Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust Joseph M. Prospero 1, *, Edmund Blades 2 , George Mathison 3 & Raana Naidu 4,5 1 Cooperative Institute for Marine and Atmospheric Studies, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami FL 33149, USA; 2 Faculty of Pure and Applied Sciences, University of the West Indies and Queen Elizabeth Hospital, Barbados, West Indies; 3 Faculty of Pure and Applied Sciences, University of the West Indies, Barbados, West Indies; 4 Faculty of Medical Sciences, University of the West Indies and Queen Elizabeth Hospital, Barbados, West Indies; 5 Present address: Greenville Hospital System, 701 Grove Rd, Greenville SC 29605 (*Author for correspondence, E-mail: [email protected]; Fax: +305-421-4457) (Received 4 May 2004; accepted in final form 22 October 2004) Key words: African dust, bacteria, fungi, intercontinental transport, microorganisms Abstract Daily aerosol samples collected in trade winds at Barbados, West Indies, throughout 1996–1997 yielded significant concentrations of viable (culture-forming) bacteria and fungi only when African dust was present. Air masses from the North Atlantic, North America, and Europe yielded no cultivable organisms. The strong association of cultivable organisms with African dust suggests various factors that might be relevant to viability. Although we did not specifically look for pathogens, these same mechanisms could protect them as well. Our results suggest that arid regions could be an important source for the long-range transport of viable microorganisms. The transport of microorganisms to Barbados follows a clear mete- orological and seasonal pattern, which suggests that it should be possible to model the transport process and to predict events. Microorganism and dust concentrations were unusually great in 1997, possibly in response to the strong El Nin˜o. This suggests that the long-range transport of microorganisms might be particularly responsive to climate variability in general. 1. Introduction Winds serve as a mechanism that enables the rapid transport of microorganisms (MOs) among widely dispersed habitats (Isard and Gage, 2001). These include organisms pathogenic to humans, animals, and plants (Brown and Hovmøller, 2002). It is well known that plant pathogens can be transported by winds over hundreds of kilometres, for example, the periodic transport of Tobacco Blue Mold (Peronospora tabacina Adam) from Cuba to the southeastern United States (Davis and Monahan, 1991). There is, however, only anecdotal indirect evidence for the long-range transport (LRT) of viable MOs on intercontinental scales. In the review by Brown and Hovmøller (2002), the attribution to over-ocean wind transport of MOs is based solely on the existence of generally favorable synoptic meteorological conditions, not on any specific measurements of MOs present in hypothesized transporting winds. For example, sugarcane rust in the Dominican Republic is attributed to the transport of urediospores from Cameroon (Purdy et al., 1985), based on the relative timing of rust outbreaks in those locations and the prevalence of wind trajectories that could Aerobiologia (2005) 21:1–19 Ó Springer 2005 DOI 10.1007/s10453-004-5872-7
Transcript
Interhemispheric transport of viable fungi and bacteria from Africa to theCaribbean with soil dust
Joseph M. Prospero1,*, Edmund Blades2, George Mathison3 & Raana Naidu4,51Cooperative Institute for Marine and Atmospheric Studies, Rosenstiel School of Marine and AtmosphericScience, University of Miami, 4600 Rickenbacker Causeway, Miami FL 33149, USA; 2Faculty of Pure andApplied Sciences, University of the West Indies and Queen Elizabeth Hospital, Barbados, West Indies;3Faculty of Pure and Applied Sciences, University of the West Indies, Barbados, West Indies; 4Faculty ofMedical Sciences, University of the West Indies and Queen Elizabeth Hospital, Barbados, West Indies;5Present address: Greenville Hospital System, 701 Grove Rd, Greenville SC 29605(*Author for correspondence, E-mail: [email protected]; Fax: +305-421-4457)
(Received 4 May 2004; accepted in final form 22 October 2004)
Daily aerosol samples collected in trade winds at Barbados, West Indies, throughout 1996–1997 yieldedsignificant concentrations of viable (culture-forming) bacteria and fungi only when African dust waspresent. Air masses from the North Atlantic, North America, and Europe yielded no cultivable organisms.The strong association of cultivable organisms with African dust suggests various factors that might berelevant to viability. Although we did not specifically look for pathogens, these same mechanisms couldprotect them as well. Our results suggest that arid regions could be an important source for the long-rangetransport of viable microorganisms. The transport of microorganisms to Barbados follows a clear mete-orological and seasonal pattern, which suggests that it should be possible to model the transport processand to predict events. Microorganism and dust concentrations were unusually great in 1997, possibly inresponse to the strong El Nino. This suggests that the long-range transport of microorganisms might beparticularly responsive to climate variability in general.
1. Introduction
Winds serve as a mechanism that enables the rapidtransport of microorganisms (MOs) among widelydispersed habitats (Isard and Gage, 2001). Theseinclude organisms pathogenic to humans, animals,and plants (Brown and Hovmøller, 2002). It is wellknown that plant pathogens can be transported bywinds over hundreds of kilometres, for example,the periodic transport of Tobacco Blue Mold(Peronospora tabacina Adam) from Cuba to thesoutheastern United States (Davis and Monahan,1991). There is, however, only anecdotal indirect
evidence for the long-range transport (LRT) ofviable MOs on intercontinental scales. In thereview by Brown and Hovmøller (2002), theattribution to over-ocean wind transport of MOsis based solely on the existence of generallyfavorable synoptic meteorological conditions, noton any specific measurements of MOs present inhypothesized transporting winds. For example,sugarcane rust in the Dominican Republic isattributed to the transport of urediospores fromCameroon (Purdy et al., 1985), based on therelative timing of rust outbreaks in those locationsand the prevalence of wind trajectories that could
conceivably effect such transport. The one unam-biguous clearly documented case of live organismtransport from Africa to the Caribbean occurredin 1988, when swarms of African desert locusts(Schistocerca gregaria) reached Trinidad andBarbados (Ritchie and Pedgley, 1989; Rosenbergand Burt, 1999).
We are aware of no long-term systematicstudies of the LRT of MOs over the oceans. A fewstudies have been carried out over the oceans andin remote (primarily high latitude) regions but thedata are sporadic and much of it is in the olderliterature. Lighthart and Stetzenbach (1994) sum-marize this literature and conclude that although ithas been shown that bacteria and fungi can betransported in the air for long distances, evidencesuggests that ‘‘most survive over relatively shorttimes.’’ They also note that the genera/speciesdistributions change with distance from the sourcebut they do not comment on any systematicbehavior that would provide insights on the fac-tors that affect the viability of the MOs.
Our study is based on Barbados (13.18�N,59.43�W), the eastern-most island in theCaribbean (Figure 1), where we have made aerosolmeasurements continuously since 1965. Duringmuch of the year the trade winds carry largequantities of African mineral dust to Barbados
(Savoie et al., 1989; Li et al., 1996; Prospero 1996;Prospero and Lamb 2003). Winds subsequentlycarry dust into the Caribbean and to Florida(Prospero, 1999; Prospero et al., 2001), to theeastern United States (Perry et al., 1997) and toBermuda (Arimoto et al., 1992, 1995).
