AIRBORNE ALGAE: THEIR PRESENT STATUS AND RELEVANCE1

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 variousnatural processes and the outcomes of human activ-ities are not only loading the atmosphere withdiverse kinds of biological particles but also chan-ging their prevalence and spatial distribution.Despite having considerable ecological and econo-mic significance, including their possible impact onhuman health, airborne algae are the least-studiedorganisms in both aerobiological and phycologicalstudies. The present review has been written tobring together all available information, including abrief survey of the literature, the ecology of air-borne algae, mechanisms involved in their aerosoli-zation, the role of environmental factors in shapingthe structure and composition of aero-algal flora,and other significant information associated with air-borne algae. This review provides information onmethodological approaches and related problems,along with suggestions for areas of future researchon 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 byautotrophic organisms to form the basis of an eco-system (Marshall and Chalmers 1997). Algae areimportant colonizers of isolated land areas (Brown1965, Wynn-Williams 1990) and water bodies (Magu-ire 1963). To establish an active population at a par-ticular site, successful dispersal of viable algae is aprerequisite. Round (1981, as quoted in Kristiansen1996, p. 151) remarked, ‘‘The occurrence of somany fresh water algae throughout the world is a

reflection of ease of transport—yet for the majoritythere is no information on transport mechanism.’’Despite this early note, dispersal of algae has beensporadically investigated. Algae are dispersed pas-sively by means of water, air, and other organisms,including humans (Kristiansen 1996). Comparedwith water, air transports algae over longer distan-ces. Parker et al. (1969) noted that some airbornealgae are resistant to desiccation for long periods oftime; however, Kristiansen (1996) reported a sur-vival time of only 4–8 h.

The presence of free-floating algae in the atmo-sphere (airborne algae) has been known for quite along period (Ehrenberg 1844), and these reportshave had considerable significance (Fig. 1). Darwin(1846) wrote: ‘‘On the 16th of January (1833),when the Beagle was ten miles off the N.W. end ofSt. Jago (Cape Verde Islands), some very fine dustwas found adhering to the underside of the hori-zontal wind-vane at the mast-head; it appeared tohave been filtered by the gauze from the air as theship lay inclined to the wind. The wind had beenfor 24 h previously E.N.E., and hence, from theposition of the ship, the dust probably came fromthe coast of Africa’’ (as cited in vide Harper 1999,p. 429). Ehrenberg (1844) reported 18 species offreshwater diatoms that had come from Africa, fromthe very dust samples sent by Darwin. Since then,direct sampling of the atmosphere over terrestrial,marine, and freshwater environments has estab-lished algae as being part of the naturally occurringaerial biota. Salisbury (1866) termed these organ-isms 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 first major effort torecover and cultivate airborne algae from the sam-ples taken by filtration at a maximal height of2000 m and lower over the Netherlands. From 24air samples taken on six different occasions, nine

1Received 19 July 2006. Accepted 8 March 2007.2Author for correspondence: e-mail rmbrown@mail.utexas.edu.

J. Phycol. 43, 615–627 (2007)� 2007 Phycological Society of AmericaDOI: 10.1111/j.1529-8817.2007.00373.x

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different algal isolates (Stichococcus, Pleurococcus, Hor-midium, and a few cyanobacteria) were recovered,among which Chlorococcum was the most frequent.Maximal abundance was recorded at 500 m. Simi-larly, Meier and Lindberg (1935) reported greenalgae in the air samples collected at 910 m overGreenland, while Saxena (1983) recovered a fila-mentous chlorophyte (Planktonema lauterbornii Schm-idle) from the clouds above Antarctica. Viable algalparticles have also been reported from rainand snow traps (Pettersson 1940, Maguire 1963).Maynard (1968a) collected viable Melosira granulata(Ehrenb.) Ralfs suspended in the air at a height of3000 m.

Along with the Antarctic and Surtsey Island, theHawaiian Islands of the Pacific Ocean are ideal nat-ural sites for many scientific inquiries, especially forthe atmospheric dispersal of microorganisms andhigher plants (Brown 1971), and thus, rightly con-sidered a model for aerobiological studies (Kristian-sen 1996). While describing the aerial dispersal ofalgae, Str¢m (1926) concluded that only reproduc-tive parts (zygospores) could become airborne. Incontrast, Messikommer (1943) reported wind as themost important factor for dispersal of airbornealgae and emphasized that the major contri-bution is from vegetative parts. A successful aerial

