May 2003 Vol 53 No 5 BioScience 469

Articles

Coral reefs throughout the world are in decline Increased incidence of coral disease decreases in reef-

building corals increases in macroalgae and lack of recoveryon damaged reefs have been widely reported The causes andprocesses driving the declines remain elusive In the past 25years mass mortalities of a major reef-building coral (90to 95 of Acropora palmata) and of a key herbivore (97 ofDiadema antillarum) have significantly altered coral reefs inthe Caribbean region Microbial pathogens are suspected inboth mortality events Twenty years later the abundance ofboth species remains low Eleven years after a cruise ship an-chor severely damaged a coral reef in the Virgin Islandsmacroalgae dominate the damaged area and stony coralabundance remains low

Although natural disturbances and human activities areknown to have caused much of the damage occurring on coralreefs they do not explain why increasing numbers of reefs arenot recovering from damage but are remaining in alternate

states that appear to be stable Nor do they adequately explainthe apparent increases in disease incidence and mortalityfrom disease or the widespread geographical distribution ofcoral diseases on reefs remote from as well as near to humaninfluence For example sea fan disease caused by a soil-associated fungus (Smith et al 1996) occurs throughout theCaribbean region including reefs off remote carbonate islandsdevoid of soil Many hypotheses have been proposed but theydo not adequately explain the declines observed on reefsworldwide (eg global warming pathogen introduction viaballast water or oceanic currents chronic low levels ofnutrients long-term intense fishing pressure and multiplelow-level stressors) Here we put forward a hypothesis that ad-dresses the widespread distribution of coral diseases and lackof recovery on coral reefs We will (a) present an overview ofthe atmospheric transport of African and Asian dust (b) re-view relevant background information and current researchon airborne microorganisms coral diseases and atmospheric

Virginia H Garrison (ginger_garrisonusgsgov) is a marine ecologist Eugene A Shinn and Charles W Holmes are geologists and Dale W Griffin and Christina AKellogg are microbiologists at the US Geological Survey (USGS) 600 Fourth Street South St Petersburg FL 33701 Garrison is a coral reef ecologist her research focuses on the effects of global-scale processes on coral reef ecosystems in the Caribbean and in the Pacific Ocean Shinn has published more than 100 scientific articlesconcerning geology limestone diagenesis and the geologic history and growth of coral reefs in Florida the Bahamas the Persian Gulf the Marshall Islands and PuertoRico Griffin studies transoceanic transport of microorganisms in the atmosphere Holmes specializes in the biogeochemical cycles of short-lived radionuclides and re-construction of the paleoenvironment from coral skeletons Kellogg works on characterizing the microbial communities in African dust and polluted sedimentsWilliam T Foreman is a research chemist at USGS National Water Quality Laboratory Box 25046 Denver CO 80225 he develops and applies methods to charac-terize the transport and fate of organic chemical contaminants in air water sediment and biota Michael S Majewski is a research chemist at USGS 6000 J StreetSacramento CA 95819 his research interests include the environmental behavior and fate of organic contaminants their long-range atmospheric transport and de-position and the effects of air pollution on water quality Laurie L Richardson is an associate professor in the Department of Biology Florida International Univer-sity Miami FL 33199 her area of expertise is microbial physiological ecology with a focus on the role of microorganisms in the etiology of coral diseases Kim B Ritchieis a scientist at MicroGenomics Inc 5935 Darwin Court Carlsbad CA 92008 her research interests include molecular biology marine microbial communities andmarine pathogens in the Atlantic and Pacific Oceans Garriet W Smith is an associate professor at the University of South CarolinandashAiken 471 University ParkwayAiken SC 29801 he is a microbial ecologist interested in the ecology of marine microorganisms particularly disease pathogens copy 2003 American Institute of Biolog-ical Sciences

African and Asian Dust FromDesert Soils to Coral Reefs

VIRGINIA H GARRISON EUGENE A SHINN WILLIAM T FOREMAN DALE W GRIFFINCHARLES W HOLMES CHRISTINA A KELLOGG MICHAEL S MAJEWSKI LAURIE L RICHARDSONKIM B RITCHIE AND GARRIET W SMITH

Many hypotheses have been proposed to explain the decline of coral reefs throughout the world but none adequately accounts for the lack of recov-ery of reefs or the wide geographical distribution of coral diseases The processes driving the decline remain elusive Hundreds of millions of tons ofdust transported annually from Africa and Asia to the Americas may be adversely affecting coral reefs and other downwind ecosystems Viable microorganisms macro- and micronutrients trace metals and an array of organic contaminants carried in the dust air masses and deposited inthe oceans and on land may play important roles in the complex changes occurring on coral reefs worldwide

Keywords aeromicrobiology African dust Asian dust contaminants coral reefs

transport of chemical contaminants and (c) suggest causalmechanisms and strategic avenues of investigation

The hypothesisWe propose that the hundreds of millions of tons of dust trans-ported annually from Africa and Asia to the Americas may bea significant factor in coral reef decline and may be adverselyaffecting other downstream ecosystems as well (Shinn et al2000) Why would these changes occur now after millenniaof African and Asian dust transport We suggest that the quan-tities of dust transported have increased and that the com-position of the dust has changed Synthetic organic chemicalsand anthropogenic pollutants viable microorganisms macro-and micronutrients and trace metals are likely to be carriedin the dust air masses and deposited in the oceans and on landSingly or in combination they may play important roles inthe complex changes occurring on coral reefs worldwide

Atmospheric transport of dustAs Charles Darwin traveled across the tropical North At-lantic dust from Africa reduced visibility and coated theHMS Beagle (Darwin 1846) More than 100 years laterDelaney and colleagues (1967) and Prospero (1968) werethe first to measure soil dust particles in the tropical NorthAtlantic atmosphere and to hypothesize that the trade windstransport dust from the Sahara to Barbados Confirmation ofthe hypothesis came from satellite imagery (figure 1) and frommeasurements of dust flux over Caribbean islands the Ba-hamas Miami (Florida) (eg Prospero 1968) and several na-tional parks in southeastern North America (Perry et al1997) Since the late 1960s geologists and atmospheric

chemists and physicists have studied the mineralogy ele-mental composition geologic processes transport depositionoptical properties atmospheric chemistry and particle size dis-tribution of globally transported dust and the linkages betweendust and global climate

Hundreds of millions of tons of dust derived from mineralsoil are transported annually from the African Sahara and Sahel to the Mediterranean and Europe and across the trop-ical Atlantic to the Americas (figure 2 Moulin et al 1997) Asimilar global system transports dust from the Gobi andTakla Makan deserts (western China) across Korea Japan andthe northern Pacific (Duce et al 1980 Husar et al 2001) tothe Hawaiian Islands (figure 2)The Asian air masses peri-odically reach western North America and infrequently con-tinue eastward to the Atlantic Ocean

The primary source of African dust is thought to shiftfrom the Bilma-Faya Largeau area of Lake Chad (October toApril) to the southern Sahel such as the Niger Delta in Mali(May to September McTainsh et al 1997) The annual vari-ation in exported dust mass correlates with the North AtlanticOscillation (NAO) which affects precipitation over NorthAfrica and atmospheric circulation in the Northern Hemi-sphere (Moulin et al 1997) and is coupled with the Arctic andPacific Oscillations of the Northern Hemisphere and with theEl Nintildeo Southern Oscillation (ENSO) Flux of dust is greaterduring positive phases of NAO The NAO Index and averageannual surface concentration of African dust at Barbadoshave gradually increased since the 1960s (Prospero and Nees1986) with both showing maxima during the strong ENSOof 1983ndash1984 (Moulin et al 1997) The mass of dust trans-ported may be an indicator of desertification of the Sahel (egProspero and Nees 1977 Swap et al 1996) and may be linkedwith both changing land-use practices and a drier climate (egTegen et al 1996) Climate is thought to be the major forc-ing factor in dust transport (Prospero and Nees 1986 Moulinet al 1997) Since the early 1970s the frequency of intense con-vective disturbances and associated rainfall in the Sahara hasdecreased while the number of weaker disturbances thatmobilize large quantities of dust has increased Rosenfeldand colleagues (2001) describe a feedback loop wherein highconcentrations of small dust particles suppress precipitationover the desert The combination of (a) more frequent weakdisturbances mobilizing large quantities of dust and (b) scantrainfall scavenging dust from the atmosphere results in greaterquantities of dust available for atmospheric transport

Extending thousands of kilometers (km) downwind andlasting up to 10 days per event (Perry et al 1997) maximumdust transport to the Americas centers in winter at approxi-mately 5deg N (GuyanaSouth America) and moves north to 20degN (northern Caribbean) in summer in association with theshift of the Intertropical Convergence Zone (Moulin et al1997) The concentration of atmospheric dust in the NigerDelta (Mali) can exceed 13000 micrograms (microg) per cubic me-ter (m3) with mean background concentrations of 575 microg perm3 (Gillies and Nickling 1996) Aerosol concentrations during heavy dust events range from 200 to 600 microg per m3 over

470 BioScience May 2003 Vol 53 No 5

Articles

Figure 1 National Aeronautics and Space Administration(NASA) satellite image of dust cloud from Africa crossingthe Atlantic Ocean Photograph SeaWiFS (Sea-viewingWide Field-of-view Sensor) Project NASAGoddard SpaceFlight Center and ORBIMAGE (Enhanced true color)

the mid-Atlantic and Barbados (Prospero et al 1981 Talbotet al 1986) and exceed 100 microg per m3 in the Virgin Islands (fig-ure 3) with mean concentrations of 3 to 20 microg per m3 in theCaribbean (Prospero and Nees 1986 Perry et al 1997) Meanmass diameters of African dust particles transported de-crease with increasing distance from Africa and average lessthan 1 micrometer (microm) in the Virgin Islands (Perry et al1997) The finest particles are carried into the Gulf of Mex-ico and over the continental United States as far west as theRocky Mountains and as far north as Maine (Perry et al1997)

Composition of dust The chemical composition of aerosols is a product of the ori-gin and history of the dust (eg Duce et al 1976 Arimoto etal 1995 Perry et al 1997) African and Asian dust consists pri-marily of clay soil minerals such as illite quartz kaolinitechlo-rite microcline plagioclase and calcite (Prospero 1981)which may undergo chemical change during aerosol trans-port (Ravishankara 1997) Some elements (eg manganeseiron scandium cobalt) occur on African dust particles in con-centrations similar to average crustal abundance whereasother elements (eg mercury selenium lead) accumulate viascavenging at concentrations three orders of magnitudegreater than mean crustal abundance (Duce et al 1976) Inthe late 1990s the AtmospherendashOcean Chemistry Experi-ment investigated the chemical composition of Atlanticaerosols (Arimoto et al 1995) Trace metal analysis showedlarge-scale differences in pollution emissions from North

America Europe and Africa Emissions from industry andpossibly biomass burning were more evident in the aerosolsfrom Europe and Africa The relative abundance of chemicalelements particularly the metals has been used to distinguishsoil derived from volcanic dust (Muhs et al 1990) To definethe source various elemental ratios such as calcium to alu-minum (CaAl) and aluminum to silicon have been sug-gested Perry and colleagues (1997) using a particle diameterof less than 25 microm and a CaAl ratio greater than 38 to in-dicate Saharan dust identified African dust in the atmosphereof the Caribbean and of the eastern and central United StatesUsing the metal ratios in volcanic material from the Antillesand soils from Africa Muhs and colleagues (1990) identifiedSaharan dust as the source of clay soils on carbonate platformsin the western Atlantic (Barbados Jamaica Bermuda and theFlorida Keys) Age dating of the soils suggests the transportof African dust to the region has been occurring for mil-lions of years The ratios of beryllium to lead (7Be210Pb) inaerosols can be used to differentiate continental from oceanicsources and these ratios show promise in elucidating aerosoltransport history (eg Arimoto et al 1999)

