RESEARCH PAPER
New findings of airborne fungal spores in the atmosphere of Havana, Cuba, using aerobiological non-viable methodology
1
Department of Microbiology and Virology, Faculty of Biology, University of Habana, La Habana 10400, Cuba
2
Department of Botany, Faculty of Pharmacy, University of Santiago, Santiago de Compostela 15782, Spain
3
Department of Plant Biology and Soil Sciences, Faculty of Sciences, University of Vigo, 32004 Ourense, Spain
Ann Agric Environ Med. 2018;25(2):349–359
KEYWORDS
TOPICS
ABSTRACT
Introduction:
Although airborne fungal diversity in tropical countries is known to be considerable, aerobiological research to-date has identified only a part of the fungal mycobiota that may have an impact both on human health and on crops. Previous studies in Havana city identified only 30 genera and 5 spore types; therefore,new research is required in these latitudes. This study sought to investigate airborne spore levels in Havana, with a view to learning more about local fungal diversity and assessing its influence in quantitative terms.
Material and methods:
A Hirst type volumetric sampler was located on the rooftop of a building 35 meters above ground level, in a busy area of the city. Sampling was carried out continuously (operating 24hours/day), at 10 L per minute during the year 2015. The fungal spores were collected on a Melinex tape coated with a 2% silicone solution. The results were expressed as spores per cubic meter (spores/m3) of air when to referring to daily values, and spores count if referring to annual value.
Results:
Fourteen new genera were identified in the course of volumetric sampling: six produce ascospores and eight conidia. Morphobiometric characteristics were noted for all genera, and airborne concentrations were calculated. These genera accounted for 56.4% of relative fungal frequency over the study year.
Conclusions:
Many airbone fungi are primary causes of both respiratory disease and crop damage. These new findings constitute a major contribution to Cuba’s aerobiological database.
Although airborne fungal diversity in tropical countries is known to be considerable, aerobiological research to-date has identified only a part of the fungal mycobiota that may have an impact both on human health and on crops. Previous studies in Havana city identified only 30 genera and 5 spore types; therefore,new research is required in these latitudes. This study sought to investigate airborne spore levels in Havana, with a view to learning more about local fungal diversity and assessing its influence in quantitative terms.
Material and methods:
A Hirst type volumetric sampler was located on the rooftop of a building 35 meters above ground level, in a busy area of the city. Sampling was carried out continuously (operating 24hours/day), at 10 L per minute during the year 2015. The fungal spores were collected on a Melinex tape coated with a 2% silicone solution. The results were expressed as spores per cubic meter (spores/m3) of air when to referring to daily values, and spores count if referring to annual value.
Results:
Fourteen new genera were identified in the course of volumetric sampling: six produce ascospores and eight conidia. Morphobiometric characteristics were noted for all genera, and airborne concentrations were calculated. These genera accounted for 56.4% of relative fungal frequency over the study year.
Conclusions:
Many airbone fungi are primary causes of both respiratory disease and crop damage. These new findings constitute a major contribution to Cuba’s aerobiological database.
REFERENCES (82)
1.
Frenguelli G. The contribution of aerobiology to agriculture. Aerobiologia. 1998; 14(2–3): 95–100.
2.
Mandrioli P, Ariatti A. Aerobiology: future course of action. Aerobiologia. 2001; 7(1): 1–10.
3.
Haddrell AE, Thomas RJ. Aerobiology: experimental considerations, observations, and future tools. Appl Environ Microbiol. 2017; 83(17): e00809–17.
4.
Ayesha T, Bhajbhuje MN. Diversity of air-borne mycoflora from indoor environment of library. Int J Life Sci. 2017; 5(2): 203–10.
5.
Bezerra GFDB, Gomes SM, Silva MACND, Santos RMD, Muniz Filho WE, et al. Diversity and dynamics of airborne fungi in São Luis, State of Maranhão, Brazil. Rev Soc Bras MedTrop. 2014; 47(1):69–73.
6.
Quintero E, Rivera-Mariani F, Bolaños-Rosero B. Analysis of environmental factors and their effects on fungal spores in the atmosphere of a tropical urban area (San Juan, Puerto Rico). Aerobiologia. 2010;26(2): 113–124.
7.
Hasnain SMFK, Al-Frayg A, Al-Sedairy ST. Prevalence of airborne basidiospores in three coastal cities of Saudi Arabia. Aerobiologia. 2005; 21: 139–45.
8.
Venero SJ, Varona P, Fabret D, Suárez R, Bonet M, Molina E. Asma bronquial y rinitis en escolares de Ciudad de La Habana (2001 a 2002). Revista Cubana de Higiene y Epidemiología. 2010; 47(1): 1–5.
9.
