Air spora of a site in Tropical Queensland, Australia

[ 537 ] Trans. Br. mycol, Soc. 61 (3) , 537-545 (1973) Printed in Great Britain

AIR SPORA OF A SITE IN TROPICAL QUEENSLAND, AUSTRALIA By F. J. UPSHER Defence Standards Laboratories, Maribyrnong, Victoria, Australia D. A. GRIFFITHS Department of Botany, School of Biological Sciences, La Trobe University, Bundoora, Victoria, Australia AND

The 'exposed plate' method was used to trap airborne fungal spores in the open and in the jungle at]oint Tropical Research Unit (J.T.R.U.) at lnnisfail, Queensland, over a period of 3 years. One hundred and nineteen genera were recorded and distinct seasonal and diurnal variation was observed in the more common ones. Spores of Cladosporium were mor e frequently trapped than any other genus at th e cleared site and in the jungle. Curvularia, Geotrichum, Leptosphaerulina, Monilia, Penicillium and Nigrospora were also abundant and several other genera, including Aureobasidium, Fusarium, Paecilomyces and Periconia, wen: often present. The use of quantitative alginate filtration during the final year supplemented the exposed-plate data, but differences in the technique prevented close comparison of the result s.

The Joint Tropical Research Unit was established in 1962 by the British and Australian governments for studying the behaviour of materials in the tropical environment. The hot wet exposure site is near Innisfail, at latitude 17'5° S., approximately 16 km (10 miles) from the coast and at an elevation of 40 m (130 ft). It consists mainly of secondary rain-forest with a cleared area of 1 hectare (2 acres ). The average rainfall is 3600 mm (140 in), of which 2800 mm (110 in) fall between January and June. Fungi grow well on a variety of materials all th e year round, even in the dry season and are a major factor in the deterioration of some of them. In 1966, systematic studies were commenced to survey the live airborne spores of saprophytic microfungi, particularly those potentially able to colonize materials. Several conditions peculiar to this survey influenced the choice of trapping method used. As the interest was in the live spores, a culture method was necessary. It had to be simple to use, yet reveal variation in abundance. Incubation and examination were to be done at Melbourne, 3200 km (2000 miles) away so there was a need to have the catch plated at Innisfail and despatched to arrive before th e colonies had formed spores . It was realized that the 'exposed plate method has some deficien cies as a spore trap. The main criticisms are that it exhibits a bias favouring the retention of larger spores and it is not quantitative. However, it was considered suitable for sampling the air spora to determine the occurrence of the major genera. It was also compatible with the other requirements so I

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Transactions British Mycological Society

was selected for routine sampling, which was done at the open cleared area and in the jungle to find variations in spore deposition in these different environments through the year and the day. In addition, during the final year, a quantitative filtration method was used to give an indication of the actual density oflive saprophytic fungal spores in the air. The exposed plate method has been used extensively in air-spora investigations around the world, particularly in Europe and North America. There have been surveys of the air spora at some Australian cities (Clarke & Mason, 1964; Derrick & McLennan, 1963; Frey & Durie, 1962; Rees, 1964) and at several tropical locations of the world (e.g. Alvarez & Castro, 1955; Blackaller, 1950; Cammack, 1955; Dransfield, 1966; Myers, 1956; Raj an, Nigam & Shukla, 1952; Taylor & McFadden, 1962; Turner, 1966), but none in tropical parts of Australia. The conditions in which air-spora surveys elsewhere had been conducted were most variable. Factors which varied and which could have influenced the results included elevation, location, time ofday, proximity to buildings, duration of plate exposure and incubation. Sampling was done at 08.00 h (Bisby, 1935) and 20.00 h (Derrick & McLennan, 1963), but mostly between 10.00 and 12.00 h; as low as I ft above ground (Ainsworth, 1952) or on top of multistorey buildings (Blumstein & McReynolds, 1945; DiazRubio, Orta & Lamadrid, 1950; Targow & Plunkett, 195I). Methods of reporting the results also varied. A comparison of results is hindered by the irregular inclusion ofsuch groups ofmicro-organisms as yeasts, bacteria, actinomycetes and non-sporulating fungi, which directly affect the percentages of the fungal genera present. METHODS AND MATERIALS