Dust chronologies in coral skeletons Corals incorporate particles (Barnard et al 1974) and chem-ical components from the surrounding water into their skele-tons during growth preserving a record of the environmen-tal conditions under which the calcium carbonate skeletonformed For example mineral dust and dust from the 1883eruption of Krakatoa (Indonesia) have been isolated and

May 2003 Vol 53 No 5 BioScience 471

Articles

Figure 2 Dust is transported in two major global dust transport systems (1) from the Sahara and Sa-hel of Africa to the Americas Europe and Near East and (2) from the Takla Makan and Gobi desertsof China across China Korea Japan and the northern Pacific to North America sometimes exitingover the Atlantic Ocean Illustration Betsy Boynton

identified from annual bands of the reef-building coral Mon-tastraea annularis from the Florida reef tract (Merman 2001)The study conclusively demonstrated that dust can be in-corporated in the coral skeletonAnthropogenic air pollutantssuch as lead and cadmium (Shen and Boyle 1987) and cesiumradioisotope 137Cs from nuclear testing have been detected incoral skeletons Current studies indicate that a record of pastenvironmental conditions including dust deposition may bereconstructed using laser ablation inductively coupled plasmamass spectrometry (LA-ICP-MS) to extract the record pre-served in coral skeleton annual bands (Sinclair et al 1998)

Nutrient influx and biogeochemical effectsOur understanding of the impact of dust on biogeochemicalcycles is limited Aeolian dust contributes significant quan-tities of water-soluble nutrients to the oligotrophic Caribbean(Jickells 1999) the Gulf of Mexico (eg Talbot et al 1986)and the Pacific (eg Young et al 1991 Behrenfeld and Kol-ber 1999) and provides essential nutrients to the rain forestsof Hawaii (Chadwick et al 1999) and the Amazon (Swap etal 1992) The atmosphere deposits an estimated 50 of thephosphorus transported to the oceans (Duce et al 1991)The influx of nutrients from Asian dust events is reported tofuel phytoplankton productivity in the northern Pacific (egYoung et al 1991)

Atmospheric deposition is thought to be the dominantsource of iron in the oceanrsquos photic zone (Duce and Tindale

1991) Iron a micronutrient can limit phy-toplankton productivity in oligotrophic wa-ters newly deposited iron is quickly depletedby phytoplankton (eg Martin and Fitz-water 1988 Coale et al 1996 Behrenfeld andKolber 1999) and bacteria (Butler 1998)Turner and colleagues (1996) showed thatiron flux to the oceans leads to the bioticproduction of dimethylsulfide (DMS) and itsrelease into the atmosphere Subsequent ox-idation of DMS and formation of sulfate inturn produces sulfuric acid which with at-mospheric mixing could increase the solu-bility of iron (in the form Fe [III]) in themineral aerosols (eg Duce and Tindale1991) Walsh and Steidinger (2001) and Lenesand colleagues (2001) linked African dustto the development of extensive red tides inthe Gulf of Mexico Lenes and colleagues(2001) also showed that iron in African dust deposited by rain fuels blooms ofTrichodesmium an iron-limited cyano-bacterium The nitrogen-fixing Trichodes-mium produces nutrients (eg nitrates ni-trites) that in combination with selectivepredation by zooplankton and meteorolog-ical conditions fuel blooms of the red tidedinoflagellate Karenia brevis Recently Bishopand colleagues (2002) documented an in-

crease in carbon biomass in the North Pacific in response toiron influx from a strong Asian dust event

Some scientists question the importance of atmosphericdust as a source of iron in the oceanrsquos photic zonearguing thatthe most stable and abundant form of iron (Fe [III]) in dustis relatively insoluble in seawater and not readily available bi-ologically However little is known of the chemistry occur-ring on dust particles of small volume and high surface areaduring atmospheric transport and biogeochemical ocean-ographers are just beginning to understand the oceanrsquos complex biogeochemical pathways Dust from Africa andAsia is transported long distances in chemically and physicallyextreme environments where the small particles are exposedto high levels of solar radiation multiple freezendashthaw cyclesrelatively acidic conditions and predominantly inorganicsalts (Jickells 1999) On its deposition to the ocean the dustenters a radically different environment The thin surfacelayer of the ocean is characterized by concentrations of phy-toplankton and zooplankton and by a steep concentration gradient of organic compounds and inorganic salts It has beensuggested that during atmospheric transport photoreductionof Fe (III) which is stable and relatively insoluble producesFe (II) a biologically available and soluble species (egGraedel et al 1986 Duce and Tindale 1991) Saydam andSenyuva (2002) propose that oxalate released by fungi indesert dust facilitates photoreduction of Fe (III) Complex-ation of Fe (II and III) with organic ligands (Butler 1998) or

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Figure 3 African dust event (bottom) and nondust (top) atmospheric conditions in the Virgin Islands Distance to islands in background is 2 to 5kilometers Photographs Courtesy of Christina Kellogg

with clay minerals in the aerosol acts to stabilize the iron ina bioavailable form On their deposition to the ocean surfacelayer insoluble Fe (III) and some of the more soluble first-rowtransition metals form stable complexes with siderophoreslow-molecular-weight organic ligands produced by somespecies of oceanic bacteria facilitating uptake by micro-organisms and phytoplankton (Butler 1998 and referencestherein) Young and colleagues (1991) suggested that thesmaller the dust particle the longer the residence time in thephotic zone and therefore the greater the amount of iron thatcould be released and made available for phytoplankton andmicrobes In a more direct mechanism Fe (III) deposited inreducing environments (eg carbonate muds in Florida Bay)can be reduced to Fe (II) Iron limitation is known to keepmany microbial pathogens at low concentrations that di-rectly counteract the expression of pathogenicity (Weinberg1996) Hayes and colleagues (2001) proposed that iron in dustmay play a similar role in promoting microbial diseases oncoral reefs

Biomagnification and bioaccumulation processes add an-other layer of complexity in marine systems Small dust par-ticles (05 to 50 microm) deposited in the ocean surface layer areselectively ingested by zooplankton (eg Syvitski and Lewis1980) incorporated into fecal pellets and excreted in a moreconcentrated form into the water column Zooplankton fe-cal pellets singly or aggregated could efficiently carry the bio-concentrated micronutrients and chemical contaminants tobenthic organisms larger zooplankton or planktivores (Syvit-ski and Lewis 1980) Doses of synthetic organic chemicals andmicro- or macronutrients could affect reproduction or im-mune function of benthic organisms and contribute to main-taining the shift to seemingly alternative stable states (egmacroalgae dominated) observed on disturbed reefs world-wide Threshold effects may be involved Exploration of theroles of atmospheric transport of dust in the biogeochemi-cal cycles of marine and terrestrial ecosystems is in the ear-liest stages

Living components of globally transported dustDust air masses transport more than mineral particles and nu-trients Sediment core studies conducted in the AtlanticOcean off the West African coast reported the presence offreshwater diatoms and phytoliths in sediment cores and at-tributed their presence to African dust deposition (egMaynard 1976) African desert locusts (Schistocerca gregariaup to 8 centimeters [cm] long) have been carried in Saharandust air masses across the tropical Atlantic and arrived aliveon eastern Caribbean islands (Ritchie and Pedgley 1989)If organisms as large as desert locusts have survived the multi-day trip it is likely that viable smaller organisms may be riding with the dust as well

Airborne transport of pathogens Many well-known patho-genic bacteria fungi and viruses are transmitted throughairborne transport (eg the organisms causing plague an-thrax tuberculosis influenza and aspergillosis) Most of the

systemic fungal diseases and viruses such as hantavirus aretypically transmitted in dust The World Health Organizationhas identified drought and dust storm activity in the sub-Saharan region of Africa as causing regional outbreaks ofmeningococcal meningitisNeisseria meningitidis the infectiousagent causes approximately 500000 cases and 50000 deathsevery year (see wwwwhointvaccinesenmeningococcusshtml) Other disease outbreaks are associated with expo-sure to desert dust clouds in the Americas One example is coccidioidomycosis in humans caused by the fungus Coccidioides immitis

It is generally believed that most airborne pathogens areonly transmitted over short distances Although the trans-mission of coccidioidomycosis or meningococcal meningitishas been documented through desert dust cloud exposure ithas only been shown to occur within the confines of a con-tinent Can desert dust clouds move viable pathogens aroundthe planet and is there a limit to the type of airborne pathogenthat can be transported in this way

There are a surprising number of reports of long-rangetransport of plant pathogens Most of these infectious invadersare fungi whose dispersal spores provide protection from ultraviolet (UV) light and other harsh environmental con-ditions Culturing of air samples and species-specific detec-tion are relatively new developments so in most studies thefungal diseases were tracked based on the geography of theoutbreaks prevailing winds and timing Examples include thepotato blight fungus (Phytophthora infestans) potato black-leg bacteria (Erwinia carotovora and E chrysanthemi) lentilanthracnose (Colletotrichum truncatum) fungal wheatpathogen (Puccinia graminis) sugarcane rust (Pucciniamelanocephala) coffee rust (Hemileia vastatrix) and bananaleaf spot (Mycospherella musicola Brown and Hovmoslashller2002)

Less information is available concerning the aerosol trans-mission of animal pathogens Several studies of dust col-lected from surfaces on poultry swine and dairy farms haveshown that the dust contained fungi such as Aspergillus andCladosporium (Fiser et al 1994) as well as the bacterium Salmonella (eg Letellier et al 1999) Windblown desert dustthat carried fungi caused an outbreak of aspergillosis indesert locusts (Venkatesh et al 1975) Meteorological data andmolecular techniques were employed to determine the sourceof the pseudorabies virus (cause of Aujeszkyrsquos disease inswine) after outbreaks occurred in Denmark in December1988 The evidence suggested the infections were a result ofairborne transport of the viral pathogen from Germany(Christensen et al 1993)

Microbes and African dust We are investigating the possi-bility that viable microbes are being transported across oceansin dust events Research to date has shown that the numberof bacteria and fungi that can be cultured from air samplesfrom the Virgin Islands is two- to threefold greater whenAfrican dust is in the atmosphere than when it is not (Grif-fin et al 2001) Comparisons of data from these cultures

May 2003 Vol 53 No 5 BioScience 473

Articles

with clay minerals in the aerosol acts to stabilize the iron ina bioavailable form On their deposition to the ocean surfacelayer insoluble Fe (III) and some of the more soluble first-rowtransition metals form stable complexes with siderophoreslow-molecular-weight organic ligands produced by somespecies of oceanic bacteria facilitating uptake by micro-organisms and phytoplankton (Butler 1998 and referencestherein) Young and colleagues (1991) suggested that thesmaller the dust particle the longer the residence time in thephotic zone and therefore the greater the amount of iron thatcould be released and made available for phytoplankton andmicrobes In a more direct mechanism Fe (III) deposited inreducing environments (eg carbonate muds in Florida Bay)can be reduced to Fe (II) Iron limitation is known to keepmany microbial pathogens at low concentrations that di-rectly counteract the expression of pathogenicity (Weinberg1996) Hayes and colleagues (2001) proposed that iron in dustmay play a similar role in promoting microbial diseases oncoral reefs

