthesis at 4 and 10 °0. However, at temperatures of 24 °0 or higher, the OOll exchange rates are negative due to the influence of high respiratory rates. Higher light intensities partially compensate for this respiratory effect. Temperature optima vary as a function of the light intensity and the species (Fig. 2). For the Parmelia the optimum varies from 4-10 °0 range at the low light intensity of 40 pE . m- 2 - S-1 to approximately 24 °0 at 750 pE . m- 2 • S-1. In contrast, the Acarospora has a temperature optimum near 10 °0 at 40 pE' m- 2 • S-1 and near 17 °0 at 750 pE . m- 2 • S-1. Furthermore, the Parmelia exhibits a much more sharply defined peak than the Acarospora. These patterns are similar to those reported by LANGE (1969) for the Negev desert lichen Ramalina maciformis, where temperature optima vary from 0-5 °0 at 1,800 Ix to 20 °0 at 48,500 Ix. Similar trends were also observed in 3 Antarctic lichens (LANGE & KAPPEN 1972), although the corresponding temperature optima occurred at lower temperatures. For 3 Oladonias from a temperate

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TEMPERATURE °C Fig. 2. Gas exchange (C0 2 uptake and output) of Parmelia kurokawae and Acarospora schleicheri in relation to thallus temperature under various levels of photosynthetically active radiation. The points plotted represent the maximum gas exchange value obtained over a range of thallus water content conditions.

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Photosynthetic Patterns of Sonoran Desert Lichens. II.

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region (Wisconsin), LECHOWICZ & ADAMS (1974) reported temperature optima of 15-25°e at light saturated conditions (ca. 600,uE· m-2 • S-1 or greater). Overall temperature optima for lichens do not vary markedly. For examp'e, at relatively high light intensities (ca. 48,000 Ix) temperature optima for Antarctic lichens are approximately 10 °e and for desert lichens are approximately 20 °e. This is remarkable in so far as temperatures vary between these habitats by much more than 10 °e. The apparent reason for the convergence of temperature optima is that the temperatures at which the lichens are photosynthesizing are not greatly different between the two habitats. Ecological Implications of the Data with Respect to Lichen Distribution Patterns in the Interior Sonoran Desert Within the interior regions of the Sonoran Desert, lichen species and biomass are strongly restricted to north-facing slopes, although a few species are found on south-facing slopes as well (NASH et al. 1977). In the first paper of this series (NASH et al. 1982), it was clearly established that the winter wet season is the most favorable time for lichen photosynthesis. Because the Sonoran Desert lies at a north latitude (Phoenix is approximately 34° N, for example), the winter sun lies at a relatively low angle, and consequently north-facing exposures are continuously shaded during daylight hours. Lichen thallus temperature measurements on north-facing slopes (NASH et al. 1982 and unpublished data) showed them to "?e approximately in equilibrium with air temperatures, whereas on sunny days lichen thallus temperatures on south-facing exposures exceeded air temperatures by 10-20 °e within the first hour after sunrise. A moist lichen on the south-facing exposure would have a short burst of high photosynthetic activity with the duration limited by the rapid drying phenomenon. A corresponding lichen on the north-facing exposure would have a prolonged period of sustained, but lower photosynthetic activity. Thus, the trade-off between the two types of exposures involves a high light intensity, dry and warm environment versus a low light intensity, wetter and cooler environment. Lichens do exist in both microhabitats, but clearly on the basis of biomass estimates (NASH et al. 1977), the north-facing exposures are the more favorable ones. Acknowledgements The senior author wishes to thank Mrs. ELLEX KILIAN and other members of Lehrstuhl fUr Botanik II der Universitiit 'Viirzburg for their assistance in the execution of the experiments. He also gratefully acknowledges the financial support of a stipendium from the ALEXANDER VON HUMBOLDT Stiftung. The other authors are grateful for continued support from the Deutsche Forschungsgemeinschaft.

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References AHMADJIAN, V. (1967): The lichen symbiosis. 'Waltham, Toronto, London: Blaisdell. KERSHAW, K. A. (1972): The relationship between moisture content and net assimilation rate of lichen thalli and its ecological significance. Can J. Bot. 50: 543-555. _ (1975): Studies on lichen-dominated systems. XIV. The comparative ecology of Alectoria nitidula and Cladina alpestris. Can. J. Bot. 53: 2608-2613. KERSHAW, K. A. (1977 a): Physiological-environmental interactions in lichens II. The pattern of net photosynthetic acclimation in Peltigera canina (L.) WILLD. var. praetextata (FLOERKE in SOMM.) HUE, and P. polydactyla (NECK.) HOFFM. New Phytol. 79: 377 - 390. (1977b): Physiological-environmental interactions in lichens III. The rate of net photosynthetic acclimation in Peltigera canina (L.) WILLD. var. praetextata (FLOERKE in SOMM.) HUE, and P. polydactyla (NECK.) HOFFM. New Phytol. 79: 391- 402. & SMITH, M. M. (1978): Studies on lichen-dominated systems. XXI. The control of seasonal rates of net photosynthesis by moisture, light, and temperature in Stereocaulon paschale. Can. J. Bot. 56: 2825-2830. LANGE, 0. L. (1969): Experimentell-6kologische Untersuchungen an Flechten der Negev-Wuste. I. CO 2 -Gaswechsel von Ramalina maciformis (DEL.) BORY unter kontrollierten Bedingungen im Laboratorium. Flora, Abt. B 158: 324-359. (1980): Moisture content and CO 2 exchange of lichens. I. Influence of tempe.rature on moisturedependent net photosynthesis and dark respiration in Ramalina maciformis. Oecologia 45: 82-87. & KAPPEN, L. (1972): Photosynthesis of lichens from Antarctica. Antarctic Res. Ser. 20:

83-95. & TENHUNEN, J. D. (1981): Moisture content and CO exchange of lichens. II. Depression of net photosynthesis in Ramalina maciformis at high water content is caused by increased thallus carbon dioxide diffusion resistance. Oecologia 51: 426-429. LARSON, D. W., & KERSHAW, K_ A. (1975): Measurement of CO 2 exchange in lichens: a new method. Can. J. Bot. 53: 1535-1541. LECHOWICZ, M. J., & ADAMS, M. S. (1974): Ecology of Cladonia lichens. II. Comparative physiological ecology of C. mitis, C. rangiferina and C. uncialis. Can. J. Bot. 52: 411- 422. MACFARLANE, J. D., & KERSHAW, K. A. (1978): Thermal sensitivity in lichens. Science 201: 739-741. NASH III, T. H. (1975): Lichens of Maricopa County, Arizona. J. Ariz. Acad. Sci. 10: 119-125. WHITE, S. L., & MARSH, J. E. (1977): Lichen and moss distribution and biomass in hot desert ecosystems. The Bryologist 80: 470-479. MOSER, T. J., BERTKE, C. C., LINK, S. 0., SIGAL, L. L., WHITE, S. L., & Fox, C. A. (1982): Photosynthetic patterns of Sonoran Desert lichens. I. Environmental considerations and preliminary field meaS\1fement~. Flora 172: 335-345. SNELOAR, \V. P., BROWN, D. R., & GREEN',. T. G. A. (1980); A provisional survey of the interaction between net photosynthetic rate, respiratory, and thallus ",