International Journal of Biometeorology

, Volume 53, Issue 1, pp 61–73

The effects of meteorological factors on airborne fungal spore concentration in two areas differing in urbanisation level

Authors

  • M. Oliveira
    • Grupo de Ambiente, Sociedade e Educação do Centro de Geologia & Departamento de Botânica, Faculdade de CiênciasEdificio FC4
  • H. Ribeiro
    • Grupo de Ambiente, Sociedade e Educação do Centro de Geologia & Departamento de Botânica, Faculdade de CiênciasEdificio FC4
  • J. L. Delgado
    • Serviço e Laboratório de Imunologia, Faculdade de MedicinaUniversidade do Porto
    • Grupo de Ambiente, Sociedade e Educação do Centro de Geologia & Departamento de Botânica, Faculdade de CiênciasEdificio FC4
Original Paper

DOI: 10.1007/s00484-008-0191-2

Cite this article as:
Oliveira, M., Ribeiro, H., Delgado, J.L. et al. Int J Biometeorol (2009) 53: 61. doi:10.1007/s00484-008-0191-2

Abstract

Although fungal spores are an ever-present component of the atmosphere throughout the year, their concentration oscillates widely. This work aims to establish correlations between fungal spore concentrations in Porto and Amares and meteorological data. The seasonal distribution of fungal spores was studied continuously (2005–2007) using volumetric spore traps. To determine the effect of meteorological factors (temperature, relative humidity and rainfall) on spore concentration, the Spearman rank correlation test was used. In both locations, the most abundant fungal spores were Cladosporium, Agaricus, Agrocybe, Alternaria and Aspergillus/Penicillium, the highest concentrations being found during summer and autumn. In the present study, with the exception of Coprinus and Pleospora, spore concentrations were higher in the rural area than in the urban location. Among the selected spore types, spring-autumn spores (Coprinus, Didymella, Leptosphaeria and Pleospora) exhibited negative correlations with temperature and positive correlations both with relative humidity and rainfall level. On the contrary, late spring-early summer (Smuts) and summer spores (Alternaria, Cladosporium, Epicoccum, Ganoderma, Stemphylium and Ustilago) exhibited positive correlations with temperature and negative correlations both with relative humidity and rainfall level. Rust, a frequent spore type during summer, had a positive correlation with temperature. Aspergillus/Penicillium, showed no correlation with the meteorological factors analysed. This knowledge can be useful for agriculture, allowing more efficient and reliable application of pesticides, and for human health, by improving the diagnosis and treatment of respiratory allergic disease.

Keywords

Meteorological factorPortugalRural areaSpore concentrationUrban area

Introduction

Fungal spores are an ever-present component of the atmosphere and are present in almost all seasons of the year (Burch and Levetin 2002; Troutt and Levetin 2001). Nevertheless, sporulation and the dispersion of spores are closely related to variations in meteorological conditions (Angulo-Romero et al. 1999; Sabariego et al. 2000).

Knowledge of the relationships between spore production and different environmental growth conditions, such as meteorological factors, can be used to effect more efficient and reliable application of pesticides, or to improve diagnosis and treatment of respiratory allergic diseases (Rodríguez-Rajo et al. 2005).

Cladosporium, Alternaria, Epicoccum, and Dreschlera spores tend to be found in higher concentrations during warm, dry weather conditions with high wind speeds (Burch and Levetin 2002; Troutt and Levetin 2001). However, ascospores and basidiospores tend to be more frequent during wet or humid conditions. Precipitation is required for the release of many ascospores, their concentrations usually increasing during and after rainstorms; nevertheless, excessive rain tends to wash spores out of the atmosphere (Burch and Levetin 2002; Troutt and Levetin 2001).

The study of fungal spores is of critical importance since many of these bioparticles can induce considerable economic losses, acting as plant pathogens or triggering respiratory diseases and allergenic processes in humans. Most aeromycological studies are conducted in urban environments, with very little data from rural settings. Consequently, it is difficult to compare the presence and concentration of airborne fungal spores in the atmospheres of both urban and rural areas (Kasprzyk and Worek 2006). Nonetheless, previous studies have reported higher spore concentrations in inland rural areas than in coastal areas (Rodríguez-Rajo et al. 2005). In the present study, fungal spore concentrations in Porto (coastal urban area) and Amares (inland rural area) were correlated with meteorological data from 2005 to 2007. The purpose of this study was to analyse the content of several spore types in the air of two locations differing in urbanisation level, and to determine how different weather conditions affected spore concentrations in both locations.

Materials and methods

Daily spore concentrations were sampled between 1 January 2005 and 31 December 2007, using two 7-day Hirst-type volumetric spore traps (Burkard Manufacturing, Rickmansworth, UK) with a flow rate of 10 L min−1. Spores were trapped onto a Melinex adhesive tape, and then cut into daily segments. The slides with adhesive segments were covered with fucsin-stained glycerol jelly and with a cover glass. The daily mean concentration of the number of fungal spores was determined using an optical microscope at a magnification of ×400 along two full lengthwise traverses. Spore counts were then converted to spores per cubic metre of air sampled per day (spores m−3 day−1). Fungal spores were classified by appearance and morphological characteristics (colour, size and shape) and identified, where possible, by comparison with bibliographic material (Lacey and West 2006; Nilsson 1983).