Biomagnification and bioaccumulation processes add an-other layer of complexity in marine systems Small dust par-ticles (05 to 50 microm) deposited in the ocean surface layer areselectively ingested by zooplankton (eg Syvitski and Lewis1980) incorporated into fecal pellets and excreted in a moreconcentrated form into the water column Zooplankton fe-cal pellets singly or aggregated could efficiently carry the bio-concentrated micronutrients and chemical contaminants tobenthic organisms larger zooplankton or planktivores (Syvit-ski and Lewis 1980) Doses of synthetic organic chemicals andmicro- or macronutrients could affect reproduction or im-mune function of benthic organisms and contribute to main-taining the shift to seemingly alternative stable states (egmacroalgae dominated) observed on disturbed reefs world-wide Threshold effects may be involved Exploration of theroles of atmospheric transport of dust in the biogeochemi-cal cycles of marine and terrestrial ecosystems is in the ear-liest stages

Living components of globally transported dustDust air masses transport more than mineral particles and nu-trients Sediment core studies conducted in the AtlanticOcean off the West African coast reported the presence offreshwater diatoms and phytoliths in sediment cores and at-tributed their presence to African dust deposition (egMaynard 1976) African desert locusts (Schistocerca gregariaup to 8 centimeters [cm] long) have been carried in Saharandust air masses across the tropical Atlantic and arrived aliveon eastern Caribbean islands (Ritchie and Pedgley 1989)If organisms as large as desert locusts have survived the multi-day trip it is likely that viable smaller organisms may be riding with the dust as well

Airborne transport of pathogens Many well-known patho-genic bacteria fungi and viruses are transmitted throughairborne transport (eg the organisms causing plague an-thrax tuberculosis influenza and aspergillosis) Most of the

systemic fungal diseases and viruses such as hantavirus aretypically transmitted in dust The World Health Organizationhas identified drought and dust storm activity in the sub-Saharan region of Africa as causing regional outbreaks ofmeningococcal meningitisNeisseria meningitidis the infectiousagent causes approximately 500000 cases and 50000 deathsevery year (see wwwwhointvaccinesenmeningococcusshtml) Other disease outbreaks are associated with expo-sure to desert dust clouds in the Americas One example is coccidioidomycosis in humans caused by the fungus Coccidioides immitis

It is generally believed that most airborne pathogens areonly transmitted over short distances Although the trans-mission of coccidioidomycosis or meningococcal meningitishas been documented through desert dust cloud exposure ithas only been shown to occur within the confines of a con-tinent Can desert dust clouds move viable pathogens aroundthe planet and is there a limit to the type of airborne pathogenthat can be transported in this way

There are a surprising number of reports of long-rangetransport of plant pathogens Most of these infectious invadersare fungi whose dispersal spores provide protection from ultraviolet (UV) light and other harsh environmental con-ditions Culturing of air samples and species-specific detec-tion are relatively new developments so in most studies thefungal diseases were tracked based on the geography of theoutbreaks prevailing winds and timing Examples include thepotato blight fungus (Phytophthora infestans) potato black-leg bacteria (Erwinia carotovora and E chrysanthemi) lentilanthracnose (Colletotrichum truncatum) fungal wheatpathogen (Puccinia graminis) sugarcane rust (Pucciniamelanocephala) coffee rust (Hemileia vastatrix) and bananaleaf spot (Mycospherella musicola Brown and Hovmoslashller2002)

Less information is available concerning the aerosol trans-mission of animal pathogens Several studies of dust col-lected from surfaces on poultry swine and dairy farms haveshown that the dust contained fungi such as Aspergillus andCladosporium (Fiser et al 1994) as well as the bacterium Salmonella (eg Letellier et al 1999) Windblown desert dustthat carried fungi caused an outbreak of aspergillosis indesert locusts (Venkatesh et al 1975) Meteorological data andmolecular techniques were employed to determine the sourceof the pseudorabies virus (cause of Aujeszkyrsquos disease inswine) after outbreaks occurred in Denmark in December1988 The evidence suggested the infections were a result ofairborne transport of the viral pathogen from Germany(Christensen et al 1993)

Microbes and African dust We are investigating the possi-bility that viable microbes are being transported across oceansin dust events Research to date has shown that the numberof bacteria and fungi that can be cultured from air samplesfrom the Virgin Islands is two- to threefold greater whenAfrican dust is in the atmosphere than when it is not (Grif-fin et al 2001) Comparisons of data from these cultures

May 2003 Vol 53 No 5 BioScience 473

Articles

with data from direct counts of aerial microbes indicate thatless than 1 of the total microbial population present was re-covered on the nutrient agar used for analysis This findingis in agreement with other microbial ecology studies thathave shown a culturable rate of 1 or less obtained from nat-ural samples (Torsvik et al 1990 Eilers et al 2000) It is im-portant to note that microbes that do not grow on one nu-trient agar may grow on a different nutrient agar or source(eg lung tissue) In short the bacteria and fungi that we havecultured from atmospheric samples most likely representonly a small percentage of what is actually viable and capa-ble of growth Furthermore microbial ecology studies haveshown that in environmental samples the total viral popula-tion present is usually 10 to 100 times the total bacterial pop-ulation (Borsheim et al 1990) Nonculturable microbes canbe identified using whole genomic DNA extraction followedby polymerase chain reaction (PCR) amplification cloningand sequencing of ribosomal RNA genes This type of analy-sis is invaluable for total microbial population comparisonsof dust and marine microbes and provides genetic access tothe large number of microbes (gt 99) that cannot be cul-tured

The fungus known to cause sea fan disease in the tropicalwestern Atlantic (Aspergillus sydowii Smith et al 1996) wasisolated in its active pathogenic form from air samples takenduring dust events in the Virgin Islands in 1997 (Weir et al2000) Since that time the pathogenic strain of A sydowii hasbeen found only in diseased sea fans and sea plumes and inair samples collected during dust events in the Virgin Is-lands The pathogenicity of A sydowii isolates from air sam-ples collected in Mali is currently being tested Recently Grif-fin and colleagues (2001) isolated numerous species of viablemicroorganismsmdashbacteria and fungimdashfrom air samplestaken in the Virgin Islands during dust events Using riboso-mal sequencing via PCR to identify the isolates they foundthat at least 25 of those identified are known plant pathogensand 10 are opportunistic human pathogens (Griffin et al2001) The fungal isolate Cladosporium cladosporioides whichhas been identified as a plant and human pathogen is one ofthe most common species of fungi recovered from air sam-ples Several of the bacteria isolated have previously beenidentified in marine environments (Pseudomonas alcalophilaParacoccus spp and Kocuria erythromyxa) Microorganismscan move from the marine environment to the atmospherevia physical surface activity that results in the formation of seaspray and sea foam (eg Blanchard and Syzdek 1970) It ispossible that dust clouds traversing marine environmentsserve as a vehicle for long-range transport of aerosolized marine microorganisms Further sampling midocean and inthe Virgin Islands and Mali is necessary before we can conclusively demonstrate what viable microorganisms aretransported from Africa and in what concentrations (seesidebar)

In a current study of a recent disease outbreak in Caribbeansea urchins (Meoma ventricosa) two of the authors (K B Rand G W S) found that bacteria associated with the spines

of burrowing and nonburrowing sea urchins and present inthe water column are genetically identical to bacteria purifiedfrom air samples collected in the Virgin Islands during dustevents One isolate was a novel bacterium that showed 98identity to Bacillus mojavensis which was initially isolated fromthe Mojave Desert (Southern California) and associated witharid soils The sea urchinndashassociated bacterium proved to begenetically and morphologically identical to a bacterium isolated from a Virgin Islands dust event sample Moreoveranother bacterium isolated from a Sargassum species in SanSalvador (Bahamas) was found to be genetically and mor-phologically identical to isolates from both sea urchins andVirgin Islands air samples during dust events Thus it appearsthat some bacteria found in desert soils also occur in a viablestate in the atmosphere over the Virgin Islands during Africandust events and in the marine environment in the Western AtlanticWhether these bacteria are actually transported long

474 BioScience May 2003 Vol 53 No 5

Articles

To distinguish between contaminants transported longdistances and those generated locally background sam-ples are collected to control for sources other thanAfrican or Asian dust Ambient or background samplesare used to identify and quantify the microorganismsand chemical contaminants in the atmosphere whendust air masses are not present Sources of backgroundcontaminants include local winds advecting soil shiptraffic across oceans upwind of the affected areas com-plex interactions between air layers in the atmosphereand pollutants in the troposphere In addition it isessential to sample the source region midocean anddownwind sites during dust events and nondust (back-ground) conditions to conclusively demonstrate long-distance transport of contaminants

A microorganism or chemical contaminant is consid-ered to have been transported long distances in a dustevent to downstream sites when criteria 1 (a or b) 2and 3 are met

1 The microorganism or chemical (a) is identified onlyin dust event samples and not found in backgroundsamples or (b) occurs in significantly higher concentra-tions in dust event samples than in background sam-ples

2 The microorganism or chemical occurs in higherconcentrations in the source region than in the down-stream and midocean dust event samples

3 The microorganism or chemical occurs in sourceregion midocean and downstream site dust eventsamples

Local contamination or long-distance transport

distances in dust events or can reproduce in the marine environment is unknown

Analysis of other marine and dust isolates reveals thatother bacterial types remain viable in the atmosphere and marine environments as well Bacteria isolated from Mventricosa from the sea urchin Echinometra variegates fromthe water column and from a Virgin Islands dust event airsample were 100 identical to Bacillus pumilus Similarly bac-teria isolated from the long-spined sea urchin Diademaantillarum and from the nonburrowing urchin Lytochinusvariegates are identical to a bacterium isolated from anAfrican dust event air sample from the Virgin Islands with99 identity to Pseudomonas aeruginosa a ubiquitous species

It had been thought that exposure to UV light duringlong-range transport would inactivate any microbes Dust inthe upper altitudes of dust clouds attenuates UV light andcould act as a UV screen for microbes at lower altitudes(Herman et al 1999) Also microorganisms may attach toand survive within cracks and crevices of inorganic dustparticles which would shield them from UV light Prelim-inary findings indicate that UV resistance in microorganismsmay play an important role in their survival during atmos-pheric transport

Coral diseases and microbial pathogens of coralsCoral diseases were first reported in the 1970s (eg Antonius1973) on reefs in the Caribbean and in the Florida KeysSince that time they have been observed on reefs worldwide(Richardson and Aronson 2002) Presumably diseases havealways occurred on coral reefs but they remained unde-tected until the 1970s because of the low incidence of diseaseon reefs and the state of knowledge at the time The currentlevels of coral mortality are unprecedented It is now ac-cepted that coral diseases are an active and important factorin the continued degradation of coral reefs Although up to29 coral diseases are currently being monitored in various pro-grams worldwide the pathogens of only five diseases (blackband aspergillosis bacterial bleaching white plague andwhite pox) have been identified Four of these have beenproved to be pathogens following the procedures of fulfill-ment of Kochrsquos postulates aspergillosis (Smith et al 1996)white plague type II (Richardson et al 1998) bacterial bleach-ing (Kushmaro et al 2001) and white pox (Patterson et al2002) The fifth disease black band is caused by a pathogenicbacterial consortium not a single pathogen Reservoirs areknown for only two coral diseases black band disease and as-pergillosis (Richardson 1998 Weir et al 2000)

Of the 10 coral diseases or disease-like states being mon-itored throughout the Caribbean and the Florida Keys(Richardson 1998) four are of particular interest in terms ofdefining a connection with African dust events aspergillosisblack band disease white pox and white plague

Aspergillosis One of the few coral diseases to be character-ized fully aspergillosis is also one of the most common Thisdisease primarily affects two types of sea fans Gorgonia

ventalina (figure 4 left) and G flabellum As discussed aboveit is caused by the common terrestrial fungus A sydowii(Geiser et al 1998) which has a worldwide distribution in soilsSpores are generally less than 2 microm in diameter a size easilycarried by winds and dispersed over great distances

