Seasonal distribution and abundance of fungi in two desert grassland communities

Journal of Arid Environments (1979) 2, 295-312

Seasonal distribution and abundance of fungi in two desert grassland communities

Elsa C. Taylor* Seasonal variation in soil mycoflora from hillside and valley sites was determined from samples isolated by soil-baiting and dilution-plate techniques. Of 84 species from baits and 47 species from dilution plates, 79 and 45 respectively showed seasonal patterns of presence-absence, while 5 and 2 respectively were continuously present and exhibited differential habitat abundance. Results are related to within-habitat differences and to yearly variation in the physical environment.

Introduction Over the years there has been an increasing body of literature on desert soil fungi (Friedman & Galun, 1974) from a variety of desert types throughout the world. Most of this work can be divided into two categories: that examining fungi present at a particular site (Durrell & Shields, 1960; Kuehn, 1960) and that comparing fungi over a range of sites in a larger geographical area (Nour, 1956; Borut, 1960; Ranzoni, 1968; Ali, Batanouny & Salama, 1975; Ismail & Abdullah, 1977; States, 1978). However, desert fungi generally have not been studied seasonally, despite the pronounced variations in seasonal climates of most deserts. In contrast, seasonal activity (growth, abundance and diversity) of soil fungi in other ecosystems has been demonstrated in terms of both organism density (Mohling Ma, 1933; Thornton, 1956; England & Rice, 1957; Virzo de Santo, 1978) and species abundance (Warcup, 1957; Katz & Lieth, 1974; Mabee & Carner, 1974; Couehenaur, 1978; l\1oubasher & Abdcl-Hafen, 1978). Deserts, therefore, might also be expected to show seasonal variation in fungal activity. Community change in a desert ecosystem is probably subject more to control by the physical environment than by biotic interactions (Connell, 1976). Since periods of moderate temperature, abundant rainfall and nutrient availability rarely coincide in deserts, each of these factors may be highly influential at different times. It is difficult to sort out their effects and to determine which exert dominant control over a soil fungal community at any given time. This paper describes seasonal activity in soil fungal communities in a North American desert grassland, and also considers how the physical environment might control seasonal fluctuations in their abundance and diversity. • Department of Biology, The University of New Mexico, Albuquerque, New Mexico 87131, U.S.A. 0140-1963/79/040295 + 18 $02.00/0 20

© 1979 Academic Pres8 Inc. (London) Limited

E. C. TAYLOR

296

Methods Study sites

Sites chosen for this study were located on and below the volcanic escarpment immediately northwest of Albuquerque, New Mexico. Two sites, each approximately 1·3x 8 m were chosen for comparison. One, hereafter termed 'valley' was located approximately 5 m below the escarpment base. The other, hereafter termed 'hillside' was located approximately 7 m above the escarpment base and 12 m from the valley site. The level valley site is sparsely covered by Oryzopsis bunchgrass, relatively few forbes, and a scattering of medium-sized rocks. A relatively homogeneous habitat, its soil microcommunities (as defined by Dindal, 1973) are therefore greatly exposed to direct effects of weather. In addition, its soil is low in nutrients and moisture-holding capacity, and has a high pH (Table 1). The hillside site, which has a southeastern exposure, is covered by large, dark basalt boulders interspersed with a mixture of small shrubs (mainly Gutierrezia sarothrae) and low-growing grasses. The vegetation and boulders on this site, in addition to offering greater protection to soil microcommunities, also provide a greater variety of microhabitats for fungi to colonize. The hillside also has greater moisture-holding capacity, larger amounts of organic matter and a less alkaline pH (Table 1). This is a hot-summer, cold-winter desert (see Fig. 1). Winter snowfall contributes to soil moisture in early spring. Warm, dry conditions in late spring and early summer last until the onset of annual summer rains. 40

140

35

I

."

25

~ 20 Q. E

~

:.< 15

0

\

J

/-"

-

10 5

/",-

/ -\ \\ / "\ / -

30 ~

120

0

F

100

eo E

5 c;

60~

.

'0.

G

40 Q: 20

-

10 0

Figure 1. Climatological data for Albuquerque, N.M. from 1977 Comparative Climatic Data, U.S. Department of Commerce, NOAA (means for 30 years). - A - , Mean maximum air temperature; -e-, mean air temperature; _, precipitation, 1978; 0, incubation temperature.

Physical environment In order to determine the degree of within-site and between-site microhabitat variation, a total of 40 soil samples was collected (20 from the valley and 20 from the hillside) in November 1977 and analyzed for (1) per cent rocks, sticks, sand, silt and clay (Lamott Soil Texture Kit no. 1067); (2) wilting point and field capacity (Pressure Membrane Extractor, Soil Moisture Equipment Company); (3) per cent nitrogen (N) (semi-micro-Kjeldahl

P 1'04 ( ± 0'099) 1'69 (± 0'455) 0·05

14'75 (± 1-399) 8·937 (± 3-645) 0'05

t Sample size =

- Sample size = 20 samples/site. 10 samples/site.