Caraballo L, Zakzuk J, Lee BW, et al. Particularities of allergy in the Tropics. World Allergy Organ J. 2016; 9: 20. doi:10.1186/s40413-016-0110-7.
10.
Caraballo L, Puerta L, Fernandez-Caldas E, Lockey RF, Martinez B. Sensitization to mite allergens and acute asthma in a tropical environment. J Investig Allergol Clin Immunol. 1998; 8(5): 281–4.
11.
Almaguer M, Aira MJ, Rodríguez-Rajo FJ, Rojas TI. Study of airborne fungus spores by viable and non-viable methods in Havana, Cuba. Grana. 2013; 52(4): 289–298.
12.
Sánchez KC, Almaguer M. Efecto de la temperatura sobre aislados de Cladosporium cladosporioides recolectados del aire de La Habana, Cuba. NACC. 2018; 25:21–29.
13.
Fernández-González M, Ramos-Valcárcel D, Aira MJ, Rodríguez-Rajo FJ. Prediction of biological sensors appearance with ARIMA models as a tool for Integrated Pest Management protocols. Ann Agric Environ Med. 2016; 3(1): 129–37. doi: 10.5604/12321966.1196868.
14.
Manzano JMM, Molina RT, Rodríguez SF, Barroso PD, Palacios IS, Garijo AG. Airborne propagules of Phytophthora and related taxa in SW Spain including a predictive model. Eur J Plant Pathol. 2015; 143(3): 473–483.
15.
Levetin E. Aerobiology of Agricultural Pathogens, p 3.2.8–1–3.2.8–20. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. 2016.
16.
Almaguer M, Rojas TI, Rodríguez-Rajo FJ, Aira MJ. Airborne fungal succession in a rice field of Cuba. Eur J Plant Pathol. 2012; 133: 473–482.
17.
Di Carlo E, Chisesi R, Barresi G, Barbaro S, Lombardo G, Rotolo V, Sebastianelli M, Travagliato M, Palla F. Fungi and bacteria in indoor cultural heritage environments: microbial-related risks for artworks and human health. Environ Ecol Res. 2016; 4(5): 257–264.
18.
Rojas TI, Aira MJ. Fungal biodiversity in indoor environments in Havana, Cuba. Aerobiologia. 2012; 28(3): 367–374.
19.
Anaya M, Borrego S, Gámez E, Castro M, Molina A, Valdés O. Viable fungi in the air of indoor environments of the National Archive of the Republic of Cuba. Aerobiologia. 2016; 32: 513–527.
20.
Prasla I, Duman K, Ciochetto Z, Burman A, Mahon A, Park S. et al. Significant heterogeneity in airborne mold quantities on the Caribbean Island of St. Kitts: Health implications and impact on food preservation. Virol Mycol. 2013; 3(1):1–5.
21.
Ravikala KL, Nagalakshamma KV. Survey on outdoor airborne fungal spores of Tumkur city, Karnataka state, India. Int J Pharma BioSciences. 2016; 7(1): 575–577.
22.
Almaguer M, Aira MJ, Rodríguez-Rajo FJ, Rojas TI. Temporal dynamics of airborne fungi in Havana (Cuba) during dry and rainy seasons: influence of meteorological parameters. Int J Biometeorol. 2014; 58(7): 1459–1470.
23.
Katelaris C H, Beggs, PJ. Climate change: allergens and allergic diseases. Internal Medicine Journal. 2018; 48(2): 129–134.
24.
Castillo L, Pastrana JC. Diagnóstico del arbolado viario de El Vedado: composición, distribución y conflictos con el espacio construido. Arquitectura y Urbanismo. 2015; 36(2): 93–118.
25.
Rosete CS, Pérez CJ, Ricardo NE, Sánchez O. Bosques de Cuba. Editorial Científico Técnica, La Habana, 2011.
26.
Hirst JM. An automatic volumetric spore trap. Ann Appl Biol. 1952; 39: 257–65. doi:10.1111/j.1744–7348.1952.tb00904.x.
27.
Galán, C., P. Cariñanos, P. Alcázar, and E. Dominguez. Manual of quality and management of the Spanish aerobiology network. Servicio de Publicaciones de la Universidad de Córdoba, Spain, 2007.
28.
Cotos-Yáñez TR, Rodríguez-Rajo FJ, Pérez-González A, Aira MJ, Jato V. Quality control in aerobiology: comparison different slide reading methods. Aerobiologia. 2013; 29(1): 1–11.
29.
Oteros J, Galán C, Alcázar P, Domínguez-Vilches E. Quality control in bio-monitoring networks, Spanish Aerobiology Network. Sci. Total Environ. 2013; 443: 559–565.
31.
Ellis MB. Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew, Survey, England, CMI, 1971.
32.
Ellis MB. More Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew. England, 1976.
33.
Grant E. Sampling and identifying allergenic pollens and molds. Blewstone Press, San Antonio, 1990.