The exposed plate method A site was selected on the cleared area at J.T.R.D., not adjacent to buildings, the road or the jungle. Preliminary tests also indicated that there was no appreciable difference in the air spora at heights up to 12 ft, so all subsequent exposures were done on a platform I ft above the ground. The platform was covered with a Perspex disk, 36 in diameter, I ft above. Exposures in the jungle were done on a similar platform under a complete canopy of trees. Potato Dextrose Agar (PDA, Oxoid) and Cornmeal Agar (CMA, Oxoid) were most suitable because they supported sparse vegetative growth but encouraged good sporulation and pigmentation. The media were always exposed concurrently in pre-sterilized polystyrene Petri dishes, 87 mm diameter. We aimed to trap about 15 spores on a plate, the greatest number that could grow without overcrowding, overgrowth or antagonism. An earlier spore-trapping programme at Innisfail during 1966-7 (Upsher, 1968, 1969), in which there was daily trapping for I min and 15 sec showed that plate exposures here should be for the shorter time. Plates were prepared, exposed and packed using methods which minimized the chance of spores becoming deposited on the agar other than during sampling. The operator faced the wind when exposing plates so (I)

Air spora. P.]. Upsher and D. A. Griffiths

539

that he should not contribute to the spores approaching the plate. After exposure, the plates were replaced in a polyethylene bag, returned to the laboratory, and there sealed into individual bags in which they were air freighted to and incubated at Defence Standards Laboratories (D.S.L.), Melbourne. Plates were incubated (20-30°) for 4 weeks, the developing colonies examined and identified to genera. Yeasts, bacteria and actinomycetes although present were not recorded; colonies failing to develop recognizable spores were recorded as 'sterile'. To study diurnal variation, plates were exposed hourly during fifteen 24-h periods during the 4 years of the survey; three each in October 1966, April 1967, October 1967, July 1968 and January-February 1969. To study seasonal variation, between November 1967 and October 1970, samples were taken on Tuesdays at about 08.30 h. Previous trials had shown that day- and night-spores were present in the air at that time. At the cleared site, six plates (3 x PDA and 3 x CMA) were exposed for 15 sec simultaneously. In the jungle, two plates (I x PDA and 1 x CMA) were also exposed weekly, between February and January (1969-71).

(2) Alginate filtration A method was devised to obtain an indication of the density of live spores in the air. Spores were quantitatively recovered by forced air filtration, on a soluble filter of calcium alginate. It was used during the final year of the survey. Sampling was done at the same site as the plate exposures at the cleared site and directly after them. No sample was taken when rain was falling. Fibrous calcium alginate (Calgitex, supplied by Messrs GoUin and Co, South Melbourne), diameter 10 usu, was ball milled for 24 hand 0'4 g portions suspended in 10 ml distilled water and sterilized by autoclaving. The slurry was poured into a sterile sintered glass crucible (Pyrex, no. 3) which was then covered with an aluminium foil cap. The water was allowed to drain away and the crucible dried at 60°. To sample air, the crucible was clamped in an upright position and suction provided, with the flow governed at 10 ljmin. The cover was removed immediately before and replaced immediately after sampling for 1 min. A sterile rubber bung was placed in the open end of the crucible to avoid loss or contamination of the sample in transit. On receipt at Melbourne, the alginate was dissolved in 100 ml of Calgon-Ringer solution (Oxoid). Ten 1 ml aliquots were plated with PDA, incubated for 4 weeks and then all growth examined. The generic identity of each colony was recorded. Those colonies that did not produce recognizable characters were recorded as 'sterile'. Yeasts, bacteria and actinomycetes were not recorded.

35

M YC

6r

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54°

Table Month

Auereobasidium Cladosporium Curvularia Epicoccum Fusarium Geotrichum Leptosphaerulina Monilia Nigrospora Penicillium Periconia Trichoderma Sterile colonies All others

J.

Monthly totals of major genera at the cleared site, November J 967-0ctober 1970 F, M. A. M. J. J. A. S, O. N. D.

I.

3

88 7

6 8

Cladosporium Curvularia Fusarium Geotrichum Leptosphaerulina Monilia Penicillium Periconia Pestalotia Trichoderma Sterile colonies All others

17 110 8 27

23 27

3 4

4

2

2

2

3

o

6

13

3

17 21

II

42 15

I

38

101

131

8

3

I

7

5

3 21

31

4

4

60 116 45 22 12 10 3 257 15 1 2

4

2

4

3

24 18 3 29 2 12 43

I

I

44

5 8

I

8 8 3

6

64 185

3

26

3

.. J. 5

2.

F.

132 10

5 4 8 3

17 7 3

9

10

71

4

393 658 56 125 83

4

15 1

5

9

26 4

10

154 3'0 843 16'2 106 2'0 1'0 54 ['4

7,6 12'7 1'[

2'4 1,6 2'9

28 c'5 97 157 2112 40'6 7'0 14 27 362 I

I

Monthly totals of major genera in the jungle, February 1969-January 1971 M.