In the coastal urban area (Porto), the sampler was located at Faculdade de Ciências (41°11′ N, 8°39′ W; height: 20 m) (Fig. 1). Porto district, in the Douro Litoral Region, has an area of 2,395 km2 and a population of nearly 1,900,000 inhabitants. Ornamental and non-ornamental trees, shrubs and herbaceous species surrounded the sampler. The west of this city borders the Atlantic Ocean while the south borders the river Douro. According to the reference values for Porto, from 1961 to 1990, the average maximum temperature was 19.1°C, and the average minimum temperature was 9.9°C (Meteorologia 1992). The total rainfall level during the reference period was 1,265 mm, concentrated mainly from December to February and largely absent during summer (Meteorologia 1992).
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Fig. 1

Sampler location in the two studied areas. In the coastal urban area of Porto, the sampler is surrounded by several buildings of different heights, and the surrounding flora is constituted by ornamental and non-ornamental trees, shrubs and herbaceous species. In the inland rural area of Amares, only a few small houses and greenhouses are present in the proximity of the sampler and the surrounding flora is constituted mainly by pine and eucalyptus forests, grape and kiwi vines and crop fields

In the inland rural area (Amares; near Braga), the sampler was located on a farm (41°38′N, 8°23′W; height: 5 m) (Fig. 1). The Braga District, in the ‘Vinhos Verdes’ Demarcated Region, has an area of 2,673 km2 and a population of around 830,000 inhabitants. This sampler was surrounded by greenhouses, forests and crop-producing fields.

During this study, the most abundant fungal spore types were divided in two sets. Alternaria, Cladosporium, Epicoccum, Drechslera, Ganoderma and Stemphylium were considered as dry-air spores, while Coprinus, Didymella, Leptosphaeria, Pleospora, and Ustilago were selected as wet-air spores. Moreover, Aspergillus/Penicillium spores were counted due to their role in human health. Rust (including species such as Puccinia and Uromyces) and Smuts spores (including species such as Urocystis and Tilletia) were chosen for their phytopathological importance.

The airborne spore concentration observed in both regions were standardised using a Z-scores transformation (the raw value to be standardised is subtracted from the sample mean and divided by the sample standard deviation) to allow comparisons between the two different locations.

Meteorological data were correlated with the airborne spore concentrations of the selected types by means of the Spearman rank correlation test, with a significance level of 99% and 95%. Afterwards, a multivariate hierarchical cluster analysis was carried out on the correlation coefficients obtained in both locations in order to identify possible homogeneous groups of fungal spores having similar relationships to meteorological parameters. To perform this analysis, the correlation coefficient values were recoded as 1 when significantly positive, −1 when significantly negative, and 0 when they were not significant. The number of clusters was determined using the Square Euclidean Distance as a distance measure, and the linking method used was the Ward method.

Results

In Porto and Amares, the lowest temperatures were recorded in the first months of the year, with the maximum temperatures being reached in August (Fig. 2). During the study period, the annual average, maximum and minimum temperatures, were 15.4°C, 20.2°C and 11.1°C, respectively, in Porto, and 15.7°C, 22.0°C and 10.3°C in Amares (Table 1).
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Fig. 2

Weather conditions registered in Porto and Amares (daily average values from 2005 to 2007). Both locations had similar temperatures and relative humidity values. Rainfall level was the most distinctive meteorological factor analysed, Amares being rainier than Porto

Table 1

Meteorological factors registered in the city of Porto and the rural area of Amares (2005–2007)

 

Tmeana

Tmaxa

Tmina

RHmeanb

RHmaxb

RHminb

Rtotalc

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

2005

15.0 ± 5.5

15.7 ± 6.0

19.8 ± 5.9

21.9 ± 7.0

10.9 ± 5.6

10.5 ± 5.8

72.5 ± 15.4

76.5 ± 18.4

90.5 ± 12.4

93.9 ± 12.5

52.3 ± 16.0

54.1 ± 20.9

698.7

1,011.8

2006

16.0 ± 5.5

15.8 ± 6.2

20.9 ± 6.2

21.8 ± 7.2

11.6 ± 5.4

10.8 ± 5.8

74.4 ± 14.4

82.1 ± 16.1

92.7 ± 10.6

96.1 ± 10.3

52.6 ± 15.5

60.6 ± 22.1

1,291.6

2,675.0

2007

15.1 ± 4.6

15.2 ± 5.2

20.6 ± 5.1

21.9 ± 5.8

11.2 ± 4.6

9.2 ± 5.4

73.0 ± 13.5

82.6 ± 13.3

91.7 ± 11.2

97.7 ± 7.1

51.0 ± 15.0

58.7 ± 19.4

661.0

856.6

Average

15.4 ± 5.3

15.7 ± 5.8

20.2 ± 5.8

22.0 ± 6.7

11.1 ± 5.3

10.3 ± 5.7

73.5 ± 14.5

80.2 ± 16.3

91.7 ± 11.5

95.9 ± 10.3

52.2 ± 15.6

57.4 ± 20.9

883.8 ± 353.7

1,514.5 ± 1,008.0

aTemperature (in °C)

bRelative humidity (in %)

cRainfall (in mm)

In both regions, the highest relative humidity values were recorded in the first month of the year, with minimum values being reached in the summer months (Fig. 2). In the urban area, the annual average relative humidity was 73.5%, the average maximum was 91.7% and the average minimum was 52.2%. In the rural area, the annual average relative humidity was 80.2%, the average maximum was 95.9% and the average minimum was 57.4% (Table 1).

