J. Phycol. 43, 615627 (2007) 2007 Phycological Society of America DOI: 10.1111/j.1529-8817.2007.00373.

AIRBORNE ALGAE: THEIR PRESENT STATUS AND RELEVANCE 1

Naveen Kumar Sharma
School of Studies in Microbiology, Jiwaji University, Gwalior 474002, Madhya Pradesh, India

Ashwani Kumar Rai

Department of Botany, Banaras Hindu University, Varanasi 221005, Uttar Pradesh, India

Surendra Singh
School of Studies in Microbiology, Jiwaji University, Gwalior 474002, Madhya Pradesh, India

and Richard Malcolm Brown Jr.2

Molecular Genetics and Microbiology, University of Texas at Austin, Austin, Texas 78712, USA

Ongoing climatic changes coupled with various natural processes and the outcomes of human activities are not only loading the atmosphere with diverse kinds of biological particles but also changing their prevalence and spatial distribution. Despite having considerable ecological and economic signicance, including their possible impact on human health, airborne algae are the least-studied organisms in both aerobiological and phycological studies. The present review has been written to bring together all available information, including a brief survey of the literature, the ecology of airborne algae, mechanisms involved in their aerosolization, the role of environmental factors in shaping the structure and composition of aero-algal ora, and other signicant information associated with airborne algae. This review provides information on methodological approaches and related problems, along with suggestions for areas of future research on airborne algae. Key index words: aerosolization; airborne algae; allergy; biogeography; climatic factors; dispersal; health hazards; microalgae; samplers; sampling; soil algae; source; terrestrial algae

Pristine environments require colonization by autotrophic organisms to form the basis of an ecosystem (Marshall and Chalmers 1997). Algae are important colonizers of isolated land areas (Brown 1965, Wynn-Williams 1990) and water bodies (Maguire 1963). To establish an active population at a particular site, successful dispersal of viable algae is a prerequisite. Round (1981, as quoted in Kristiansen 1996, p. 151) remarked, The occurrence of so many fresh water algae throughout the world is a
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Received 19 July 2006. Accepted 8 March 2007. Author for correspondence: e-mail rmbrown@mail.utexas.edu.

reection of ease of transportyet for the majority there is no information on transport mechanism. Despite this early note, dispersal of algae has been sporadically investigated. Algae are dispersed passively by means of water, air, and other organisms, including humans (Kristiansen 1996). Compared with water, air transports algae over longer distances. Parker et al. (1969) noted that some airborne algae are resistant to desiccation for long periods of time; however, Kristiansen (1996) reported a survival time of only 48 h. The presence of free-oating algae in the atmosphere (airborne algae) has been known for quite a long period (Ehrenberg 1844), and these reports have had considerable signicance (Fig. 1). Darwin (1846) wrote: On the 16th of January (1833), when the Beagle was ten miles off the N.W. end of St. Jago (Cape Verde Islands), some very ne dust was found adhering to the underside of the horizontal wind-vane at the mast-head; it appeared to have been ltered by the gauze from the air as the ship lay inclined to the wind. The wind had been for 24 h previously E.N.E., and hence, from the position of the ship, the dust probably came from the coast of Africa (as cited in vide Harper 1999, p. 429). Ehrenberg (1844) reported 18 species of freshwater diatoms that had come from Africa, from the very dust samples sent by Darwin. Since then, direct sampling of the atmosphere over terrestrial, marine, and freshwater environments has established algae as being part of the naturally occurring aerial biota. Salisbury (1866) termed these organisms as disease producing algoid or Palmellae. Similarly, Molish (1920) reported diatoms from dust rains and coined the term aeroplankton to describe such organisms. It was van Overeem (1936, 1937) who made the rst major effort to recover and cultivate airborne algae from the samples taken by ltration at a maximal height of 2000 m and lower over the Netherlands. From 24 air samples taken on six different occasions, nine
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Source of airborne algae 1. Soil 2. Water surfaces 3. Trees, buildings, and rock surfaces

N A V E E N K U M A R S H A R MA E T A L .