The primary purpose of this study is to char-acterize the day-to-day variability of commonairborne MOs and to place the variability in thecontext of the large-scale synoptic meteorology ofthe tropical Atlantic. To this end we collected dailyaerosol filters and cultured them for bacteria andfungi using standard techniques. Concurrently wemeasured an array of inorganic aerosol species:mineral dust from soils; non-sea-salt (nss) SO4
=
i.e., SO4= from sources other than the salts in
ocean-water spray droplets, primarily pollutionsources and the oxidation of dimethyl sulfideemitted by marine phytoplankton (Davis et al.,1999); NO3
), derived from both natural and pol-lution sources (Holland et al., 1999); sea-salt fromocean spray droplets (Savoie et al., 2002). Becauseof our long history of studies on Barbados we havea good understanding of the factors that controlaerosol composition and concentration in theNorth Atlantic trade winds. By combining mea-surements of conventional inorganic aerosols,including mineral dust, with those of bacteria andfungi, we would expect to gain a better under-standing of the factors affecting the large scaletransport of viable MOs. Because we collect dailysamples we can more readily relate our measure-ments to specific meteorological situations and tospecific back-trajectories. In this study we examineand compare the daily temporal record of aerosoland microorganism concentrations over the period1996–1997.
2. Methods
2.1. Sampling techniques
Sampling is carried out at Ragged Point, Barbados,(Figure 1) at the top of a 17 m high walk-up towerstanding on a 30 m high bluff located immediatelyon the easternmost coast of the island. Daily filtersamples are collected at a nominal 10 l min)1 (i.e.,about 14 m3 day)1) using sterile microbiologicalfilters (cellulose nitrate, 47 mm in diameter, 0.2 lmpore size). We paid considerable attention tothe location of the sampling site and sampling
Figure 1. Map of Barbados with inset map of the tropicalAtlantic. The Barbados map shows the location of the Uni-versity of Miami sampling station at East Point immediately tothe north of Kitridge Point. The ‘‘X’’ shows the location of thesampling site at the University of the West Indies, Cave Hill; the‘‘star’’ sign (q), the location of the inland sampling site on thewestern side of the island. 1 km from the east coast. Inset: Mapof the North Atlantic showing the location of Barbados alongwith other aerosol sampling stations occupied at various timesin the University of Miami aerosol program.
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protocols so as to minimize the possibility of im-pacts from local sources. We later show that airsampled a short distance inland from the coast ofBarbados can yield cultivable MO concentrationsthat are about 100–1000 times higher than thoseobtained at our tower site. Among other precau-tions we have used smoke tests to show that the topof the tower lies above the turbulent air layergenerated by the wind flowing up the face of thebluff and over the top of the bluff. The pump iscontrolled by a wind sensor via a computer so as tosample only over-ocean winds in the sector 335�through North to 130� at wind speeds greater than1 m sec)1. Within the sampling sector the closestland is the Cape Verde Islands and the coast ofAfrica, 3800 and 4600 km, respectively, to the east.Sampling is continuous during the 24-hour periodso long as the wind sector condition is met (onaverage, about 95% of the time) and it is notraining.
Two filters are deployed at the top of the towereach day, one serving as a blank, which is pro-cessed in the same way as the sample. Working on-site in a HEPA filtered clean bench, filters areplaced in sterile Petri dishes and transported to themicrobiology laboratory of the Queen ElizabethHospital where the School of Clinical Medicineand Research, University of the West Indies, islocated. All subsequent manipulations were car-ried out in the Microbiology Department of thePathology Laboratory using procedures normallyused in the hospital’s microbiological analyses.
2.2. Culturing techniques and identifications
Bioaerosol measurements are very sensitive tocollection and culturing techniques (Burge, 1995;Lacey and Venette, 1995; Griffiths et al., 1999,2001). In this study our objective was to charac-terize the temporal variability of bacteria andfungi that are commonly found over land. Tofacilitate comparisons with previous work we usedtechniques that are frequently used in such studies.Filters were cut in half with a sterile scalpel. Onesection was placed (sample side up) on blood–agarmedium for bacterial growth. Blood-based nutri-ents are non-selective media which are widely usedfor broad-spectrum studies (Lacey and Venette,1995). The other half filter was placed on Sabou-raud’s medium for fungi. The cultures wereinitially incubated at 37 �C for 48 hours and then
at 30 �C for up to 2 weeks. The number of colo-nies was counted and the results reported as thenumber of colony-was forming units (CFU) percubic meter of air (CFU m)3). The resulting cul-tures were subcultured onto similar media. Withrare exceptions, blanks yielded no cultures. Stan-dard light microscopy and phase contrast micros-copy were used to examine fungal cultures andidentify spores produced in culture. Phenotypicidentifications were based on the macroscopic andmicroscopic morphology of the cultures andspores, respectively. When a clear identificationcould not be made, the sample was sent to theUniversity of Texas Health Science Center, SanAntonio (M.G. Rinaldi), where reference collec-tions are maintained.
Bacterial endospores are formed by certaingenera. Under favorable conditions these sporesgerminate to produce vegetative cells. Unstainedendospores are not readily detectable under lightmicroscopy, especially with the high loading ofdust on the surface of the filters. Identification isbased primarily on morphology, gram stain, andspore stain of the cultures. Staining for spores wasperformed on 1-week-old cultures (Murray et al.,1999). Bacteria were typically gram positive (stainpurple) or gram variable (some stain purple andsome stain pinkish). Some gram positive organ-isms, especially Bacillus species, lose their grampositive properties with age and therefore tend tostain pink.
On a limited number of samples we searchedfor anaerobic species (e.g., Clostridia). We culturedfilters anaerobically, using Oxoid Anerogen gasgenerating kits with indicator; none were found.
Because there is some debate about the relativemerits of rich culture media, such as Sabouraud’s,and weaker media (Lacey and Venette, 1995;Burge, 1995), we ran tests to compare Sabouraud’s(the one normally used in our program) with R2A,a weaker nutrient commonly used in the cultureof stressed organisms (Burge, 1995; Muilenberg,1995). Cultures of daily filters collected over17 days of concurrent sampling yielded similarresults with both media. Linear regressionof Sabouraud vs. R2A yields: b(0) ¼ 0.038,b(1) ¼ 1.19, r2 ¼ 0.99. One sample yielded con-centrations (CFU) about ten times greater that thehighest measured in the remaining 16 samples;eliminating this one outlier, the regression yieldscomparable values: b(0) ¼ 0.157, b(1) ¼ 0.88,
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r2 ¼ 0.78. We conclude that there is no substantialdifference between these two media with regard tothe culturing of organisms associated with Africandust.