Sticks (%)t

Rocks (%)t

Silt (%)t

16·35 (± 1-068) 14·37 (± 2-10) >0·1

Sand (%)t

65'53 (± 1-697) 72'34 (±4'471) 0·05

0·557 (± 2·04 x IO- Z) 1'27 (± 10'0 x 10- 2 ) <0'001

3'44 x 10-1 (± 9·19 x 10-f ) 6'98 x 10-1 (± 5·49 x 10-3) <0·001

7·72 (±0'176) 20·57 (± 2'074) <0·001

3'73 (±0'452) 5·58 (±0·304) 0'005

Valley Hillside p

Valley Hillside

Carbon (%)-

Nitrogen ('Yo)-

Field capacity ('Yo)-

Wilting point ('Yo)-

error

2·45 (± 0,257) 2·67 (± 0'41) >0·1

Clay (%)t

7'851 (± 1·34 x 10-2 ) 7'7 (± 2·19 x 10- 1 ) <0'001

pHt

Table 1. Microhabitat analysis. Wilting point determined at -15 bars; field capacity at -1/3 bar. Values are means ± one standard

E. C. TAYLOR

298

method, ([Bremner, 1960]); (4) per cent carbon (C) (Chapman & Pratt, 1961); and (5) pH. Mean percentages were compared using a two-tailed t-test. Seasonal variation in nutrient availability and pH at both sites was determined by analysis of soil samples collected at the time baits (see below) were collected. In addition to carbon and nitrogen, percentages of phosphorous and potassium were determined using a La Mott Soil Test Kit no. 5679. Measurements used in computing mean soil temperatures were based upon data obtained at sampling times and from data previously collected (C. S. Crawford, personal communication). Precipitation data are from NOAA Climatological Data (1978). Field methods

Since the main purpose of this study was to determine what fungi were actually growing during various seasons of the year, the main method employed was that of soil baiting. Sample packets consisted of a bait embedded within soil inside a screen envelope (Fig. 2).

Screen envelope

metal frame } filter paper

BOlt

nylon acetate Soil

............ Icm

Figure 2. Sample packet used in soil bai ting,

Baits were metal frames, 5 x 7 em, covered with nylon acetate to provide a biologically inert substrate for colonization (Parkinson, Gray & Williams, 1971). A strip of Whatman no. 1 filter paper was stapled to half of one side of each bait as a carbon source for cellulolytic fungi. Envelopes were made of metal screen (mesh size 144 cm- 2 ) that excluded all microfauna larger than mites and collembola. Bait within envelopes was surrounded on all sides by 0·5 cm of sterile soil. Each packet was assembled, autoclaved at 220°C, 20 psi for 20 min, then dried at 160 °C for 48 h to insure sterilization and subsequent removal of moisture. I anticipated that by this method only fungi which grew through the screen and onto the bait would be isolated. Four bait packets (the largest number of manageable samples) were buried at each site for the following l-rnonth periods during 1978: 10 January-lO February, 13 May-17 June, 1 August-7 September and 7 September-l0 October. Acquisition offungi was maximized by situating the top of each bait flush with the soil surface (Warcup, 1951). Bait placement maximized the range of microhabitats sampled (base of shrub; base of grass; soil next to large rocks or boulders; soil in open, vegetation-free area), yet insured sampling of the same range of microhabitats each season. The second method of isolation, the soil dilution plate (Warcup, 1960, 1967), utilized soil collected each time baits were removed. Eight samples (approximately 10 g each) of soil from the top 5 em were taken from each site (again maximizing microhabitats sampled) and mixed thoroughly for dilution plates and measurement of physical factors. Laboratory methods

Bait packets were collected in the morning and plated out the same afternoon. Baits were removed from screen envelopes, cut from the frame, quartered and placed in large (150 x

FUNGI IN TWO DESERT COMMUNITIES

299

25 mm) petri dishes. All equipment for this procedure was sterilized in 70 per cent alcohol. Quartering enhanced ease of colony isolation and increased the number of isolated colonies by one-fourth to one-third over those isolated from uncut baits. For January, May and August a 1 : 10 dilution from 10 g of soil was used. In September the first plates showed such intense crowding that a 1 : 100 dilution was employed. For each sample 1 ml of dilution was raised to 10 ml with distilled water, poured into large petri dishes, and covered with molten agar which was then swirled to provide an even distribution of spores (Warcup, 1951). The principal agar used was Czapek-Dox (BBL) with the addition ofO'S per cent carboxymethylcellulose (Hankin & Anagnostakis, 1977) for cellulolytic fungi, together with 1 : 30,000 rose bengal and 1 : 15,000 streptomycin (Martin, 1950) to decrease bacterial growth. pH was adjusted to the mean pooled soil-sample pH for that month. Cooled agar was poured over the baits, which were incubated in environmental chambers at the mean soil habitat temperature for the month during which bait colonization had occurred. Colonies were isolated as they appeared for 6 weeks, then further incubated until sporulation occurred. For colonies which failed to sporulate on Czapek-Dox agar, potato dextrose (BBL) and malt extract (BBL) agars were used. Colonies failing to sporulate on any of these media were considered sterile. Major taxonomic works used for identification were: Raper & Thorn (1949); Raper & Fennell (1965); Barron (1968); Toussoun & Nelson (1968); Booth (1971); Gilman (1971); and Barnett & Hunter (1972).

Statistical analysis of fungal samples The following indices of diversity were employed to test for significant differences between fungal communities found on the hillside and in the valley during a given month and during the season: (1) Shannon's index of species diversity (Zar, 1974) which estimates community richness as k

H= -LPilogpj' i=1

where Pi = proportion of species i in sample, and k = species, and the corresponding test for evenness H H m nx

]=--, where H mnx = maximum possible diversity, was determined from the data at each site for each season. (2) Coefficient of community (Pileu, 1976) (hereafter termed ICC') which estimates species overlap between communities based on presence or absence of species as

where Sz and SIJ = number of species in samples X and Y, and S%IJ = number of species common to both samples. If the same species are found in both samples, then CC= 100.