Transmission Diffusion Dispersion

1. Downward molecular diffusion 2. Surface impaction 3. Rain and electrostatic deposition 4. Gravitational settling

Deposition 1. On soil and rock surfaces 2. On water surfaces 3. On buildings, trees, and other surfaces 4. In nasal mucosa, lungs, and on skin of humans

Impact 1. Effect of air pollution on the morphology and physiology of airborne (i.e., biological indicator) particles 2. Role in transport of chemicals (i.e., radionuclides, etc.) 3. Role in origin, evolution, and structure of island ecosystems 4. Toxicological and allergenic impact of airborne algae 5. Role in biodeterioration 6. Extension and development of blooms
Fig. 1. Summary of the events and impacts associated with airborne algae (modied after Schlichting, Brown, and Smith 1972).

different algal isolates (Stichococcus, Pleurococcus, Hormidium, and a few cyanobacteria) were recovered, among which Chlorococcum was the most frequent. Maximal abundance was recorded at 500 m. Similarly, Meier and Lindberg (1935) reported green algae in the air samples collected at 910 m over Greenland, while Saxena (1983) recovered a lamentous chlorophyte (Planktonema lauterbornii Schmidle) from the clouds above Antarctica. Viable algal particles have also been reported from rain and snow traps (Pettersson 1940, Maguire 1963). Maynard (1968a) collected viable Melosira granulata (Ehrenb.) Ralfs suspended in the air at a height of 3000 m. Along with the Antarctic and Surtsey Island, the Hawaiian Islands of the Pacic Ocean are ideal natural sites for many scientic inquiries, especially for the atmospheric dispersal of microorganisms and higher plants (Brown 1971), and thus, rightly considered a model for aerobiological studies (Kristiansen 1996). While describing the aerial dispersal of algae, Strm (1926) concluded that only reproductive parts (zygospores) could become airborne. In contrast, Messikommer (1943) reported wind as the most important factor for dispersal of airborne algae and emphasized that the major contribution is from vegetative parts. A successful aerial

dispersal depends on the tolerance of the algae to desiccation and UV radiation. Dispersal distance is very much related to the dispersal method, and different modes may result in very dissimilar distribution patterns (Bullock et al. 2003). Furthermore, combinations of dispersal modes may occur for a given species. It is quite difcult to assign any maximal distance for the transportation of algae through the air, as even the most remote islands have a ora of freshwater algae. Marshall (1996) suggested that algal propagules have the ability to survive long-distance transport and provide potential inocula for colonization of Antarctica, as regional warming continues to expose fresh habitats. Similarly, the volcanic island of Surtsey, off Iceland, which came into existence after an undersea eruption in 1963, harbored 106 algal taxa by 1966, the majority of which were freshwater and microscopic (Schwabe and Behre 1972). Darby et al. (1974) found that freshwater diatoms such as Melosira granulata and Stephanodiscus astraea (Kutz.) Grunow in the Arctic, 500 km north of Alaska, possibly originated in Siberia. Therezien and Coute (1977) noted that the algal ora of Kerguelen and other Antarctic islands was similar to that of Arctic islands. Technically, dispersal is a simple act of moving individuals from one area to another. However, it has far-reaching ecological and evolutionary consequences (Kokko and Lo pez-Sepulcre 2006). Dispersivity is one of the important attributes governing the global distribution of species (i.e., biogeography). Knowledge of biogeography is a key to the understanding of diversity, evolution, range, abundance, and the ecological role of any taxon. Despite a recent surge in literature, most hypotheses on microbial biogeography are theoretical and largely extrapolated from the biogeography of macroorganisms (Hedlund and Staley 2004). Nonetheless, microbial biogeography is quite different from that of animal and large plant groups (Hedlund and Staley 2004). Currently, two divergent opinions exist on the biogeography of microorganisms. One, strongly supported by Finlay (2002), holds that owing to small body size and absolute abundance, essentially all prokaryotes, as well as microbial eukaryotes, are ubiquitous (Finlay and Clarke 1999, Finlay 2002). On the contrary, Staley and Gosink (1999), Papke et al. (2003), Hedlund and Staley (2004), Martiny et al. (2006), and Foissner (2006) believe that ubiquity of microorganisms might be correct, but only up to certain taxa. Finlay et al. (2004) and Fenchel (2005) strongly advocate the morphospecies as the basic biogeographical unit, especially for protists. How ever, based on molecular evidence, Slapeta et al. (2005, 2006) and Foissner (2006) have expressed reservations over the appropriateness of the morphospecies and have argued that in reality, the morphospecies is a complex of similar appearing sibling species that differ from each other genetically as well as physiologically.