We also ran tests for the effects of varyingsampling duration to see if viability is affected bylong exposure to air streaming through the filterand to high loadings of sea salt, factors that canaffect MO viability (Lighthart, 2000). We usedthree parallel samplers. One ran continuously (aslong as the wind condition was satisfied) for anominal 24 hours, the normal sampling protocol.The other two samplers were run (also wind-sectorcontrolled) on skip timers with one runningintermittently for six equally spaced 1-hour peri-ods (total 6 hours) over a nominal day and theother running intermittently for six quarter-hourperiods (total 1.5 hours). Filter halves were cul-tured on both Sabouraud’s and R2A media. Over16 days of daily sampling we found no substantialdifferences between the two nutrients regardless ofsampling time. The 24-hour samples yielded amean of 0.51 CFU/m3 (standard deviation ¼ 0.38)with Sabouraud’s and 0.40 CFU/m3 (0.38) withR2A. Yields for 6-hour samples: Sabouraud’s,0.47 CFU/m3 (0.71); R2A, 0.89 CFU/m3 (1.33).For 1.5-hour samples: Sabouraud’s, 0.96 CFU/m3
(1.48), R2A, 0.22 CFU/m3 (0.86). As expected theshorter sampling times yielded poorer statisticsbecause of the small volumes and low colonycounts.
2.3. Inorganic aerosol sampling
In addition to the biological samples, we concur-rently collected daily aerosol samples usingWhatman-41 filters and the same wind-sectorcontroller. Filters were returned to Miami wherethe soluble fraction was extracted and analyzed forSO4
=, NO3), and Na+ (Savoie et al., 2002). Sul-
fate and NO3) concentrations were measured with
1r uncertainties of ±5% using suppressed ionchromatography and Na+ with a 1r uncertaintyof ±2% by flame atomic absorption spectropho-tometry. Sodium was used to calculate sea-saltaerosol concentrations, multiplying by 3.252, theNa+/total-salts ratio in sea water. The concen-tration of SO4
= from sources other than the dis-solved salts in seawater (nss-SO4
=) was calculatedas total SO4
= minus the Na+ concentration times0.2516, the SO4
=/Na+ mass ratio in bulk sea-
water. The absolute 1r analytical uncertainties formeasurements of nss-SO4
= were usually less than0.1 lg m)3; uncertainties due to blank correctionswere typically about an order of magnitude lower.
The extracted filters were then placed in amuffle furnace for about 14 hours (overnight) at550 �C; the ash residue weight (less filter blank) isassumed to be mineral dust. The standard error inthe mineral aerosol concentration is ±10% forconcentrations greater than about 1 lg m)3; below1 lg m–3 the standard error is essentially constantat ±0.1 lg m)3. The parallel analyses of samplesfor Al yields an Al content of about 8%, a valueconsistent with average crustal composition(Prospero, 1999).
3. Results
3.1. Temporal variability
The cultivable fungi and bacteria were primarilyspore-formers (Table 1). Concentrations variedover a wide range (Figure 2), from 0 to about20 CFU m)3. Concentrations were mostly zeroduring the winter; they increased sporadicallyduring the spring, remained relatively high throughthe summer, and then showed sporadic behavioronce again in the fall. There was a close match inthe temporal spacing of the peaks of fungi andbacteria but there were often substantial differencesin their relative concentrations. For exampled inthe spring and summer of 1996 fungi tend, to besomewhat greater than bacteria whereas bacteriastrongly dominated in the fall. In 1997 bacteriadominated in the spring but there are specificevents where fungi concentrations are much higher.Indeed, scatter plots of the concentrations of bac-teria against fungi (not shown) yield a very broaddistribution with no apparent correlation.
There are also substantial differences betweenthe years. In particular, during February–Marchand most notably in June 1997 the concentrationsof both bacteria and fungi were markedly higherthan in 1996. In fact concentrations in June 1997were substantially higher than any other period inthe record. The June 1997 anomaly stands outclearly in Figure 2. Figure 3 shows the dailyrecord of fungal and bacterial concentrations in1996–1997 displayed along with the concentrationsof mineral dust, nss-SO4
=, and sea-salt. Note thatthe monthly means in many months (e.g., Fall
4
Table
1.Comparisonoffungiin
BarbadostradewindswithAfricanandMiddle
East
regionsa
Thiswork
Barbados
Dransfield(1966)b
NorthernNigeria
Davies(1969)c
Kuwait
Halwagy(1989)d
Kuwait
Abdalla(1988)e
Khartoum,Sudan
Al-Subai(2002)f
Qatar
Al-Suwaine
etal.(1999)g
Ridyadh
%Air
%Air
%Soil
%Air
%Air
%Air
%Air
%Air
Myceliasterila
47.9
6.6
5.4
6
Arthrinium
21.6
0.3
Periconium
12.0
Black/grey
6.9
Brown/tan
3.1
Penicillium
2.9
1.8
32.7
6.5
3.95
19
Curvularia
1.6
25.1
0.6
0.8
4.1
Cladosporium
1.5
38.8
3.7
66
59.9
2.4
40.1
41
Aspergillus(total)
1.1
1.7
32.5
70.7
4.3
18
A.niger
0.72
22.8
1.3
A.fumigatus
0.24
2.4
A.clavatus
0.08
A.terreus
0.05
13.0
0.06
A.flavus
0.03
24.4
A.nidulans
–8.1
A.sydowi
–0.06
Neurospora
0.08
0.06
Pink/red
0.03
Alternaria
0.02
46
21
6
Epicoccum
–5.8
0.0
0.36
Fusarium
–8.2
4.9
0.4
0.3
Nigrospora
–4.3
0.0
0.5
0.12
Pullularia
–4.0
0.4
Ulocladium
–1.6
9.2
5
Ustilago
–8
9.3
aWereportallculturesidentified
inBarbadostower
samples,thecorrespondingspeciesfoundin
theliterature
citedhereaswellasmajorspeciesfoundin
oneormore
ofthecited
literature
butnotfoundin
Barbadossamples.
bDransfeld(1966):Airdepositionbysettlingto
Pietridish;culture
on2%
Difco
maltagar.Soil:Czapek-D
oxagar.
cDavies(1969):Spore
trap,microscope.
dHalwagy(1989):Spore
trap,microscope.
eAbdalla(1988):Settlingfrom
aironpotato
dextrose
agar.Focusedmostly
onAspergillus.ListinghereforJune.
f Al-Subai(2002):Settlingonto
glucose
agar.
gAl-Suwaineet
al.(1999):Suctionairsamplingonto
agarplates.Averageoftw
osites.
5
Figure 2. The concentration of cultivable fungi (right axis) and bacteria (left axis) in the trade winds at Barbados, 1996–1997. Units:number of colony-forming units (CFU) of fungi and bacteria per cubic meter of air sampled through the filter (CFU m3). The scale onthe right-hand axis is offset for clarity.
Figure 3. The daily concentration of cultivable fungi and bacteria in Barbados trade winds during 1996 and 1997 in comparison tovarious aerosol constituents: (a) bacteria and mineral dust; (b) fungi and dust; (c) fungi and nss-sulfate (nss-SO4
=); (d) fungi and seasalt. Units: fungi and bacteria, CFU m)3; aerosols, lg m)3. In each panel the MO concentration is shown in blue and the comparisonaerosol (dust, nss-SO4
=, sea-salt) in red.
6
1996) are strongly driven by a few samples withrelatively high concentrations. This is especiallytrue for bacteria. Fungal concentrations do notseem to be quite so variable.