M,

2

A.

2

S,

7

O.

N.

D.

01

10,6

10

3

I

8

2 2 1 8 17 10 3 5 4 2 5 3 345 2 352

6

2

73

1'3 1'7 8'0

I

2

14 14

1'5 1'5

8

2

51

6

2

14 16

2 2 28 62 26 657

30

4

2

5

4

7

I

2

I

4

2 I

I

3

8

5

44 I

I

3 I

2413 37 37 39 51 186 3

12

Total

33

2

5

J,

97 12 16

II

2

J.

34

6

8

A,

5

10

8

4

16

21 21 10

I I 2 45 7 II 10 8 6 8 2 6 9 10 10 3 22 2 2 I 13 8 I 3 89 3 6 I I 2 2 9 5 194 196 219 216 165 186 167 198 159 158 28 26 34 36 29 20 42 41 29 36

Table Month

8

0/

Total

12 62 53 33 488

[7 2[

503 78

5,6 1'5 1'7 I'g 56 ' 2

RESULTS

(I) Exposed plate method During the whole survey, 119 genera of fungi were recognized. Seventyeight were Moniliales, twelve Melanconiales, eleven Sphaeropsidales, twelve ascomycetes, five phycomycetes and two Mycelia Sterilia. Variation through the year. Number of colonies recorded for the most common genera at the cleared site are given in Table J. Geotrichum was most abundant in the middle of the wet season, Leptosphaerulina through the latter part of the wet season and the cooler months, Cladosporium all through the dry season, Epicoccum and Nigrospora through the hotter part of the dry season and Curvularia and Trichoderma through the hotter part of the wet season. The seasonal variation in other genera was less pronounced, but Monilia was generally more abundant through the dryer hot months and Paecilomyces in the hot wet months. Aureobasidium, Fusarium, Penicillium and Periconia were present through most of the year and showed no obvious frequency pattern. Sampling in the jungle (weekly at 08.30 h on Tuesdays) between

8'5

Air spora. F.]. Upsher and D. A. Griffiths

541

Table 3. Incidence of the major genera at the cleared site at hourly intervals through the day Time

Aureobasidium Cladosporium Curvularia Epicoccum Fusarium Geotrichum Leptosphaerulina Monilia Nigrosopora Penicillium Trichoderma Verticillium

27

Aureobasidium Cladosporium Curvularia Epicoccum Fusarium Geotrichum Leptosphaerulina Monilia Nigrospora Penicillium Trichoderma Verticillium