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Ever since Beijerinck (1913) performed his famous enrichment culture experiments, it has become a cited principle in microbiology that everything is everywhere, and the environment selects (Finlay et al. 2004, p. 17). The idea is that free-living microorganisms are small enough to become windborne and dispersed over the entire planet, and a particular species can occur wherever the habitat is suitable (Wilkinson 2001). Characteristics, like small body size, absolute abundance, and efcient dispersal mechanisms, do indicate that algae are likely to have a global (cosmopolitan) distribution. However, there is ample evidence that endemicity does exist for a majority of algae (Foissner 2006 and references therein). This apparent endemicity is probably due to environmental factors, historical legacy, or both (Martiny et al. 2006). The inuence of geographical isolation (historical events) and environmental factors in regulating the biogeography depends on the sampling scale. Generally, historical events have great inuence at a large spatial scale (>10,000 km), while environmental factors occur at small (<10 km) scales. However, both factors seem to operate at the intermediate scale (103000 km; Martiny et al. 2006). Air transports a great number of algal propagules and resting spores (Brown et al. 1964, Brown 1972, Schlichting et al. 1972, Benninghoff 1991, Schlichting 2000, Broady 1996, Sharma et al. 2006a) and may provide reliable evidence for the biogeography of algae. The ease of passive dispersal is one factor that is important for the global distribution of algae. Little is known about other measures that confer a cosmopolitan distribution of microorganisms. The belief that relying solely on the mathematical proposition that organisms (or viable parts thereof) smaller than 1 mm will have ubiquitous dispersal needs rethinking. If so, spores of bryophytes, pteridophytes, and seeds of many angiosperms that are sufciently minute and produced in great numbers would have resulted in a global distribution of these plants. Thus, before reaching any conclusion on the global distribution of algae, several unresolved issues need to be addressed. The information available is meager and fragmentary; thus, only data that are more empirical can resolve the issue. Diversity and abundance. Microalgal unicells, laments, and colonies sampled from the atmosphere vary in shape and size. Their sizes range from 1 to 150 lm for unicellular organisms, and from 2 to 300 lm for clumps of unicells (Schlichting 1986). The shape of unicells varies from spherical to ellipsoidal, fusiform, and lunate, whereas laments are either single or in packets. Colonies are spherical, ellipsoidal, cubical, and amorphous. In the atmosphere, most of the microalgae occur in the vegetative stage, but spores and cysts are also common (Schlichting 1969). Available studies indicate that green algae, cyanobacteria, diatoms, and tribophytes constitute the

bulk of aero-algal ora (Table 1). However, the diversity and abundance of airborne algal particles show climatic, topographical, geographical, diurnal, and seasonal variations. For example, Foged (1975) analyzed the contents of dust lters collected at 3 m above the ground in southern Jutland, Denmark, and reported the occurrence of 59 species of diatoms, mostly freshwater forms. Schlichting (1961) found 22 viable algal species in the air samples, mainly green algae, but also diatoms, six cyanobacteria, one chrysophyte, and one euglenoid. Rosas et al. (1989) recoded 16 species of living algae, mainly chlorophytes in air samples collected at 4 m above the ground. Sharma et al. (2006a) recorded 34 genera from the atmosphere of Varanasi City (India), dominated by cyanobacteria. Quantitatively, airborne algal particles seem to contribute little to the community of aerobiological particles (Tormo et al. 2001). However, a total of 62 species and a maximum of 3000 algae per m3 were recorded from the samples taken from an automobile moving at 96 km h)1 through a dust cloud near Austin, Texas, USA (Brown et al. 1964). Tropical regions, with abundant soil and subaerial algae, exhibit higher diversity and abundance than other climatic regions (Schlichting 1974). Cyanobacteria dominate the aero-algal ora of tropical areas, while chlorophytes dominate the temperate regions (Schlichting 1961, Brown et al. 1964, Mittal et al. 1979a, Sharma et al. 2006a). Harper (1999) reported that besides marine forms, the aero-algal ora of Antarctica contains an abundance of freshwater diatoms. Schlichting (1974) observed that maximal algal diversity occurred during winter and early spring, while Tiberg et al. (1983) found maximal diversity during summer. Schlichting (1964) recorded a slightly higher airborne algal concentration during the afternoon and evening hours. In a later work, Schlichting (1969) observed that the semiarid areas where winds commonly raise dust into the air have great species diversity, and large numbers, of airborne algae. Likewise, sampling in a valley and the countryside yielded more organisms than hill and urban areas. Many of the algae are resistant to desiccation for long periods (Parker et al. 1969). Nevertheless, algae are not always present in aerial samples (Parker 1970). Sampling over the open Pacic and Atlantic oceans by ships and aircraft produced negative results (Schlichting 1969, Brown 1971). Table 1 lists airborne algal genera reported by different investigators from a variety of biogeographical regions of the world. Launching mechanisms and response to environmental factors. The launching of bioaerosols is mainly from terrestrial and aquatic sources. However, in many instances, algae growing on rooftops, towers, trees, and buildings may also contribute signicantly to the total atmospheric algal load (Schlichting 1969).