dispersal depends on the tolerance of the algae todesiccation and UV radiation. Dispersal distance isvery much related to the dispersal method, anddifferent modes may result in very dissimilar distri-bution patterns (Bullock et al. 2003). Furthermore,combinations of dispersal modes may occur for agiven species. It is quite difficult to assign any max-imal distance for the transportation of algaethrough the air, as even the most remote islandshave a flora of freshwater algae. Marshall (1996)suggested that algal propagules have the ability tosurvive long-distance transport and provide potentialinocula for colonization of Antarctica, as regionalwarming continues to expose fresh habitats. Simi-larly, the volcanic island of Surtsey, off Iceland,which came into existence after an undersea erup-tion in 1963, harbored 106 algal taxa by 1966, themajority of which were freshwater and microscopic(Schwabe and Behre 1972). Darby et al. (1974)found that freshwater diatoms such as Melosira gran-ulata and Stephanodiscus astraea (Kutz.) Grunow inthe Arctic, 500 km north of Alaska, possibly origin-ated in Siberia. Therezien and Coute (1977) notedthat the algal flora of Kerguelen and other Antarcticislands was similar to that of Arctic islands.

Technically, dispersal is a simple act of movingindividuals from one area to another. However, ithas far-reaching ecological and evolutionary conse-quences (Kokko and Lopez-Sepulcre 2006). Disper-sivity is one of the important attributes governing theglobal distribution of species (i.e., biogeography).Knowledge of biogeography is a key to the under-standing of diversity, evolution, range, abundance,and the ecological role of any taxon. Despite a recentsurge in literature, most hypotheses on microbialbiogeography are theoretical and largely extrapola-ted from the biogeography of macroorganisms(Hedlund and Staley 2004). Nonetheless, microbialbiogeography is quite different from that of animaland large plant groups (Hedlund and Staley 2004).

Currently, two divergent opinions exist on thebiogeography of microorganisms. One, strongly sup-ported by Finlay (2002), holds that owing to smallbody size and absolute abundance, essentially allprokaryotes, as well as microbial eukaryotes, are ubi-quitous (Finlay and Clarke 1999, Finlay 2002). Onthe contrary, Staley and Gosink (1999), Papke et al.(2003), Hedlund and Staley (2004), Martiny et al.(2006), and Foissner (2006) believe that ubiquity ofmicroorganisms might be correct, but only up tocertain taxa. Finlay et al. (2004) and Fenchel (2005)strongly advocate the morphospecies as the basicbiogeographical unit, especially for protists. How-ever, based on molecular evidence, Slapeta et al.(2005, 2006) and Foissner (2006) have expressedreservations over the appropriateness of the mor-phospecies and have argued that in reality, the mor-phospecies is a complex of similar appearing siblingspecies that differ from each other genetically aswell as physiologically.

Deposition1. On soil and rock surfaces 2. On water surfaces3. On buildings, trees, and other surfaces4. 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

Source of airborne algae

1. Soil2. Water surfaces3. Trees, buildings, and

rock surfaces

TransmissionDiffusionDispersion

1. Downward molecular diffusion2. Surface impaction3. Rain and electrostatic deposition4. Gravitational settling

Fig. 1. Summary of the events and impacts associated with air-borne algae (modified after Schlichting, Brown, and Smith 1972).

616 NAVEEN KUMAR SHARMA ET AL.

Ever since Beijerinck (1913) performed his famousenrichment culture experiments, it has become acited principle in microbiology that ‘‘everything iseverywhere, and the environment selects’’ (Finlayet al. 2004, p. 17). The idea is that free-living micro-organisms are small enough to become windborneand dispersed over the entire planet, and a particularspecies can occur wherever the habitat is suitable(Wilkinson 2001). Characteristics, like small bodysize, absolute abundance, and efficient dispersalmechanisms, do indicate that algae are likely tohave a global (cosmopolitan) distribution. However,there is ample evidence that endemicity does existfor a majority of algae (Foissner 2006 and refer-ences therein). This apparent endemicity is prob-ably due to environmental factors, historical legacy,or both (Martiny et al. 2006). The influence of geo-graphical isolation (historical events) and environ-mental factors in regulating the biogeographydepends on the sampling scale. Generally, historicalevents have great influence at a large spatial scale(>10,000 km), while environmental factors occur atsmall (<10 km) scales. However, both factors seemto operate at the intermediate scale (10–3000 km;Martiny et al. 2006).