3

4

2 38

35

29

I

-

I

I I 2 2 2 5 98 93 122 I 2 3 4 73 119 108 95 I I 4 6 6 :, 3 4 4 3

5 2 21

14

I

I

61 3 3 3 10 5 9 2 4 3 7

72 4 16 6 13 2 8 5 6 8

15 2 91 2 18 6 6 8 7 7 6 3 2

16 5°

:,

6 4 18 I

10 I

6

6

8

9

10

57 6 2 7 66 15 55

79 10 7 6 38 10 28 2 10 3 35

37 2 3 4 3° 8 12 2 4

59 2

48 6

II

17

I

14 6 26

4 18 6 10

58 2 10 5 16 5 15

7

3

4

20

21

22

41

25 3

34 3 5 3 108 10 70

25 3 5 2 79 4 87

3 2

7 I

6 2

I

2

I

3 3 55 8 66

5

6

4

13

4 2 2

17

18

19

I

I

3 16 4 9

2 54 3 3 2 37 12 22

8

6

9 3° 2

-

12

II I

9 69 2 71

57 2 2 6 7° 7 34

79 6 66

5 3 7

7 3 3

I

I

I

I

2

5

I

I

I

4 76 6 80

23

24 21 I I

2 51 4 69

I

2

5

7

I

26

I

I

3 107

., 13

Time

2

2

3

7 2

Table 4. Incidence of the major general in the jungle through the day Time

Cladosporium Fusarium Geotrichum Monilia Paecilomyces Penicillium Trichoderma

3 12 3 31 I I

5 4

37 3 19 4 16 4 8

5 28 9 19 7 I II

6

7 23 5 18 2 4 2 5

9 25 6 18 3 2 3

3

II

5° 7 6 5 12 4

13 64 4 6 4 3 10 2

15

17

67 5 8 3

63 7 5 3 9

17

II

5

5

19 76 4 15 4 3 4 9

21

23

15 4 27 5 2 3 7

25 I

38 4 3 5 3

February 1969 and January 1971 indicated that seasonal variation was less marked there than at the cleared site; only Cladosporium and Geotrichum showed distinct variation and their times of greatest abundance corresponded to those at the cleared site. The monthly totals for the more abundant genera are shown in Table 2 above. Variation through the day. Sampling was done hourly at the cleared site and at each alternate hour in the jungle. Tables 3 and 4 show the accumulated results of the fifteen trapping sessions. At the cleared site, spores of Cladosporium, Epicoccum, Geotrichum, Leptosphaerulina, Aureobasidium, Fusarium, Penicillium, Trichoderma and Verticillium were trapped at all times of the day, but most of these genera showed a distinct diurnal variation in abundance. Spores of Cladosporium were most often trapped between 07.00 and 19.00 h with a greatest abundance at 15.00 h and another peak at 08.00 h, 35-2

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Leptosphaerulina irregularly between 06.00 and 22.00 h with a peak at 07.00 hand Epicoccum most often between 01.00 and 15.00 h; Curvularia showed greatest abundance at 08.00 h. Geotrichum and Monilia were trapped most often through the hours of darkness and in the early morning, between 19.00 and 07.00 h, and 20.00 and 07.00 h respectively. In the jungle diurnal variation was less distinct, though Cladosporium was most abundant between 11.00 and 19.00 h, with its morning flush 4 h later than at the cleared site; Geotrichum was most abundant between 19.00 and 09.00 h. (2) Alginatefiltration Sampling with the alginate filter during the final year gave clear indications of the density of the viable air spora. Density was greatest during the wet months, February, March and April, when the mean was about 150 spores/l, The highest single sampling was of 270/1 (24 March). The air spora was least dense during the coolest months, July and August, when the mean was about 50/1 and the least recorded, II/I (14July). DISCUSSION

The composition of the air spora differed in the jungle and the clearing. 'Sterile colonies', which mostly developed abortive ascal primordia, were commoner in the jungle, depressing the apparent proportions of the recognized genera. After allowing for this difference, it is clear that some genera were relatively more abundant at one site than the other, especially Epicoccum, Leptosphaerulina and Nigrospora which favoured the cleared site and Chloridium, Fusarium, Geotrichum, Penicillium, Periconia and Trichoderma which favoured the jungle. Cladosporium has been found to be a major component of the air spora throughout the world. It was the most abundant airborne spore at Innisfail through the dry season, particularly in the hotter months. This pattern had previously been observed in tropical areas with distinct 'wet' and 'dry' seasons (Dransfield, 1966; Turner, 1966), which may be compared to temperate areas of Europe and America, where it is most abundant in summer and autumn which also tend to be warm and dry. Its greater incidence at Innisfail through the hours of daylight agreed with reports from elsewhere. The double-peak phenomenon (Gregory & Stedman, 1958; Rich & Waggoner, 1962), in which greatest incidences were observed before and after noon, was apparent in this survey with peaks at 08.00 and 15.00 h. Several species of Cladosporium were noted including C. herbarum, C. sphaerospermum, C. macrocarpum and C. elatum. The loculo-ascomycete Leptosphaerulina, present as L. australis, was the second most abundant type at the cleared site but was less prominent in the jungle. It had previously only been reported as a significant part of the air spora at Brisbane (Rees, 1964) where it was present mostly during the wet season and particularly after rain. At Sydney, Pleospora, a superficially similar genus, had been reported (Frey & Durie, 1962). The highest incidences of Epicoccum reported in air spora surveys have been in Australia: 13'7 % at Brisbane (Rees, 1964) and I I % at Sydney

