Sulfur Emissions from Roots of the Rain Forest Tree - American

Chapter 5

Sulfur Emissions from Roots of the Rain Forest Tree Stryphnodendron excelsum

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Ecosystem, Community, and Physiological Implications 1

2

2

Bruce Haines , Marilyn Black , and Charlene Bayer 1

Botany Department, University of Georgia, Athens, GA 30602 Analytical and Instrumentation Branch, Georgia Tech Research Institute, Georgia Institute of Technology, Atlanta, GA 30332

2

Roots of Stryphnodendron excelsum trees in a lowland rain forest in eastern Costa Rica emit sulfur gases. Extrapolated annual estimates of emissions, based on S. excelsum tree density, are on the order of 0.29 kg S.ha .yr . At the ecosystem level, this flux is too small to account for the 11 kg S.ha .yr . SO -S input-output discrepancy and acid rain reported earlier. At the physiological level, emission of CS is stimulated by disturbance to the roots of S. excelsum. Considering the known toxicity of CS to nematodes, root rot fungi, insects, and nitrifying bacteria we suggest that CS emission may, at the community level, be a defensive mechanism against root predators, and pathogens and a nitrogen conserving mechanism. -1

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Sulfur gas flux from living vascular plants to the atmosphere is a little studied part of the global sulfur cycle. Sulfurfluxesfromother parts of the biosphere to the atmospnere are more studied. For example, sulfur gas emissions are known from marine systems (1-6). from coastal estuarine ana marsh systems (7-16). from fresh waterfloodplainlakes (12), from temperate soils (18-20). and from tropical forests (20-22). Laboratory studies have demonstrated sulfur gas emissions from soils (23-26). from intact higher plants (27-30). and plant parts (see review by Rennenberg 21). An inventory of reduced sulfur gas emissions from soil, crops, and trees in the United States has been started (32.33.34). General reviews of the sulfur cycle are provided by Smil (25) and by Ivanov and Freney (26). From these studies, the geographic distribution of biogenic sulfur gas source strengths on a global basis and the phylogenetic distribution of sulfur gas emissions within the plant kingdom are still relatively unknown. During a survey of sulfur gas emissions from a central American rainforest (22), Stryphnodendron excelsum Harms (Mimosaceae) was found to be a sufficiently strong sulfur emitter that its location in the forest could be detected by odor. The present study attempted to quantify sulfur emissions from 5. excelsum to the atmosphere. 0

0097-6156/89/0393-0058$06.00A) 1989 American Chemical Society

Saltzman and Cooper; Biogenic Sulfur in the Environment ACS Symposium Series; American Chemical Society: Washington, DC, 1989.