Air transports a great number of algal propagulesand resting spores (Brown et al. 1964, Brown 1972,Schlichting et al. 1972, Benninghoff 1991, Schlichting2000, Broady 1996, Sharma et al. 2006a) and mayprovide reliable evidence for the biogeography ofalgae. The ease of passive dispersal is one factor thatis important for the global distribution of algae. Littleis known about other measures that confer a cosmo-politan distribution of microorganisms. The beliefthat relying solely on the mathematical propositionthat organisms (or viable parts thereof) smaller than1 mm will have ubiquitous dispersal needs rethin-king. If so, spores of bryophytes, pteridophytes, andseeds of many angiosperms that are sufficientlyminute and produced in great numbers would haveresulted in a global distribution of these plants. Thus,before reaching any conclusion on the global distri-bution of algae, several unresolved issues need to beaddressed. The information available is meager andfragmentary; thus, only data that are more empiricalcan resolve the issue.

Diversity and abundance. Microalgal unicells, fila-ments, and colonies sampled from the atmospherevary in shape and size. Their sizes range from 1 to150 lm for unicellular organisms, and from 2 to300 lm for clumps of unicells (Schlichting 1986).The shape of unicells varies from spherical to ellip-soidal, fusiform, and lunate, whereas filaments areeither single or in packets. Colonies are spherical,ellipsoidal, cubical, and amorphous. In the atmo-sphere, most of the microalgae occur in the vegetat-ive stage, but spores and cysts are also common(Schlichting 1969).

Available studies indicate that green algae, cyano-bacteria, diatoms, and tribophytes constitute the

bulk of aero-algal flora (Table 1). However, thediversity and abundance of airborne algal particlesshow climatic, topographical, geographical, diurnal,and seasonal variations. For example, Foged (1975)analyzed the contents of dust filters collected at 3 mabove the ground in southern Jutland, Denmark,and reported the occurrence of 59 species of dia-toms, mostly freshwater forms. Schlichting (1961)found 22 viable algal species in the air samples,mainly green algae, but also diatoms, six cyanobac-teria, one chrysophyte, and one euglenoid. Rosaset al. (1989) recoded 16 species of living algae,mainly chlorophytes in air samples collected at 4 mabove the ground. Sharma et al. (2006a) recorded34 genera from the atmosphere of Varanasi City(India), dominated by cyanobacteria. Quantitatively,airborne algal particles seem to contribute little tothe community of aerobiological particles (Tormoet al. 2001). However, a total of 62 species and amaximum of 3000 algae per m3 were recorded fromthe samples taken from an automobile moving at96 km Æ h)1 through a dust cloud near Austin,Texas, USA (Brown et al. 1964).

Tropical regions, with abundant soil and sub-aerial algae, exhibit higher diversity and abun-dance than other climatic regions (Schlichting1974). Cyanobacteria dominate the aero-algal floraof tropical areas, while chlorophytes dominate thetemperate regions (Schlichting 1961, Brown et al.1964, Mittal et al. 1979a, Sharma et al. 2006a).Harper (1999) reported that besides marineforms, the aero-algal flora of Antarctica containsan abundance of freshwater diatoms. Schlichting(1974) observed that maximal algal diversityoccurred during winter and early spring, whileTiberg et al. (1983) found maximal diversityduring summer.

Schlichting (1964) recorded a slightly higher air-borne algal concentration during the afternoonand evening hours. In a later work, Schlichting(1969) observed that the semiarid areas wherewinds commonly raise dust into the air have greatspecies diversity, and large numbers, of airbornealgae. Likewise, sampling in a valley and the coun-tryside yielded more organisms than hill and urbanareas. Many of the algae are resistant to desiccationfor long periods (Parker et al. 1969). Nevertheless,algae are not always present in aerial samples (Par-ker 1970). Sampling over the open Pacific andAtlantic oceans by ships and aircraft producednegative results (Schlichting 1969, Brown 1971).Table 1 lists airborne algal genera reported bydifferent investigators from a variety of biogeograph-ical regions of the world.

Launching mechanisms and response to environmentalfactors. The launching of bioaerosols is mainly fromterrestrial and aquatic sources. However, in manyinstances, algae growing on rooftops, towers, trees,and buildings may also contribute significantly tothe total atmospheric algal load (Schlichting 1969).

AIRBORNE ALGAE 617

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

618 NAVEEN KUMAR SHARMA ET AL.

Table 1. (Continued)

AIRBORNE ALGAE 619

Table 1. (Continued)

620 NAVEEN KUMAR SHARMA ET AL.

Based on their nature and dynamics, sources maybe primarily classified as point, linear, or areasources and may be further subdivided into instanta-neous and continuous processes. Soil and aquaticbodies containing algae act as major natural sourcesof airborne algae (Stevenson and Collier 1962,Brown et al. 1964, Broady 1996).