Rainfall in Porto and Amares was concentrated mainly in the spring and autumn months (Fig. 2). The average value in the urban area was 883.3 mm, while it was 1,514.5 mm in the rural area. The maximum rainfall levels were registered in 2006 (Porto: 1,291.6 mm; Amares: 2,675.0 mm), while the minimum values were registered in 2007 in both locations (Porto: 661.0 mm; Amares: 856.6 mm) (Table 1).

A total of 50 fungal spore types were identified in the atmosphere, with the majority being present throughout the year (Table 2). In Porto, a total of 568,244 spores were recorded, reaching a maximum value of 8,509 spores/m−3 on 8 October 2007 (Table 3). The most abundant fungal spores were Cladosporium (60%), Agaricus (6%), Ganoderma (3%), Agrocybe (1%), Alternaria (1%), Smuts (1%), Rusts (1%) and Aspergillus/Penicillium (1%) (Fig. 3). In Amares, a total of 1,013,901 spores were recorded, reaching a maximum value of 8,761 spores/m−3 on 8 December 2007 (Table 3). The most abundant fungal spores were Cladosporium (64%), followed by Agaricus (4%), Agrocybe (1%), Alternaria (1%) and Aspergillus/Penicillium (1%) (Fig. 3).
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Fig. 3

Average annual distribution of the main spore types present in the atmosphere of Porto (urban area) and Amares (rural area), from 2005 to 2007. Only spore types constituting more than 1% of the airborne fungal spectrum are represented

Table 2

Fungal spore types found in the atmosphere of Porto and Amares from 2005 to 2007

Aerobasidium

Agaricus

Agrocybe

Albugo

Alternariaa

Aspergillus/Penicilliuma

Boletus

Botrytis

 

Cercospora

Cladosporiuma

Coprinusa

Corynespora

Curvularia

 

Didymellaa

Diplocladiella

Drechsleraa

Entomphthora

Epicoccuma

Erysiphe

Fusarium

  

Ganodermaa

Geoglossum

 

Helicomyces

  

Leptosphaeriaa

  

Nectria

Nigrospora

 

Oidium

  

Paraphaeosphaeria

Periconia

Peziza

Phoma

Pithomyces

Pleosporaa

Polythrincium

Puccinia

 

Rhizopus

Russula

Rustsa

Smutsa

Spegazinnia

Sporobolomyces

Sporomiella

Stachybotis

Stemphyliuma

Tilletia

Torula

 

Uromyces

Ustilagoa

 

Venturia

  

Xylaria

  

aFungal spore types considered in this study

Table 3

Spore distribution in the atmosphere of Porto and Amares from 2005 to 2007. Values are in spores/m−3

 Spore type

Year

Totala

Average

Maximum

Peak datea

Z score

Value above thresholdb

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Alternaria

2005

1,975

3,743

5 ± 9

10 ± 13

48

80

18 August

 

30 July

 

225

281

0

0

2006

1,882

3,175

5 ± 9

9 ± 14

81

104

29 August

 

22 June

 

203

225

0

1

2007

2,625

3,542

7 ± 12

10 ± 13

85

109

8 October

 

4 October

 

214

266

0

1

Aspergillus/Penincillium

2005

2,416

4,981

7 ± 17

14 ± 29

152

303

1 November

 

22 November

 

141

171

ndc

nd

2006

1,697

3,704

5 ± 13

10 ± 22

122

242

9 August

 

2 October

 

126

167

nd

nd

2007

1,054

2,419

3 ± 8

7 ± 13

87

98

4 June

 

17 April

 

127

180

nd

nd

Cladosporium

2005

111,536

216,988

306 ± 458

594 ± 679

2,972

4,682

31 July

 

4 June

 

243

319

0

4

2006

99,716

188,296

273 ± 494

516 ± 833

3,958

5,885

21 August

 

29-Sep

 

201

225

1

8

2007

127,054

229,226

348 ± 707

628 ± 966

8,297

7,567

8 October

 

4 October

 

179

237

4

13

Coprinus

2005

1,999

2,685

5 ± 8

7 ± 12

55

106

24 October

 

22 October

 

241

223

nd

nd

2006

1,466

2,589

4 ± 5

7 ± 13

35

133

9 March

27 March

7 October

 

282

202

nd

nd

2007

351

725

1 ± 2

2 ± 4

10

42

8 January

4 March

7 December

 