Figure 3 shows the daily record of fungal andbacterial concentrations in 1996–1997 displayedalong with those for mineral dust, nss-SO4
=, andsea-salt. Fungi and bacteria show a seasonal cyclethat is very similar to that of dust (Figure 3a, b):extremely low concentrations in winter, high insummer. Dust concentrations were much higher inFebruary–March 1997 and the summer and earlyfall of 1997 compared to 1996, similar to the pre-viously noted differences in the interannual con-centrations of fungi and bacteria.
Furthermore there is a close match in the tem-poral spacing of individual pulses of dust and thepeaks of fungi and bacteria. The close correspon-dence between dust pulses and those of fungi andbacteria is especially notable in June 1997. Al-though the timing of the peaks matches well, theconcentrations of fungi and dust were not corre-lated; scatter plots (not shown) yield very broaddistributions. Scatter plots of bacteria against dustagainst (not shown) are similar.
In contrast to dust, there is no coherence be-tween the peak patterns of bacteria and fungi andthose of nss-SO4
= and sea-salt (Figure 3c, d).Note in particular the winter and spring periods (1January to late April 1996; December 1996 to lateMay 1997) when fungi and bacteria concentrationswere extremely low (usually zero) along with dustexcept for occasional brief pulses. During this timesea-salt concentrations were quite high because ofstrong winter winds while those of nss-SO4
= wereoften substantial. Ocean spray droplets can carrylarge concentrations of bacteria and fungi butculturing these would require specific nutrientmedia.
To examine more carefully the relationshipbetween dust concentrations and those of bacteriaand fungi we show data (Figure 4) for three majordusty periods. In early 1996 (Figure 4a) fungiconcentrations increased dramatically from back-ground levels with the first pulse of dust on 31March. Bacteria also increased but only moder-ately. Fungi concentrations dropped sharply on 13April with the end of the extended 2-week dustyperiod. Throughout this dust event fungi concen-trations were always much greater than those ofbacteria. After 13 April fungi and bacteria
remained at background levels until 5 May whenthe next pulse of dust arrived. After 5 May fungiconcentrations were generally greater than bacte-ria although the difference was not so great as inthe April event; on some days bacteria dominatedfungi. This example more clearly shows a pointmade previously: that we only see MOs duringdust events but that within dust events MOs arenot correlated with dust. Indeed, some dust eventsyield very low cultivable MOs. Note in particularduring 5–7 April when dust concentrations werehigh, fungi dropped to low levels. Similar examplesare noted elsewhere in this time series.
In early 1997 (Figure 4b), we see once againthat MO concentrations are at background levels(i.e., essentially none) until the first dusty period.Although we obtained no MO samples during thevery beginning of this dust event which started on6–7 February, it is clear that MO concentrations
Figure 4. Time series of dust concentrations and of cultivablefungi and bacteria during three major dust events. (a) March–May 1996; (b) January–March 1997; (c) May–June 1997. Units:fungi and bacteria, CFU m)3; dust, lg m)3.
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increased sharply during the dusty period anddropped to background levels once it ended on 28February; they remained low until dust concen-trations jumped again on 4 March. During thisevent bacteria levels were substantially higher thanduring the spring 1996 example (Figure 4a). Heretoo we note that although MOs are associatedwith dust episodes, they are not tightly correlatedto dust concentrations. For example, peak, dustconcentrations were measured on 11–13 Marchwhen MOs were at intermediate levels. In contrastbacteria peaked on 9 March, just before the peakdust concentrations.
The highest concentrations of dust, bacteriaand fungi were measured in early June 1997 (Fig-ure 4c). During much of this dust event bacteriaand fungi concentrations were roughly equal andthe peaks-and-valleys of the three species wereclosely matched. The results in 1997 are of par-ticular interest because of the El Nino that beganin that year, one of the strongest on record in the20th century (McPhaden, 1999). Dust concentra-tions in 1997 were among the very highest mea-sured over the entire record at Barbados, startingin 1965 (Prospero, 1996; Prospero and Lamb,2003). Prior to 1997, comparably high dust con-centrations were only measured in 1983–1984when a very strong El Nino was in effect (Prosperoand Lamb, 2003).
3.2. Transport characteristics of African dust,bacteria and fungi
The close match (in a broad sense) between thetemporal variability of dust with that of fungi andbacteria suggests that they are transported fromNorth Africa. Dust emerges from North Africa inpulses. During the summer, dust is generally car-ried behind easterly waves. The highest concen-trations are usually found in a layer that extendsfrom the top of the marine boundary layer (MBL),at about 1 km over the western Atlantic, to analtitude of 3–4 km (Karyampudi et al., 1999; Reidet al., 2002, 2003). The elevated layer, because ofits desert origin, is hot and dry, making it easy toidentify in meteorological soundings. Because ofthese properties it is commonly referred to as theSaharan Air Layer (SAL) (Carlson and Prospero,1972; Karyampudi et al., 1999). It is notable thatthe seasonal period of dust transport coincideswith the hurricane season in the tropical Atlantic;
indeed, the SAL and the entrained dust may play arole in modulating the frequency and intensity oftropical cyclones in the region (Dunion and Velden2004).
The African dust plume undergoes a seasonaldisplacement that follows the seasonal changes inlarge-scale circulation over the Atlantic. Duringthe winter months the dust plume is carried in thelow latitudes to the NE coast of South America(Prospero et al., 1981; Swap et al., 1992). In thesummer months it reaches its northernmost posi-tion; then the plume passes Barbados and extendsdeep into the Caribbean, the Gulf of Mexico, andthe southern and eastern US. The seasonal oscil-lation of the dust plume is consistent with theseasonal cycle of dust concentrations as measuredin Barbados (Prospero and Lamb, 2003), Miami(Prospero, 1999), and Bermuda (Arimoto et al.,1992, 1995). While dust transport is greatest in thesummer at Barbados, dust is occasionally trans-ported during winter and more frequently duringspring (Prospero and Lamb, 2003) as seen inFigures 3 and 4.
Various satellite aerosol products (Hermanet al., 1997; Husar et al., 1997; Kaufman et al.,2002) enable us to trace individual dust out-breaks from the time the dust clouds emergefrom the coast of West Africa until they reachthe western Atlantic and Caribbean about oneweek later. A number of these are available onthe web in near-real time. The Total OzoneMapping Satellite (TOMS) absorbing aerosolproduct (Herman et al., 1997) is particularlyuseful because it provides a measure of theatmospheric loading of UV-absorbing aerosols(i.e., mineral dust and soot from anthropogenicand natural combustion sources) on a globalscale on a daily basis.
In contrast to most aerosol-sensing satelliteswhich are most effective over water surfaces,TOMS provides observations over both waterand land surfaces and thereby yields informationon sources (Prospero et al., 2002). An exampleof the TOMS product is given in Figure 5 for 13and 14 June 1997. These show a plume of dustextending from the west coast of Africa to theCaribbean. On these 2 days the concentration ofdust and MOs increased sharply on Barbados(Figure 4c). During the summer months on mostdays TOMS shows large areas of the tropicalAtlantic covered with dust.