5. HAINES ETAL.

Sulfur EmissionsfromRoots ofa Rain Forest Tree

59


Study Site and Methods Sampling was performed at the L a Selva Biological Station of the Organization for Tropical Studies, Puerto Viejo de Sarapiqui, Provincia Heredia, Costa Rica, 10°24-26 ' N lat, 84° 00-02 ' W long. Three S. excelsum trees ranging from 0.87 to 0.96 m dia and from 22 to 32 m in height were selected within 100 m of the laboratory to facilitate rapid processing of gas samples. Preliminary sampling suggested that roots of one of the trees extended more than 16 m from the trunk. Later sampling was performed at 4 m intervals on transects on each of the compass quadrants centered on two trees. For one tree near a forest edge, one transect line was run toward the forest interior for 16 m. A t each sampling point on each transect a 25 x 25 cm template was used to cut leaf litter a n d roots. L i t t e r was removed to a 250 m l Naleene polypropylene wide mouth centrifuge jar (Nalge Co. Rochester, N Y ) . Soil and associated roots were excavated to a depth of 10 cm and removed to the lab where they were separated by 4 mm sieves without addition of water. Dry sieving avoided the possibility of flooding and anaerobism changing the quality and amount of reduced sulfur gas emission. The total root mass was sorted by odor into sulfur emitting roots and non-emitting roots. Sulfur emitting roots were placed in 250 ml polypropylene centrifuge jars and incubated at ambient rainforest temperature. The time course of sulfur gas accumulation i n the centrifuge jars was quantified by use of a P e r k i n - E l m e r Sigma 4 B gas chromatograph (Perkin-Elmer, Norwalk, C T ) fitted with a sulfur specific flame photometric detector, a 2 mm internal dia. 9 m teflon column packed with 5% polyphenyl ether + 0.5% H P ( U on 40/60 teflon, at 90C, with 99 mis N carrier mm* . Reference hydrogen sulfide, carbon disulfide, dimethyl sulfide, and ethyl mercaptan were supplied from permeation tubes (VICI Metronics, Santa Clara, C A ) inserted into a Tracor Model 432 Tri-Perm Permeation Calibration system (Tracor, Inc., Austin, T X ) . Standards and unknown samples were pulled either from sample incubation bottles or from the permeation system to the gas chromatograph through multiposition zero dead volume sampling valves and a 2 ml teflon sample loop using a 10 m l syringe. Sample loop, valves, and connecting teflon lines were heated to 65°C to minimize surface adsorption of sulfur gases. Verification of C S as the principal sulfur gas from the roots of each of the three trees sampled in this study was performed with a Finnigan O W A 3B gas chromatograph-mass spectrograph (Finnigan Corp., Sunnyvale, C A ) . Three incubation regimes were used for sulfur emitting roots. 1) Field moist roots. A l l root samples were physically pulled from field collected soil and incubated at existing moisture conditions. 2) Vigorously washed roots. Following incubations of field moist roots,they were removed from the bottles and squeezed repeatedly under running water to dislodge adhering soil particles i n preparation for dry weight determinations. When the odor of increased sulfur emissions was noted during washing, one subset of samples was re-incubated and reanalyzed by gas chromatography to determine the magnitude of change in emission rate. 3) Gently rinsed roots. F o r another set of 12 root samples, following incubation at field moist conditions, the roots were kept i n the incubation jars and the gas was displaced by 3 changes of water i n immediate succession. This was done to determine i f wetting alone or both wetting and squeezing were required to stimulate sulfur gas emissions. Following the various incubation regimes, all roots were washed free of soil and dried to constant weight at 65°C. Dry roots were sorted into diameter 3

1

2


2

60

BIOGENIC SULFUR IN THE ENVIRONMENT

classes of 0-1.9, 2.0-4.9, 5.0-9.9 and greater than 10 mm. Means, standard deviations, and correlations were computed with the Statistical Analysis System

(28). Results Field Moist Samples. Emissions of the sulfur gases hydrogen sulfide, carbon disulfide, dimethyl sulfide + ethyl mercaptan from forest floor litter, roots, and soil calculated from the initial slopes or time course incubations are given in Table I. Rates are given for distances of 4, 8,12, and 16 m from trunks of 5. excelsum trees as g S. m^.min" . Summing outward from the tree trunk, the annual extrapolated emission rate multiplied by the areas of each successive circle (Figure 1), estimated an overall emission of 100 g S. tree^.year from a 200 area. The fractional contribution of S. excelsum trees to the stem cross sectional area (basal area) of the forest is 0.06 (22). From the extrapolated annual emission rate and the proportional contribution of S. excelsum to the cross sectional area, an annual emission of 0.29 kg S. h a ' . y r was calculated. This assumes constant emission rates instead of possible diurnal and seasonal cycling of rates. 1


1

1

1

Vigorously Washed Roots. The time courses of C S at field moist conditions and after two vigorous washings are given in Figure 2a. Results from each of the two washings are replotted i n Figures 2b and 2c synchronizing the beginnings of the re-incubations in order to facilitate comparisons of initial slopes. For this particular set of roots, CSo was detectable in 5 incubations of field moist roots, but detectable in 7 incuoations after the first wash and in 8 after the second wash. F o l l o w i n g r a p i d i n i t i a l accumulation of C S 2 , concentrations either increased more slowly, remained the same or decreased. 2

G e n t l y R i n s e d Roots. The field moist incubations showed rapid C S accumulation followed by declining concentration. C S production was not continuous. The initial slopes for the C S time courses were greater for the field moist incubations (Figure 3a) than for post-rinse incubations (Figure 3b). C S was detectable in 7 of the field moist incubations but continued in only 5 of them following rinsing.