204

182

nd

nd

Didymella

2005

88

156

0 ± 1

0 ± 1

9

7

30 December

 

6 July

 

101

147

nd

nd

2006

213

235

1 ± 1

1 ± 2

9

12

15 November

5 December

13 September

28 September

147

138

nd

nd

2007

146

325

0 ± 2

1 ± 3

20

26

1 May

 

27 April

 

93

103

nd

nd

Drechslera

2005

55

76

0 ± 0

0 ± 1

4

6

30 July

 

22-Mar

 

121

134

nd

nd

2006

33

17

0 ± 0

0 ± 0

4

2

28 June

   

89

66

nd

nd

2007

70

58

0 ± 1

0 ± 0

4

2

20 September

7 October

  

124

135

nd

nd

Epicoccum

2005

546

1,310

1 ± 2

4 ± 5

15

28

30 July

 

18 October

 

232

279

nd

nd

2006

297

706

1 ± 1

2 ± 4

12

34

27 August

 

3 October

 

207

187

nd

nd

2007

623

1,180

2 ± 4

3 ± 6

52

63

7 October

 

5 October

 

152

199

nd

nd

Ganoderma

2005

7,807

633

21 ± 35

2 ± 3

190

21

9 September

 

30 August

 

220

235

nd

nd

2006

6,630

553

18 ± 28

2 ± 2

180

16

11 September

 

27 August

 

233

234

nd

nd

2007

4,934

370

14 ± 19

1 ± 2

121

11

14 September

 

7 September

 

255

219

nd

nd

Leptosphaeria

2005

185

688

1 ± 2

2 ± 5

16

43

29 October

 

4 April

 

111

143

nd

nd

2006

181

1,207

0 ± 2

3 ± 19

20

321

15 August

 

20 October

 

108

64

nd

nd

2007

150

494

0 ± 2

1 ± 4

32

38

19 November

 

7 December

 

74

117

nd

nd

Pleospora

2005

146

189

0 ± 1

1 ± 1

5

9

27 March

9 May

20 March

17 April

169

158

nd

nd

2006

275

263

1 ± 2

1 ± 2

15

14

18 March

 

20 October

 

158

152

nd

nd

2007

217

205

1 ± 2

1 ± 3

15

41

6 February

 

7 February

 

141

77

nd

nd

Rusts

2005

1961

2,597

5 ± 9

7 ± 12

97

105

8 November

 

7 November

 

211

223

nd

nd

2006

2,745

3,436

8 ± 12

9 ± 14

88

153

17 October

 

10 October

 

233

251

nd

nd

2007

1,141

1,555

3 ± 3

4 ± 8

20

127

19 September

 

5 October

 

328

199

nd

nd

Smuts

2005

2,575

2,436

7 ± 17

7 ± 8

200

50

8 August

 

4 April

 

150

293

nd

nd

2006

2,553

2,162

7 ± 17

6 ± 11

157

73

30 May

 

10 May

 

147

201

nd

nd

2007

1,664

1,603

5 ± 10

4 ± 9

113

87

12 May

 

9 May

 

167

170

nd

nd

Stemphylium

2005

179

150

0 ± 1

0 ± 1

8

5

4 July

 

27 June

16 October

176

186

nd

nd

2006

191

153

1 ± 1

0 ± 1

11

9

17 June

 

15 June

 

157

142

nd

nd

2007

258

228

1 ± 1

1 ± 1

17

12

4 July

 

3 October

 

157

181

nd

nd

Ustilago

2005

251

338

1 ± 2

1 ± 2

19

16

8 May

 

13 August

 

159

188

nd

nd

2006

173

221

0 ± 1

1 ± 1

15

12

6 February

19 June

29 June

 

122

159

nd

nd

2007

97

132

0 ± 1

±1

12

22

15 July

 

9 October

 

105

97

nd

nd

Total

2005

180,488

325,223

494 ± 533

891 ± 775

3,248

4,755

31 July

 

4 June

 

338

419

nd

nd

2006

195,874

336,926

537 ± 593

923 ± 1,069

4,153

7,119

21 August

 

29 September

 

329

314

nd

nd

2007

191,882

351,752

525 ± 784

964 ± 1,123

8,509

8,761

8 October

 

8 December

 

244

312

nd

nd

aWhen spore concentrations presented more than two peaks, dates are not shown

bAlternaria threshold value: 100 spores/m3; Cladosporium threshold value: 3,000 spores/m3

cNot determined

Among the spore types analysed, it was possible to distinguish spores present throughout the year in variable concentrations (Alternaria, Cladosporium, Coprinus, Rusts and Smuts) and spores with sporadic occurrence (Aspergillus/Penicillium) or present in annual concentrations below 1,000 spores (Didymella, Drechslera, Leptosphaeria, Pleospora, Stemphylium and Ustilago). Epicoccum and Ganoderma had different patterns according to location, being frequent in Porto, but sporadic in Amares. On a seasonal basis, in both locations, the selected spore types presented higher airborne concentrations during late summer and early autumn (September and October) while the lowest concentrations were registered in the winter months (January–February) (Figs. 4, 5).
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Fig. 4