To date pathogenic and nonpathogenic fungi from severaldifferent genera (Aspergillus Penicillium and Blastomyces) havebeen isolated and identified from samples collected duringAfrican dust events in the Virgin Islands Inoculations con-firmed that some dust event isolates were pathogenic tohealthy G ventalina because inoculations produced charac-teristic signs of aspergillosis such as purpling and loss oftissue In each case where disease was observed the originalpathogen was reisolated and morphologically identified ful-filling Kochrsquos postulates During the reisolations several typesof fungi in addition to A sydowii were isolated from exper-imentally inoculated sea fans indicating that (a) pathogenicfungi can be reisolated from inoculated and diseased seafans and (b) nonpathogenic opportunistic marine fungimay secondarily colonize diseased sea fans The absence ofAspergillus species in control samples (not inoculated) revealedthat Aspergillus is not typically found on healthy sea fans Thepresence of at least one nonpathogenic fungus in such con-trols indicated that it is possible for some marine fungi to col-onize sea fans without causing signs of disease

The data collected from these experiments suggest thatAfrican dust storms may be a source of Caribbean sea fanpathogens In the last year aspergillosis occurred on at leasttwo other species of soft corals Pseudopterogorgia americanain Bermuda and P acerosa in St Croix (Virgin Islands) Bothof these species displayed similar signs of disease which in-cluded gall formation and loss of tissue along the axial skele-ton Aspergillus species were morphologically identified fromdiseased specimens only This may indicate an extended hostrange of pathogenic strains of Aspergillus Interestingly whenhyphae of pure A sydowii strains are extracted and separatedusing high-performance liquid chromatography uniquecompounds are found associated with the pathogenic strainsbut not with the nonpathogenic strains We do not know theidentities of these compounds but we suspect that somemay play a role in the disease process

Black band disease Black band disease was the first coral dis-ease reported (Antonius 1973) and is one of the most wellcharacterized A cyanobacterium sulfide-oxidizing and sulfate-reducing bacteria and many heterotrophic bacteria together form a complex pathogenic microbial consortiumthat closely resembles microbial mats such as those found inilluminated sulfide-rich aquatic environments (Richardson1998) Black band disease can affect both soft corals (such assea fans) and stony corals but it appears to be a greater threatto the reef-building corals in particular Montastraea annu-laris and Colpophyllia natans Compared with other coraldiseases the disease is slow in terms of both degradation ofcoral tissue (normally 3 to 4 millimeters per day) and the timeit takes to kill a coral colony (months to years) (Ruumltzler and

May 2003 Vol 53 No 5 BioScience 475

Articles

Santavy 1983) The incidence is generally low less than 1 ofcoral colonies on reefs in the Virgin Islands (Edmunds 1991)and in the Florida Keys but up to 6 on reefs in Jamaica (re-viewed in Richardson and Aronson 2002) The low incidenceof black band disease and the low rate of black-band-inducedcoral mortality have led investigators to suggest that the slowdeath of corals caused by this disease may be balanced by thebeneficial effect of opening up reef substrate for recruitmentof stony corals thereby potentially increasing genetic diversity(Edmunds 1991) However such recruitment has not beenfound in two studies that documented recruitment of corals(both stony and soft) onto black-band-exposed substrate inthe Virgin Islands (Edmunds 1991 2000) and the northernFlorida Keys (Richardson and Aronson 2002)

The potential connection of black band disease with Africandust may relate not only to potential pathogen transport butalso to the iron present within dust Iron may act as a triggerthat activates black band disease reservoirs to become path-ogenicRichardson (1997) found that the reservoir of the blackband microbial consortium resides in biofilms on sedimentpatches in depressions on healthy coral colonies of species sus-ceptible to the disease These biofilms are present as thin lay-ers of filaments of the black band cyanobacterium When sam-ples are viewed under a microscope the presence of thesulfide-oxidizing black band member Beggiatoa is seenBecause this genus only lives in environments with sulfideoxygen interfaces the presence of sulfate reducers (the thirdmajor component of the black band consortium) is inferred

It has been proposed that the black band reservoir biofilmsare transformed into the pathogenic microbial mat commu-nity by an accumulation of biomass As biofilm communitymembers increase in biomass oxygen demand increaseswhich leads to increased areas of anoxia within the microbialcommunity As anoxic microzones develop the sulfate-reducing population can increase and a zone of permanentanoxia can develop When this occurs sulfide concentra-tions may build up within the anoxic microzone to the toxiclevel that kills coral tissue (Richardson 1998) The triggerthat may induce the buildup in biomass may very well be ironknown to be a limiting micronutrient in tropical and sub-tropical marine waters

White plague To date three forms of white plague havebeen reported on reefs of the northern Florida Keys whiteplague type I white plague type II (figure 4 right) a more vir-ulent form that emerged on the same reefs in 1995 and whiteplague type III first seen in 1999 (Richardson and Aronson2002) These three forms exhibited identical disease signsbut had very different short-term effects on the reef Whiteplague type I affected six species of stony corals and was de-scribed as having minimal impact on the reefs White plaguetype II was much more destructive affecting 17 species of stonycorals along 400 km of Floridarsquos reef tract and causing thedeath of entire colonies in as little as 2 to 3 days (Richardsonet al 1998) White plague type III appeared on the same reefsin 1999 (Richardson and Aronson 2002) but caused the most

476 BioScience May 2003 Vol 53 No 5

Articles

Figure 4 On left diseased sea fan (Gorgonia ventalina approximately 60 centimeters high)showing characteristic lesions of aspergillosis (Aspergillus sydowii) On right close-up of stonycoral (Montastraea annularis) with white plague type II White areas are bare coral skeletonwhere tissue has been recently killed by disease Photographs Sea fan courtesy of Garriet Smithstony coral courtesy of US Geological Survey

rapid tissue destruction of the three white plagues primar-ily affecting the largest colonies of M annularis and C natansEntire colonies (2 to 3 meters in diameter) were observed tohave been killed within days

The pathogen of white plague type II was isolated andidentified as a new genus of gram-negative bacteria Auran-timonas coralicida (Denner et al 2002) The white plaguepathogen may well be one of the dust-associated bacteria anddust may serve as an inoculum that triggers white plague out-breaks White plague types II and III have spread throughoutthe Caribbean in the last 2 years even to ldquopristinerdquo reefs thatare far from human populations Although this has been amystery in the past the dust hypothesis may explain regionwide disease distribution patterns

White pox White pox a coral disease that forms circular lesions on colonies of elkhorn coral (Acropora palmata) wasrecently shown to be caused by the gram-negative enter-obacterium Serratia marcescens (Patterson et al 2002) Thismicroorganism is ubiquitously distributed and could be introduced onto coral reefs via a number of pathwaysincluding soil runoff river discharge arthropod or mammalfeces and atmospheric transport of soil

Microorganisms and marine ecology Microbiota play a sig-nificant role in marine ecology Marine microorganisms havebeen shown to be significant with respect to the survivabil-ity and competitiveness of key coral reef species drasticallyaltering the composition and possibly the viability of somereefs The composition and function of the microbial com-munities associated with healthy marine organisms are justbeginning to be explored The first priority is to identify thepathogens or agents causing the 20 to 30 disease-like states being followed on reefs today some of which may not be diseases (Richardson 1998) Once pathogens have been iden-tified the sources and mechanisms of transmission and distribution need to be addressed It is equally important to identify the environmental conditions needed to activatea disease to induce a microorganism to become pathogenicor to initiate a chain of events that will lead to an outbreakof disease

Many questions remain to be answered including thesource of identified coral disease pathogens African dustmay be one mechanism through which pathogens of coral reeforganisms are distributed and deposited in the Atlantic andPacific It is still unclear whether pathogens responsible forcoral disease outbreaks are newly introduced microorganismsmore virulent forms of normally present pathogens or nor-mal bacterial populations that become virulent due to de-creased host resistance to infection We believe that atmo-spheric deposition of dust to coral reefs is involved

Chemical contaminantsAlthough dust events have occurred for millennia the pro-duction use and release of synthetic organic chemicals intothe environment is a relatively recent phenomenon During

and after their manufacture and use many of these com-pounds become airborne through direct emission combus-tion volatilization or wind erosion of soil particles to whichthey are sorbed (Majewski and Capel 1995) Once airbornesemivolatile organic compounds move through the atmo-sphere in the gas phase or sorbed to dust particles and are de-posited by wet and dry depositional processes (Majewski andCapel 1995 Bidleman 1999) Persistent organic pollutants(eg DDT other organochlorine insecticides and poly-chlorinated biphenyls [PCBs]) can be transported great dis-tances continuously cycle between Earthrsquos surface and the atmosphere become globally distributed and eventually ac-cumulate in polar regions and the deep seas (Bidleman et al1989 Looser et al 2000)

Dust air masses transport chemical contaminants from thedust source regions and from populated areas over which theair masses move (Uematsu et al 1992) thousands of kilo-meters across continents and oceans Long-range atmo-spheric transport and deposition of some persistentorganochlorine pollutants (especially polychlorinateddibenzo-p-dioxin and furan [PCDDFs] PCBs and somechlorinated insecticides like DDT chlordaneand toxaphene)and of anthropogenic and biogenic aliphatic hydrocarbons(eg n-alkanes) and polycyclic aromatic hydrocarbons(PAHs)are well documented (eg van Pul et al 1999) Somestudies have focused specifically on transport to the oceans(eg Simoneit et al 1988 Atlas and Schauffler 1990 Duce etal 1991 Bidleman 1999 MacDonald et al 2000) Other per-sistent halogenated organic pollutants have recently beenidentified as important atmospherically transported persis-tent contaminants (see Lipnick et al 2001) including poly-chlorinated n-alkanes and naphthalenes polybrominateddiphenyl ethers (used as flame retardants) and perfluori-nated chemicals (eg perfluorooctane sulfonate Giesy andKannan 2001) Limited information is available on the atmo-spheric transport and deposition for some current-use pes-ticides (Majewski and Capel 1995 van Dijk and Guicherit1999) Other pesticides antibiotics pharmaceuticals andmany other organic chemical contaminants and their degra-dates have not been studied Potential synergistic toxicity oractivity of transported chemical contaminants is essentiallyunknown (Kolpin et al 2002) The contaminants may ad-versely affect downwind marine and terrestrial ecosystemsthrough a number of pathways

We suggest that a combination of regional geomorphologysynthetic organic chemical use and socioeconomic and cul-tural factors may be altering the quality of transported dustIn the Sahara and Sahel of West Africa all forms of garbageare burned for fuel and for the ash that fertilizes agriculturalplots The continual burning severely degrades air quality andrespiratory complaints are common Before the late 1980sgarbage consisted primarily of animal and plant waste Sincethen the composition of garbage has fundamentally changedToday plastic products (primarily plastic bags) tires andother manufactured goods are routinely burned Combus-tion of synthetic materials is known to release hazardous