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Table 1. List of viable airborne algal genera reported from different biogeographical regions.

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Table 1. (Continued)

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Table 1. (Continued)

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Based on their nature and dynamics, sources may be primarily classied as point, linear, or area sources and may be further subdivided into instantaneous and continuous processes. Soil and aquatic bodies containing algae act as major natural sources of airborne algae (Stevenson and Collier 1962, Brown et al. 1964, Broady 1996). Airborne algae experience severe dehydration stress, especially immediately after being aerosolized (Ehresmann and Hatch 1975). This phenomenon adversely affects their survival. It is likely that the algae adapted to terrestrial habitats are more resistant to a state of dehydration and, thus, better adapted to aerial dispersal than their aquatic counterparts (Schlichting 1969, Ehresmann and Hatch 1975). In general, bioaerosols range from 0.02 to 100 lm in diameter and follow the same physical rule as any particle of a similar aerodynamic diameter. They disperse via air movements and settle according to the settling velocity, available impaction surface, and climatic factors prevailing in the area (Burge and Rogers 2000). Air movements within a laminar boundary layer surrounding the source usually release such particles. Many of the particles remain in the layer and eventually settle near the source (<100 m), while some are carried aloft with turbulence and transported by the wind over a long distance. The processes responsible for the release and atomization of bioaerosols from natural sources are as follows: 1. Sweeping of the surface or rubbing together of adjacent surfaces by wind and gusts dislodges the bioparticles from the surface. Dried algae caught by the wind are carried away like dust particles (Gro nblad 1933, Folger 1970). 2. Formation of oceanographic aerosols by wave action and the bursting of bubbles at the waterair interface (Woodcock 1948, Stevenson and Collier 1962, Maynard 1968b, Schlichting 1974). Fragments of scums and foams with algal contents along the shoreline of water bodies can be picked up by the wind and carried aloft (Maynard 1968b). 3. During heavy rainfall, algae are splashed up by raindrops and can be entrained into the atmospheric air by thermal winds (Burge and Rogers 2000). 4. Storm activity over land and sea where great turbulence is experienced. 5. Human activities, such as agricultural practices, construction and maintenance practices, sewage treatment plants (Mahoney 1968 as cited in Schlichting 1974), garbage dumping, highway trafc, and to a limited extent weapons testing and spacecraft launching, can result in the atomization of constituting algae (Schlichting 1974, Kring 2000). 6. Atomization of aerosols to a low height also occurs when surface water containing blooms is

used for irrigation and recreational activities like boating, jet skiing, and so forth. (Benson et al. 2005). The role of atmospheric conditions on survival and dispersal of airborne algae is poorly understood. Studies concerning the impact of different climatic factors on survival and distribution of airborne algae have revealed that the distribution is not random, but follows precise meteorological conditions (Schlichting 1969, Smith 1973, Balakrishnan and Gunale 1980, Roy-Ocotla and Carrera 1993). The minimum on-site meteorological data that should be recorded include rainfall, air temperature, relative humidity, radiation, direction and speed of the prevailing winds, and elevation angle (Smith 1973). Concentration of algae in the air is associated not only with variation in meteorological conditions (Rosas et al. 1989, Sharma et al. 2006b) but also the abundance and dynamics of source vegetation, and the presence of natural and anthropogenic barriers (Fig. 2). Environmental factors regulate the distribution of airborne algae in both direct and indirect ways (Fig. 2). Indirectly, the climatic conditions regulate the dynamics of various sources, either by supporting or inhibiting the algal growth, while processes such as entrainment and dispersal of algae (from the source) are direct inuences. Increasing eutrophication of water bodies and adverse land-use patterns, assisted by ongoing climatic changes, are also expected to change the diversity and abundance of air biota in many parts of the world.
Climatic conditions Air temperature, relative humidity, rainfall, wind speed, sunshine, etc.

Indirect effect (on the source)

Direct effect

Source dynamics Growth of different groups of algae in an algal community, which influences the dynamics of the source community

Aerosolization Processes of aerosolization of algae through source vegetation

Natural and anthropogenic obstacles

Airborne algae Diversity and abundance of algae in the atmosphere

Fig. 2. Schematic presentation of the impact of climatic factors on the distribution of airborne algae in the atmosphere.