8
The TOMS images in Figure 5 also provide anindication of the dominant dust sources and,possibly, MOs. On 13 and 14 June 1997 (Figure 5),the red-coded (maximum aerosol index) areas overWest Africa suggest major dust activity inMauritania and northern Mali, regions known tocontain major dust sources (Prospero et al., 2002).
While satellite images such as those fromTOMS are useful in interpreting our data records,they do have limitations. TOMS does not producereliable data in the presence of cloud and cloudbecomes increasingly more common over thewestern Atlantic and the Caribbean. Moreover,TOMS requires relatively high concentrations ofdust to yield an unambiguous response (Chiapelloet al., 1999). Indeed, on most occasions the con-centration of dust over the western Atlantic andCaribbean is relatively low compared to the situ-ation depicted in Figure 5 and the TOMS productdoes not show the presence of aerosols as shown inthe examples. Indeed, at low dust concentrations,the TOMS response is attributable largely to thepresence of other types of absorbing aerosols, e.g.,black carbon (Chiapello et al., 1999).
Nonetheless satellite observations in general,and TOMS in particular, when coupled withmeteorological data and air mass trajectories (asdiscussed in the following section) provide strongsupport for the interpretation of our data in termsof source and transport paths. Unfortunately, theNIMBUS 7 detector has degraded over the pastseveral years and current performance is marginal.However a new replacement satellite, Aura-OMI,was launched in July 2004.
3.3. Dust variability and transport trajectories
Air parcel back trajectories provide insights onthe source of aerosols arriving at Barbados.During the summer months, when dust is presentalmost every day, trajectories from within theclimatological SAL altitudes generally lead backto the coast of Africa 5–7 days earlier. Figure 6(NOAA ARL HYSPLIT4 1997) shows backtrajectories on 4 June 1997 when the concen-trations of dust, fungi and bacteria reached asimultaneous peak. Trajectories are shown forthree starting altitudes over Barbados: 500 m,within the MBL at Barbados; 2000 m, within theSAL which typically extends from about 1000 toabout 3000 m over Barbados; 4000 m, normallyabove the top of the SAL. During the 10-dayback-trajectory period, the 500 m trajectorynever touches land; it sinks from the middletroposphere over the northwestern and centralNorth Atlantic. The 2000 m trajectory leadsback to Africa crossing the coast in Senegal7 days earlier; it then hooks north into Mauri-tania where some of the world’s most intensedust sources are located (Prospero et al., 2002).The 4000 m trajectory crosses the coast of Africa8 days earlier passing over the Gulf of Guineacoastal states, a region where there are no majordust sources.
The example in Figure 6a for 4 June 1997 istypical of the summer months. During the 30 daysof June 1997, only three 500 m trajectories tracedback into Africa; the mean back-transit time was9.0 days. Only one other 10-day 500-m trajectory(8 June) crossed onto land, passing over the NEcoast of Arctic Canada 10 days earlier. Of the 302000 m trajectories, 19 traced back to Africa witha mean transit time of 6.6 days while 15 of the4000 m trajectories crossed into Africa with amean transit time of 6.9 days.
Figure 5. TOMS absorbing aerosol distributions. 13–14 June1997; Top: 13 June; Bottom: 14 June. Color code: Red – highconcentrations of absorbing aerosols (i.e., dust and smoke);Yellow – intermediate; Gray – low. http://toms.gsfc.nasa.gov/aerosols/aerosols.html.
9
The fact that so few 500 m trajectories reachAfrica would seem to be inconsistent with the factthat we measured substantial concentrations ofdust in the MBL at Barbados almost every day inJune 1997. The dust that we measure at the surfacein Barbados is not necessarily transported acrossthe Atlantic at this low altitude. As stated earlier,
the primary transport path of dust is in the SAL(Reid et al., 2002, 2003). Aerosols initially presentin the SAL could settle into the MBL or betransferred there through convective mixing asso-ciated with small trade-wind clouds. This trans-port mode would not be reflected in back-trajectory calculations. In fact the monthly meandust concentrations measured at the surface onBarbados are highly correlated with the monthlymean column aerosol optical depth (r ¼ 0.93) butthe day-to-day concentrations are not (Smirnovet al., 2000).
It should be noted, however, that the compu-tation of back trajectories in the tropical Atlanticis difficult because of the dearth of data over theocean and the complex meteorology in the tropics.They become less dependable the longer the back-calculation times. Thus trajectories should not beinterpreted too closely. As an example, in Fig-ure 6b we show the back trajectories for 15 June1997 when dust and MOs were peaking. Thelooping paths reflect the influence of a depressionpassing to the north of Barbados, complicating thecalculation of trajectories. Indeed on the followingday, 16 June, all three paths looped in a similarfashion with none tracing back to Africa; yet dustand MO concentrations remained moderatelyhigh. In contrast back trajectories computed froma point several degrees to the east of Barbados dotrack back to Africa. Such discrepancies empha-size the point made earlier – that the dearth ofmeteorological data in the tropical Atlantic andthe complex meteorology make such calculationsdifficult. Despite these shortcomings, the trajecto-ries do present a generally consistent picture ofaerosol transport paths over the region and theirseasonal variability.
In contrast to the summer trajectory picture,trajectories during the winter and through much ofthe spring generally trace back to the NorthAtlantic, many hooking westward to NorthAmerica or sometimes eastward to Europe. Thesewinds sometimes carry substantial concentrationsof pollutant SO4
= and NO3) (Savoie et al., 1992,
2002) but, as we show here, they carry no organ-isms cultivable on our media.
A good example of the effect of changes in airmass trajectory is found in March through April1996 (Figure 4a). Until about mid-March, dustand fungi concentrations are at minimum valuesand nss-SO4
= is close to background levels for this
Figure 6. HYSPLIT back trajectories from Barbados, WestIndies, at three altitudes: 500, 2000, 4000 m. (a) 4 June 1997; (b)15 June 1997. Trajectories obtained from the NOAA ARLREADY web site: www.arl.noaa.gov/ready.html. In each panelsymbols mark 24-hour time periods; the lower portion of eachpanel shows the altitude history of the back trajectories startingover Barbados at 500 m, 2000 m and 4000 m.
10
region. On 22 March, nss-SO4= increases sharply
and rises to a plateau at about 1.1–1.2 lg m)3
which extends to 12 April and then drops sharply.In contrast, mineral dust and fungi concentrationsremain at minimum values until 31 March whenthey rise sharply and remain high into early April.Back trajectories show that on 30 March, imme-diately prior to the arrival the dust pulse, airparcels at 500 m over Barbados trace back tonorthern North America a week earlier; the 2000and 4000 m trajectories hook back toward theGulf of Mexico. The altitude tracks show that alltrajectories descended from moderately high alti-tudes, over 4000 m. The concentrations of nss-SO4
= (Figure 3) and NO3) (not shown) are rela-
tively high along with sea-salt but dust and fungiremain extremely low.