Airborne algae experience severe dehydrationstress, especially immediately after being aerosolized(Ehresmann and Hatch 1975). This phenomenonadversely affects their survival. It is likely that thealgae adapted to terrestrial habitats are more resist-ant to a state of dehydration and, thus, better adap-ted to aerial dispersal than their aquatic counterparts(Schlichting 1969, Ehresmann and Hatch 1975).

In general, bioaerosols range from 0.02 to100 lm in diameter and follow the same physicalrule as any particle of a similar aerodynamic diam-eter. They disperse via air movements and settleaccording to the settling velocity, available impac-tion surface, and climatic factors prevailing in thearea (Burge and Rogers 2000). Air movementswithin a laminar boundary layer surroundingthe source usually release such particles. Many ofthe particles remain in the layer and eventuallysettle near the source (<100 m), while some arecarried aloft with turbulence and transported by thewind over a long distance. The processes respon-sible for the release and atomization of bioaerosolsfrom natural sources are as follows:

1. Sweeping of the surface or rubbing together ofadjacent surfaces by wind and gusts dislodges thebioparticles from the surface. Dried algae caughtby the wind are carried away like dust particles(Gronblad 1933, Folger 1970).

2. Formation of oceanographic aerosols by waveaction and the bursting of bubbles at the water-air interface (Woodcock 1948, Stevenson andCollier 1962, Maynard 1968b, Schlichting 1974).Fragments of scums and foams with algal con-tents along the shoreline of water bodies can bepicked up by the wind and carried aloft (May-nard 1968b).

3. During heavy rainfall, algae are splashed up byraindrops and can be entrained into the atmo-spheric air by thermal winds (Burge and Rogers2000).

4. Storm activity over land and sea where great tur-bulence is experienced.

5. Human activities, such as agricultural practices,construction and maintenance practices, sewagetreatment plants (Mahoney 1968 as cited in Schl-ichting 1974), garbage dumping, highway traffic,and to a limited extent weapons testing andspacecraft launching, can result in the atomiza-tion of constituting algae (Schlichting 1974,Kring 2000).

6. Atomization of aerosols to a low height alsooccurs when surface water containing blooms is

used for irrigation and recreational activities likeboating, jet skiing, and so forth. (Benson et al.2005).

The role of atmospheric conditions on survivaland dispersal of airborne algae is poorly under-stood. Studies concerning the impact of differentclimatic factors on survival and distribution of air-borne algae have revealed that the distribution isnot random, but follows precise meteorological con-ditions (Schlichting 1969, Smith 1973, Balakrishnanand Gunale 1980, Roy-Ocotla and Carrera 1993).The minimum on-site meteorological data thatshould be recorded include rainfall, air tempera-ture, relative humidity, radiation, direction andspeed of the prevailing winds, and elevation angle(Smith 1973). Concentration of algae in the air isassociated not only with variation in meteorologicalconditions (Rosas et al. 1989, Sharma et al. 2006b)but also the abundance and dynamics of sourcevegetation, and the presence of natural and an-thropogenic barriers (Fig. 2).

Environmental factors regulate the distribution ofairborne algae in both direct and indirect ways(Fig. 2). Indirectly, the climatic conditions regulatethe dynamics of various sources, either by support-ing or inhibiting the algal growth, while processessuch as entrainment and dispersal of algae (fromthe source) are direct influences. Increasing eutro-phication of water bodies and adverse land-use pat-terns, assisted by ongoing climatic changes, are alsoexpected to change the diversity and abundance ofair biota in many parts of the world.

Climatic conditions

Air temperature, relative humidity, rainfall, wind speed, sunshine, etc.

Source dynamics

Growth of different groups of algae in an algal community, which

influences the dynamicsof the source community

Airborne algae

Diversity and abundance of algae in the atmosphere

Aerosolization

Processes of aerosolization of algae

through source vegetation

Indirect effect(on the source)

Natural and anthropogenic obstacles

Direct effect

Fig. 2. Schematic presentation of the impact of climatic fac-tors on the distribution of airborne algae in the atmosphere.

AIRBORNE ALGAE 621

The release of algae from the surface of the soilor vegetation into the air is generally a passiveprocess (Carson and Brown 1978). Among thevarious climatic factors that control the concentra-tion of algae in the atmosphere, air temperatureand humidity are the most important, as they affectevery process, such as source dynamics, launching,and transmission of algae. Rainfall and wind speedaffect the release of algae into the atmosphere. Thelatter factors also play an important role in the sub-sequent dispersal of the airborne particles. Rainfall,while stimulating a profuse and vigorous growth ofalgae, can also remove or ‘‘scrub’’ them from theatmosphere. This dual role of rainfall makes predic-tion difficult. Rain removes airborne particles byboth rainout and washout effects (Burge and Rogers2000). In rainout, algae act as condensation nucleiand fall with the resultant droplets, while duringwashout, raindrops capture airborne particles asthey fall. Rain also causes release of algae by splashand tap and puff mechanisms (Burge and Rogers2000). Light showers have little effect on the con-centration of airborne algae.