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The release of algae from the surface of the soil or vegetation into the air is generally a passive process (Carson and Brown 1978). Among the various climatic factors that control the concentration of algae in the atmosphere, air temperature and humidity are the most important, as they affect every process, such as source dynamics, launching, and transmission of algae. Rainfall and wind speed affect the release of algae into the atmosphere. The latter factors also play an important role in the subsequent dispersal of the airborne particles. Rainfall, while stimulating a profuse and vigorous growth of algae, can also remove or scrub them from the atmosphere. This dual role of rainfall makes prediction difcult. Rain removes airborne particles by both rainout and washout effects (Burge and Rogers 2000). In rainout, algae act as condensation nuclei and fall with the resultant droplets, while during washout, raindrops capture airborne particles as they fall. Rain also causes release of algae by splash and tap and puff mechanisms (Burge and Rogers 2000). Light showers have little effect on the concentration of airborne algae. Wind speed, elevation angle, and direction govern the dispersal rate of airborne algae. In general, the greater the wind speed, the higher the concentration of algae in the atmosphere. However, Schlichting (1964) observed the highest species diversity in winds of 2229 km h)1, but only a few species in wind speeds of 5156 km h)1. In the Northern Hemisphere, the transport of airborne particles takes place from the south to the north. In the mesosphere, the number of microorganisms was higher during storms than in the absence of strong wind (Imshenetsky et al. 1978). Strong winds remove moisture from the soil and other algal sources and thereby cause drying and fragmentation of algal colonies. Dry ambient conditions favor the resuspension of algae from the soil by ascending currents (Tormo et al. 2001). Schlichting (1964) reported that the wind elevation angle is more crucial than the wind direction and speed. Humidity affects both the survival and settling of airborne algae. Like other microorganisms, algae also undergo an initial inactivation during the process of aerosolization (Ehresmann and Hatch 1975). For long-term survival in the air, inactivation of algae should be minimal (Ehresmann and Hatch 1975). Inactivation is inversely related to the relative humidity of the environment. With other factors being close to optimal, high humidity decreases the algal concentration in the atmosphere, while low humidity increases it. Under high humidity, the hygroscopic walls of algal cells absorb water, which results in an increased settling velocity. In one study, cyanobacteria remained viable throughout a wide range of relative humidities, whereas eukaryotic algae only survived near saturation (Ehresmann and Hatch 1975). Atomization of algae requires the coordination of algal surface desiccation and

the lifting (takeoff) capacity of the wind current. Generally, these events occur under clear atmospheric conditions. However, Carson and Brown (1978) observed high concentrations of airborne algae under overcast conditions due to the splash dispersal mechanism, and during cloudy or partly cloudy days when the total radiation was 767 W m)2 or less (Schlichting 1964). Site characteristics are also important in regulating the aerosolization of algae from the source. Increasing numbers of secondary colonizers (mosses and lichens) decrease the ability of soil algae to become airborne by increasing the thickness of the boundary layer and slowing the drying rate of the soil surface. Likewise, the presence of physical hindrances, such as buildings near the source, inversely affects the aerosolization of algae. Changes in the aero-algal community are also due to the effect of climatic conditions on the growth of individual algal groups at the source. Prokaryotic and eukaryotic forms are differentially susceptible to the various atmospheric stresses (Ehresmann and Hatch 1975). For example, the growth curves of cyanobacteria level off at comparatively higher temperatures than those of green algae, resulting in the dominance of cyanobacteria in natural communities during warmer months. Marshall and Chalmers (1997) reported that the diversity and abundance of atmospheric algae could not be correlated with any single meteorological variable. In accordance with this nding, Sharma et al. (2006b) observed that a single climatic factor and event is not exclusively responsible for loading algae into the atmosphere, and Schlichting (1961) determined that viable algae could occur in the atmosphere under a wide range of conditions, such as relative humidities of 28%98%, temperatures of 2.8C28C, and wind speeds of 6.424.1 km h1. Impacts and effects of airborne algae. Deterioration of architectural structures or works of art: The role of cyanobacteria has been documented in the deterioration of architectural structure and glass alteration under moist and humid conditions (Arin and Saizo Jimenez 1996a,b, Wakeeld et al. 1996). Gorbushina and Palinska (1999) noted characteristic patterns, like micropitting, crack formation, color change, and biogenic mineral deposition, over the exposed glass surfaces. The crack formation pattern was strain specic and independent of the chemical composition of the glass. However, the degree of deterioration depended on the sensitivity of the glass in question to corrosion (Gorbushina and Palinska 1999). Though not clearly stated, the work indicates that cyanobacteria reaching the window glass panes, placed high on the walls, is possible only via aerosolization. Environmental pollution indicators: Algae may be used as indicators of air quality due to their ease of handling; range of species; specic sensitivity; and rapid morphological, physiological, and biochemical

