CO2 fluxes of cryptogamic crusts

Transcription

1 New Phytol. (1993), 125, CO2 fluxes of cryptogamic crusts II. Response to dehydration BY D. L. JEFFRIES\ S. O. LINK' AND J. M. KLOPATEK^ ^ Division of Science and Mathematics, University of the Ozarks, Clarksville, Arkansas ^Pacific Northwest Laboratory, Richland, Washington ^Department of Botany, Arizona State U?tiversity, Tempe, Arizona , U.S.A. {Received 19 December 199; accepted 3 February 1993) SUMMARY Tlie carbon dioxide exchange of Mkrocoleus- and Scytonema-dom'mated cryptogamic crusts as related to dehydration was measured in the laboratory with a modified discrete sampling technique and infrared gas analysis. The dehydration curves predicted that carboxylation and dark respiration rates for both crust types would become zero at from 4 to 5 % water content (W) (approximately % soil saturation), with the water contents at which the rates became zero significantly lower in the second treatment cycle than the first. The dehydration curves predicted that net photosynthesis rates would become zero at "^ W (27-44 'o soil saturation), with the water contents at which the rates became zero significantly higher in the second cycle of treatment than the first. Key words: Cryptogamic crusts, CO^ exchange, dehydration, Microcoteus, Scytonema. INTRODUCTION The blue-green algae are reported to be highly resistant to desiccation (Shields, Mitchel & Drouet, 1957; Henrikson & Simu, 1971; Fogg et al., 1973; Brock, 1975), and several blue-green algae have been revived after long-term dehydration (Bristol, 1919; Lipman, 1941). Although growth resumes quickly after wetting, moisture is usually the liiniting factor in development of crusts (Shields & Durrell, 1964; Fogg et al., 1973; West & Skujins, 1977), and temperature may become limiting during the wet spring (Rychert & Skujins, 1974). The moisture optimum for most blue-green algae is 4-6% of the soil moisture-holding capacity (Stokes, 194). Brock (1975) found Microeoleus to be sensitive to water potentials below 7 bar. Round (1981) suggests that desert blue-green algal species are selected by evolution for the ability to survive desiccation, rather than the ability to metabolize in dry conditions. The vegetative thallus of many bluegreen algae is capable of surviving long periods of desiccation without akinetes or other specialized structures (Whitton, 1987). Blue-green algal-dominated cryptogamic crusts occur throughout the semi-arid western United States as well as in semi-arid locations world-wide. Mierocoleus- and Seytonema-dom'mated crusts occur in relative abundance in the shallow, sandy soils of undisturbed blackbrush communities of northern Arizona and southern Utah (Jeffries & Klopatek, 1987). West (1983) hypothesizes that the presence of crusts in blackbrush communities is due to winter moisture, and the summer convection storms probably have little effect. This study investigated the carbon dioxide fluxes associated with dehydration for blue-green algaldominated cryptogamic crusts that were typical of blackbrush communities in the Kaiparowits Basin of southern Utah. MATliIUALS AND METHODS Sample collection, carbon dioxide exchange rate measurements and experimental conditions are described in Jeffries, Link & Klopatek (1993). The two cycles of dehydration were performed twice for each crust type and are as follows. (1) c. 1 "o soil saturation treatment: crust samples were saturated with glassdistilled water equalling 2% of the air-dried weight (relative water content (W) = 25",,) of the sample (crust and soil) and maintained in a saturated state for 24 h. Samples were then allowed to air-dry slowly with the air-dried state being approximately 4% W. The second cj'cle of dehydration was initiated after 5-7 d in the air-dried state. (2) c. 5% soil saturation