Wind speed, elevation angle, and direction gov-ern the dispersal rate of airborne algae. In general,the greater the wind speed, the higher the concen-tration of algae in the atmosphere. However, Schl-ichting (1964) observed the highest species diversityin winds of 22–29 km Æ h)1, but only a few speciesin wind speeds of 51–56 km Æ h)1. In the NorthernHemisphere, the transport of airborne particlestakes place from the south to the north. In the mes-osphere, the number of microorganisms was higherduring storms than in the absence of strong wind(Imshenetsky et al. 1978). Strong winds removemoisture from the soil and other algal sources andthereby cause drying and fragmentation of algal col-onies. Dry ambient conditions favor the resuspen-sion of algae from the soil by ascending currents(Tormo et al. 2001). Schlichting (1964) reportedthat the wind elevation angle is more crucial thanthe wind direction and speed.

Humidity affects both the survival and settling ofairborne algae. Like other microorganisms, algaealso undergo an initial inactivation during the pro-cess of aerosolization (Ehresmann and Hatch 1975).For long-term survival in the air, inactivation ofalgae should be minimal (Ehresmann and Hatch1975). Inactivation is inversely related to the relativehumidity of the environment. With other factorsbeing close to optimal, high humidity decreases thealgal concentration in the atmosphere, while lowhumidity increases it. Under high humidity, thehygroscopic walls of algal cells absorb water, whichresults in an increased settling velocity. In onestudy, cyanobacteria remained viable throughout awide range of relative humidities, whereas eukaryot-ic algae only survived near saturation (Ehresmannand Hatch 1975). Atomization of algae requiresthe coordination of algal surface desiccation and

the lifting (takeoff) capacity of the wind current.Generally, these events occur under clear atmo-spheric conditions. However, Carson and Brown(1978) observed high concentrations of airbornealgae under overcast conditions due to the splashdispersal mechanism, and during cloudy or partlycloudy days when the total radiation was767 W Æ m)2 or less (Schlichting 1964).

Site characteristics are also important in regula-ting the aerosolization of algae from the source.Increasing numbers of secondary colonizers (mossesand lichens) decrease the ability of soil algae tobecome airborne by increasing the thickness of theboundary layer and slowing the drying rate of thesoil surface. Likewise, the presence of physical hin-drances, such as buildings near the source, inverselyaffects the aerosolization of algae.

Changes in the aero-algal community are alsodue to the effect of climatic conditions on thegrowth of individual algal groups at the source.Prokaryotic and eukaryotic forms are differentiallysusceptible to the various atmospheric stresses(Ehresmann and Hatch 1975). For example, thegrowth curves of cyanobacteria level off at comparat-ively higher temperatures than those of green algae,resulting in the dominance of cyanobacteria in nat-ural communities during warmer months.

Marshall and Chalmers (1997) reported that thediversity and abundance of atmospheric algae couldnot be correlated with any single meteorologicalvariable. In accordance with this finding, Sharmaet al. (2006b) observed that a single climatic factorand event is not exclusively responsible for loadingalgae into the atmosphere, and Schlichting (1961)determined that viable algae could occur in theatmosphere under a wide range of conditions, suchas relative humidities of 28%–98%, temperatures of2.8�C–28�C, and wind speeds of 6.4–24.1 km Æ h–1.

Impacts and effects of airborne algae. Deterioration ofarchitectural structures or works of art: The role ofcyanobacteria has been documented in the deterior-ation of architectural structure and glass alterationunder moist and humid conditions (Arino and Saiz-Jimenez 1996a,b, Wakefield et al. 1996). Gorbushinaand Palinska (1999) noted characteristic patterns,like micropitting, crack formation, color change,and biogenic mineral deposition, over the exposedglass surfaces. The crack formation pattern wasstrain specific and independent of the chemicalcomposition of the glass. However, the degree ofdeterioration depended on the sensitivity of theglass in question to corrosion (Gorbushina and Pal-inska 1999). Though not clearly stated, the workindicates that cyanobacteria reaching the windowglass panes, placed high on the walls, is possibleonly via aerosolization.