Monthly seasonal variation of Alternaria, Aspergillus/Penincillium, Cladosporium, Coprinus, Didymela, Drechslera and Epicoccum in the atmosphere of Porto (urban area) and Amares (rural area) from 2005 to 2007. Higher airborne concentrations were found during late summer and early autumn while the lowest concentrations were registered in winter months

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Fig. 5

Monthly seasonal variation of Ganoderma, Lepthosphaeria, Pleospora, Rusts, Smuts, Stemphylium and Ustilago in the atmosphere of Porto (urban area) and Amares (rural area) from 2005 to 2007. Higher airborne concentrations were found during late summer and early autumn while the lowest concentrations were registered in winter months

Coprinus, Didymella, Lepthosphaeria and Pleospora presented two peaks during the year, one during spring and other during autumn (Figs. 4, 5). Coprinus spore concentration was in the range of 351–1,999 spores/m−3 in Porto, and 725–2,685 spores/m−3 in Amares; Didymella spore concentration in the urban area varied from 88 to 213 spores/m−3 and from 156 to 325 spores/m−3 in the rural area; Lepthosphaeria spore concentration oscillated from 150 to 185 spores/m−3 in Porto, and from 494 to 1,207 spores/m−3 in Amares; and Pleospora spore concentration ranged from 146 to 275 spores/m−3 in the urban area, and from 189 to 263 spores/m−3 in the rural area (Table 3).

Smuts spores were most frequent during late spring and summer (Figs. 4, 5). Spore concentration ranged from 1,664 to 2,575 spores/m−3 in Porto, and from 1,603 to 2,436 spores/m−3 in Amares, with a peak in May (Table 3).

During summer, the most frequent spores were Alternaria and Cladosporium (Figs. 4, 5). Alternaria spore concentration ranged from 1,882 to 2,625 spores/m−3 in Porto, and from 3,175 to 3,743 spores/m−3 in Amares, the highest values being registered from June to October. In the rural area, the Alternaria threshold (100 spores/m−3) was surpassed once in 2006 and 2007. Cladosporium spore concentration in the urban area varied from 99,716 to 127,054 spores/m−3, and in the rural area from 188,296 to 229,226 spores/m−3, the highest values being registered from June to October. In Porto, the Cladosporium threshold (3,000 spores/m−3) was exceeded 30 times, five in Porto and 25 in Amares (Table 3).

In late summer and early autumn, Epicoccum, Ganoderma, Stemphylium and Ustilago spores were abundant in the atmosphere (Figs. 4, 5). Epicoccum spore concentration ranged from 297 to 623 spores/m−3 in Porto, and 706 to 1,310 spores/m−3 in Amares, and maximum value dates were registered in July and October. Ganoderma spore concentration in the urban area varied from 4,934 to 7,807 spores/m−3 and from 370 to 633 spores/m−3 in the rural area, peak dates being registered from August to September. Stemphylium spore concentration oscillated from 179 to 258 spores/m−3 in the city, and from 150 to 228 spores/m−3 in the country, maximum value dates being registered in June, July and October. Ustilago concentration ranged from 97 to 251 spores/m−3 in Porto, and 132 to 338 spores/m−3 in Amares, maximum dates being registered in February, May, June and July in the urban area and in June, August and October in the rural location (Table 3).

The maximum value of Rusts as well as the maximum monthly values of Aspergillus/Penicillium were registered during autumn (Figs. 4, 5). Rusts spore concentration varied from 1,141 to 2,745 spores/m−3 in Porto, and from 1,555 to 3,436 spores/m−3 in Amares while Aspergillus/Penicillium spore concentration oscillated from 1,054 to 2,416 spores/m3 in the urban area, and from 2,419 to 4,981 spores/m−3 in the rural area, peak dates being registered in April, June, August, October and November (Table 3).

Finally, Drechslera spore concentration ranged from 33 to 70 spores/m−3 in Porto, and from 17 from 76 spores/m−3 in Amares, maximum value dates being registered in March and June–October.

The standardised values of each airborne spore concentration observed in both regions showed that higher concentrations of Alternaria, Aspergillus/Penicillium, Cladosporium and Smuts were found in the rural area during the 3 years of the study, while Coprinus and Pleospora had higher concentrations in the urban area. However, Didymella, Leptosphaeria, Drechslera, Epicoccum, Stemphylium, Rust and Ustilago spores did not exhibit a consistent behaviour (Table 3).