May 2003 Vol 53 No 5 BioScience 477

Articles

contaminants For example burning of municipal or house-hold waste containing various chlorinated materials such aspolyvinyl chloride plastics is a major source of PCDDFemissions to the atmosphere (eg Lemieux et al 2000) Thesecombustion practices are believed to concentrate heavy met-als The primary source of PAHs in the atmosphere is com-bustion of fuels ranging from petroleum to woodAlthough low compared with the levels in some regions ofthe world pesticide use in the Sahel region of Africa is in-creasing in order to control disease vectors and protect cropsfrom plant and insect pests Organochlorine pesticides (egDDT) historically have been used but newer-generation pesticides (eg synthetic pyrethroids) are increasingly beingapplied in dust source regions (van der Valk and Diarra2000) Many of these pesticides are known to volatilize or sorbto small clay particles which can be transported over long dis-tancesAntibiotics and pharmaceuticals are widely used to treatthe numerous diseases and infections that occur in WestAfrica Basic sanitary facilities such as pit toilets and sewagetreatment are lacking and a large river (Niger) the primarydepository of waste floods annually in a country with less than2 cm of precipitation a year The result is a stew of excretedantibiotics pharmaceuticals microorganisms pesticidescombustion products other organic compounds contami-nant breakdown products and silt deposited on the floodplainChemical contaminants sorbed to the small dry soil particlescould be advected into the atmosphere by strong convectivestorms and transported thousands of kilometers Known orsuspected compounds that are toxic carcinogenic or muta-genic or that act as endocrine disruptors may be carriedsorbed on dust particles or in the gas phase in the dust air mass(Bidleman 1999) These chemical contaminants may ad-versely affect the marine and terrestrial ecosystems on whichthe contaminants are deposited (eg Solomon 1998Daughton and Ternes 1999) Similar source considerations exist in Asian dust regions In addition Asian dust air massesmove across areas especially China Korea and Japan wherechemical emissions have increased substantially in recentyears because of extensive construction of major chemical production facilities and increased use of industrial and agri-cultural chemicals

The aquatic toxicology of numerous chemical contami-nants such as PAHs organochlorines (eg DDT) and met-als has been studied extensively These compounds havebeen found to act as neurotoxins narcotics endocrine dis-ruptors mutagens carcinogens or disruptors of growth andreproductive processes (Rand 1995) Concentrations as lowas a few parts per trillion of some contaminants have beenshown to produce significant effects in marine organismsand humans The effects of atmospherically transported anddeposited chemical contaminants on coral reefs at the mol-ecular cellular organismal and system levels are essentiallyunknownWe propose four questions for investigation (1) Arechemical contaminants transported with African or Asian dustimpairing immune response or reproduction in coral reeforganisms (2) Are these contaminants interfering with the

ability of coral larvae to settle and grow or with the survivalof young corals (3) Are effects at the cellular or molecular levelaffecting metabolism reproduction calcification or im-munocompetency (4) What synergistic cumulative orthreshold effects are at work The implications of atmospherictransport and deposition of chemical contaminants on coralreefs and other ecosystems may be substantial

ConclusionsWe suggest that African and Asian dust air masses transportchemical and viable microbial contaminants to downwindecosystems in the Americas the Caribbean and the northernPacific and may be adversely affecting those ecosystemsAtmospheric flux of pathogenic microorganisms may be responsible for the widespread distribution of some diseasesoccurring on coral reefs and associated habitats Chemical con-taminants in dust air masses may alter the resistance of coralreef organisms to disease pathogens affect reproduction orsurvival of larvae interfere with calcification or act as toxinsinitiating a cascade of effects Episodic pulses of micro- andmacronutrients are known to initiate phytoplankton bloomsand may similarly trigger pathogen reservoirs or act to sustain the shift from coral- to algae-dominated reefs Thresh-old effects may be at work Human health may also be ad-versely affected primarily by inhalation of known or suspectedcomponents in dust events including nonpathogenic andpathogenic viable microorganisms chemical contaminantssuch as carcinogens toxins endocrine disruptors and toxicmetals and small particles that may trigger other physiolog-ical reactions (eg asthma cardiovascular events) To un-derstand the effects of these global-scale transport systems onecosystems and their organisms collaborative teams of re-searchers from diverse disciplines will be needed to elucidatethe linkages of the biotic chemical and physical factors at spa-tial scales from molecular to global

AcknowledgmentsThe authors thank the US Geological Survey the NationalAeronautics and Space Administration the US Embassy in theRepublic of Mali the Friends of Virgin Islands National Parkand the American International School of Bamako (MaliWest Africa) for providing funding and in-kind support forthis project Special thanks go to Ray Smith and Mark Ranneberger for sample collection and to Scott Carr and PatChavez for their innovative ideas We also thank our col-leagues for hours of stimulating discussions and the review-ers for their constructive comments

References citedAntonius A 1973 New observations on coral destruction in reefs 10th

Meeting of the Association of Island Marine Laboratories of the Caribbean10 3

Arimoto R Duce RA Ray BJ Ellis WG Jr Cullen JD Merrill JT 1995 Traceelements in the atmosphere over the North Atlantic Journal of Geo-physical Research 100 1199ndash1213

Arimoto R Snow JA Graustein WC Moody JL Ray BJ Duce RA TurekianKK Maring HB 1999 Influences of atmospheric transport pathways on

478 BioScience May 2003 Vol 53 No 5

Articles

distances in dust events or can reproduce in the marine environment is unknown

Analysis of other marine and dust isolates reveals thatother bacterial types remain viable in the atmosphere and marine environments as well Bacteria isolated from Mventricosa from the sea urchin Echinometra variegates fromthe water column and from a Virgin Islands dust event airsample were 100 identical to Bacillus pumilus Similarly bac-teria isolated from the long-spined sea urchin Diademaantillarum and from the nonburrowing urchin Lytochinusvariegates are identical to a bacterium isolated from anAfrican dust event air sample from the Virgin Islands with99 identity to Pseudomonas aeruginosa a ubiquitous species

It had been thought that exposure to UV light duringlong-range transport would inactivate any microbes Dust inthe upper altitudes of dust clouds attenuates UV light andcould act as a UV screen for microbes at lower altitudes(Herman et al 1999) Also microorganisms may attach toand survive within cracks and crevices of inorganic dustparticles which would shield them from UV light Prelim-inary findings indicate that UV resistance in microorganismsmay play an important role in their survival during atmos-pheric transport

Coral diseases and microbial pathogens of coralsCoral diseases were first reported in the 1970s (eg Antonius1973) on reefs in the Caribbean and in the Florida KeysSince that time they have been observed on reefs worldwide(Richardson and Aronson 2002) Presumably diseases havealways occurred on coral reefs but they remained unde-tected until the 1970s because of the low incidence of diseaseon reefs and the state of knowledge at the time The currentlevels of coral mortality are unprecedented It is now ac-cepted that coral diseases are an active and important factorin the continued degradation of coral reefs Although up to29 coral diseases are currently being monitored in various pro-grams worldwide the pathogens of only five diseases (blackband aspergillosis bacterial bleaching white plague andwhite pox) have been identified Four of these have beenproved to be pathogens following the procedures of fulfill-ment of Kochrsquos postulates aspergillosis (Smith et al 1996)white plague type II (Richardson et al 1998) bacterial bleach-ing (Kushmaro et al 2001) and white pox (Patterson et al2002) The fifth disease black band is caused by a pathogenicbacterial consortium not a single pathogen Reservoirs areknown for only two coral diseases black band disease and as-pergillosis (Richardson 1998 Weir et al 2000)

Of the 10 coral diseases or disease-like states being mon-itored throughout the Caribbean and the Florida Keys(Richardson 1998) four are of particular interest in terms ofdefining a connection with African dust events aspergillosisblack band disease white pox and white plague

Aspergillosis One of the few coral diseases to be character-ized fully aspergillosis is also one of the most common Thisdisease primarily affects two types of sea fans Gorgonia

ventalina (figure 4 left) and G flabellum As discussed aboveit is caused by the common terrestrial fungus A sydowii(Geiser et al 1998) which has a worldwide distribution in soilsSpores are generally less than 2 microm in diameter a size easilycarried by winds and dispersed over great distances

To date pathogenic and nonpathogenic fungi from severaldifferent genera (Aspergillus Penicillium and Blastomyces) havebeen isolated and identified from samples collected duringAfrican dust events in the Virgin Islands Inoculations con-firmed that some dust event isolates were pathogenic tohealthy G ventalina because inoculations produced charac-teristic signs of aspergillosis such as purpling and loss oftissue In each case where disease was observed the originalpathogen was reisolated and morphologically identified ful-filling Kochrsquos postulates During the reisolations several typesof fungi in addition to A sydowii were isolated from exper-imentally inoculated sea fans indicating that (a) pathogenicfungi can be reisolated from inoculated and diseased seafans and (b) nonpathogenic opportunistic marine fungimay secondarily colonize diseased sea fans The absence ofAspergillus species in control samples (not inoculated) revealedthat Aspergillus is not typically found on healthy sea fans Thepresence of at least one nonpathogenic fungus in such con-trols indicated that it is possible for some marine fungi to col-onize sea fans without causing signs of disease

The data collected from these experiments suggest thatAfrican dust storms may be a source of Caribbean sea fanpathogens In the last year aspergillosis occurred on at leasttwo other species of soft corals Pseudopterogorgia americanain Bermuda and P acerosa in St Croix (Virgin Islands) Bothof these species displayed similar signs of disease which in-cluded gall formation and loss of tissue along the axial skele-ton Aspergillus species were morphologically identified fromdiseased specimens only This may indicate an extended hostrange of pathogenic strains of Aspergillus Interestingly whenhyphae of pure A sydowii strains are extracted and separatedusing high-performance liquid chromatography uniquecompounds are found associated with the pathogenic strainsbut not with the nonpathogenic strains We do not know theidentities of these compounds but we suspect that somemay play a role in the disease process

Black band disease Black band disease was the first coral dis-ease reported (Antonius 1973) and is one of the most wellcharacterized A cyanobacterium sulfide-oxidizing and sulfate-reducing bacteria and many heterotrophic bacteria together form a complex pathogenic microbial consortiumthat closely resembles microbial mats such as those found inilluminated sulfide-rich aquatic environments (Richardson1998) Black band disease can affect both soft corals (such assea fans) and stony corals but it appears to be a greater threatto the reef-building corals in particular Montastraea annu-laris and Colpophyllia natans Compared with other coraldiseases the disease is slow in terms of both degradation ofcoral tissue (normally 3 to 4 millimeters per day) and the timeit takes to kill a coral colony (months to years) (Ruumltzler and

May 2003 Vol 53 No 5 BioScience 475

Articles

Santavy 1983) The incidence is generally low less than 1 ofcoral colonies on reefs in the Virgin Islands (Edmunds 1991)and in the Florida Keys but up to 6 on reefs in Jamaica (re-viewed in Richardson and Aronson 2002) The low incidenceof black band disease and the low rate of black-band-inducedcoral mortality have led investigators to suggest that the slowdeath of corals caused by this disease may be balanced by thebeneficial effect of opening up reef substrate for recruitmentof stony corals thereby potentially increasing genetic diversity(Edmunds 1991) However such recruitment has not beenfound in two studies that documented recruitment of corals(both stony and soft) onto black-band-exposed substrate inthe Virgin Islands (Edmunds 1991 2000) and the northernFlorida Keys (Richardson and Aronson 2002)

The potential connection of black band disease with Africandust may relate not only to potential pathogen transport butalso to the iron present within dust Iron may act as a triggerthat activates black band disease reservoirs to become path-ogenicRichardson (1997) found that the reservoir of the blackband microbial consortium resides in biofilms on sedimentpatches in depressions on healthy coral colonies of species sus-ceptible to the disease These biofilms are present as thin lay-ers of filaments of the black band cyanobacterium When sam-ples are viewed under a microscope the presence of thesulfide-oxidizing black band member Beggiatoa is seenBecause this genus only lives in environments with sulfideoxygen interfaces the presence of sulfate reducers (the thirdmajor component of the black band consortium) is inferred

It has been proposed that the black band reservoir biofilmsare transformed into the pathogenic microbial mat commu-nity by an accumulation of biomass As biofilm communitymembers increase in biomass oxygen demand increaseswhich leads to increased areas of anoxia within the microbialcommunity As anoxic microzones develop the sulfate-reducing population can increase and a zone of permanentanoxia can develop When this occurs sulfide concentra-tions may build up within the anoxic microzone to the toxiclevel that kills coral tissue (Richardson 1998) The triggerthat may induce the buildup in biomass may very well be ironknown to be a limiting micronutrient in tropical and sub-tropical marine waters