Environmental pollution indicators: Algae may beused as indicators of air quality due to their ease ofhandling; range of species; specific sensitivity; andrapid morphological, physiological, and biochemical

622 NAVEEN KUMAR SHARMA ET AL.

responses to changes in air chemistry. Schlichtingand his BioControl Company Inc. (Port Sanilac, MI,USA) have constructed air biomonitors with twotypes of chambers, one for experimental purposesand another as a control. Algae that were used astest organisms in the experimental chamber of thebiomonitors, after rapid accumulation of aerialpollutants, exhibited changes in biomass, pigmentcomposition, respiration, and photosynthesis com-pared to that of the test organisms in the controlchamber. Some of the selected taxa used in air bio-monitors were Chlorella, Chlorococcum, Oscillatoria,Nostoc, Navicula, and Nitzschia species (Schlichting1975, 1986). Owing to acclimatization to the atmo-spheric pollutants, aerophilous algae showed betterresponses compared to their soil and aquatic coun-terparts. Hence, these organisms may prove to be abetter choice as bioindicators.

Contamination of drinking water and transport ofchemicals: In certain parts of the world, depositionof airborne algae in reservoirs may result in the for-mation of massive blooms. These blooms pose seri-ous health threats to human and livestock users,clog water filters and industrial cooling towers, andproduce odors, in addition to the deleterious effectson the underlying flora and fauna of the waterbodies (Schlichting 1974).

Health hazards: Airborne algae are permanentconstituents of indoor and outdoor environments(Tiberg et al. 1983). The quality of air has seriousimplications on human health. Environments ofagriculture, biotechnology, industrial settings, andnonindustrial indoor surroundings present uniqueexposure concerns, which depend on the natureand concentration of the microorganisms encoun-tered, and the susceptibility of the exposed popula-tion (Burge and Rogers 2000). The role of airbornealgae in transportation of radionuclides; heavymetals; pesticides; herbicides; carcinogenic andmutagenic agents; and pathogenic bacteria, fungi,and viruses is little explored (Schlichting 1974).However, the large surface areas of airborne algalparticles may provide substrata for adhesion of suchcompounds or organisms. Because of rapid growthrates, algae can take up xenobiotic elements fromthe atmosphere and concentrate them within andaround the cells (Schlichting 1974).

(a) Allergenicity: Although the contribution ofalgae to the total outdoor allergen-bearing particlesis less than that of fungi, pollen, and bacteria(Tormo et al. 2001), their role in inducing certaintypes of respiratory problems has long been recog-nized (Woodcock 1948). Particles of 3–30 lmdiameter (later identified as brevitoxins) in oceanicair caused cough and nasopharyngeal burningin individuals frequenting the local beaches duringonshore winds (Woodcock 1948). Heise (1949, 1951)correlated airborne algae with symptoms of hayfever and obtained strong positive skin reactions ofthe immediate wheal and flare type in patients tested

with extracts of cyanobacteria. The unicellular algaPrototheca has a long etiological history of causingcutaneous and systematic infection in animals (Coxet al. 1974). However, McElhenney et al. (1962) andMcGovern et al. (1966) conducted the first compre-hensive study of the role of airborne algae in caus-ing rhinitis and asthma. They reported 80% positiveskin reactions among atopic patients with four dis-tinct airborne green algae. Brown (1971), whilesampling along the Pali highway in Hawaii, reportedthat people traveling along the highway are exposedto varying concentrations of airborne algae havingmedical significance.

McGovern et al. (1965) and Bernstein and Saffer-man (1970) documented the allergenic potency ofmicroalgae collected from house dust. Patients withskin sensitivity to house dust and Chlorella and Chlo-rococcum (as test species) exhibited similar leukocytehistamine release responses (Bernstein and Saffer-man 1973). Holland et al. (1973) collected 40 viablealgal genera from house dust samples and discussedthe distinct possibility of the chemical constituentsof these algae in causing allergy.

Normally, airborne algae range between 0.3 and15.0 lm in diameter, which is appropriate tocausing respiratory disease and allergy (Schlichting1969). In this size range, the particles can beretained on the mucosal membrane of the respirat-ory system (Cheng et al. 2005). In addition, thelong airborne residence time of these small particlesincreases the risk of exposure to the allergens(Burge and Rogers 2000). Schlichting (1969) hasestimated that a human at rest inhales about 7 L ofair per minute. If eight algal cells are present per14 L of clear air, that would allow for a minimum of1500 cells inhaled per day.