300

E. C. TAYLOR

(3) Percent similarity (Pileu, 1976) (hereafter termed PS) which estimates the similarity in the relative abundance of species between samples as

. (Xi Z' YZi)

PS= 200~mm

where Xi and Y j = quantities of speciesj in samples X and Y, andZ = total individuals from all species in both samples. If all species are evenly divided between samples, then PS = 100. In comparing species from baits with those from dilution plates, only CC was used. Statistical comparisons utilized genera except where classification to species was possible (e.g. Aspergillus, Fusarium) or where species could be distinguished (e.g. Phoma 1,2,4). In order to facilitate discussion the term 'species' will be used for genera which have been identified to species level and for those which have not. Results

Physical environment Microhabitat analysis (Table 1) revealed the hillside to have a generally greater range of microhabitat variation than the valley. Water-holding potential, reflected both in wilting point and field capacity, was significantly greater on the hillside. As expected for desert soils, Nand C levels were low at both sites; hillside values were more than twice those of the valley. Both sites were alkaline, although the hillside was less so. Differences between the two sites in percentages of rocks, sticks, sand, silt and clay were not statistically significant; however, the hillside consistently showed greater microhabitat variation (as reflected by standard error). Seasonal variation (Table 2) was evident in the total abundance of nutrients. Levels of C and N were highest and lowest, respectively, in January. Between-site variation also occurred on a seasonal basis. Carbon levels fluctuated greatly in the valley, while on the hillside greatest nutrient fluctuation was seen in abundance of N. Phosphorus and potassium showed a pattern of low winter, high spring-summer availability. Most of the precipitation for January was due to snowfall. Temperatures listed in Table 2 were those used in plate incubation and reflected means of those to which fungi were exposed for the month of bait colonizing. Comparisons made between incubation temperatures and mean daily maximum and minimum soil temperatures as recorded by the nearest appropriate weather station (Los Lunas, New Mexico) showed that the former were realistic approximations of habitat temperatures.

Speciesisolated A total of 5506 colonies was isolated and identified during the course of this study, 4744 from baits and 762 from soil dilution plates. From these, 84 species were isolated from baits and 47 species from soil dilution plates. Of the bait isolates, 49 species comprising 97 per cent of the colonies were included in Appendix I. * Twelve species produced 62 per cent of the colonies, while 72 species accounted for the remaining 38 per cent. Of the dilution plate isolates, 32 species, comprising 98 per cent of the colonies were included in Appendix 11.* Fifteen species comprised 82 per cent of the dilution plate colonies; 32 species comprised the remaining 18 per cent. Spore count averaged 2·44 x 1()3 g-l of soil, which is within the range found for similar deserts (Cameron, 1969). Comparisons of the percentage of species for each month which fell into major taxa (Figs 3 and 4) indicated wide seasonal and between-site variation for the baits except for August, when both sites were relatively similar. For soil dilutions variations were not as striking, with August and September in the valley showing very similar results. Comparisons of both bait and soil dilution results indicated that the Moniliaceae was the dominant group • A complete list is available from the author.

January May August September

January May August September

Valley

Hillside

41·63 10·64 8·05 10·64

4'1 X 10-1 (± H x 10-7) 6·42 x 10-1 (± 1·8 x 10-7) 4·72 X 10-1 (± 1·6 x 10-8) 4'22 X 10-1 (± 1·6 x 10-8) 3'90 X 10-1 (± 6·4 x 10-8) 7·44 X 10-1 (± 3'0 x 10-7) 9·65 x 10-1 ( ± 1·6 x 10-1) 7·07 X 10-1 (± 9'4 x 10-8 )

1'707 (± 1·2 x 10-3 ) 0·683 ( ± 0'0) 0·3795 (± 2·2 x 10-3 ) 0'4485 (± 1'3 x 10-4)

1·609 (± 2·2 x 10-3) 0·805 (± 1·7 x 10-3) H21 (±O'O) 0·8265 (± 8·9 x 10-8)

t Sample size J:: 1 data pointj16 pooled samples/month.

41'26 10'83 11-62 11'70

C/N

Nitrogen (%)*

Carbon (%)*

• Sample size ee 2 data pointsj8 pooled samples/site/month.

Month

Area

Med.-Iow Very high High High

Med.-Iow Very high Medium High

Potassium"

High Very high Very high Very high

High Very high Very high Very high

Phosphorus *

8'43 7'65 7·6 7·9

pHt

Table 2. Seasonal variation in physical environment. Values are means ± one standard error

15±2 35 ±2 30±2 25 ±2

COC)

Temp.

159'3 7·6 63·2 15·0

(rom)

Precipitation

302

E. C. TAYLOR 90r---------------,-----------------, 80 _ 70

.,

u

~o 60

~ 50

J

MAS Month (Volley)

J

MAS Month (Hillside)

Figure 3. Percentage of colonies in major taxa isolated from baits. lID = Moniliaceae, Tuberculariaceae; • = Dematiaceae, Sphaeropsidales, Mycelia sterilia; Eil = Phycomycetes; 0 = Ascomycetes, Stilbaceae. 100 90 80 --o 70

.,

~

.!!