According to the correlation coefficients obtained and the cluster analysis performed, it was possible to establish four different groups: (1) Aspergillus/Penicillium, Ustilago and Rusts spores lacking any correlation or consistent correlation with the meteorological factors analysed; (2) Alternaria, Cladosporium, Epicoccum and Smuts spores exhibiting positive correlations with temperature and negative correlations with relative humidity and rainfall level; (3) Coprinus, Didymella, Leptosphaeria and Pleospora spores with negative or inconsistent correlations with temperature and positive correlations with relative humidity and rainfall level; (4) Drechslera, Ganoderma and Stemphylium spores, which presented positive correlations with temperature and inconsistent or no correlation with relative humidity or rainfall level (Table 4, Fig. 6).
https://static-content.springer.com/image/art%3A10.1007%2Fs00484-008-0191-2/MediaObjects/484_2008_191_Fig6_HTML.gif
Fig. 6

Dendogram of fungal spores studied derived by hierarchical cluster analysis from the dissimilarity matrix of the correlation coefficients between spore atmospheric concentrations and meteorological factors (mean maximum and minimum temperature, relative humidity, and total precipitation). Distances between accessions are shown by the length of the horizontal connecting segments, with their values given by a bar at the top of the figure

Table 4

Correlations between fungal spore concentrations and meteorological factors in Porto and Amares (2005–2007)