Dust peaks on 3 April (Figure 3a). On that daythe 500 m (MBL) back trajectory traces back tothe African coast a week earlier and penetratesinto southern Mauritania and Mali, a regionknown to have major dust sources (Prospero et al.,2002). The 2000 m trajectory passes somewhatfurther to the south while the 4000 m trajectorycrosses into the South Atlantic, never touchingland in its 10-day history. Nss-SO4
= and NO3)
remain high during this period reflecting thepresence of soil materials and also pollutants, mostlikely from European sources (Savoie et al., 1992).On 14 April, when dust levels are again low, thetrajectories once again trace back to the NorthAtlantic and North America. A similar trajectoryscenario holds for the February–March dust event(Figure 4b).
The task of calculating back-trajectories isespecially difficult in the spring months when Bar-bados lies on the northern boundary of the trans-Atlantic dust transport belt (Husar et al., 1997).
At such times it is not unusual to measure highconcentrations of dust and MOs on days when thetrajectories do not trace back to Africa but, rather,wander aimlessly in the tropical–subtropicalAtlantic. Ultimately the best confirmation of anAfrican origin is the presence of dust in filtersamples; the dust produces a distinct red-browncolor that is quite visible to the naked eye.
3.4. Comparisons with other regions
It is difficult to compare literature reports of air-borne bacteria and fungi concentrations in differ-
ent regions because of the wide variety ofcollection and culturing practices used (Comtoisand Isard, 1999). Nonetheless, a summary ofmeasurements (Lighthart and Stetzenbach 1994)shows concentrations in rural (non-agricultural)regions ranging from 1 to 3802 CFU m)3; typicalranges are from low units to several hundredCFU m)3. Lacey and Venette (1995) report typicalpeak concentrations of about 104–105 m)3. Withregard to bacteria, Lacey and Venette (1995) findthat concentrations are higher in cities (up to4000 CFU m)3, average 850) than in rural areas(up to 3400 CFU m)3, average 99). Muilenberg(1995) cites concentrations of cultivable bacteriaoutdoors in the range of 100–1000 CFU m)3.Thus bacteria and fungi concentrations inBarbados trade winds are at the extreme low endof the range of continental values and 100–1000times lower than typical continental values.
3.5. Genera and species characteristics
Table 1 shows the frequency of occurrence ofcolony-forming bacteria and fungi in 1996–1997based on identifications of a total of 13,410 colo-nies. The colony counts were evenly split betweenfungi (48.8%) and bacteria (51.2%), the latter al-most exclusively Bacillus. The dominant funguswas Mycelia sterila which comprised 48% of thefungal colonies. Arthrinium (22%) and Periconium(12%) were also common along with unidentifiedblack/gray (7%) and brown/tan (3%) colonies.
Review articles attempt to compare speciesdistributions in different environments. Lacey(1991) states that Cladosporium is the most abun-dant spore type on an annual basis in temperateand most tropical regions although other sporesmight be regionally dominant in some seasons;Alternaria spores are the second most abundantoverall and in warm, dry regions can exceed theconcentrations of Cladosporium. In tropical re-gions Curvularia and Nigrospora sometimes makelarge contributions and Aspergillus species areparticularly characteristic of humid tropicalregions. Lighthart and Stetzenbach (1994) findthat the most prevalent genus of fungi at remotesites is often Cladosporium although Alternaria isfrequently observed. Alternaria and Cladosporiumare dematiaceous Hyphomycetes (asexual fila-mentous fungi); both are pigmented. MoreoverCladosporium spores are often clustered.
11
There is little information on airborne MOs inthe region of Africa from which Barbados dustoriginates. Also the limited literature from aridregions is based on a variety of techniques thatmakes direct comparisons questionable. Table 1summarizes literature from arid regions in Africaand the Middle East. In northern Nigeria, some-what to the south of the major dust sources thatimpact Barbados, cultures were dominated byCladosporium (36.8%) and Curvularia (25.1%)(Dransfield, 1966). In Kuwait, the most commonfungal spore was Cladosporium (66%) followedby Ustilago (8%), Alternaria (4%), Helminthos-porium (3%), Basidiospores (4%), and Mycelialfragments (6%) (Davies, 1969). Halwagy (1989)measured the seasonal concentration of spores atthree sites in Kuwait in 1977–1982. He found thatCladosporium was most common by far (ca.60%). Next was Ustilago, 9–10% and Alternaria,about 6%.
Al-Subai (2002) made daily measurements ofairborne fungi at Doha, Qatar, over a 1-year per-iod. He found that Cladosporium was most com-mon (40.1% of total fungi) followed by Alternaria(21%) and Ulocladium (9.2%). Two fungi that areusually dominant in soils, Aspergillus and Penicil-lium, were relatively minor in air (4.3% and3.95%, respectively).
In a 1-year study at two sites in Riyadh, SaudiArabia, (Al-Suwaine et al., 1999), Cladosporiumwas dominant at about 40% of the total airbornefungi. Penicillium was second in frequency (23%and 14%) and Aspergillus about the same (18.7%and 17.2%). Alternaria and Ulocladium were bothroughly about 5%. Al-Suwaine made measure-ments by pumping air onto agar plates using twonutrients, one of which, Sabouraud’s was used inour work. Of the reports cited in Table 1, only thisone yields quantitative volume concentrationswhich enable comparisons to our data. They re-port mean monthly concentrations in the range ofabout 100–800 CFU m)3.
Thus, to the extent that comparisons are war-ranted, the airborne concentrations of cultivablefungi in Africa and the Middle East and therelative concentrations of the various genus/spe-cies appear to be quite different from those ob-served in Barbados trade winds. The dominance ofCladosporium is apparent in these studies regard-less of location whereas in Barbados trade winds itis a minor component.
It is notable that Aspergillus makes up only avery small fraction of the fungal spores.Aspergillus is widely distributed and is commonin soil and on decaying vegetation, dust, andother organic debris (Levetin 1995). Many speciesof Aspergillus are tolerant of temperatures at orabove 37 �C (Levetin 1995) which might lead usto expect relatively high abundances in our sam-ples. Nonetheless, in Barbados trade winds con-centrations were low, only 1.1%, spread across 5species (Table 1).
3.6. Comparison with airborne fungi over inlandBarbados
We made measurements at inland sites onBarbados to compare gross concentrations andgenera/species profiles with those obtained at ourcoastal site. Measurements were made concur-rently over a period of 2 weeks at the tower on theeast coast, where all the samples discussed thus farin this paper were taken, and at the University ofthe West Indies (UWI) Cave Hill campus, 22 km tothe west of the tower (Figure 1). A few sampleswere also taken at a site approximately 1 km inlandfrom the east coast and 5 km south of our towersite (Figure 1). Results are shown in Table 2. Theinland samples were only 15 min duration becauseof the high concentrations of spores and bacteria.Thus the inland concentrations measured on anyone day are not necessarily directly comparable tothose at the tower where samples are nominallycollected over an entire day. At the tower site themean concentrations of fungi and bacteria were0.36 and 0.13 CFU m)3, respectively. At UWI thevalues were 213 and 120 CFU m)3, 591 and 923times the tower values, respectively. Although onlytwo filter samples were taken at the site 1 km in-land, even here the concentrations are well over 100times higher than the tower values. Samples werealso collected with a Rotorod sampler, a whirling-arm impactor, and the spores counted by micro-scope (Frenz et al., 1995). The spore concentra-tions at the UWI site were in general about 100times greater than at the tower site (Table 2).