2 392 D. L. Jeffries, S. O. Link andj. M. Klopatek treatment: as above, except using glass-distilled water equalling 1% of the air-dried weight (W = o) of the sample. Net photosynthesis (P^), carboxylation (/-*,.) and dark respiration {R^) are as defined in Jeffries et al. (1993). Rates of dark respiration and photosynthesis related to dehydration were estimated with the following modified Michaelis Menten equations (Thornley, 1976; Link & Nash, 1984; Matthes- Sears & Nash, 1986; Matthes-Sears, Nash & Larson, 1987): p Wc-I-(W-Wi) ' p (W Wi) ^ n. max Wc-f(W-Wi)' p _n.,,.,, (W-Wi) Wc-I-(W-Wi)'. j where R.^ ^^^^ is the estimated maximal rate of dark respiration, P^ ^^^ the estimated maximal rate of net photosynthesis, P,. max the estimated maximal rate of carboxylation, W the relative water content, Wi the value of W where R^, P^ or P^. equals zero, and We the value of W where i?,,, P,, or P^. is half maximal (Matthes-Sears et al, 1987). Wi, We, P, ^ax, ^n.max and JR, ^^^^ of different crust types and treatments were compared using confidence intervals constructed from the asymptomatic standard errors of the NLIN program (Bard 1974; SAS Institute, Inc. 1985). All computations were performed with the Statistical Analysis System software package (SAS Institute, Inc., 1985). Nonlinear parameter estimates were obtained with the SAS NLIN program using the method of Marquardt (197). The maximum rates for P^, P^ and i?^ were compared using the computer-generated confidence intervals from the NLIN program (SAS Institute, Inc., 1985) for the maximum rate of each predicted curve ''^ 2 \ O 4 o E ib) Figure 1. Means and 95 % confidence intervals for carboxylation associated with dehydration from 25 % water content for Microcoleus and (6) Scytonema crusts Michaelis-Menten equations (Table 1). RESULTS Curves for net photosynthesis and carboxylation during dehydration from 25 % W saturation were reversed, positive exponential curves, and dark respiration had reversed, negative exponential curves (Figs 1-3) The estimated maximum initial rates of carbon flux were higher and the curves were steeper for the first dehydration than the second for both crust types, except for the P,, curves for Microcoleus crusts. The initial water content of the crusts, and the air-dried state where water loss became negligible, was approximately 4% W for both types of erust. Maximum rates of carboxylation for dehydration from 25% W ranged from 767 to 155 nmol Figure 2. Means and 95 % confidence intervals for dark respiration associated with dehydration from 25% water content for Microcoleus and {h) Scytonema crusts in two dehydration cycles. Open circles represent the first Michaelis-Menten equations (Table 2).

3 fluxes of cryptogamie crusts. II Figure 3. Means and 95 % confidence intervals for net photosynthesis associated with dehydration from 25 % water content for {a) Microeoleus and {b) Scytonema crusts Michaelis-Menten equations (Table 3). CO2 m ^ s ' (Table 1). The highest value of P^ was for the first dehydration of the Scytonema crust, and the lowest was for the Microeoleus crust during the second dehydration. Estimated water contents (W) at which carboxylation rates became zero were 5-6% and 5-8 % W for Microeoleus and Scytonema crusts in the first of cycle of hydration, and 4- % and 4-4 % W for the second. Carboxylation rates of zero were reached at significantly higher water contents during 24 the first dehydration of both crust contents than the second. Maximal carbon dioxide efflux ranged from 556 to 16nnol CO2 m - s~' for dehydration from 25% W (Table 2). The general pattern of R^ was similar to those for P^. The dark respiration rate of Scytonema crust during its first dehydration was significantly higher than that during the dehydration of either crust type; the Microeoleus crust during its second dehydration was the lowest. Estimated water contents at which the dark respiration rates became zero had the same pattern as for carboxylation. The rates became zero at 5-3 % W for both Microeoleus and Scytonema crusts in the first dehydration cycle, and 4-% and 4-3 % W in the second. Again, during the first dehydration of both crusts dark respiration rates reached zero at significantly higher water contents than during the second. Estimated maximum rates of net photosynthesis for dehydration from 25% W ranged from 71 to 349 nmol CO^ m"' s~\ with significantly higher rates during the first dehydration of Scytonema crusts for the Mierocoleus crust (Table 3). Predicted water contents at which net photosynthesis rates became zero were 6-7% and 9-4% W for Microeoleus and Scytonema crusts in the first dehydration cycle, and 1-7 % and 11-2 % W for the second. The pattern for net photosynthetic rates to reach zero was the opposite of both carboxylation and dark respiration, with the second cycle having zero P,, activity at higher water contents than the first. The predicted curves and estimated water contents at which COj flux rates become zero for dehydration from 12 % W were generally similar in pattern to the equivalent portion of the curves for dehydration from 25% W, except as noted below (Figs 4 6). Exponential dehydration curves could not be fitted to the data for net photosynthesis for the first Mieroeoleus dehydration and second Seytonema crust Table 1. Parameter values of carboxylation associated with dehydration from 25 and 12% water content {W) for Microeoleus (M) and Scytonema {S) crusts in two consecutive dehydration cycles. The Prob > F and R'^ statistics are from the NLIN program of SAS {SAS Institute, Inc. 1985). Values in the same column with the same letter are not significant {P ^ -5) Crust/ cycle Wi We cmax (ninol m~ s" ) Prob > F M/1 5-6a M/2 4- be S/1 5-8a S/2 4-4 b Dehvd ration from M/l' 3-6c M/2 4-6 b S/1 S/2 5-7 a 25% W 4-4 b 7-9 ab 9-6a ll-6a 12% W 8-3 ab 5-6ab 9-9 a 92 cd 767 d 155 a 1152 be 124abed 782abcd 152ab For abbreviations in this and other tables see Materials and Methods. 27