Spore type

Year

Tmean

Tmax

Tmin

RHmean

RHmax

RHmin

Ptotal

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Porto

Amares

Alternaria

2005

0.546**

0.755**

0.554**

0.761**

0.504**

0.673**

-0.182**

-0.282**

-0.114*

-0.162**

-0.153**

-0.274**

-0.250**

-0.302**

2006

0.582**

0.705**

0.590**

0.709**

0.531**

0.628**

-0.361**

-0.256**

-0.189**

-

-0.367**

-0.276**

-0.285**

-0.340**

2007

0.601**

0.567**

0.640**

0.624**

0.524**

0.381**

-0.349**

-0.324**

-0.284**

-

-0.288**

-0.298**

-0.312**

-0.320**

Aspergillus/Penincillium

2005

-

-

-

-

-

-

-

-

-

-

-

-

-

-

2006

-

-

-

-

-

-

-

-

-

-

-

-

-

-

2007

-

-

-

-

-

-

-

-

-

-

-

-

-

-

Cladosporium

2005

0.353**

0.608**

0.340**

0.585**

0.359**

0.587**

-

-0.109*

-

-

-

-0.124*

-0.106*

-

2006

0.472**

0.633**

0.456**

0.619**

0.454**

0.602**

-0.336**

-0.170**

-0.187**

-

-0.303**

-0.191**

-0.271**

-0.210**

2007

0.473**

0.364**

0.520**

0.409**

0.403**

0.217**

-0.319**

-0.125*

-0.255**

-

-0.276**

-0.124

-0.264**

-0.194**

Coprinus

2005

-0.257**

-0.205**

-0.283**

-0.269**

-0.203**

-

0.318**

0.487**

0.293**

0.296**

0.281**

0.483**

0.292**

0.424**

2006

-0.451**

-0.348**

-0.423**

-0.401**

-0.424**

-0.228**

0.348**

0.550**

0.241**

0.284**

0.277**

0.543**

0.251**

0.441**

2007

-0.326**

-0.252**

-0.362**

-0.289**

-0.294**

-0.145**

0.290**

0.356**

0.287**

0.189**

0.218**

0.290**

0.307**

0.276**

Didymella

2005

-

-0.107*

-0.185**

-0.211**

-

-

0.292**

0.402**

0.138**

0.281**

0.297**

0.376**

0.459**

0.462**

2006

-0.125*

-0.212**

-0.182**

-0.289**

-

-

0.224**

0.432**

-

0.193**

0.209**

0.416**

0.456**

0.506**

2007

-0.109*

-0.121*

-0.192**

-0.214**

-

-

0.282**

0.362**

0.229**

0.187**

0.232**

0.377**

0.371**

0.319**

Drechslera

2005

0.192**

0.148**

0.193**

0.140**

0.183**

0.123*

-

-

-

-

-

-

-

-

2006

0.103*

0.147**

-

0.144**

-

0.127*

-

-

-

-

-

-

-

-

2007

0.262**

0.239**

0.294**

0.274**

0.231**

0.153**

-

-0.166**

-

-

-

-0.175**

-0.169**

-0.160**

Epicoccum

2005

0.328**

0.512**

0.333**

0.516**

0.307**

0.462**

-

-

-

-

-

-0.113*

-0.159**

-0.151**

2006

0.329**

0.476**

0.340**

0.475**

0.303**

0.427**

-0.184**

-

-

-

-0.171**

-0.121*

-0.199**

-0.173**

2007

0.390**

0.249**

0.423**

0.341**

0.338**

-

-0.207**

-0.147**

-0.199**

-

-0.182**

-0.168**

-0.274**

-0.231**

Ganoderma

2005

0.478**

0.646**

0.426**

0.659**

0.507**

0.587**

0.288**

-

0.234**

-

0.268**

-0.103*

-

-0.130*

2006

0.479**

0.555**

0.457**

0.541**

0.462**

0.496**

-0.133*

-0.117*

-

0.109*

-0.113*

-0.138**

-

-0.227**

2007

0.535**

0.371**

0.548**

0.436**

0.469**

0.241**

-

-0.123*

-

-

-

-0.137**

-0.168**

-0.207**

Leptosphaeria

2005

-

-0.172**

-0.133*

-0.241**

-

-

0.293**

0.467**

0.156**

0.326*

0.277**

0.447**

0.393**

0.426**

2006

-

-

-

-0.151**

-

-

0.137**

0.448**

-

0.261**

-

0.464**

0.332**

0.447**

2007

-

-

-0.126*

-0.179**

-

-

0.136**

0.275**

-

-

0.118*

0.294**

0.225**

0.234**

Pleospora

2005

-0.181**

-0.155**

-0.233**

-0.249**

-0.110*

-

0.240**

0.324**

0.131*

0.175**

0.272**

0.330**

0.389**

0.405**

2006

-0.207**

-0.162**

-0.257**

-0.260**

-0.127*

-

0.221**

0.470**

-

0.227**

0.168**

0.454**

0.444**

0.505**

2007

-0.229**

-

-0.304**

-0.111**

-0.161**

0.109*

0.218**

0.225**

0.168**

-

0.178**

0.238**

0.348**

0.269**

Rusts

2005

-0.280**

-0.250**

-0.266**

-0.250**

-0.268**

-0.219**

-

-

-

-

-

-

0.125*

0.175**

2006

0.216**

0.164**

0.205**

0.156**

0.207**

0.183**

-

-

-

-

-

-

-

-

2007

0.281**

0.340**

0.286**

0.334**

0.245**

0.272**

-0.234**

-0.119*

-0.224**

-

-0.194**

-

-0.111*

-

Smuts

2005

0.349**

0.454**

0.351**

0.449**

0.344**

0.380**

-0.146**

-0.228**

-0.175**

-0.124*

-0.105*

-0.221**

-0.174**

-0.238**

2006

0.376**

0.485**

0.337**

0.520**

0.372**

0.390**

-0.275**

-0.329**

-0.236**

-

-0.214**

-0.349**

-0.300**

-0.341**

2007

0.300**

0.319**

0.278**

0.292**

0.264**

0.278**

-0.137**

-0.104*

-

-

-0.124*

-

-

-0.156**

Stemphylium

2005

0.386**

0.391**

0.369**

0.364**

0.380**

0.381**

-

-

-

-

-

-

-0.121*

-

2006

0.386**

0.325**

0.385**

0.320**

0.379**

0.283**

-0.187**

-

-

-

-0.188*

-

-0.171**

-

2007

0.374**

0.497**

0.342**

0.449**

0.338**

0.459*

-

-0.156**

-

-

-

-0.113*

-

-

Ustilago

2005

-

0.133*

-

0.180**

-

-

-0.208**

-0.314**

-0.158**

-0.263**

-0.199**

-0.301**

-0.233**

-0.264**

2006

-

-

-

0.103*

-

-

-

-0.220**

-

-

-

-0.234**

-0.124*

-0.248**

2007

-

-

-

-

-

-0.195*

-0.167**

-

-

-

-0.186**

-0.111*

-

-

*P < 0.05; **P < 0.01; only significant correlations are presented

Discussion

During 2005, Amares suffered two heat waves, the first from 30 May to 11 June, and the second from 13 to 25 June (Meteorologia 1992). No data was available for the other study years, which might explain the reduced values of Aspergillus/Penicillium and total spores observed in May and June in the rural area not matching the same behaviour as in the urban area. Also, in July, Alternaria, Cladosporium and total spore concentration in Amares was higher in 2005 than in other years, and did not correspond to the same pattern as in Porto, which may also have been influenced by the high temperatures registered during the preceding months.

Only 2006 had a rainfall level comparable to the reference value, although in the other years approximately half of the average annual value was registered. Again, in Amares, the reference rainfall value was surpassed only in 2006. During this year, high values of Didymella, Leptosphaeria, Pleospora, Rusts and Smuts and low values of Alternaria, Cladosporium, Drechslera, Epicoccum and Ustilago were observed in Amares, particularly in October and November — the months with the heaviest rainfall levels of the year.

The seasonal behaviour of Alternaria spores registered in this work has also been observed by several other authors (Bruno et al. 2007; Corden and Millington 2001; Mitakakis and Guest 2001; Myszkowska et al. 2002; Oliveira et al. 2005). However, in Murcia and Córdoba (Spain), these spores presented as two peaks as a consequence of the summer drop in concentration (Angulo-Romero et al. 1999; Giner et al. 2001). As shown here, Alternaria spores had a positive correlation with temperature and negative correlations with relative humidity and rainfall level. Similar results were obtained in a previous study that demonstrated positive correlations between Alternaria spore concentration and temperature (maximum and minimum) and sunshine hours, and a negative correlation with relative humidity (Fernández et al. 1998).

Aspergillus/Penicillium spore concentration was rather constant throughout the study years, with a slight increase in middle autumn. Using different sampling techniques, the highest concentrations of Aspergillus spores were found in October or during winter (Mullins et al. 1984; Rosas et al. 1990). A previous work on Penicillium spore concentrations in a tropical region reported a constant spore concentration between the dry and rainy season, while no differences were observed in locations of different urbanisation index (Rosas et al. 1993). In this study no correlations were found between Aspergillus/Penicillium spore concentrations and the meteorological factors analysed. This result was consistent with that of a previous study where this spore type did not present any correlation with temperature (Li and Kendrick 1995). This lack of association between spore occurrence and the analysed meteorological data could be explained by the sporadic behaviour of these spores.