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responses to changes in air chemistry. Schlichting and his BioControl Company Inc. (Port Sanilac, MI, USA) have constructed air biomonitors with two types of chambers, one for experimental purposes and another as a control. Algae that were used as test organisms in the experimental chamber of the biomonitors, after rapid accumulation of aerial pollutants, exhibited changes in biomass, pigment composition, respiration, and photosynthesis compared to that of the test organisms in the control chamber. Some of the selected taxa used in air biomonitors were Chlorella, Chlorococcum, Oscillatoria, Nostoc, Navicula, and Nitzschia species (Schlichting 1975, 1986). Owing to acclimatization to the atmospheric pollutants, aerophilous algae showed better responses compared to their soil and aquatic counterparts. Hence, these organisms may prove to be a better choice as bioindicators. Contamination of drinking water and transport of chemicals: In certain parts of the world, deposition of airborne algae in reservoirs may result in the formation of massive blooms. These blooms pose serious health threats to human and livestock users, clog water lters and industrial cooling towers, and produce odors, in addition to the deleterious effects on the underlying ora and fauna of the water bodies (Schlichting 1974). Health hazards: Airborne algae are permanent constituents of indoor and outdoor environments (Tiberg et al. 1983). The quality of air has serious implications on human health. Environments of agriculture, biotechnology, industrial settings, and nonindustrial indoor surroundings present unique exposure concerns, which depend on the nature and concentration of the microorganisms encountered, and the susceptibility of the exposed population (Burge and Rogers 2000). The role of airborne algae in transportation of radionuclides; heavy metals; pesticides; herbicides; carcinogenic and mutagenic agents; and pathogenic bacteria, fungi, and viruses is little explored (Schlichting 1974). However, the large surface areas of airborne algal particles may provide substrata for adhesion of such compounds or organisms. Because of rapid growth rates, algae can take up xenobiotic elements from the atmosphere and concentrate them within and around the cells (Schlichting 1974). (a) Allergenicity: Although the contribution of algae to the total outdoor allergen-bearing particles is less than that of fungi, pollen, and bacteria (Tormo et al. 2001), their role in inducing certain types of respiratory problems has long been recognized (Woodcock 1948). Particles of 330 lm diameter (later identied as brevitoxins) in oceanic air caused cough and nasopharyngeal burning in individuals frequenting the local beaches during onshore winds (Woodcock 1948). Heise (1949, 1951) correlated airborne algae with symptoms of hay fever and obtained strong positive skin reactions of the immediate wheal and are type in patients tested

with extracts of cyanobacteria. The unicellular alga Prototheca has a long etiological history of causing cutaneous and systematic infection in animals (Cox et al. 1974). However, McElhenney et al. (1962) and McGovern et al. (1966) conducted the rst comprehensive study of the role of airborne algae in causing rhinitis and asthma. They reported 80% positive skin reactions among atopic patients with four distinct airborne green algae. Brown (1971), while sampling along the Pali highway in Hawaii, reported that people traveling along the highway are exposed to varying concentrations of airborne algae having medical signicance. McGovern et al. (1965) and Bernstein and Safferman (1970) documented the allergenic potency of microalgae collected from house dust. Patients with skin sensitivity to house dust and Chlorella and Chlorococcum (as test species) exhibited similar leukocyte histamine release responses (Bernstein and Safferman 1973). Holland et al. (1973) collected 40 viable algal genera from house dust samples and discussed the distinct possibility of the chemical constituents of these algae in causing allergy. Normally, airborne algae range between 0.3 and 15.0 lm in diameter, which is appropriate to causing respiratory disease and allergy (Schlichting 1969). In this size range, the particles can be retained on the mucosal membrane of the respiratory system (Cheng et al. 2005). In addition, the long airborne residence time of these small particles increases the risk of exposure to the allergens (Burge and Rogers 2000). Schlichting (1969) has estimated that a human at rest inhales about 7 L of air per minute. If eight algal cells are present per 14 L of clear air, that would allow for a minimum of 1500 cells inhaled per day. Bernstein et al. (1969) and Bernstein and Safferman (1973) demonstrated that Chlorella causes skin, nasal, and bronchial reactions, giving a positive reaction to the PrausnitzKustner test for the presence of immediate hypersensitivity in humans. The clinical signicance of sensitization against algae is supported by the fact that on many occasions, the quantity of airborne algae exceeds other common allergens (Brown et al. 1964). In India, a study showed that 400 respiratory allergy patients who were tested for 10 different microalgae showed 2% 20% skin positivity, and the percentage was higher for cyanobacteria than for green algae (Mittal et al. 1979b). This nding might be due to the abundance of airborne cyanobacteria in the region (Mittal et al. 1979a). Tiberg et al. (1990, 1995) reported that Chlorellasensitized children show a high incidence of allergy to other common allergens, especially molds, possibly due to immunological cross-reactivity. This simultaneous sensitization is plausible as the growth of both molds and algae is favored by increased humidity. Brown and Lester (1965) found similar results with two green algal genera, Tetracystis and