35.
Hoog GS, Guarro J, Gené J, Figueras MJ. Atlas of Clinical Fungi. 2 nd edition Centraalbureau voor Schimmelcultures/ Universitat Rovira i Virgili, 2000.
36.
Barnett HL, Hunter BB. Illustrated genera of imperfect fungi. (4th ed.). St Paul, Minnesota: APS Press, 2003.
38.
Seifert K, Morgan-Jhones G, Gams W, Kendrick B. The Genera of Hyphomycetes. CBS-KNAW Fungal Biodiversity Centre, Utrecht. The Netherlands, 2011.
40.
Zhao GZ, Cao AX, Zhang TY, Liu XZ. Acrodictys (Hyphomycetes) and related genera from China. Mycol Progress. 2011; 10:67–83.
41.
Zhang Y, Crous PW, Schoch CL, Hyde KD. Pleosporales. Fungal Diversity. 2012; 53(1): 1–221.
42.
Crous PW, Groenewald JZ. A phylogenetic re-evaluation of Arthrinium. International Mycological Association. IMA fungus. 2013; 4(1): 133–154.
43.
Stat. Soft Inc. STATISTICA for Windows. 2001; Computer program manual. Tulsa, OK.
44.
Agashe SN, Caulton E. Pollen and Spores: Applications with special emphasis on Aerobiology and Allergy, CRC Press, 2009.
45.
Kaczmarek J, Jędryczka M. Characterization of two coexisting pathogen populations of Leptosphaeria spp., the cause of stem canker of Brassicas. Acta Agrobotanica. 2001; 64(2):3–14.
46.
Sabariego S, Díez A, Gutiérrez M. Monitoring of airborne fungi in Madrid (Spain). Acta Botanica Croata. 2007; 66(2): 117–126.
47.
Nikkels AH, Terstege P, Spieksma FThM. Ten types of microscopically identifiable airborne fungal spores at Leiden, The Nethertlands. Aerobiologia. 1996; 12: 107–112.
48.
Hasnain S, Akhter T, Waqar M. Airborne and allergenic fungal spores of the Karachi environment and their correlation with meteorological factors. J Env Monit. 2012; 14: 1006–1013.
49.
Ezike DN, Nnamani CV, Ogundipe OT, Adekanmbi OH. Airborne pollen and fungal spores in Garki, Abuja (North-Central Nigeria). Aerobiologia. 2016; 32:697–707.
50.
Grinn-Gofroń A. The variation in spore concentrations of selected fungal taxa associated with weather conditions in Szczecin, Poland, 2004–2006. Grana. 2008; 47(2): 139–146.
51.
Ibáñez V, Villegas GR, Nolla JMR. Airborne fungi monitoring in Santiago, Chile. Aerobiologia. 2001; 17(2): 137–142.
52.
Herrera L, Carrazana D, Quiñones, R. Los hongos anemófilos de la ciudad de Santa Clara, Cuba. Centro Agrícola. 2003; 3(30): 78–83.
53.
Almaguer M, Sánchez KC, Díaz L. Lasiodiplodia theobromae en la atmósfera de La Habana. Revista Cubana de Ciencias Biológicas. 2016; 5(1): 130–134.
54.
Camino M, Mena J, Minter DW. Fungi of Cuba. www.cybertruffle.org.uk/cubafung (access: 2016.11.02).
55.
Martyn E B. A note on banana leaf speckle in Jamaica and some associated fungi. Mycol Papers. 1945; 13: 1–5.
56.
Huanyu L, Zhang R, Guangyu S, Batzer JC, Gleason ML. New species and record of Zygophiala on apple fruit from China. Mycol Progress. 2010; 9(2): 245–251.
57.
Poonyth AD, Hyde KD, Aptroot A, Peerally A. Mauritiana rhizophorae gen. et sp. nov. (Ascomycetes, Requienellaceae), with a list of terrestrial saprobic mangrove fungi. Fungal Diversity. 2000; 4: 101–116.
58.
Sousa L, Camacho IC, Grinn-Gofroń A, Camacho R. Monitoring of anamorphic fungal spores in Madeira region (Portugal), 2003–2008. Aerobiologia. 2016; 32(2), 303–315.
59.
Green B, Sercombe J, Tovey E. Fungal fragments and undocumented conidia function as new aeroallergen sources. J Allergy Clin Immunol. 2005; 115: 1043–1048.
60.
Mitakakis T, Guest D. A fungal spore calendar for the atmosphere of Melbourne, Australia, for the year 1993. Aerobiologia. 2001; 17: 171–176.
61.
Herrero A D, Ruiz SS, Bustillo MG, Morales PC. Study of airborne fungal spores in Madrid, Spain. Aerobiologia. 2006; 22(2), 133.
62.