2

2

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Root Weight and S Emission per Unit Root Weight. Dry weights of non-sulfur emitting and of sulfur emitting roots (Table II) show about the same total amount of roots but decreasing amounts of sulfur emitting roots with increasing distance away from S. excelsum trunks. The dry weights of 0-1.9 mm dia. nonsulfur emitting roots were negatively correlated (r -0.3, P < 0.049, n=36) with the dry weights of 2-4.9 mm diameter sulfiir emitting roots. We do not interpret this as evidence for allelopathy. Emission rates first calculated as g.nr forest in Table I are recalculated using individual sample root weights to give sulfur emission rates per gram root dry weight in Table III to facilitate comparison of data with data from future studies. 2

Di$cu$§iQn Results of this study have implications for ecosystem ecology, community ecology, and for physiological-evolutionary ecology. Ecosystem L e v e l . T h i s study was designed to estimate the potential roportional contribution of sulfur gas emissions from S. excelsum to the 11 g . h a ^ . y r SO4-S input-output discrepancy of the rainforest (4Q). A gas

E

1


5. HAINES ETAL.

Sulfur Emissionsfrom Roots ofa Rain Forest Tree

Table I. Potential Sulfur Emission, Mean (Standard Deviation) g S x lO* m-^min from Roots, Litter and Soil at 4 Distances from S. excelsum Trees. Sample Size = 9 at Each Distance


9

-1

Source

Distance, m

Sulfur Compound

4

8

12

16

2959(2010) 41.6(83.2)

1663(1417) 3.5(10.7)

1049(1242) 0(0)

281(416) 0(0)

0.006(0.22)

0.23(0.62)

0.18(0.49)

0.17(0.38)

0(0)

0(0)

0(0)

0(0)

3000(1981)

1666(1420)

1049(1242)

281(410)

Roots

cs,-s H S-S Litter (CH ) S-S 2

3

2

C H SH-S Soil 2

5

5

Total


61

62



Sfryphnodwdron

*

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I

j j \

j ;

!

%%

V

%

La Selva 1985-'86

* -l.57giir x 12.5m - 19.7 g 0 . 8 7 g m" x 37.7m • 33.09 0.35 gm" x 62.8m* - 34.6g 0.14 g-m-*x 87.9m • I2.9g 201 m I00.3g l

2

2

2

2

2

2

2

0.29 kg ^ 11 kg S0 -S Discrepancy 4

F i g u r e 1. E s t i m a t i o n scheme for sulfur e m i s s i o n f r o m an average Stryphnodendron tree where emissions from roots, leaf litter, and soil were sampled at 4 m intervals on transects radiating out from trunk. Emissions at each distance (Table I) were multiplied by the area of circular sampling band between that distance and the previous distance, and the emissions summed through the circular bands for the whole tree.


Sulfur Emissionsfrom Roots of a Rain Forest Tree

5. HAINES ETAL.

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Figure 2. Time course of C S - S concentrations in incubations of 5. excelsum roots. A ) time course for individual incubations (identified by numbers) starting as field moist roots and later subjected to two episodes of vigorous washing ( W ) . B ) time courses following the first washing replotted synchronizing the starting times of re-incubation. C ) replot for the second wash as in B . 2

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Figure 3. Time course of C S 2 - S gas concentrations incubations of 5. excelsum roots. A ) time courses for individual incubations starting as field moist roots then gases displaced by 3 gentle rinsings with water (W). b) time courses after washing re-drawn with starting times synchronized.



5.0(5.5)

13.4(13.4)

Total

Compound

2

2

CS -S H S-S

1.8(1.1)

1.2(0.76) 0.57(0.65) 0(0) 0(0)

5.2(23) 4.2(3.8) 3.3(3.4) 4.6(4.9) 17.3(7.8)

RS

R

8

19.8(12.5)

6.7(3.2) 4.1(2.3) 1.9(1.3) 7.1(9.0)

R

12

1.8(1.3)

1.0(0.5) 0.8(1.2)

RS

14.3(7.4)

6.4(2.6) 4.1(3.7) 1.2(2.8) 1.2(2.8)

R

1

1

8 78.7(120) 0.49(1.5)

4 63.2(53.5) 0.67(1.7)

32.3(51.2) 0(0)