Air spora. F.]. Upsher and D. A. Griffiths

543

(Frey & Durie, 1962), though it has been reported in significant numbers elsewhere. At Innisfail, as at Sydney, its greatest abundance was in the hottest part of the dry season (Oct.-Jan.), but its greatest incidence at Samaru was in the rainy season (Dransfield, 1966), at Brisbane in the warm dry (Aug.-Nov.) months (Rees, 1964), at Los Angeles in spring (Targow & Plunkett, 1951), and in Denmark (Ripe, 1962) and England (Pawsey & Heath, 1964) during autumn. It was present at Innisfail as E. nigrum. The greatest incidence of Nigrospora at Innisfail was in the hottest of the relatively dry months with a peak before the onset of heavy rain. It was noted in 1969 that a high incidence of Nigrospora continued into January until one inch of rain fell in a day after which its incidence declined sharply. Nigrospora had been recognized as a significant member of the air spora in other tropical areas and in Western Nigeria showed similar seasonal incidence (Cammack, 1955). N. sphaerica and N. panici were recorded. Geotrichum, which formed a significant part of the Innisfail air spora, has been rarely recorded elsewhere; 1 % at Cadiz (Diaz-Rubio, Orta & Lamadrid, 1950) and 0'4 % at Kansas (Kramer et al. 1959). Monilia, which was present at Innisfail mainly as M. sitophila, was also a major component of the air spora at Honolulu (Myers, 1956) and Johannesburg (Ordman & Etter, 1956). At Innisfail it was found to be associated with sugar cane debris and the same association may also account for its presence at Havana (Alvarez & Castro, 1955) and Honolulu. Penicillium has been recognized as a major component of the air spora at many locations and was frequently trapped at Innisfail, particularly in the jungle. Many species of Penicillium were present (Upsher, 1972). Aureobasidium is also a widespread airborne constituent and formed 1 % of the cleared site total but was only rarely recorded from the jungle. Fusarium occurred irregularly through the year at Innisfail and was more abundant in the jungle where it made up 1·8 % of the trapped total. It was prominent in the air spora at Honolulu (Myers, 1956), Panama (Taylor & McFadden, 1962) and Paris (Vallery-Radot et al. 1950). Results from the alginate filtration sampling supplement those from the exposed plate trappings in terms of spora density, but basic differences in the techniques of the two methods mean that the results cannot be directly compared. An aggregate of airborne spores trapped on an exposed plate would be recorded as a single unit, whereas the same trapped on an alginate filter would be recorded as the number of its components. Thus fungi producing large numbers of spores adhering in heads or long chains such as Cladosporium or Penicillium would appear more numerous by the filtration method. Although longevity of fungal spores is generally thought of in terms of days or weeks, some are more shortlived; Spaulding found some losing viability within 10 min of discharge (cited by Doran, 1922). Even if most of those at Innisfail are not so ephemeral, the delay of at least 24 h before plating the alginate trappings may depress the apparent representation of the more short-lived types. Whereas the sampling bias ofthe exposed plate method favours recovery oflarger particles, filtration sampling using an applied suction favours the recovery of smaller ones. The extent of these two influences is not known.

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Transactions British Mycological Society

Because sampling by the two methods was not done simultaneously, it would be possible for a spore cloud to be trapped by one method and missed by the other. During the first year of sampling at the cleared site, it was noted that the number of colonies developing on the' I min' plates was only twice as great as those on the plates exposed for 15 sec. Further investigations are being made into some aspects of the exposed plate method, including the influence of the turbulence associated with lid movement. The authors wish to thank the staff at Joint Tropical Research Unit, Innisfail, Queensland, for much of the spore trapping, and Messrs R. Bird and H. Sokol for their technical assistance. These investigations formed part of a thesis for the degree of M.Sc. at La Trobe University (F.J. U.). REFERENCES

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RIPE, E. (1962). Mould allergy. 1. An investigation of the airborne fungal spores in Stockholm, Sweden. Acta allergologica 17, 130-150. TARGow, A. M. & PLUNKETT, A. O. (1951). Fungus allergy. I. Incidence of atmospheric spores in the Los Angeles area. Annals of Allergy 9, 428-445. TAYLOR, R. L. & McFADDEN, A. W. (1962). Study of the airborne mould flora in Panama. Mycopathologia 17, 159-164. TURNER, P. D. (1966). The fungal spora of Hong Kong as determined by the agar plate method. Transactions of the British Mycological Society 49 (2), 255-267. UPSHER, F.J. (1968). Fungal spora of the air at the Joint Tropical Research Unit, Innisfail, Queensland. Proceedings t st International Biodeterioration Symposium, Southampton, 9-14 Sept., 1968, 131-142. UPSHER, F. J. (1969). Fungal spora of the air at Joint Tropical Research Unit, Innisfail, Nov. 1966-Oct. 1967. Department of Supply, AustralianDefence Scientific Service, Defence Standards Laboratories ReportNo. 332. UPSHER, F.J. (1972). Fungi at Joint Tropical Research Unit, Innisfail, Queensland. Part 2. Species of fungi isolated. Department of Supply Australian Defence Scientific Service, Defence Standards Laboratories, Technical Note no. 235. VALLERy-RADOT, P., HALPERN, B. N., SECRETAIN, A. & DOMART, A. (1950). Etude de la nature et la densite de la flore mycologique dans I'atmosphere de Paris durante I'annee 1948. Acta allergologica 3, 179-197.

iAcceptedfor publication

12

April 1973)