White plague To date three forms of white plague havebeen reported on reefs of the northern Florida Keys whiteplague type I white plague type II (figure 4 right) a more vir-ulent form that emerged on the same reefs in 1995 and whiteplague type III first seen in 1999 (Richardson and Aronson2002) These three forms exhibited identical disease signsbut had very different short-term effects on the reef Whiteplague type I affected six species of stony corals and was de-scribed as having minimal impact on the reefs White plaguetype II was much more destructive affecting 17 species of stonycorals along 400 km of Floridarsquos reef tract and causing thedeath of entire colonies in as little as 2 to 3 days (Richardsonet al 1998) White plague type III appeared on the same reefsin 1999 (Richardson and Aronson 2002) but caused the most

476 BioScience May 2003 Vol 53 No 5

Articles

Figure 4 On left diseased sea fan (Gorgonia ventalina approximately 60 centimeters high)showing characteristic lesions of aspergillosis (Aspergillus sydowii) On right close-up of stonycoral (Montastraea annularis) with white plague type II White areas are bare coral skeletonwhere tissue has been recently killed by disease Photographs Sea fan courtesy of Garriet Smithstony coral courtesy of US Geological Survey

rapid tissue destruction of the three white plagues primar-ily affecting the largest colonies of M annularis and C natansEntire colonies (2 to 3 meters in diameter) were observed tohave been killed within days

The pathogen of white plague type II was isolated andidentified as a new genus of gram-negative bacteria Auran-timonas coralicida (Denner et al 2002) The white plaguepathogen may well be one of the dust-associated bacteria anddust may serve as an inoculum that triggers white plague out-breaks White plague types II and III have spread throughoutthe Caribbean in the last 2 years even to ldquopristinerdquo reefs thatare far from human populations Although this has been amystery in the past the dust hypothesis may explain regionwide disease distribution patterns

White pox White pox a coral disease that forms circular lesions on colonies of elkhorn coral (Acropora palmata) wasrecently shown to be caused by the gram-negative enter-obacterium Serratia marcescens (Patterson et al 2002) Thismicroorganism is ubiquitously distributed and could be introduced onto coral reefs via a number of pathwaysincluding soil runoff river discharge arthropod or mammalfeces and atmospheric transport of soil

Microorganisms and marine ecology Microbiota play a sig-nificant role in marine ecology Marine microorganisms havebeen shown to be significant with respect to the survivabil-ity and competitiveness of key coral reef species drasticallyaltering the composition and possibly the viability of somereefs The composition and function of the microbial com-munities associated with healthy marine organisms are justbeginning to be explored The first priority is to identify thepathogens or agents causing the 20 to 30 disease-like states being followed on reefs today some of which may not be diseases (Richardson 1998) Once pathogens have been iden-tified the sources and mechanisms of transmission and distribution need to be addressed It is equally important to identify the environmental conditions needed to activatea disease to induce a microorganism to become pathogenicor to initiate a chain of events that will lead to an outbreakof disease

Many questions remain to be answered including thesource of identified coral disease pathogens African dustmay be one mechanism through which pathogens of coral reeforganisms are distributed and deposited in the Atlantic andPacific It is still unclear whether pathogens responsible forcoral disease outbreaks are newly introduced microorganismsmore virulent forms of normally present pathogens or nor-mal bacterial populations that become virulent due to de-creased host resistance to infection We believe that atmo-spheric deposition of dust to coral reefs is involved

Chemical contaminantsAlthough dust events have occurred for millennia the pro-duction use and release of synthetic organic chemicals intothe environment is a relatively recent phenomenon During

and after their manufacture and use many of these com-pounds become airborne through direct emission combus-tion volatilization or wind erosion of soil particles to whichthey are sorbed (Majewski and Capel 1995) Once airbornesemivolatile organic compounds move through the atmo-sphere in the gas phase or sorbed to dust particles and are de-posited by wet and dry depositional processes (Majewski andCapel 1995 Bidleman 1999) Persistent organic pollutants(eg DDT other organochlorine insecticides and poly-chlorinated biphenyls [PCBs]) can be transported great dis-tances continuously cycle between Earthrsquos surface and the atmosphere become globally distributed and eventually ac-cumulate in polar regions and the deep seas (Bidleman et al1989 Looser et al 2000)

Dust air masses transport chemical contaminants from thedust source regions and from populated areas over which theair masses move (Uematsu et al 1992) thousands of kilo-meters across continents and oceans Long-range atmo-spheric transport and deposition of some persistentorganochlorine pollutants (especially polychlorinateddibenzo-p-dioxin and furan [PCDDFs] PCBs and somechlorinated insecticides like DDT chlordaneand toxaphene)and of anthropogenic and biogenic aliphatic hydrocarbons(eg n-alkanes) and polycyclic aromatic hydrocarbons(PAHs)are well documented (eg van Pul et al 1999) Somestudies have focused specifically on transport to the oceans(eg Simoneit et al 1988 Atlas and Schauffler 1990 Duce etal 1991 Bidleman 1999 MacDonald et al 2000) Other per-sistent halogenated organic pollutants have recently beenidentified as important atmospherically transported persis-tent contaminants (see Lipnick et al 2001) including poly-chlorinated n-alkanes and naphthalenes polybrominateddiphenyl ethers (used as flame retardants) and perfluori-nated chemicals (eg perfluorooctane sulfonate Giesy andKannan 2001) Limited information is available on the atmo-spheric transport and deposition for some current-use pes-ticides (Majewski and Capel 1995 van Dijk and Guicherit1999) Other pesticides antibiotics pharmaceuticals andmany other organic chemical contaminants and their degra-dates have not been studied Potential synergistic toxicity oractivity of transported chemical contaminants is essentiallyunknown (Kolpin et al 2002) The contaminants may ad-versely affect downwind marine and terrestrial ecosystemsthrough a number of pathways

We suggest that a combination of regional geomorphologysynthetic organic chemical use and socioeconomic and cul-tural factors may be altering the quality of transported dustIn the Sahara and Sahel of West Africa all forms of garbageare burned for fuel and for the ash that fertilizes agriculturalplots The continual burning severely degrades air quality andrespiratory complaints are common Before the late 1980sgarbage consisted primarily of animal and plant waste Sincethen the composition of garbage has fundamentally changedToday plastic products (primarily plastic bags) tires andother manufactured goods are routinely burned Combus-tion of synthetic materials is known to release hazardous

May 2003 Vol 53 No 5 BioScience 477

Articles

contaminants For example burning of municipal or house-hold waste containing various chlorinated materials such aspolyvinyl chloride plastics is a major source of PCDDFemissions to the atmosphere (eg Lemieux et al 2000) Thesecombustion practices are believed to concentrate heavy met-als The primary source of PAHs in the atmosphere is com-bustion of fuels ranging from petroleum to woodAlthough low compared with the levels in some regions ofthe world pesticide use in the Sahel region of Africa is in-creasing in order to control disease vectors and protect cropsfrom plant and insect pests Organochlorine pesticides (egDDT) historically have been used but newer-generation pesticides (eg synthetic pyrethroids) are increasingly beingapplied in dust source regions (van der Valk and Diarra2000) Many of these pesticides are known to volatilize or sorbto small clay particles which can be transported over long dis-tancesAntibiotics and pharmaceuticals are widely used to treatthe numerous diseases and infections that occur in WestAfrica Basic sanitary facilities such as pit toilets and sewagetreatment are lacking and a large river (Niger) the primarydepository of waste floods annually in a country with less than2 cm of precipitation a year The result is a stew of excretedantibiotics pharmaceuticals microorganisms pesticidescombustion products other organic compounds contami-nant breakdown products and silt deposited on the floodplainChemical contaminants sorbed to the small dry soil particlescould be advected into the atmosphere by strong convectivestorms and transported thousands of kilometers Known orsuspected compounds that are toxic carcinogenic or muta-genic or that act as endocrine disruptors may be carriedsorbed on dust particles or in the gas phase in the dust air mass(Bidleman 1999) These chemical contaminants may ad-versely affect the marine and terrestrial ecosystems on whichthe contaminants are deposited (eg Solomon 1998Daughton and Ternes 1999) Similar source considerations exist in Asian dust regions In addition Asian dust air massesmove across areas especially China Korea and Japan wherechemical emissions have increased substantially in recentyears because of extensive construction of major chemical production facilities and increased use of industrial and agri-cultural chemicals

The aquatic toxicology of numerous chemical contami-nants such as PAHs organochlorines (eg DDT) and met-als has been studied extensively These compounds havebeen found to act as neurotoxins narcotics endocrine dis-ruptors mutagens carcinogens or disruptors of growth andreproductive processes (Rand 1995) Concentrations as lowas a few parts per trillion of some contaminants have beenshown to produce significant effects in marine organismsand humans The effects of atmospherically transported anddeposited chemical contaminants on coral reefs at the mol-ecular cellular organismal and system levels are essentiallyunknownWe propose four questions for investigation (1) Arechemical contaminants transported with African or Asian dustimpairing immune response or reproduction in coral reeforganisms (2) Are these contaminants interfering with the

ability of coral larvae to settle and grow or with the survivalof young corals (3) Are effects at the cellular or molecular levelaffecting metabolism reproduction calcification or im-munocompetency (4) What synergistic cumulative orthreshold effects are at work The implications of atmospherictransport and deposition of chemical contaminants on coralreefs and other ecosystems may be substantial

ConclusionsWe suggest that African and Asian dust air masses transportchemical and viable microbial contaminants to downwindecosystems in the Americas the Caribbean and the northernPacific and may be adversely affecting those ecosystemsAtmospheric flux of pathogenic microorganisms may be responsible for the widespread distribution of some diseasesoccurring on coral reefs and associated habitats Chemical con-taminants in dust air masses may alter the resistance of coralreef organisms to disease pathogens affect reproduction orsurvival of larvae interfere with calcification or act as toxinsinitiating a cascade of effects Episodic pulses of micro- andmacronutrients are known to initiate phytoplankton bloomsand may similarly trigger pathogen reservoirs or act to sustain the shift from coral- to algae-dominated reefs Thresh-old effects may be at work Human health may also be ad-versely affected primarily by inhalation of known or suspectedcomponents in dust events including nonpathogenic andpathogenic viable microorganisms chemical contaminantssuch as carcinogens toxins endocrine disruptors and toxicmetals and small particles that may trigger other physiolog-ical reactions (eg asthma cardiovascular events) To un-derstand the effects of these global-scale transport systems onecosystems and their organisms collaborative teams of re-searchers from diverse disciplines will be needed to elucidatethe linkages of the biotic chemical and physical factors at spa-tial scales from molecular to global

AcknowledgmentsThe authors thank the US Geological Survey the NationalAeronautics and Space Administration the US Embassy in theRepublic of Mali the Friends of Virgin Islands National Parkand the American International School of Bamako (MaliWest Africa) for providing funding and in-kind support forthis project Special thanks go to Ray Smith and Mark Ranneberger for sample collection and to Scott Carr and PatChavez for their innovative ideas We also thank our col-leagues for hours of stimulating discussions and the review-ers for their constructive comments

References citedAntonius A 1973 New observations on coral destruction in reefs 10th

Meeting of the Association of Island Marine Laboratories of the Caribbean10 3

Arimoto R Duce RA Ray BJ Ellis WG Jr Cullen JD Merrill JT 1995 Traceelements in the atmosphere over the North Atlantic Journal of Geo-physical Research 100 1199ndash1213