12

Distance from 5. excelsum tree, m

9

30.6(40) 0(0)

16

Table III. Potential Sulfur Emissions, Mean (Standard Deviation) g S x 10" . g.Root Dry Weight" m n r . Sample Size = 9 at Each Distance

2.3(1.3) 1.6(2.4) 1.1(2.4) 0(0)

RS

4.2(2.9) 2.9(2.5) 2.0(2.1) 4.2(9.9)

R

0-1.9 2.0-4.9 5.0-9.9 > 10.0

Diameter classes, mm

4

Distance from tree, m 16

0.63(1.0)

sis

039(.49) 0.24(0.55)

RS

Table II. Root Dry Weights, Means (Standard Deviation), in Grams by Diameter Classes, and Total for Non-sulfur Emitting Roots (R) and Sulfur Emitting Roots (RS) from 25 X 25 X 10 cm Deep Soil Volumes Sampled on Transects Radiating out From 3 S. Excelsum Trees. Sample Size = 9 at Each Distance


5. HAINES ETAL.

Sulfur Emissionsfrom Roots of a Rain Forest Tree 1

65 2

emission of 11 kg S. h a ^ . y r to the atmosphere its subsequent oxidation to SO4and dilution i n rain, might explain the acid rain (41) reported for this forest (4Q). A literal interpretation of emissions estimates calculated from roots incubated at field moist conditions and extrapolated to annual estimates,then adjusted for the proportion of 5. excelsum trunk cross sectional area of the forest indicates annual emission rates of 0.29 kg S-ha^.yr . Emissions from S. excelsum may be incorrectly estimated for three reasons. First, maximum emission rates may have been missed. Emission rates were rapid at first, then declined. For individual samples, between 15 and 25 min were needed to carry the soil from the forest to the laboratory, to extract sulfur emitting roots from the soil, and to place the roots in the incubation bottles. Incubations for determining rates were usually between 5 and 10 min duration. Second, the decrease i n concentration of CS i n the headspace of the incubation jars, Figure 2, suggests that two reactions namely CS^ production and CS consumption were simultaneously in progress. A s long as production was greater than consumption, the concentration of CS^ appeared to increase. When consumption exceeds production, the concentrations appears to decrease. With both reactions in progress, the gross gas production would be the sum of the two rates. Whether CSo was simply adsorbed to the surface of the incubation vessel or was oxidized to S 0 and SO4- is unknown, thus the magnitude of the consumption rate is unknown. Potential CS emission rates may thus have been underestimated in these incubations. Third, the stimulation of gas emission from roots by washing raises the question about the effect of the passage of wetting fronts through the rainforest soil with each of the numerous rain showers. Future quantification of sulfur gas emissions from 5. excelsum roots should avoid possible mechanical damage to roots caused by their excavation from soils as in the present study. Instead, plants need to be grown in soil in containers to which simulated rainfall additions are made while sampling for sulfur gases above the soil surface. Once the relations of sulfur gas emission rates to the frequency and amounts of soil wetting are determined, these data can be coupled with a rainfall frequency and quantity model to simulate potential sulfur gas emission for S. excelsum on an annual oasis. Perhaps more important than the exact quantities of these emissions with the three sources of uncertainty, are the qualities of the sulfur emissions. Qualitatively, C S emissions have community and physiological implications. 1


2

2

2

2

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2

Community Level. Sulfur gas emissions from S. excelsum roots may influence the species composition of biological communities through actions as antibacterial, anti-fungal, anti-nematode, anti-herbivore, anti-plant (allelopathy) agents. Anti-bacterial properties of C S can inhibit nitrification, the oxidation of ammonia to nitrate (42-441 The anti-fungal properties of C S have been used to control root rot fungi in agriculture and in forestry (45-47). It is a registered fungicide and nematicide (4§). Its anti-nematode properties have been used in soil fumigation in agriculture (42). Its anti-herbivore properties have been used to kill insects in stored grains The anti-plant or allelopathic effects have not been investigated as far we know. 2

2

Physiological and Evolutionary Level. In field and pot studies Acacia pulchella roots suppressed the soil fungus Phytophthora cinnamomi and promoted the survival 01 Eucalyptus marginata trees. This fungus is an important pathogen for Eucalyptus. Investigating the Acacia-Phytophthora-Eucalyptus interaction, Whitfield et al. (51) found C S to be a major constituent of the Acacia root volatile compounds. 2