60

~ 50

.~

c o

40

830 20 10

J

MAS Month (Volley)

J

MAS Month (Hillside)

Figure 4. Percentage of colonies in major taxa isolated from soil dilution plates. lID = Monliaceae, Tuberculariaceae; • = Dematiaceae, Sphaeropsidales, Mycelia Sterilia; Ea = Phycomycetes; 0 = Ascomycetes, Stilbaceae. overall and that the Dematiaceae tended to occur more in the valley than on the hillside. Dissimilarities between the two methods were reflected in the percentages of colonies in each category and, to a lesser extent, in what taxonomic groups were present each month.

Community comparisons Diversity estimates from baits (Table 3) With one exception (May) the hillside consistently showed a larger number of species than the valley, as well as a greater number of total colonies isolated. However, examination of

J,

CC (%) \

(

Hillside Jan. May Aug. Sept.

Valley Jan. May Aug. Sept.

35-56 10·25 31·37 56·0 40'0 46'15 39·13 52'38 57'14

31'11 22'64 38'71 42'86 35'29 33'90

65'0

5·70

, t

Jan.

11'68

,

30·65

Sept.

\

14·18 18·48 31'57 18·68 23·56

32-22

May Aug.

J.

Hillside

28'87 50·80

J,

PS (%)

Sept.

2·22 8·62 17-21 17·95 19'53

Valley Hillside Valley Site A J. J. , t and \ t f month Jan. May Aug. Sept. Jan. May Aug. Sept. Jan. May Aug.

f

Table 3. Diversity estimates from baits

344 696 869 803

238 678 751 365

28 17 25 34

22 23 17 29

No. of No. of colonies species

1-170 1-030 1·130 1·090

0'964 0·971 0'775 1-170

H

0·806 0'841 0·809 0·715

0·720 0·714 0·630 0·802

J

304

E. C. TAYLOR

Appendix I (with quantitative substantiation by the values of Hand 1) revealed a similar pattern of community structure for the two sites during all seasons; e.g. communities in each had a few common species and a large number of relatively rare species. Species composition in these communities varied greatly, both between sites and on a seasonal basis. That seasonal variation exceeded between-site differences is apparent when the former is compared with relative abundance (PS) and presence or absence (CC) for each site. Measurements for CC are consistently higher than those for PS, indicating that species present each month were not necessarily correlated with what species were most common for that month. Examination of results in Appendix I indicates that PS values were high because five species (Fusarium solani var. 1, Aspergillus fumigatus var. 1, unknown no. 21, Cunninghamella bertolothea and Cunninghamella echinulata) occurred nearly every month, and in similar abundance at each site during any given month. Adding to the above those species producing one or two colonies nearly year-round accounts for most of the PS and much of the CC. The remaining species appeared to be active only during specific seasons of the year.

Diversity estimates from dilution plates (Table 4) In determining PS for these colonies, September data were multiplied x 10 so that all calculations were based on the number of colonies found in a 1 : 10 dilution. Calculations comparing results of the 1 : 100 dilution of September with the 1 : 10 dilution of other months are given in parentheses, and seem to indicate that the relatively low PS of September was probably not an artifact of the difference in dilution. Results indicated a larger seasonal than between-site variation in numbers of colonies, especially in numbers of species present. Low overlap was found between sites at anyone time (CC), and in abundance of shared species (PS). Only two species, Fusarium solani var, 1 and Aspergillus fumigatus var. 1, were distributed throughout the year (see Appendix II).

Comparisons of bait and dilution diversity (Table 5)

There appeared to be low similarity between results from baits and soil dilution plates for all seasons. With two exceptions (May in the valley, January on the hillside) all CC values were below 50 per cent, indicating that less than half the species isolated each month were present in both sampling methods. Of the five species found growing in the soil during most seasons only two, Aspergillus fumigatus var. 1 and Fusarium solani var. I, appeared to be present as spores nearly all the year round.

Discussion Analysis of physical factors

From an analysis of soil variables (Table 1) the hillside appears to have superior nutrient availability and water-holding capacity. The effect of incoming solar radiation is more difficult to evaluate since soil characteristics, sun angle and heat flux between boulders and air must also influence heat load of the soil and, to some extent, therefore, control fungal organisms therein. Providing seasonal changes in the physical environment are indeed the dominant factors controlling structure of the fungal communities, biotic factors may regulate the community within constraints imposed by the physical environment. While seasonal CfN ratios in this desert grassland are within optimal limits for rapid decomposition (Pugh, 1974), N is so low that it probably limits the amount of fungal flora that can be supported. If one uses the number of fungal propagules per gram of soil as an index of biologic activity, it becomes apparent that densities of fungal populations are a direct function of soil organic content (Orpurt & Curtis, 1957; Christensen, 1969). A comparison of

55'56 47-1

Sept.

Aug.

May 10'0

9'52

* See text for explanation.

11'76

15·38 16'0

6·90

50'0

Hillside Jan.

41·67

8'33

20'0

Valley Sept.

I A

Hillside ,

No. of

No. of

14-89 12·23 0·28 (1'14)* 26·74 0·30 (1'5)* 0'28 (1'15)*

12012

0·629 0·659 0·514 0'569 0·918 0·850

9 8 12

73 114 60

0·954 0·776

0'884 0·752

0·795 0·833

0·694 0·728

0·836 0·715

J

17

15

9

9

15

H

115

72

114

101

113

Jan. May Aug. Sept. colonies species

PS (%)

14'95 19'38 16·33 40·35 (40'0)* 45·98 10'23 2-68 (4-62)* 13-67 46'49 (17-20)*

Jan. May Aug. Sept. Jan. May Aug.