4 394 D. L.Jeffries, S. O. Link andjf. M. Klopatek Table 2. Parameter values of dark respiration associated with dehydration from 25 and 12% water content (W) for Microcoleus (M) and Scytonema (S) crusts in two consecutive dehydration cycles. The Prob > F and R^ statistics are from the NLIN program of SAS {SAS Institute, Inc. 1985). Values in the same column with the same letter are not significant {P ^ -5) Crust/ cycle Wi We Rd.max (nmol m ^ s ') Prob > F M/1 5-3 a M/2 4- b S/1 5-3a S/2 4-3 b M/1 3-2b M/2 4-3 b S/1 S/2 5-5a 25% W 5-7a 3-2a 6- a 4-9 a 12% W 16-1 a 2-8a 4-8 a -87ab -556c -16 a -793b 7abc -484c -876ab Table 3. Parameter values of net photosynthesis associated with dehydration from 25 and 12% water content {W)for Microcoleus (M) and Scytonema (S) crusts in two dehydration cycles. The Prob > F and R'^ statistics are from the NLIN program of SAS {SAS Institute, Inc. 1985). Values in the same column with the same letter are not significantly different {P < -5) Crust/ cycle Wi We Prob > F 25 % W M/1 6-7 c M/2 1-7 abc S/1 9-4b S/2 ll-2a M/1 M/2 6-8 c S/1 2-8d S/2 5-4a 18-la 9-5 a 5-3a 12% W 36-8a -35-6a 142b 193ab 349 a 71b 768 ab 3O33ab debydration or tbe carboxylation and dark respiration rates for tbe first Scytonema debydration from 12% W. The net photosyntbesis rates for tbe first debydration from 12% W for botb crust types differ from tbat of the debydration from 25 % W in tbat neither crust had positive mean net photosynthesis rates for any water content (Tables 1~3). DISCUSSION Respiratory and photosynthetic activity for crusts of both Microcoleus and Scytonema began to diminish rapidly at about 12% water content (5% soil saturation). Rates of both carboxylation and dark respiration for both types of crust exhibited higher initial flux rates and steeper dehydration curves for tbe first treatment cycle than for the second. The first treatment cycle reached zero fluxes of carbon dioxide at water contents slightly above the air-dried state ( % W or approximately 21-23% soil saturation). The second treatment cycle had lower rates initially, but did not cease carbon dioxide activity until reaching the air-dried condition near 4% W (approximately 16 % soil saturation). In spite of this apparent 'adjustment' tbat allowed carbon dioxide activity at lower water contents, because the carboxylation rates decreased more rapidly with decreasing W than did dark respiration, the net photosynthetic rates became zero at relatively higher water contents than eitber carboxylation or dark respiration. Because the relative difference in the decreasing rates between carboxylation and dark respiration was greater in tbe second cycle, net photosynthesis reached zero and then became negative at bigher water contents in the second than in the first treatment cycle. The water contents of 1-7% W for Microcoleus and 11-2% W for Scytonema (approximately 43 % and 44 % soil saturation)