66


Carbon disulfide emissions are knownfromonly five plant species: minced leaves of Brassica oleraceae (52), intact leaves of Meaicago sativum L., Zea mays, L., Quercus lobata Nee (22) and steam distilled roots of Acacia pulchella (IDContinuation of surveys of plant species for sulfur gas emission will expand our understanding of the phylogenetic and biogeographic distribution of the sulfur emission phenomenon. The physiological controls of C S emission from plants apparently are unknown. We offer two interrelated suggestions about controls to C S emission. Removal of C S from around the roots either by extracting roots from soil (Figures 2 & 3) or by vigorous washing (Figure 2) or by gentle rinsing (Figure 3) leads to rapid C S emission followed by relatively steady concentration (Figures 2 & 3). This suggests a feedback mechanism in which lowered C S concentration at the root surface leads to rapid C S release from the root. A related control of C S release from S. excelsum roots is disturbance. In the present study the gentle disturbance of rinsing with water stimulated C ^ release (Figure 3). More vigorous washing stimulated higher rates of release (Figure 2). In the field, the odor of C S became stronger during the beginning of a rain storm. Given the toxicity of CS , to nematodes and insects and the stimulation of C S release by disturbance, we suggest that disturbance to 5. excelsum roots by root-eating nematodes and insects stimulates CS production as a defense mechanism. The emission of C S from these legumes may also be a mechanism removing excess SO4- from the rhizosphere where SO4" might otherwise inhibit the uptake of the Mo required for nitrogen fixation. Rennenberg Q l ) argues that H S emission from plants is a mechanism against excess sulfur accumulation in plants. While Rennenberg's study ( H ) dealt with H?S, emission of C S and other sulfur gases could have similar roles. Cole et al (Si) showed that SO4* can inhibit Mo uptake by algae and bacteria. Sulfur emissions from these trees may have multiple selective advantages. 2

2

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2

2

2

2

2

2

2

2

2

2

2

2

2

Acknowledgements Research supported by U.S. National Science Foundation grants BSR8104700, BSR8012093 and by U . S . D . A . Forest Service, Southeastern Forest Experimental Station, Coweeta Hydrologic Lab., Otto, North Carolina to the University of Georgia. We thank the Organization for Tropical Studies for logistical support. We thank L. Boring, D. Coleman, B. Michel, C. Monk, and M. Watwood for criticism of the manuscript. Literature on the pathological effects of C S was provided by D. Freckman, S. Garabedian and R. Gross to whom we are grateful. 2

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Journal of Geophysical Research 1982, 87(C11) 8787-93.

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Sulfur EmissionsfromRoots ofa Rain Forest Tree 67

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1352-7. 47. Filip, G . M.; Roth, L . F. Canadian Journal of Forest Research 1977, 7, 226-31.


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Sulfur Emissionsfrom Roots of a Rain Forest Tree 69

48. Carter, E. P.; Betz, D. O. Jr.; Mitchell C. T. Annotated index of registered fungicides and nematicides; their uses in the United States; Pesticides Regulation Division, Agricultural Research Service; U . S. Department of Agriculture, 1969. 49. Chandler, W. A. Plant Disease Reporter 1969, 53(1), 49-53. 50. Punj, G . K.; Girish, G . K. Journal of Stored Products Research 1969, 4, 339-42. 51. Whitfield, F. B.; Shea, S. R.; Gillen, K. J.; Shaw, K. J. Australian Journal of Downloaded by AUBURN UNIV on December 27, 2017 | http://pubs.acs.org Publication Date: April 27, 1989 | doi: 10.1021/bk-1989-0393.ch005

Botany 1981, 29, 195-208. 52. Bailey, S. D.; Bazinet, M . L.; Driscoll, J. L.; McCarthy, A . I. Journal of Food Science 1961, 26, 163-70. 53. Cole, J. J.; Howarth, R. W.; Nolan, S. S.; Marino, R. Biogeochemistry 1986, 2, 179-96. RECEIVED December 27, 1988


Sulfur Emissions from Roots of the Rain Forest Tree - American

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