Gonianakis M, Neonakis I, Darivianaki E, Gonianakis I, Bouros D. et al. Airborne Ascomycotina on the island of Crete: Seasonal patterns based on an 8-year volumetric survey. Aerobiologia. 2005; 21: 69–74.
63.
Chew F, Lim S, Shang S, Dahlia S, Goh D et al. Evaluation of the allergenicity of tropical pollen and airborne spores in Singapore. Allergy. 2000; 55: 340–347.
64.
Adhikari A, Sen M, Gupta-Bhattacharya S, Chanda S. Airborne viable, non-viable, and allergenic fungi in a rural agricultural area of India: a 2-year study at five outdoor sampling stations. Sci Total Env. 2004; 326: 23–141.
65.
Das S, Gupta-Bhattacharya S. Monitoring and assessment of airborne fungi in Kolkata, India, by viable and non-viable air sampling methods. Env Monit Assess. 2012; 184: 4671–4684.
66.
Simon-Nobbe B, Denk U, Pöll V, Rid R, Breitenbach M. The spectrum of fungal allergy. Int Archives Allergy Immunol. 2008; 145: 58–86.
67.
Díez A, Sabariego S, Gutiérrez M, Cervigón C, Morales M. Study of airborne fungal spores in Madrid, Spain. Aerobiologia, 2006; 22: 135–142.
68.
Martínez X, Tejera L, Beri Á. First volumetric record of fungal spores in the atmosphere of Montevideo City, Uruguay: a 2-year survey. Aerobiologia. 2016; 32: 317–333.
69.
Almaguer M, Aira MJ, Rodríguez-Rajo FJ, Rojas TI. Thirty four identifiable airborne fungal spores at Havana, Cuba. Ann Agric Env Med. 2015; 22(2): 220–225.
70.
Gaikwad K, Sonawane M. Fungi as bio-indicators of air quality. Int J Life Sci Pharm Reviews. 2012; 2(3), 25–28.
71.
La-Serna I, Dopazo A, Aira MJ. Airborne fungal spores in the Campus of Anchieta (La Laguna, Tenerife). Grana. 2002; 41: 119–123.
72.
Bruno A, Pace L, Tomassetti B, Coppola E, Verdecchia M et al. Estimation of fungal spore concentrations associated to meteorological variables. Aerobiologia. 2007; 23: 221–228.
73.
Pyrri I, Kapsanaki-Gosti E. A comparative study on the airborne fungi in Athens, Greece, by viable and nonviable sampling methods. Aerobiologia. 2007; 23: 3–15.
74.
Arnold GR. Lista de hongos fitopatógenos de Cuba. Ministerio de Cultura. Editorial científico técnico, Cuba, 1986.
75.
Picos-Muñoz PA, García-Estrada RS, León-Félix J, Sañudo-Barajas A, Allende-Molar R. Lasiodiplodia theobromae en cultivos agrícolasde México: Taxonomía, Hospedantes, Diversidad y Control. Rev Mex Fitopatol. 2015; 33(1): 54–74.
76.
Herrera A. Impacto de la agricultura urbana en Cuba. Novedades Población, CEDEM, Centro de Estudios Demográficos, Universidad de La Habana, 5(9): 1–14, 2009.
77.
Ataygul E, Celenk S, Canitez Y, Bicakci A, Malyer H, Sapan N. Allergenic fungal spore concentrations in the atmosphere of Bursa, Turkey. J Biol Environ Sci. 2007; 1(2): 73–79.
78.
Rivera-Mariani FE, Nazario-Jimenez S, Lopez-Malpica F, Bolanos-Rosero B. Skin test reactivity of allergic subjects to basidiomycetes’ crude extracts in a tropical environment. Med Mycol. 2011; 49(8): 887–91.
79.
Blatter J, Forno E, Brehm J, Acosta-Perez E, Alvarez M, Colon-Semidey A, Thorne PS, Metwali N, Canino G, Celedon JC. Fungal exposure, atopy, and asthma exacerbations in Puerto Rican children. Ann Am Thorac Soc. 2014; 11(6):925–32.
80.
Crandall SG, Gilbert GS. Meteorological factors associated with abundance of airborne fungal spores over natural vegetation. Atmos Environ. 2017; 162: 87–99.
81.
Rosas I, McCartney HA, Payne RW, Calderon C, Lacey J, Chapela R, Ruiz-Velazco S. Analysis of the relationships between environmental factors (aeroallergens, air pollution, and weather) and asthma emergency admissions to a hospital in Mexico City. Allergy. 1998; 53(4): 394–401.
82.
Njokuocha RC, Agwu CO, Okezie CE. Effects of weather conditions on selected airborne fungal spores in the Southern part of the Atate of Enugu, Nigeria. Grana. 2017; 56(4): 263–272.
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