Hillside

37·04

11,11

33,33 25'0

,

Sept.

Aug.

May

Valley Jan.

J.

Site Valley and, month Jan. May Aug. Sept.

CC(%)

Table 4. Dicersity estimates from soil dilution plates

E. C. TAYLOR

306

fungal colony densities in both study sites with respective seasonal changes of N abundance suggests that the larger number of hillside colonies is related to higher N levels there. High temperature and low moisture in May seem to limit activity to those species that can tolerate these conditions. Conversely, in January cold temperature probably overrides Table 5. Coefficient of community comparisons of bait and dilution plate diversity

Valley Hillside

Jan.

May

Aug.

Sept.

27·03 53·33

50·0 38-46

46'15 24·24

45-45 43-48

the effect of higher available moisture, which favors those fungi that grow well at low temperatures. Effects of pH are probably of lesser importance. High soil alkalinity perhaps provides competitive advantages to bacteria and actinomycetes, but since most fungi have wide ranges of tolerance to pH (Park, 1968), seasonal variation is probably not great enough to be significant.

Analysis of results from baits Two main biological types of fungi are believed to exist in deserts. The first is a slow-growing, darkly pigmented type, and includes mycelia sterilia that produce chlamydospores and bulbils. The second type resembles desert annuals that exploit short periods of favorable conditions by growing and reproducing rapidly and abundantly (Nicot, 1960). (These are not to be confused with the taxonomic groups presented in Figs 3 and 4.) In the relatively benign desert grassland of central New Mexico, there appears to be an intermediate type which is brightly pigmented, grows at a moderate rate and then sporulates abundantly when available resources decrease. Examples are Trichocladium and Heterocephalum. These three types show differences in seasonal distribution. In January the valley is dominated by the darkly pigmented forms and by darker members of the rapid growers. The hillside has more species composed of all three morphological types. It is at first surprising to see the large number of colonies and species that grow in January. Winter months, however, are not necessarily inimical to short-lived organisms. Time-series analysis of weather patterns indicates that the periods of warmer weather between cold fronts on the east coast of the United States last 4-7 days, while on the west coast they last approximately 2 weeks (Landsberg, Mitchell & Cruther, 1959; Polowchak & Panofsky, 1968). For a fungus with a fairly short generation time the warmer period between fronts could provide enough time to grow and sporulate (Hawker, 1957; Warcup, 1967). This would be especially true for fungi growing on the hillside, where there is a coverage of perennial vegetation and where heat absorbance and transmittance to soil by the basalt boulders occurs. May can be a hot, dry month in central New Mexico because major rains in this area do not occur until late summer and early fall. Fungus communities are composed primarily of darkly pigmented types and rapid sporulators. The large number of colonies in May perhaps reflects abundant sporulation by species which grew into the bait. By August and September, while ambient temperatures are still high, rainfall has added moisture to the habitats under consideration. August seems to reflect a transition from the early summer dominance by Dematiaceae and quick sporulators to a late summer proliferation of intermediate types that continues into September. Results derived from CC and PS indicate several trends. The first is that hillside and valley, although in close proximity, show wide variation in species growing on them at a given time. This is apparent from the CC, which reflects the number of species common to both, and even more so from the comparison of numbers of individuals in these species growing in each place (PS). Highest similarity is found in May, when both sites are hot and dry. During other

FUNGI IN TWO DESERT COMMUNITIES

307

seasons, similarity is low, indicating strong micro-habitat variation within a relatively small area (Crawford, 1978). Seasonal variation on the hillside is quite evident and is attributable to a number of factors, most important of which is probably climatic variation. It has been found that increased ecological heterogeneity allows more species to coexist in an area (Ricklefs, 1979), so perhaps some of the high hillside species diversity can be attributed to the large number of microhabitats present. Within these habitats biotic interactions are assumed to further structure the community, particularly as changes in temperature, nutrients and moisture shift competitive advantages from, for example, mesophilic to more xerotolerant or thermotolerant species (as defined by Ainsworth, 1971) (Tansey & Jack, 1977). The seemingly low microhabitat variation in the valley leads one to expect more species uniformity than is actually present. However, lack of protection from vegetation and boulders should render it more strongly controlled by changes in temperature and rainfall than is the hillside. This supposition is borne out by the low similarities among months. While temperatures in May and August are similar, an increase in rainfall in August seems to favor less xerotolerant species. By September, decreasing temperature appears to promote a community of organisms better able to survive and compete under more moderate conditions. It would seem, then, that the hillside and valley exhibit a high degree of seasonal variation for two different reasons: the valley provides a fairly uniform soil surface which is strongly controlled by changes in moisture and temperature, while the hillside provides a more protected area displaying a wide range of microhabitats which can be differentially exploited. Analysis of results from soil dilution

Colonies from dilution plates belong mostly to the quick sporulators and darkly pigmented types. Comparisons of morphological types indicate less diversity in the valley, perhaps due in part to greater microhabitat uniformity or to consistently poor conditions favoring survival of hardier spores (e.g. darkly pigmented) or those which are produced abdundantly (e.g. Penicillia). The high number of spores present in September does not appear to be due to a prewinter sporing effort, since the spores produced to not seem to be a product of current colony growth as reflected from the baits. The large number of colonies for January may be from germination of chlamydospores which overwinter. Results indicate large seasonal variation in spores present in the soil. Seasonal variation is indicated by number and kind of species present rather than by number of propagules, which remains fairly constant. Species overlap (as represented by CC) is low for all months, indicating that there is probably a large turnover in viable spores during the course of a year. To what extent the large differences in PS for September are due to, difference in the dilution factor is not known. Soil plates for other months showed some crowding, but colony density did not warrant a higher dilution. Since CC is not strongly affected by the dilution factor, low September values indicate small overlap between September and the other months. Bait and dilution analysis