5 .2 fluxes of cryptogamic crusts. II r 2 r 6 o "5 Ec r (W 1 12 ~ -4 \ E -1 (fl '(fl (U 2 r- J I L ro o Figure 4. Means and 95 % confidence intervals for carboxylation associated with dehydration from 12% water content for Microcoleiis and (i) Scytonema crusts cycle. Fitted curves were obtained form modified Michaelis-^Menten equations (Table 1) Figure 6. Means and 95 "o confidence intervals for net photosynthesis associated with dehydration from 12% water content for Microcoleus and {b) Scytonema crusts Michaelis-Menten equations (Table 3). n 2 r- ib) ^ ^ , 1, Figure 5. Means and 95 "o confidence intervals for net photosynthesis associated with dehydration from 12% water content for Microcoleus and (b) Scytonema crusts cycle. Fitted curves were obtained from Michaelis-Menten equations (Table 2). modified for zero net photosynthesis obtained from the second dehydration cycle would tend to support the conclusions of Block (1975) and Round (1981) that even though blue-green algae are well adapted to desiccation, they are not well adapted to metabolizing under low water conditions. Net photosynthetic activity of cryptogamic crusts in a blackbrush community would apparently be greatest during the wet spritig, when soil moisture would be sustained at near soil saturation for extended periods of time, as has been suggested by West (1983). Occasional heavy summer rain storms accompanied by cooler temperatures would probably allow the crusts to experience a net carbon gain, even if some carbon was lost near the end of the drying process. Summer convection storms that deposit relatively small amounts of precipitation occur frequently in the evenings in the Kaiparowits Basin, followed by rapid drying conditions of full sunlight and high temperatures the following day. Rapid drying would reduce the amount of time the crust would be at water potentials that result in negative net photosynthesis and would ultimately reduce the amount of carbon loss. Since the crusts have a high resaturation respiration rate, slow net photosynthetic recovery after rehydration (Jeffries et al., 1993), and negative net photosynthesis at relatively high water contents, it can be concluded that they are not adapted to the moisture conditions of summer 27-2

6 396 D. L. Jeffries, S. O. Link and J. M. Klopatek convection storms. That they persist during dry years in undisturbed communities would indicate that this lack of adaptation is not fatal. It was difficult to fit exponential curves to the dehydration phenomenon from 12 % W, since that water content represented the logistic phase of the total dehydration response, and net photosynthesis was very near zero. ACKNOWLEDGEMENTS This research was supported by NORCUS (the Northwest College and University Association for Science, University of Washington) under contract DE-AM6-76-RL2225 with the U,S, Department of Energy, and by Battelle Pacific Northwest Laboratory under contract DE-AC6-76-RL183 with the U.S. Department of Energy. REFERENCES Bard Y Nonlinear parameter estimation. New York: Academic Press. Bristol MB On the retention of vitality by algae from old stored soils. New Phytotogist 18: Brock TD Effect of water potential on a Microcoleus (Cyanophyceae) from the desert crust. Journal of Ptiycology 11: Fogg GE, Stewart WDP, Fay P, Walsh AE The blue-green algae. New York: Academic Press. Henriksson E. & Simu B Nitrogen fixation by lichens. Oikos 22: Jeffries DL, Klopatek JM Effects of grazing on vegetation of the blackhrush association, jfournat of Range Management 4: Jeffries, DL, Link SP, Klopatek JM CO^ fluxes of cryptogamic crusts. I. Response to resaturation. Nezo Plivtologist 125: Link SO, Nash III TH The influence of water on CCj exchange in the lichen Parmelia praesigyiis Nyl. Oecologia 64: Lipman CB The successful revival of Nosloc commune from a herbarium specinnen eighty-seven years old. Butte/in of the Torrey Botanical Ctub 68: Marquardt DW Generalized inverses, regression, biased linear estimation and nonlinear estimation. Tectinometrics 12: Matthes-Sears U, Nash III TH A mathematical description of the net photosynthetic response to thallus water content in the lichen Rainalina menzieii. Pholosvnthetica 2; Matthes-Sears U, Nash III TH, Larson DW The ecology of Ramalina menziesii. VI. Laboratory responses of net COj exchange to moisture, temperature, and light. Canadian jfournat of Botany 65: Round FE The ecology of algae. Cambridge: Cambridge University Press. Rychert, RC, Skujins J Nitrogen fixation by blue-green algae-lichen crusts in the Great Basin Desert. Soil Science Society of Proceedings 38: SAS Institute Inc SAS user's guide: statistics, 5th edn. Cary, NC: SAS Institute Inc. Shields LM, Durrell LW Algae in relation to soil fertility. Botanicat Review 3: Shields LM, Mitchel C, Drouet F Algae- and lichenstabilized surface crusts as soil nitrogen sources. American Journal of Botany 44: Stokes JL The influence of environmental factors upon the development of algae and other microorganisms in the soil. Soil Science 49: Thornley JHM, Mathematical tnodets in ptant physiology. London: Academic Press. West NE Colorado Plateau-Mohavian blackbrush semidesert. In: West NE, ed. Temperate deserts and semi-deserts, vol. 5, Ecosystems of the world. Amsterdam: Elsevier Science. West NE, Skujins, J The nitrogen cycle in North American cold-winter semi-desert ecosystems. Oecotogia Ptantarium 12: Whitton BA Survival and dormancy of blue-green algae. In : Henis Y, ed. Survival and dormancy of microorganisms. New York; John Wiley & Sons,

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