Worldwide, including several regions with different weather conditions, Cladosporium spores are reported to be the most abundant fungal spore found in the atmosphere (Damialis and Gioulekas 2006; Gillum and Levetin 2008; Hasnain et al. 2005; Henriquez et al. 2001; Herrero et al. 2006; Mitakakis and Guest 2001; Myszkowska et al. 2002; Oliveira et al. 2005; Pepeljnjak and Segvi 2003). Previous works reported results similar to those observed in our study, where increases in Cladosporium concentration were registered in April – May; a maximum was reached during autumn, with the lowest concentrations being found in January and February (Henriquez et al. 2001; Herrero et al. 2006; Oliveira et al. 2005). Nevertheless, in Australia, this spore type presented a peak spanning spring, summer and autumn (Mitakakis and Guest 2001). In the present work, Cladosporium spores presented a positive correlation with temperature and negative correlations with relative humidity and rainfall level. Previous studies also confirmed the positive influence of temperature and the negative influence of relative humidity and rainfall on the concentration of this spore type (Katial et al. 1997; Molina et al. 1998).

The present work demonstrates that Epicoccum spores showed a positive correlation with temperature and negative correlations with relative humidity and rainfall level. However, it has been reported that Epicoccum spores do not have a significant relationship with temperature (Li and Kendrick 1995).

Ganoderma spore concentration peaked from August to September, having a positive correlation with temperature. Rust maximum values were registered during autumn; these spores also had a positive correlation with temperature (in 2006 and 2007). Smut spores were most frequent during late spring and summer, and were positively correlated with temperature and negatively correlated with relative humidity and rainfall level. Ustilago, a sporadic behaviour-spore, presented similar concentrations throughout the year, being negatively correlated with relative humidity and rainfall. In Badajoz (Spain), the basidiospores, including Coprinus, Ganoderma, Rusts, Smuts and Ustilago, were present in the atmosphere mainly during autumn. The maximum concentrations were found in November, with the lowest values being found during summer (Gonzalo et al. 1997). Negative correlations were obtained with thermal factors while positive correlations were registered with relative humidity. Nevertheless, no correlation with rainfall was observed (Gonzalo et al. 1997).

Similarly to the results presented in the current work, it has been previously reported that the total number of fungal spores and the frequency of occurrence of some types are higher in rural than in urban areas (Guinea et al. 2006). However, only a few studies have compared spore concentrations in the two environments. An exception is Aspergillus/Penicillium spores, for which more isolates were found in urban than in the rural areas (Guinea et al. 2006; Rosas et al. 1993). In the case of Porto and Amares, the Aspergillus/Penicillium spore concentration was also higher in the rural area. These differences may be associated with several factors, such as the distribution of forests, occurrence of crops, weeds or even livestock that may play a role as intermediary host for mould development, increasing spore concentration. Besides that, farming operations create mechanical disturbances allowing fungal spore release.

Another interesting factor was to compare data from the z scores of transformation with data from the correlation with meteorological factors. Alternaria, Aspergilaceae, Cladosporium, Smuts, Coprinus and Pleospora had both consistent correlations and distribution among the two regions. In contrast, Didymella, Drechslera, Epicoccum, Leptosphaeria, Stemphylium, Rust and Ustilago were inconsistent in the two sets of data. This fact highlights the importance of joint studies of Aerobiology and Meteorology.

Conclusions

On a seasonal basis, in Porto (urban coastal area) and in Amares (inland rural area), the selected spore types had higher airborne concentrations during late summer and early autumn while the lowest concentrations were registered in the winter months.

In the present study, spore concentrations of the selected types were compared in both locations, it being possible to conclude that Alternaria, Aspergillus/Penincillium, Cladosporium and Smuts were found in higher concentrations in the rural area, while Coprinus and Pleospora exhibited higher concentrations in the urban area.

As a summary and in general terms, it is possible to affirm that, among the selected spore types, spring–autumn spores (Coprinus, Didymella, Leptosphaeria and Pleospora) showed a negative correlation with temperature and positive correlations with both relative humidity and rainfall level. In contrast, late spring–early summer (Smuts) and summer spores (Alternaria, Cladosporium, Epicoccum, Ganoderma, Stemphylium and Ustilago) exhibited positive correlations with temperature and negative correlations both with relative humidity and rainfall level. One exception is Rust, which, besides being frequent during summer, had a positive correlation only with temperature. Furthermore, Aspergillus/Penicillium showed no correlation with any of the meteorological factors analysed.

Acknowledgements

The authors are grateful to Prof. Dr. Manuel de Barros, from the Instituto Geofísico da Universidade do Porto, and Eng. Guerner-Moreira, from the Direcção Regional de Agricultura e Pescas do Norte - Divisão de Protecção e Controle Fitossanitário, for the meteorological data provided. This work was partially supported by Fundação Calouste Gulbenkian (project: 77161) and a grant from the Fundação para a Ciência e Tecnologia (SFRH/BD/18765/2004).

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© ISB 2008