Initially my intention was to use baits to isolate what was actively growing in the soil. and dilution plates to indicate what other fungi were present but inactive. Since there was no intention of making comparisons between methods, one dilution plate taken from a composite of soil samples at each site per month was deemed sufficient. Therefore, comparisons between methods are presented with the realization that a larger sample size of higher dilution would have given more valid results. There is low monthly overlap in the species isolated by the two methods, and no clear patterns emerge in between-site or seasonal comparisons. Colonies from dilution plates each month do not appear to be the product of spores produced by currently growing mycelia.

E. C.TAYLOR

308

The low CC comes from two factors: the first is that for each month a larger number of species was isolated from the baits than from the dilution plates. This could be due to the limitations of the dilution method, or to the small sample size employed. However, each month several species occurred on the dilution plates and not on the baits (see Appendices). A large number of these were Penicillia, which were growing in the soil in very low numbers. Similar differences were noted by Warcup (1957) in a comparison of the dilution method with direct hyphal isolation. Comparisons of morphological types reveals there is more variety in what is actually growing than results of the dilution method indicate. Some genera found to be growing abundantly (e.g. Phoma, Scolocobasisium) were not present on dilution plates. It is apparent, then, that when one attempts to ascertain seasonal activity one must use methods which will distinguish between species actively growing and resting as spores. The soil baiting technique (Luttrell, 1967) used by Mabee & Garner (1974), the screened immersion plates (Thornton, 1952) employed by Thornton (1956), or baits such as I used could be expected to give more valid results than the dilution plate technique employed in numerous studies (e.g, Moubasher, 1978; Virzo de Santo, 1978). Results from the two methods, however, point out clearly the adaptive value of being darkly pigmented in the desert, in survival of both spores and mycelia. High incidence of darkly pigmented species has been commonly reported in surveys of deserts (compared to other habitats) (Nicot, 1960; Ranzoni, 1968) and suggests a versatile fungus type with an ability to survive harmful effects of ultraviolet light in summer (Durrell & Shields, 1960) and to absorb heat from solar radiation in winter. While the soil baiting and dilution plate techniques give different results in regard to temporal patterns of species distribution, both show that desert grassland soil is inhabited by a diverse community of fungi with strong seasonal fluctuations in activity. Structuring of the community in time and space is undoubtedly controlled by the interactions of a variety of biotic and abiotic variables. A few species seem to be relatively unaffected by changes in the environment, but most species show pulses of activity. Further research to strengthen our knowledge of the environmental factors to which these pulsed species respond would greatly expand our understanding of desert fungal communities. I wish to thank Dr Jack States and Dr Keller Suberkropp for assistance with taxonomy and review of the manuscript.

Appendix 1 Seasonal numbers of coloniesin species isolated from baits

•

Valley Jan. Cladosporium herbarum Mucor sp. Arachniotus striatosporus" Fusarium solani var. 1 Tetracoccosporum paxianumr Mortierella sp. Pithomyces chartarum Alternaria tenuis Scopulariopsis sp," Dactylella sp,

Penicillium luteum series" Penicillium nigricans Chrysosporium sp." Monosporium sp.

87 36 9 15 3 27 15 1 5 2

May

11

2

Aug.

10

Sept.

55

6 16 22

\

I

Hillside

Jan.

May

Aug.

Sept.

1 27 51 71 30 5 23 12

40

47

93

6

6

8 7 25

2

4 3 4

309

FUNGI IN TWO DESERT COMMUNITIES

Appendix 1 (cont.) Hillside

Valley Jan.

May

8

41 51 16 23 95 62 303

Macrophomina sp, Phoma sp. 1· Phoma sp. 2· Phoma sp, 4· Unknown no. 21 Cunninghamella bertolothea Aspergillus fumigatus var, 1 Cunninghamella echinulata Aspergillus ornatus" Scolocobasisium sp, Fusarium roseum Helicodendron tubulosum Aspergillus niger" Aspergillus sulfureus Aspergillus fumigatus var, 2 Fusarium solani var, 2 + Trichocladium asperum" Sterile mycelia no. 7 Aspergillus flaoipes" Fusarium discolor Cephalosporium sp, 1 Fusarium concolor" Thielavia terricola" Fusarium lateritum" Septonema sp." Cylindrocarpon sp." Trichoderma oiride" Cephalosporium sp, 3 Aspergillus ustus H eterocephalum aurantiacum Bipolaris spicifera Aureobasidium pullulans Cephalosporium sp, 2 Aspergillus flaous" Aspergillus zoentii"

Aug.

(

24 68 27

30 1 17 3 3 2

4 23 3 1 128 363 41

May

Jan.

2 2

10

3

Sept.

\

2 33 57 65 75 87 116 148

2

14 18 33 3

2 1 20

44 12 11

183 57

39

15

12

Aug.

26 55

8

10 7

21 99

11

97 31 57

14

4 1 12 14

1

28

Other

24

• Isolated from bait only.