Our inland sampling results are consistent withthe expectation that MO concentrations over theocean are low and that MOs from local vegetationand soil sources will overwhelm advected MOseven at short distances inland (Lighthart 2000).The fungal species profile in the inland samples
was also quite different from the mean profilesobserved at the tower and from the 2-year towermeans (Table 1). The dominant fungi wereCladosporium (34%), Aspergillus (A. niger, 14%;A. flavus, 3%), Bipolaris (14%), Curvularia (13%),and Penicillium (8%). We caution that a directcomparison with the tower samples in this shortexperiment is not necessarily valid because of thelow colony counts in the tower samples. Also aclose comparison with the 2-year means is proba-bly not warranted because of the large seasonalvariability in fungal species concentrations thatone might expect over the island. Nonetheless theinland results are consistent with the generaliza-tions cited above – that Cladosporium is the mostabundant spore type on an annual basis in tem-perate and most tropical regions (Lacey 1991;Lighthart and Stetzenbach 1994) and thatCurvularia and Aspergillus are characteristic ofhumid tropical regions (Lacey 1991).
4. Discussion
4.1. Survival mechanisms
The MOs that we measure in aerosols at Barbadosare ubiquitous in soils and plants around the world(Lighthart and Stetzenbach, 1994; Muilenberg,1995). This raises the question: Why are MOsassociated with African dust viable after a week ormore in the atmosphere, while those from otherregions apparently are not? Also, why are thespecies/genera profiles in our samples so differentfrom those observed in the air over the continents?
There are many environmental factors that canstress and kill MOs (Cox, 1989; Marthi, 1994;Muilenberg, 1995); among the more important aredesiccation, heat, and UV radiation (Aylor, 1999).There are very few data on the survival of sporesexposed to sunlight and even fewer studies of theeffect of exposure to UV (Aylor, 1999). The fewdata that are available show a wide range ofexposure sensitivities (Aylor, 1999) and suggeststhat UV exposure during transport would have agreat impact on MO survival probabilities.Because the major dust source regions are arid(Prospero et al., 2002) we would expect thesespores to be relatively resistant to these variousstresses. Aerobic gram positive Bacillus speciesform highly resistant endospores. Many fungalspecies that we identify in Table 1 produce dark-
colored spores which would make them moreresistant to solar radiation (Tong and Lighthart,1998). Al-Subai (2002) in a study of airborne fungiin Qatar noted that the predominant species(Cladosporium, Alternaria, and Ulocladium) aredark-colored. Al-Subai also cites literature thatreports that dark-colored conidial fungi are pre-valent in sandy soils of the Sahara, Egypt and theSonoran deserts.Another factor might be that the thick clouds ofdust attenuate the UV flux which might otherwisekill the organisms (Liu et al., 1991; Mims et al.,1997). At Barbados during spring and summer,dust accounts for 60% of the light attenuation inthe mean and much more during dust events (Liet al., 1996). The monthly mean column aerosoloptical depth ranges between 0.2 and 0.3 at440 nm and is highly correlated (r ¼ 0.93) withmonthly mean dust concentrations measured atthe surface (Smirnov, 2000). Dust concentrationsand dust optical depths (and UV attenuation) aremuch higher over the eastern Atlantic and overWest Africa (Hsu et al., 1999) and thus wouldafford much more shielding against UV.
Another effective UV protective mechanismwould be the shielding of individual spores by dustparticles. The spores, many of which are a fewmicrometers diameter, might be covered with finesoil particles or they might be attached in a nichein large particles or clumps. On Barbados, undertypical dusty conditions, about 10% of the particlemass is in the size fraction greater than 10 lmaerodynamic diameter (Li-Jones and Prospero,1998); on some occasions several percent of themass exceeds 20 lm (Prospero et al., 1970;Li-Jones and Prospero, 1998). Thus during a typ-ical dust event, a cubic meter of air contains sev-eral hundred to a thousand particles above 10 lmand ten’s of particles above 20 lm. These couldeasily accommodate spore particles during transitto Barbados.
Although our study shows that cultivable MOsare only found in the presence of mineral dust, wecan not say whether the organisms were directlyassociated with individual dust particles or whe-ther they were independently suspended in the air.If the organisms were associated with individualdust particles, it would suggest that the organismsmay have been derived from soils directly when thedust was mobilized by winds. As previously stated,many of the fungi that we observe on Barbados are
14
found in soils. However there is very little infor-mation on the soils in the dust source regions inNorth Africa. Also, differences in sampling andculturing techniques make comparisons difficult.Nonetheless Dransfield (1966) in his study innorthern Nigeria cultured air samples and com-pared the results with cultured extracts from localsoils. The relative genera concentrations in airwere quite different from those in soils. Thedominant genera in soils were Penicillium andAspergillus, which each made up 33% of all colo-nies; in contrast these were minor in air in Nigeria(1.8% and 1.7%, respectively). In Qatar,Alternaria and Cladosporium, were the most com-mon genera in air (40.1% and 21%, of the total)whereas they accounted for only 4.06% and 2.8%of the total soil fungi (Al-Subai 2002).
Our work does not preclude the possibility thatthe MOs could have been derived from sourcescompletely different from the dust source regions.The MOs could have been advected over the dustsource region and subsequently became mixedwith deflating soil dust. Alternatively, MOs couldhave been injected into dusty air masses as theypassed over West Africa on their way to theAtlantic. These two scenarios would be consistentwith our observation that bacteria and fungi con-centrations are essentially uncorrelated with dustand with the fact that some major dust peaks arenot associated with any substantial increase in MOconcentrations (e.g., as shown in Figures 3, 4). Ifthe MOs are derived from non-soil sources, it ispossible the organisms could subsequently becomeattached to soil particles during transit, most likelywhen air parcels are processed through clouds.
It is clear, however, that even in relatively aridregions plants are major sources of airborne fungi.In the African and Middle-East work cited here, itis usually noted that periods of high spore con-centrations were linked primarily to the rain–veg-etation cycle.
Another possible explanation for the viabilityof MOs with African dust events is related to thetransport path of the MOs. Although the majortransport path for African dust is in the Saharanair layer that lies above the marine boundary layer,a substantial fraction of the transport can takeplace in the MBL where the relative humidity ishigh, typically above 70% (Reid et al., 2002),minimizing desiccation effects in MOs. In contrast,air trajectories that arrive in Barbados from the
North Atlantic (and North America and Europe)often sink from the middle troposphere wheretemperatures and relative humidity can be verylow and UV fluxes very high, factors that could killMOs or render spores nonviable.
4.2. Comparison with other studies of LRT
As previously stated, there have been very fewstudies of microbe LRT and none which wouldallow the association of MOs with a source region.Recently Griffin et al. (2001), in a study onSt. John in the Virgin Islands in July 2000 usingsampling and culturing techniques similar to ours,found high concentrations of viable MOs, includ-ing pathogens, which they associated with thepresence of African dust. Similar results are re-ported in a more recent paper, Griffin et al. (2003).They measured concentrations much higher thanthose obtained by us on Barbados. Their meanbacteria concentrations were 308 times greaterthan our July means and the fungi concentrations89 times greater. Moreover, they identify a widevariety of MOs that are very different from thosefound by us at our tower. Finally, we note thatGriffin et al. never made any physical measure-ments of dust concentrations; they simply inferredthe presence (or absence) of dust based on visibi-lity and on the TOMS aerosol product which, aswe noted above, is highly ambiguous over theWestern Atlantic except at very high dustconcentrations (Chiapello et al., 1999).