Bernstein et al. (1969) and Bernstein and Saffer-man (1973) demonstrated that Chlorella causes skin,nasal, and bronchial reactions, giving a positive reac-tion to the Prausnitz–Kustner test for the presenceof immediate hypersensitivity in humans. The clin-ical significance of sensitization against algae is sup-ported by the fact that on many occasions, thequantity of airborne algae exceeds other commonallergens (Brown et al. 1964). In India, a studyshowed that 400 respiratory allergy patients whowere tested for 10 different microalgae showed 2%–20% skin positivity, and the percentage was higherfor cyanobacteria than for green algae (Mittal et al.1979b). This finding might be due to the abun-dance of airborne cyanobacteria in the region (Mit-tal et al. 1979a).

Tiberg et al. (1990, 1995) reported that Chlorella-sensitized children show a high incidence of allergyto other common allergens, especially molds, poss-ibly due to immunological cross-reactivity. This sim-ultaneous sensitization is plausible as the growth ofboth molds and algae is favored by increasedhumidity. Brown and Lester (1965) found similarresults with two green algal genera, Tetracystis and

AIRBORNE ALGAE 623

Chlorococcum, while Bernstein et al. (1969) reporteda limited pattern of cross-reactivity among differentstrains of green algae and other nonalgal antigens.In nature, airborne algae never exist in pure formbut are mixed with many other biotic and abioticparticles. Villalobosa-Pietrini et al. (1995) and Burgeand Rogers (2000) reported that abiotic particles(e.g., air pollutants) and biological particulates com-bined cause a more severe effect than anticipated.Thus, there is a need to analyze the complex inter-actions and the possible synergistic ⁄ antagonisticeffects on allergenicity of various outdoor allergen-bearing particles. Another important requirement isto determine the degree of allergenicity of differentairborne algal species. Presently, acceptable levels ofairborne algal allergens have yet to be established.Since algae can occur indoors, it is possible thatsensitization in an algal-rich indoor environmentincreases the risk of a reaction to airborne algaeoutdoors (Tiberg et al. 1983).

(b) Toxicity: Freshwater algal blooms occur world-wide with ever-increasing incidence (Duy et al.2000). Despite this fact, information on the aerosoli-zation of freshwater toxins and their role in causinghealth problems is meager. Except for a few reports(Creasia 1990, Benson et al. 2005), most of theseare concerned with the marine Florida red tidecaused by the dinoflagellate Karenia brevis (C. C.Davis) G. Hansen et Moestrup and its toxin, breve-toxin (Pierce et al. 2003, Kirkpatrick et al. 2004,Cheng et al. 2005, Flewelling et al. 2005).

Exposure to algal toxins is possible either byingestion of contaminated food or inhalation ofthe aerosolized toxins (Fitzgeorge et al. 1994,Kirkpatrick et al. 2004). Differences in the routes ofexposure manifest different clinical symptoms(Kirkpatrick et al. 2004). Laboratory animals showedhigher sensitivity to inhaled toxins in comparison toingestion (Fitzgeorge et al. 1994). Benson et al.(2005) observed that the toxic effect on differentpotential target organs following inhalation occurredat relatively lower doses than that of ingestion. TheLD50 value for microcystein-LR through inhalationwas 43 lg Æ kg)1(Creasia 1990), while this value was3000 lg Æ kg)1 by ingestion (Fitzgeorge et al. 1994).

Algal toxins are produced within the cells andare released in water after cell lysis, either due towater treatment (as in making the water potable) orwhen a bloom becomes aged (Pierce et al. 2003).The released toxins are ejected into the air as jetdrops from the bursting bubbles (Pierce et al.2003). With on-shore winds and breaking waves, thetoxins become incorporated in marine aerosol,which causes respiratory irritation and other healthproblems in the exposed population (Pierce 1986,Kirkpatrick et al. 2004). Aerosolized toxins collectedfrom the coast were the same as those in the waterand from K. brevis cultures (Pierce et al. 2003).

Particles smaller than 9 lm were reported to bedeposited 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 par-ticles themselves or the associated toxins. Clinicalsymptoms included conjunctival irritation, copiouscatarrhal exudates, rhinorrhea, nonproductivecough, bronchoconstriction, dizziness, and tunnelvision (Pierce 1986, Kirkpatrick et al. 2004). Irrita-tion and bronchoconstriction symptoms are resolvedonce a person leaves the contaminated area (Baden1983). Exposure to aerosolized toxins may causesevere exacerbation of asthma in asthmatic patients(Asai et al. 1982). However, nonasthmatics may alsoexperience respiratory irritation (Kirkpatrick et al.2004). The effect of the aerosolized brevetoxinsmight be chronic (Bossart et al. 1998). Apart fromcausing respiratory problems, airborne toxins alsoaffect exposed skin, causing itching (Kirkpatricket al. 2004).