Arimoto R Snow JA Graustein WC Moody JL Ray BJ Duce RA TurekianKK Maring HB 1999 Influences of atmospheric transport pathways on

478 BioScience May 2003 Vol 53 No 5

Articles

Santavy 1983) The incidence is generally low less than 1 ofcoral colonies on reefs in the Virgin Islands (Edmunds 1991)and in the Florida Keys but up to 6 on reefs in Jamaica (re-viewed in Richardson and Aronson 2002) The low incidenceof black band disease and the low rate of black-band-inducedcoral mortality have led investigators to suggest that the slowdeath of corals caused by this disease may be balanced by thebeneficial effect of opening up reef substrate for recruitmentof stony corals thereby potentially increasing genetic diversity(Edmunds 1991) However such recruitment has not beenfound in two studies that documented recruitment of corals(both stony and soft) onto black-band-exposed substrate inthe Virgin Islands (Edmunds 1991 2000) and the northernFlorida Keys (Richardson and Aronson 2002)

The potential connection of black band disease with Africandust may relate not only to potential pathogen transport butalso to the iron present within dust Iron may act as a triggerthat activates black band disease reservoirs to become path-ogenicRichardson (1997) found that the reservoir of the blackband microbial consortium resides in biofilms on sedimentpatches in depressions on healthy coral colonies of species sus-ceptible to the disease These biofilms are present as thin lay-ers of filaments of the black band cyanobacterium When sam-ples are viewed under a microscope the presence of thesulfide-oxidizing black band member Beggiatoa is seenBecause this genus only lives in environments with sulfideoxygen interfaces the presence of sulfate reducers (the thirdmajor component of the black band consortium) is inferred

It has been proposed that the black band reservoir biofilmsare transformed into the pathogenic microbial mat commu-nity by an accumulation of biomass As biofilm communitymembers increase in biomass oxygen demand increaseswhich leads to increased areas of anoxia within the microbialcommunity As anoxic microzones develop the sulfate-reducing population can increase and a zone of permanentanoxia can develop When this occurs sulfide concentra-tions may build up within the anoxic microzone to the toxiclevel that kills coral tissue (Richardson 1998) The triggerthat may induce the buildup in biomass may very well be ironknown to be a limiting micronutrient in tropical and sub-tropical marine waters

White plague To date three forms of white plague havebeen reported on reefs of the northern Florida Keys whiteplague type I white plague type II (figure 4 right) a more vir-ulent form that emerged on the same reefs in 1995 and whiteplague type III first seen in 1999 (Richardson and Aronson2002) These three forms exhibited identical disease signsbut had very different short-term effects on the reef Whiteplague type I affected six species of stony corals and was de-scribed as having minimal impact on the reefs White plaguetype II was much more destructive affecting 17 species of stonycorals along 400 km of Floridarsquos reef tract and causing thedeath of entire colonies in as little as 2 to 3 days (Richardsonet al 1998) White plague type III appeared on the same reefsin 1999 (Richardson and Aronson 2002) but caused the most

476 BioScience May 2003 Vol 53 No 5

Articles

Figure 4 On left diseased sea fan (Gorgonia ventalina approximately 60 centimeters high)showing characteristic lesions of aspergillosis (Aspergillus sydowii) On right close-up of stonycoral (Montastraea annularis) with white plague type II White areas are bare coral skeletonwhere tissue has been recently killed by disease Photographs Sea fan courtesy of Garriet Smithstony coral courtesy of US Geological Survey

rapid tissue destruction of the three white plagues primar-ily affecting the largest colonies of M annularis and C natansEntire colonies (2 to 3 meters in diameter) were observed tohave been killed within days

The pathogen of white plague type II was isolated andidentified as a new genus of gram-negative bacteria Auran-timonas coralicida (Denner et al 2002) The white plaguepathogen may well be one of the dust-associated bacteria anddust may serve as an inoculum that triggers white plague out-breaks White plague types II and III have spread throughoutthe Caribbean in the last 2 years even to ldquopristinerdquo reefs thatare far from human populations Although this has been amystery in the past the dust hypothesis may explain regionwide disease distribution patterns

White pox White pox a coral disease that forms circular lesions on colonies of elkhorn coral (Acropora palmata) wasrecently shown to be caused by the gram-negative enter-obacterium Serratia marcescens (Patterson et al 2002) Thismicroorganism is ubiquitously distributed and could be introduced onto coral reefs via a number of pathwaysincluding soil runoff river discharge arthropod or mammalfeces and atmospheric transport of soil

Microorganisms and marine ecology Microbiota play a sig-nificant role in marine ecology Marine microorganisms havebeen shown to be significant with respect to the survivabil-ity and competitiveness of key coral reef species drasticallyaltering the composition and possibly the viability of somereefs The composition and function of the microbial com-munities associated with healthy marine organisms are justbeginning to be explored The first priority is to identify thepathogens or agents causing the 20 to 30 disease-like states being followed on reefs today some of which may not be diseases (Richardson 1998) Once pathogens have been iden-tified the sources and mechanisms of transmission and distribution need to be addressed It is equally important to identify the environmental conditions needed to activatea disease to induce a microorganism to become pathogenicor to initiate a chain of events that will lead to an outbreakof disease

Many questions remain to be answered including thesource of identified coral disease pathogens African dustmay be one mechanism through which pathogens of coral reeforganisms are distributed and deposited in the Atlantic andPacific It is still unclear whether pathogens responsible forcoral disease outbreaks are newly introduced microorganismsmore virulent forms of normally present pathogens or nor-mal bacterial populations that become virulent due to de-creased host resistance to infection We believe that atmo-spheric deposition of dust to coral reefs is involved

Chemical contaminantsAlthough dust events have occurred for millennia the pro-duction use and release of synthetic organic chemicals intothe environment is a relatively recent phenomenon During

and after their manufacture and use many of these com-pounds become airborne through direct emission combus-tion volatilization or wind erosion of soil particles to whichthey are sorbed (Majewski and Capel 1995) Once airbornesemivolatile organic compounds move through the atmo-sphere in the gas phase or sorbed to dust particles and are de-posited by wet and dry depositional processes (Majewski andCapel 1995 Bidleman 1999) Persistent organic pollutants(eg DDT other organochlorine insecticides and poly-chlorinated biphenyls [PCBs]) can be transported great dis-tances continuously cycle between Earthrsquos surface and the atmosphere become globally distributed and eventually ac-cumulate in polar regions and the deep seas (Bidleman et al1989 Looser et al 2000)

Dust air masses transport chemical contaminants from thedust source regions and from populated areas over which theair masses move (Uematsu et al 1992) thousands of kilo-meters across continents and oceans Long-range atmo-spheric transport and deposition of some persistentorganochlorine pollutants (especially polychlorinateddibenzo-p-dioxin and furan [PCDDFs] PCBs and somechlorinated insecticides like DDT chlordaneand toxaphene)and of anthropogenic and biogenic aliphatic hydrocarbons(eg n-alkanes) and polycyclic aromatic hydrocarbons(PAHs)are well documented (eg van Pul et al 1999) Somestudies have focused specifically on transport to the oceans(eg Simoneit et al 1988 Atlas and Schauffler 1990 Duce etal 1991 Bidleman 1999 MacDonald et al 2000) Other per-sistent halogenated organic pollutants have recently beenidentified as important atmospherically transported persis-tent contaminants (see Lipnick et al 2001) including poly-chlorinated n-alkanes and naphthalenes polybrominateddiphenyl ethers (used as flame retardants) and perfluori-nated chemicals (eg perfluorooctane sulfonate Giesy andKannan 2001) Limited information is available on the atmo-spheric transport and deposition for some current-use pes-ticides (Majewski and Capel 1995 van Dijk and Guicherit1999) Other pesticides antibiotics pharmaceuticals andmany other organic chemical contaminants and their degra-dates have not been studied Potential synergistic toxicity oractivity of transported chemical contaminants is essentiallyunknown (Kolpin et al 2002) The contaminants may ad-versely affect downwind marine and terrestrial ecosystemsthrough a number of pathways

We suggest that a combination of regional geomorphologysynthetic organic chemical use and socioeconomic and cul-tural factors may be altering the quality of transported dustIn the Sahara and Sahel of West Africa all forms of garbageare burned for fuel and for the ash that fertilizes agriculturalplots The continual burning severely degrades air quality andrespiratory complaints are common Before the late 1980sgarbage consisted primarily of animal and plant waste Sincethen the composition of garbage has fundamentally changedToday plastic products (primarily plastic bags) tires andother manufactured goods are routinely burned Combus-tion of synthetic materials is known to release hazardous

May 2003 Vol 53 No 5 BioScience 477

Articles

contaminants For example burning of municipal or house-hold waste containing various chlorinated materials such aspolyvinyl chloride plastics is a major source of PCDDFemissions to the atmosphere (eg Lemieux et al 2000) Thesecombustion practices are believed to concentrate heavy met-als The primary source of PAHs in the atmosphere is com-bustion of fuels ranging from petroleum to woodAlthough low compared with the levels in some regions ofthe world pesticide use in the Sahel region of Africa is in-creasing in order to control disease vectors and protect cropsfrom plant and insect pests Organochlorine pesticides (egDDT) historically have been used but newer-generation pesticides (eg synthetic pyrethroids) are increasingly beingapplied in dust source regions (van der Valk and Diarra2000) Many of these pesticides are known to volatilize or sorbto small clay particles which can be transported over long dis-tancesAntibiotics and pharmaceuticals are widely used to treatthe numerous diseases and infections that occur in WestAfrica Basic sanitary facilities such as pit toilets and sewagetreatment are lacking and a large river (Niger) the primarydepository of waste floods annually in a country with less than2 cm of precipitation a year The result is a stew of excretedantibiotics pharmaceuticals microorganisms pesticidescombustion products other organic compounds contami-nant breakdown products and silt deposited on the floodplainChemical contaminants sorbed to the small dry soil particlescould be advected into the atmosphere by strong convectivestorms and transported thousands of kilometers Known orsuspected compounds that are toxic carcinogenic or muta-genic or that act as endocrine disruptors may be carriedsorbed on dust particles or in the gas phase in the dust air mass(Bidleman 1999) These chemical contaminants may ad-versely affect the marine and terrestrial ecosystems on whichthe contaminants are deposited (eg Solomon 1998Daughton and Ternes 1999) Similar source considerations exist in Asian dust regions In addition Asian dust air massesmove across areas especially China Korea and Japan wherechemical emissions have increased substantially in recentyears because of extensive construction of major chemical production facilities and increased use of industrial and agri-cultural chemicals

The aquatic toxicology of numerous chemical contami-nants such as PAHs organochlorines (eg DDT) and met-als has been studied extensively These compounds havebeen found to act as neurotoxins narcotics endocrine dis-ruptors mutagens carcinogens or disruptors of growth andreproductive processes (Rand 1995) Concentrations as lowas a few parts per trillion of some contaminants have beenshown to produce significant effects in marine organismsand humans The effects of atmospherically transported anddeposited chemical contaminants on coral reefs at the mol-ecular cellular organismal and system levels are essentiallyunknownWe propose four questions for investigation (1) Arechemical contaminants transported with African or Asian dustimpairing immune response or reproduction in coral reeforganisms (2) Are these contaminants interfering with the

ability of coral larvae to settle and grow or with the survivalof young corals (3) Are effects at the cellular or molecular levelaffecting metabolism reproduction calcification or im-munocompetency (4) What synergistic cumulative orthreshold effects are at work The implications of atmospherictransport and deposition of chemical contaminants on coralreefs and other ecosystems may be substantial