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Chlorococcum, while Bernstein et al. (1969) reported a limited pattern of cross-reactivity among different strains of green algae and other nonalgal antigens. In nature, airborne algae never exist in pure form but are mixed with many other biotic and abiotic particles. Villalobosa-Pietrini et al. (1995) and Burge and Rogers (2000) reported that abiotic particles (e.g., air pollutants) and biological particulates combined cause a more severe effect than anticipated. Thus, there is a need to analyze the complex interactions and the possible synergistic antagonistic effects on allergenicity of various outdoor allergenbearing particles. Another important requirement is to determine the degree of allergenicity of different airborne algal species. Presently, acceptable levels of airborne algal allergens have yet to be established. Since algae can occur indoors, it is possible that sensitization in an algal-rich indoor environment increases the risk of a reaction to airborne algae outdoors (Tiberg et al. 1983). (b) Toxicity: Freshwater algal blooms occur worldwide with ever-increasing incidence (Duy et al. 2000). Despite this fact, information on the aerosolization of freshwater toxins and their role in causing health problems is meager. Except for a few reports (Creasia 1990, Benson et al. 2005), most of these are concerned with the marine Florida red tide caused by the dinoagellate Karenia brevis (C. C. Davis) G. Hansen et Moestrup and its toxin, brevetoxin (Pierce et al. 2003, Kirkpatrick et al. 2004, Cheng et al. 2005, Flewelling et al. 2005). Exposure to algal toxins is possible either by ingestion of contaminated food or inhalation of the aerosolized toxins (Fitzgeorge et al. 1994, Kirkpatrick et al. 2004). Differences in the routes of exposure manifest different clinical symptoms (Kirkpatrick et al. 2004). Laboratory animals showed higher sensitivity to inhaled toxins in comparison to ingestion (Fitzgeorge et al. 1994). Benson et al. (2005) observed that the toxic effect on different potential target organs following inhalation occurred at relatively lower doses than that of ingestion. The LD50 value for microcystein-LR through inhalation was 43 lg kg)1(Creasia 1990), while this value was 3000 lg kg)1 by ingestion (Fitzgeorge et al. 1994). Algal toxins are produced within the cells and are released in water after cell lysis, either due to water treatment (as in making the water potable) or when a bloom becomes aged (Pierce et al. 2003). The released toxins are ejected into the air as jet drops from the bursting bubbles (Pierce et al. 2003). With on-shore winds and breaking waves, the toxins become incorporated in marine aerosol, which causes respiratory irritation and other health problems in the exposed population (Pierce 1986, Kirkpatrick et al. 2004). Aerosolized toxins collected from the coast were the same as those in the water and from K. brevis cultures (Pierce et al. 2003). Particles smaller than 9 lm were reported to be deposited on the nasal, oral, and pharyngeal area of