Methodological approaches to obtain viable algae from theatmosphere. Currently, no guidelines or standardsampling methods are available to effectively char-acterize all bioaerosols and their components (Raoet al. 1996). To study airborne algae, both directand culture-based methods are in use. In the directmethod, airborne algae trapped over various kindsof substrates are observed directly under a micro-scope or cultured for the complete life cycle (Broa-dy 1992). In indirect systems, various collectiondevices, such as impactors, impingers, and differenttypes of samplers, are used (Martinez et al. 2004).Each device has its own advantages and disadvanta-ges. Particle characteristics, such as the shape, size,density, diameter, and nature of the cell wall, varygreatly and can have a dramatic effect on the col-lection efficiency of various instruments and meth-ods employed. The selection of methodology needsto be based on the availability of the device and itscost and mobility, the objective of the work, thevolume of air to be sampled, and various environ-mental conditions (Dowd and Maier 2001).Another factor that must be taken into account isthe overall biological sampling efficiency of thedevice, which is crucial for the viability of organ-isms during and after sampling (Dowd and Maier2001).

Climatic conditions of the area, location of thesampler, and the rate of air intake to the samplerall play a vital role in deciding the duration of thesampling time. The quantity of algae is likely to behigh when the sampler location is close to theground. Short sampling periods (<2 h) are expectedto produce consistent and valid results for the fol-lowing reasons: (i) there is less variation in weatherparameters; (ii) vegetative cells or spores remainviable; and (iii) there are minimal changes in thechemistry of the collection medium. Sampling peri-ods may be long in rural and remote areas (2, 4, oreven 6 h) but <2 h in industrial and urban areas toavoid the accumulation of toxic pollutants in thecollection devices. In general, low rates of intake

624 NAVEEN KUMAR SHARMA ET AL.

yield more uniform results because of minimumdamage to the cells.

Schlichting et al. (1971) made the following sug-gestions to improve the sampling regime to obtain auniform and comprehensive estimate of atmo-spheric algal particles:1. Sampling stations should be in all representative

areas (e.g., urban, rural, and remote areas) at sealevel and in hilly and mountain areas.

2. To ensure the correlation between airborne algaeand micrometeorological conditions, samplingstations should be established where air chem-istry and meteorological data are being collected.

3. Establishment of a global network of strategicallylocated sampling stations is necessary to facilitatecoordinated studies.

Future perspectives. Despite a long history of inter-est in airborne algae, various aspects are eitherunexplored or underexplored and require furtherinvestigation. These areas include the following:1. The role of airborne algae in the expansion of

HABs, which cause contamination of drinkingwater and adversely affect the underlying aquaticflora and fauna.

2. The need for controlled laboratory experimentsto ascertain whether algae are capable of toler-ating the long-distance aerial transport stresses ofdesiccation, harmful radiation, and so forth,while airborne. If so, the tolerance range, mech-anism(s) of adaptation (genetic and biochemicalchanges), and subsequent morphological andphysiological alterations need investigation.

3. Information on the role of different climatic fac-tors in the aerosolization of algae is fragmentaryand not well recognized.

4. The possible use of airborne algae as biologicalindicators of atmospheric contamination.

5. Extraction, characterization, and purification ofallergens from airborne algae.

6. The possible use of the allergenic extract of algaeto hyposensitize persons suffering from fungaland other allergies.

7. Short- and long-term inhalation effect of toxinsproduced by toxigenic airborne cyanobacteria.

8. The application of modern sensing methods, likeairborne imaging spectrometry (Panter et al.2001), chemical markers (Sebastian and Larsson2003), and molecular methods (Pace 1997) forrapid characterization of airborne algae and dustalgae.

9. The possibilities of developing culture media thatcan support the growth of the greatest diversityof algal groups, especially using dilute culturemedia.

CONCLUSION

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

roles in the dispersal of algae, colonization of newhabitats, deterioration of architectural structures orworks of art, extension of HABs, and causing aller-gies and other respiratory diseases. Furthermore,airborne algae have great potential as bioindicators.However, these aspects are not fully elucidated andneed further exploration. Use of molecular genetics,a greater variety of better-designed culture media,satellite data on weather, and information tocoordinate dynamic patterns of the winds and whatthey will carry will help to make the study of air-borne algae more reliable.

We dedicate this article to Dr. H. E. Schlichting Jr. for hisextensive contributions to the field of airborne algae. We arealso grateful to Dr. Paul Broady, Dr. Margaret Harper, andDr. Ebba Tiberg for their valuable suggestions; Dr. J¢rgenKristiansen for critically reviewing the manuscript; and Dr. W.A. Marshall for providing the reprints of his work.

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