We note that their sampling site was located atLind Point on the extreme western end of the islandof St. John. Thus under typical summer trade windconditions, winds must traverse the 15-km lengthof the island as well as a number of small islandslying to the east. Our experiences in sampling atinland sites on Barbados suggest that their samplesare highly impacted by local sources. In fact theirresults at Lind Point are quite comparable to thoseobtained by us at our inland sampling site at UWI(Table 2) both from the standpoint of the concen-trations and the species/genera profiles.
4.3. Implications of the LRT of MOs, climatechange, and health
Although we only present a 2-year record here, wesee a great difference in the concentration ofbacteria and fungi in those 2 years. The large
15
variability may be taken as an indication of thesensitivity of MO production and transport toweather and climate. In this regard, we have notedlarge climate-related changes in dust concentrationin Barbados since we began measurements in 1965.Beginning in the late 1960s North Africa entered along dry phase with periods of intense drought(Nicholson 1996). In response, the annual meandust mass concentrations over Barbados hasincreased by as much as a factor of 4, comparingthe relatively arid decade of the 1980s with therelatively wet decade of the 1950s (Prospero andLamb, 2003). Over the past 40 years, peak dustyears were associated with strong El Nino events.The high dust and MO concentrations in 1997 maybe linked in some way to the extremely strong1997El Nino (McPhaden, 1999). We also note thatthere is a high correlation between dust loads inBarbados and the North Atlantic Oscillation(NAO) index (Ginoux et al., 2004). Thus futurechanges in climate associated with global warmingcould conceivably lead to large changes in theconcentration of dust and viable MOs over a largearea of the western Atlantic, Caribbean, and theeastern US.
Although we did not specifically look forpathogens, it is reasonable to assume that somespecies could have remained viable, protected bythe same mechanisms that protected the bacteriaand fungi that we observed. While LRT MO im-pacts have been inferred to occur (Brown andHovmøller, 2002) and while they remain to bedemonstrated, our results do suggest that windtransport is indeed possible for some organismsover great distances.
Fungi are known to be a major cause of allergicreactions, most commonly with asthma and hayfever, but also with pneumonitis (Cookinghamand Solomon, 1995). Although the concentrationof cultivable fungi is low in our samples, allergicreactions can be precipitated by dead fungalmaterial as well (Levetin, 1995). There is consid-erable dead material present in our aerosol sam-ples as evidenced by the frequent presence offragments of hyphae and damaged spores onRotorod samples taken at the coastal samplingtower.
We have not measured the size distribution ofthe MO-associated aerosols so we do not knowhow readily they might be inhaled. However pre-vious measurements have shown that about a third
to a half of the African dust mass falls into the sizerange below 2.5 lm diameter and about 90% isless than 10 lm diameter (Li-Jones and Prospero,1998; Prospero, 1999; Prospero et al., 2001). Par-ticles in the less-than 2.5 lm size range are definedas ‘‘respirable’’ by the US Environmental Protec-tion Agency (EPA) because of the relatively highefficiency with which these small particles pene-trate to the lung. The EPA standard for the 2.5 lm‘‘respirable’’ fraction (PM 2.5) specifies an annualmean of 15 lg m)3 and a 24-hour mean of65 lg m)3. Our measurements (Prospero, 1999;Prospero and Lamb, 2003) suggest that duringparticularly dusty years these limits are probablyexceeded over a wide area of the Caribbean be-cause of African dust transport. However we cannot say if the dust or the microbic materialsassociated with them constitute a health threat.
5. Conclusions
Our work shows that significant concentrations ofviable (colony-forming) bacteria and fungi areroutinely transported with African dust across theAtlantic during much of the year. In contrast nocultivable organisms are found in air from otherregions. This suggests that arid regions in generalmight be good sources of LRT organisms. Itremains to be seen whether dust from other aridregions also contains viable organisms that couldsurvive LRT. In our study we did not make anyfocused attempt to identify pathogenic speciesand, indeed, none were found. Nonetheless, it ispossible that dust could harbor pathogens whichwould be cause for concern. In the case of Africandust, it has been demonstrated that readilydetectable concentrations of African dust are car-ried to the southeastern US (Prospero, 1999;Prospero et al., 2001) and over a large area of theUS east of the Mississippi as far north as the NewEngland states. Asian dust is also of interest. Eachspring, large quantities of dust are carried acrossvast areas of the North Pacific (Prospero et al.,1989, 2003; Prospero, 1996). On some occasions,spectacular dust outbreaks can extend across thePacific to North America (Husar et al., 2001).
There is increasing interest in the role and im-pact of LRT in air quality. This interest has fo-cused on the inorganic particles and gases that arecommonly regarded as pollutants. Large fieldprograms with a focus on LRT are currently
16
underway and others are planned. It would appearto be logical and advantageous to link aerobio-logical studies to such programs. In this context,many global-scale chemical transport models arebeing developed in an effort to quantify large-scaletransports. Many of these contain dust modules(e.g., Collins et al., 2001; Ginoux et al., 2001;Mahowald and Luo, 2003). Although these modelsare still under development, they often yield goodresults in predicting the occurrence of dust stormsin source regions and the subsequent transportpaths. It may be possible to adapt these models toinclude biological materials so that they can beused for making quantitative assessments of therole of LRT in global microbial ecology. Theprocess of LRT is complex and modeling willrequire addressing the entire process: starting withspore production, spore release or removal fromsubstrates, spore escape from the canopy spaceand boundary layer, transport of the spore cloudby winds, dilution through advective mixing andby vertical mixing in convective cloud and othersystems, the loss of viability during transport, andfinally spore removal from the atmosphere byprecipitation (Aylor 1999). The consistency oftransport from Africa to Barbados and the ab-sence of significant impacts from other regionssuggest that it might be a good place to begin tosort out the importance of these various processes.
Acknowledgements
We thank J. Fell and K. Goodwin (RSMAS,University of Miami) for helpful discussions aboutmicrobial ecology, and M.G. Rinaldi (Universityof Texas Health Science Center, San Antonio)for assistance with culture identifications. We alsothank H. Maring, D. Savoie, L. Custals andT. Snowdon (RSMAS, University of Miami)and C. Shea (Barbados) for technical support; andE. Manning (Dyserth, North Wales, UK) andfamily for permitting us to continue to operate ourlaboratory on their property in Barbados. We alsothank an anonymous reviewer for helpful com-ments. The authors gratefully acknowledge theNOAA Air Resources Laboratory (ARL) forproviding HYSPLIT back-trajectories from theREADY website (http://www.arl.noaa.gov/ready.html). This research is funded in part by NSFgrants ATM-9414846, 9414812, 9414808 andNASA grant NAG51210.
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