the upper respiratory tract (Cheng et al. 2005), leading to irritation due to the presence of the particles themselves or the associated toxins. Clinical symptoms included conjunctival irritation, copious catarrhal exudates, rhinorrhea, nonproductive cough, bronchoconstriction, dizziness, and tunnel vision (Pierce 1986, Kirkpatrick et al. 2004). Irritation and bronchoconstriction symptoms are resolved once a person leaves the contaminated area (Baden 1983). Exposure to aerosolized toxins may cause severe exacerbation of asthma in asthmatic patients (Asai et al. 1982). However, nonasthmatics may also experience respiratory irritation (Kirkpatrick et al. 2004). The effect of the aerosolized brevetoxins might be chronic (Bossart et al. 1998). Apart from causing respiratory problems, airborne toxins also affect exposed skin, causing itching (Kirkpatrick et al. 2004). Methodological approaches to obtain viable algae from the atmosphere. Currently, no guidelines or standard sampling methods are available to effectively characterize all bioaerosols and their components (Rao et al. 1996). To study airborne algae, both direct and culture-based methods are in use. In the direct method, airborne algae trapped over various kinds of substrates are observed directly under a microscope or cultured for the complete life cycle (Broady 1992). In indirect systems, various collection devices, such as impactors, impingers, and different types of samplers, are used (Martinez et al. 2004). Each device has its own advantages and disadvantages. Particle characteristics, such as the shape, size, density, diameter, and nature of the cell wall, vary greatly and can have a dramatic effect on the collection efciency of various instruments and methods employed. The selection of methodology needs to be based on the availability of the device and its cost and mobility, the objective of the work, the volume of air to be sampled, and various environmental conditions (Dowd and Maier 2001). Another factor that must be taken into account is the overall biological sampling efciency of the device, which is crucial for the viability of organisms during and after sampling (Dowd and Maier 2001). Climatic conditions of the area, location of the sampler, and the rate of air intake to the sampler all play a vital role in deciding the duration of the sampling time. The quantity of algae is likely to be high when the sampler location is close to the ground. Short sampling periods (<2 h) are expected to produce consistent and valid results for the following reasons: (i) there is less variation in weather parameters; (ii) vegetative cells or spores remain viable; and (iii) there are minimal changes in the chemistry of the collection medium. Sampling periods may be long in rural and remote areas (2, 4, or even 6 h) but <2 h in industrial and urban areas to avoid the accumulation of toxic pollutants in the collection devices. In general, low rates of intake

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yield more uniform results because of minimum damage to the cells. Schlichting et al. (1971) made the following suggestions to improve the sampling regime to obtain a uniform and comprehensive estimate of atmospheric algal particles: 1. Sampling stations should be in all representative areas (e.g., urban, rural, and remote areas) at sea level and in hilly and mountain areas. 2. To ensure the correlation between airborne algae and micrometeorological conditions, sampling stations should be established where air chemistry and meteorological data are being collected. 3. Establishment of a global network of strategically located sampling stations is necessary to facilitate coordinated studies. Future perspectives. Despite a long history of interest in airborne algae, various aspects are either unexplored or underexplored and require further investigation. These areas include the following: 1. The role of airborne algae in the expansion of HABs, which cause contamination of drinking water and adversely affect the underlying aquatic ora and fauna. 2. The need for controlled laboratory experiments to ascertain whether algae are capable of tolerating the long-distance aerial transport stresses of desiccation, harmful radiation, and so forth, while airborne. If so, the tolerance range, mechanism(s) of adaptation (genetic and biochemical changes), and subsequent morphological and physiological alterations need investigation. 3. Information on the role of different climatic factors in the aerosolization of algae is fragmentary and not well recognized. 4. The possible use of airborne algae as biological indicators of atmospheric contamination. 5. Extraction, characterization, and purication of allergens from airborne algae. 6. The possible use of the allergenic extract of algae to hyposensitize persons suffering from fungal and other allergies. 7. Short- and long-term inhalation effect of toxins produced by toxigenic airborne cyanobacteria. 8. The application of modern sensing methods, like airborne imaging spectrometry (Panter et al. 2001), chemical markers (Sebastian and Larsson 2003), and molecular methods (Pace 1997) for rapid characterization of airborne algae and dust algae. 9. The possibilities of developing culture media that can support the growth of the greatest diversity of algal groups, especially using dilute culture media.

roles in the dispersal of algae, colonization of new habitats, deterioration of architectural structures or works of art, extension of HABs, and causing allergies and other respiratory diseases. Furthermore, airborne algae have great potential as bioindicators. However, these aspects are not fully elucidated and need further exploration. Use of molecular genetics, a greater variety of better-designed culture media, satellite data on weather, and information to coordinate dynamic patterns of the winds and what they will carry will help to make the study of airborne algae more reliable.
We dedicate this article to Dr. H. E. Schlichting Jr. for his extensive contributions to the eld of airborne algae. We are also grateful to Dr. Paul Broady, Dr. Margaret Harper, and Dr. Ebba Tiberg for their valuable suggestions; Dr. Jrgen Kristiansen for critically reviewing the manuscript; and Dr. W. A. Marshall for providing the reprints of his work.
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CONCLUSION

The presence of algae in the atmosphere has long been known. Airborne algae play important

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