8

3

1 1 2 15 96 13

1 2 7 1 16 1

72 11

1 12

1

Sept.

3 20 68 43 5 5 18

30

15

14

15 9 158 49 47 166 9 41 7 5 29

Appendix 2

Seasonal numbers of colonies in species isolated from soil dilution plates

Valley I

Fusarium solani var, 1 Aspergillus fumigatus var, 1 Mucor sp, Cunninghamella bertolothea Penicillium citrinium series" Cladosporium herbarum

Bipolaris spicifera

Pithomyces chartarum

Hillside

A

Jan. 46 20 7 3 16 3 2 5

\

May

Aug.

Sept.

28

2 18

31 4

9

I

May

Aug.

12 13 40

1 56

44

5 15

3

,

A

Jan.

4

1 2

Sept.

10

310

E. C. TAYLOR

Appendix 2 (cont.) Valley

Hillside

,

Jan. Unknown no. 21 Myrothecium uerrucaria Penicillium nigricans Mortierella sp, Aureobasidium pullulans Penicillium jenseni Penicillium frequentens* Aspergillus ustus Helicodendrum tubulosum Cladosporium cladosporioides Aspergillus sulfureus Aspergillus fumigatus var, 2 Fusarium solani var, 2 + Dactylella sp, Ulocladium sp, Cephalosporium sp. 1 Hormiscium sp, Aspergillus sydowi* Aspergillus restrictus Alternaria tenuit Cephalosporium sp. 2 Cephalosporium sp, 3 H eterocephalum aurantiacum Penicillium [anthnellum series Other

May

Aug.

Sept.

Jan.

49

9

Aug.

7

6

3 7

May

1 2 4 24 30 18 2

5

14 6 1 6 1

3 1 8 1 3 1 1 0

4 1 4

4 1 6

Sept.

49 3 1 4

1

2 2

13

5 11 9

9

9 1 0

* Isolated from soil dilution plates only.

References Ainsworth, G. C. (1971). Ainsworth ~ Bisby's Dictionary of the Fungi. Kew, Surrey: Commonwealth Mycological Institute. 633pp. Ali, M. I., Batanouny, K. H. & Salama, A. M. (1975). Studies on the fungal flora of Egyptian soils. Pedobiologia, 15: 13-19. Barnett, H. L. & Hunter, B. B. (1972). Illustrated Genera of Imperfect Fungi. Minnesota: Burgess. 241pp. Barron, G. L. (1968). The Genera of Hyphomycetes from Soil. Baltimore: Williams & Wilkins. 364pp. Booth, C. (1971). The Genus Fusarium, Commonwealth Mycological Institute: Kew, Surrey, England. 237 pp. Borut, S. (1960). An ecological and physiological study on soil fungi of the northern Negev (Israel). Bulletin of Research Council of Israel, 3D: 65-80. Bremner, J. M. (1965). Determination of nitrogen in soil by the Kjeldahl method. Journal of Agricultural Science, 55: 1-23. Cameron, R. E. (1969). Abundance of microflora of soils of desert regions. Jet Propulsion Laboratory Technical Report 32-1378: 1-16. Chapman, H. D. & Pratt, P. F. (1961). Methods of Analysis for Soils, Plants and Waters. University of California Division of Agricultural Sciences. 309pp. Christensen, M. (1969). Soil microfungi of dry to mesic conifer-hardwood forests of northern Wisconsin. Ecology, 50: 9-27. Connell, J. H. (1976). Some mechanisms producing structure in natural communities: a model and evidence from field experiments. In Cody, M. L. & Diamond, J. (Eds), Ecology and Evolution of Communities, pp. 460-490. London: Belknap Press of Harvard University. Crawford, C. S. (1978). Seasonal water balance in Orthoporus ornatus, a desert millipede. Ecology, 59: 996-1004.

FUNGI IN TWO DESERT COMMUNITIES

311

Dindal, D. L. (1973). Microcommunities defined. In Dindal, D. L. (Ed.), Proceedings of the Soil Microcommunities Conference (First), at Syracuse, New York on 18-20 October 1971, pp. 2-6. Springfield, Virginia: U.S. Atomic Energy Commission and National Technical Information Service, U.S. Department of Commerce. Durrell, L. W. & Shields, L. M. (1960). Fungi isolated in culture from soils of the Nevada test site. Mycologia, 52: 636-641. England, C. M. & Fiee, E. L: (1957). A comparison of the soil fungi of a tall-grass prairie and of an abandoned field in central Oklahoma. Botanical Gazette, 118: 186-190. Friedmann, E. 1. & Galun, M. (1974). Desert algae, lichens and fungi. In Brown, G. W. jr (Ed.), Desert Biology, Vol. II, pp. 165-212. New York and London: Academic Press. Gilman, J. C. (1971). A Manual of Soil Fungi. Ames, Iowa: Iowa State University Press. 450pp. Gochenaur, S. E. (1978). Fungi of a Long Island oak-birch forest 1. Community organization and seasonal occurrence of the opportunistic decomposers of the A horizon. Mycologia, 70: 975-994. Hankin, L. & Anagnostakis, S. L. (1977). Solid media containing carboxymethyl cellulose to detect C cellulase activity of micro-organisms. Journal of General Microbiology, 98: 109-115. Hawker, L. E. (1957). Ecological factors and the survival of fungi. In Williams, R. E. O. & Spicer, C. C. (Eds), Microbial Ecology, pp. 238-258. Cambridge: Cambridge University Press. Ismail, A. L. S. & Abdullah, S. K. (1977). Studies on the soil fungi of Iraq. Proceedings of Indian Academy of Science, 86B: 151-154. Katz, B. A. & Lieth, H. (1974). Seasonality of decomposers. In Lieth, H. (Ed.), Ecological Studies #8, Phenology and Seasonality Modeling, pp, 163-184. New York: Springer-Verlag. Kuehn, H. H. (1960). Fungi of New Mexico. Mycologia, 52: 535-544. Landsberg, H. E., Mitchell, J. M. jr, & Cruther, H. 1. (1959). Power spectrum analysis of climatological data for Woodstock College, Maryland. Monthly Weather Review, 87: 283-298. Luttrell, E. S. (1967). A strip bait for studying the growth of fungi in soil and aerial habitats. Phytopathology, 57: 1266-1267. Mabee, H. F. & Garner, J. H. B. (1974). Seasonal variations of soil fungi isolated from the rhizosphere of Liriodendron tulipifera L. In Lieth, H. (Ed.), Ecological Studies # 8, Phenology and Seasonality Modeling, pp. 185-190. New York: Springer-Verlag. Martin, J. P. (1950). Use of acid, rose bengal and streptomycin in the plate method for estimating soil fungi. Soil Science, 69: 215-232. Mohling Ma, R. (1933). Seasonal variations of fungi in soils in the vicinity of Peiping. Peking Natural History Bulletin, 7: 293-297. Moubasher, A. H. & Abdel-Hafez, S. 1. (1978). Further study on seasonal fluctuations of Egyptian soil fungi. Mycopathologia, 63: 11-19. Nicot, J. (1960). Some characteristics of the microflora of desert soils. In Parkinson, D. & Waid, J. S. (Eds), International Symposium on the Ecology of Soil Fungi, pp. 94-97. Liverpool: Liverpool University Press. Nour, M. A. (1956). A preliminary survey of fungi in some Sudan soils. Transactions of British Mycological Society. 39: 357-360. Orpurt, P. A. & Curtis, J. T. (1957). Soil microfungi in relation to the prairie continuum in Wisconsin. Ecology, 38: 628-637. Park, D. (1968). The ecology of terrestrial fungi. In Ainsworth, G. C. & Sussman, A. S. (Eds), The Fungi, An Advanced Treatise, Vol. III, pp. 5-40. New York: Academic Press. Parkinson, D., Gray, T. R. G. & Williams, S. T. (1971). Methods for Studying the Ecology of Soil Micro-organisms. Oxford: Blackwell Scientific Publications. 116pp. Pielou, E. C. (1976). Population and Community Ecology: Principles and Methods, pp. 31(}-315. New York: Gordon & Breach. Polowchak, V. M. & Panofsky, H. A. (1968). The spectrum of daily temperatures as a climate indicator. Monthly Weather Review, 96: 596-Q00. Pugh, B. J. F. (1974). Terrestrial fungi. In Dickinson. C. H. & Pugh, B. J. F. (Eds), Biology of Plant Litter Decomposition, pp. 303-336. New York: Academic Press. Ranzoni, F. V. (1968). Fungi isolated in culture from soils of the Sonoran Desert. Mycologia, 60: 356-371. Raper, K. B. & Fennell, D. 1. (1965). The Genus Aspergillus. Baltimore: Williams & Wilkins. 686pp. Raper, K. B. & Thorn, C. (1949). A Manual of the Penicillia. Baltimore: Williams & Wilkins. 875pp. 21

312

E. C. TAYLOR

Ricklefs, R. E. (1979). Ecology. New York: Chiron Press. 966pp. States, J. S. (1978). Soil fungi of cool-desert plant communities in northern Arizona and southern Utah. Journal of the Arizona-Nevada Academy of Science, 13: 13-17. Tansey, M. R. & Jack, M. A. (1977). Growth of thermopholic and thermotolerant fungi in soil in situ and in vitro. Mycologia, 69: 563-578. Thornton, R. H. (1952). The screened immersion plate. A method for isolating soil microorganisms. Research, London, 5: 190-191. Thornton, R. H. (1956). Fungi occurring in mixed oakwood and heath soil profiles. Transactions of British Mycological Society, 39: 485-494. Toussoun, T. A. & Nelson, P. E. (1968). A Pictorial Guide to the Identification of Fusarium Species. University Park: Pennsylvania State University Press. 51pp. Virzo de Santo, A" Alfani, A. & Sapio, S. (1978). Microbial populations of two soils in the beech forests of Monte Taburno (Campania Apennines). Pedobiologia, 18: 48-56. Warcup, J. H. (1951). The ecology of soil fungi. Transactions of British Mycological Society, 34: 376-399. Warcup, J. H. (1957). Studies on the occurrence and activity of fungi in a wheat-field soil. Transactions of British Mycological Society, 40: 237-262. Warcup, J. H. (1960). Methods for isolation and estimation of activity of fungi in soil. In Parkinson, D. & Waid, J. S. (Eds), The Ecology of Soil Fungi, pp. 3-21. Liverpool: Liverpool University Press. Warcup, J. H. (1967). Fungi in soil. In Burges, A. & Raw, F. W. (Eds), Soil Biology, pp. 51-110. New York: Academic Press. Zar, J. H. (1974). Biostatistical Analysis. Englewood Cliffs, New Jersey: Prentice-Hall. 620pp.