ConclusionsWe suggest that African and Asian dust air masses transportchemical and viable microbial contaminants to downwindecosystems in the Americas the Caribbean and the northernPacific and may be adversely affecting those ecosystemsAtmospheric flux of pathogenic microorganisms may be responsible for the widespread distribution of some diseasesoccurring on coral reefs and associated habitats Chemical con-taminants in dust air masses may alter the resistance of coralreef organisms to disease pathogens affect reproduction orsurvival of larvae interfere with calcification or act as toxinsinitiating a cascade of effects Episodic pulses of micro- andmacronutrients are known to initiate phytoplankton bloomsand may similarly trigger pathogen reservoirs or act to sustain the shift from coral- to algae-dominated reefs Thresh-old effects may be at work Human health may also be ad-versely affected primarily by inhalation of known or suspectedcomponents in dust events including nonpathogenic andpathogenic viable microorganisms chemical contaminantssuch as carcinogens toxins endocrine disruptors and toxicmetals and small particles that may trigger other physiolog-ical reactions (eg asthma cardiovascular events) To un-derstand the effects of these global-scale transport systems onecosystems and their organisms collaborative teams of re-searchers from diverse disciplines will be needed to elucidatethe linkages of the biotic chemical and physical factors at spa-tial scales from molecular to global

AcknowledgmentsThe authors thank the US Geological Survey the NationalAeronautics and Space Administration the US Embassy in theRepublic of Mali the Friends of Virgin Islands National Parkand the American International School of Bamako (MaliWest Africa) for providing funding and in-kind support forthis project Special thanks go to Ray Smith and Mark Ranneberger for sample collection and to Scott Carr and PatChavez for their innovative ideas We also thank our col-leagues for hours of stimulating discussions and the review-ers for their constructive comments

References citedAntonius A 1973 New observations on coral destruction in reefs 10th

Meeting of the Association of Island Marine Laboratories of the Caribbean10 3

Arimoto R Duce RA Ray BJ Ellis WG Jr Cullen JD Merrill JT 1995 Traceelements in the atmosphere over the North Atlantic Journal of Geo-physical Research 100 1199ndash1213

Arimoto R Snow JA Graustein WC Moody JL Ray BJ Duce RA TurekianKK Maring HB 1999 Influences of atmospheric transport pathways on

478 BioScience May 2003 Vol 53 No 5

Articles

rapid tissue destruction of the three white plagues primar-ily affecting the largest colonies of M annularis and C natansEntire colonies (2 to 3 meters in diameter) were observed tohave been killed within days

The pathogen of white plague type II was isolated andidentified as a new genus of gram-negative bacteria Auran-timonas coralicida (Denner et al 2002) The white plaguepathogen may well be one of the dust-associated bacteria anddust may serve as an inoculum that triggers white plague out-breaks White plague types II and III have spread throughoutthe Caribbean in the last 2 years even to ldquopristinerdquo reefs thatare far from human populations Although this has been amystery in the past the dust hypothesis may explain regionwide disease distribution patterns

White pox White pox a coral disease that forms circular lesions on colonies of elkhorn coral (Acropora palmata) wasrecently shown to be caused by the gram-negative enter-obacterium Serratia marcescens (Patterson et al 2002) Thismicroorganism is ubiquitously distributed and could be introduced onto coral reefs via a number of pathwaysincluding soil runoff river discharge arthropod or mammalfeces and atmospheric transport of soil

Microorganisms and marine ecology Microbiota play a sig-nificant role in marine ecology Marine microorganisms havebeen shown to be significant with respect to the survivabil-ity and competitiveness of key coral reef species drasticallyaltering the composition and possibly the viability of somereefs The composition and function of the microbial com-munities associated with healthy marine organisms are justbeginning to be explored The first priority is to identify thepathogens or agents causing the 20 to 30 disease-like states being followed on reefs today some of which may not be diseases (Richardson 1998) Once pathogens have been iden-tified the sources and mechanisms of transmission and distribution need to be addressed It is equally important to identify the environmental conditions needed to activatea disease to induce a microorganism to become pathogenicor to initiate a chain of events that will lead to an outbreakof disease

Many questions remain to be answered including thesource of identified coral disease pathogens African dustmay be one mechanism through which pathogens of coral reeforganisms are distributed and deposited in the Atlantic andPacific It is still unclear whether pathogens responsible forcoral disease outbreaks are newly introduced microorganismsmore virulent forms of normally present pathogens or nor-mal bacterial populations that become virulent due to de-creased host resistance to infection We believe that atmo-spheric deposition of dust to coral reefs is involved

Chemical contaminantsAlthough dust events have occurred for millennia the pro-duction use and release of synthetic organic chemicals intothe environment is a relatively recent phenomenon During

and after their manufacture and use many of these com-pounds become airborne through direct emission combus-tion volatilization or wind erosion of soil particles to whichthey are sorbed (Majewski and Capel 1995) Once airbornesemivolatile organic compounds move through the atmo-sphere in the gas phase or sorbed to dust particles and are de-posited by wet and dry depositional processes (Majewski andCapel 1995 Bidleman 1999) Persistent organic pollutants(eg DDT other organochlorine insecticides and poly-chlorinated biphenyls [PCBs]) can be transported great dis-tances continuously cycle between Earthrsquos surface and the atmosphere become globally distributed and eventually ac-cumulate in polar regions and the deep seas (Bidleman et al1989 Looser et al 2000)

Dust air masses transport chemical contaminants from thedust source regions and from populated areas over which theair masses move (Uematsu et al 1992) thousands of kilo-meters across continents and oceans Long-range atmo-spheric transport and deposition of some persistentorganochlorine pollutants (especially polychlorinateddibenzo-p-dioxin and furan [PCDDFs] PCBs and somechlorinated insecticides like DDT chlordaneand toxaphene)and of anthropogenic and biogenic aliphatic hydrocarbons(eg n-alkanes) and polycyclic aromatic hydrocarbons(PAHs)are well documented (eg van Pul et al 1999) Somestudies have focused specifically on transport to the oceans(eg Simoneit et al 1988 Atlas and Schauffler 1990 Duce etal 1991 Bidleman 1999 MacDonald et al 2000) Other per-sistent halogenated organic pollutants have recently beenidentified as important atmospherically transported persis-tent contaminants (see Lipnick et al 2001) including poly-chlorinated n-alkanes and naphthalenes polybrominateddiphenyl ethers (used as flame retardants) and perfluori-nated chemicals (eg perfluorooctane sulfonate Giesy andKannan 2001) Limited information is available on the atmo-spheric transport and deposition for some current-use pes-ticides (Majewski and Capel 1995 van Dijk and Guicherit1999) Other pesticides antibiotics pharmaceuticals andmany other organic chemical contaminants and their degra-dates have not been studied Potential synergistic toxicity oractivity of transported chemical contaminants is essentiallyunknown (Kolpin et al 2002) The contaminants may ad-versely affect downwind marine and terrestrial ecosystemsthrough a number of pathways

We suggest that a combination of regional geomorphologysynthetic organic chemical use and socioeconomic and cul-tural factors may be altering the quality of transported dustIn the Sahara and Sahel of West Africa all forms of garbageare burned for fuel and for the ash that fertilizes agriculturalplots The continual burning severely degrades air quality andrespiratory complaints are common Before the late 1980sgarbage consisted primarily of animal and plant waste Sincethen the composition of garbage has fundamentally changedToday plastic products (primarily plastic bags) tires andother manufactured goods are routinely burned Combus-tion of synthetic materials is known to release hazardous

May 2003 Vol 53 No 5 BioScience 477

Articles

contaminants For example burning of municipal or house-hold waste containing various chlorinated materials such aspolyvinyl chloride plastics is a major source of PCDDFemissions to the atmosphere (eg Lemieux et al 2000) Thesecombustion practices are believed to concentrate heavy met-als The primary source of PAHs in the atmosphere is com-bustion of fuels ranging from petroleum to woodAlthough low compared with the levels in some regions ofthe world pesticide use in the Sahel region of Africa is in-creasing in order to control disease vectors and protect cropsfrom plant and insect pests Organochlorine pesticides (egDDT) historically have been used but newer-generation pesticides (eg synthetic pyrethroids) are increasingly beingapplied in dust source regions (van der Valk and Diarra2000) Many of these pesticides are known to volatilize or sorbto small clay particles which can be transported over long dis-tancesAntibiotics and pharmaceuticals are widely used to treatthe numerous diseases and infections that occur in WestAfrica Basic sanitary facilities such as pit toilets and sewagetreatment are lacking and a large river (Niger) the primarydepository of waste floods annually in a country with less than2 cm of precipitation a year The result is a stew of excretedantibiotics pharmaceuticals microorganisms pesticidescombustion products other organic compounds contami-nant breakdown products and silt deposited on the floodplainChemical contaminants sorbed to the small dry soil particlescould be advected into the atmosphere by strong convectivestorms and transported thousands of kilometers Known orsuspected compounds that are toxic carcinogenic or muta-genic or that act as endocrine disruptors may be carriedsorbed on dust particles or in the gas phase in the dust air mass(Bidleman 1999) These chemical contaminants may ad-versely affect the marine and terrestrial ecosystems on whichthe contaminants are deposited (eg Solomon 1998Daughton and Ternes 1999) Similar source considerations exist in Asian dust regions In addition Asian dust air massesmove across areas especially China Korea and Japan wherechemical emissions have increased substantially in recentyears because of extensive construction of major chemical production facilities and increased use of industrial and agri-cultural chemicals

The aquatic toxicology of numerous chemical contami-nants such as PAHs organochlorines (eg DDT) and met-als has been studied extensively These compounds havebeen found to act as neurotoxins narcotics endocrine dis-ruptors mutagens carcinogens or disruptors of growth andreproductive processes (Rand 1995) Concentrations as lowas a few parts per trillion of some contaminants have beenshown to produce significant effects in marine organismsand humans The effects of atmospherically transported anddeposited chemical contaminants on coral reefs at the mol-ecular cellular organismal and system levels are essentiallyunknownWe propose four questions for investigation (1) Arechemical contaminants transported with African or Asian dustimpairing immune response or reproduction in coral reeforganisms (2) Are these contaminants interfering with the

ability of coral larvae to settle and grow or with the survivalof young corals (3) Are effects at the cellular or molecular levelaffecting metabolism reproduction calcification or im-munocompetency (4) What synergistic cumulative orthreshold effects are at work The implications of atmospherictransport and deposition of chemical contaminants on coralreefs and other ecosystems may be substantial

ConclusionsWe suggest that African and Asian dust air masses transportchemical and viable microbial contaminants to downwindecosystems in the Americas the Caribbean and the northernPacific and may be adversely affecting those ecosystemsAtmospheric flux of pathogenic microorganisms may be responsible for the widespread distribution of some diseasesoccurring on coral reefs and associated habitats Chemical con-taminants in dust air masses may alter the resistance of coralreef organisms to disease pathogens affect reproduction orsurvival of larvae interfere with calcification or act as toxinsinitiating a cascade of effects Episodic pulses of micro- andmacronutrients are known to initiate phytoplankton bloomsand may similarly trigger pathogen reservoirs or act to sustain the shift from coral- to algae-dominated reefs Thresh-old effects may be at work Human health may also be ad-versely affected primarily by inhalation of known or suspectedcomponents in dust events including nonpathogenic andpathogenic viable microorganisms chemical contaminantssuch as carcinogens toxins endocrine disruptors and toxicmetals and small particles that may trigger other physiolog-ical reactions (eg asthma cardiovascular events) To un-derstand the effects of these global-scale transport systems onecosystems and their organisms collaborative teams of re-searchers from diverse disciplines will be needed to elucidatethe linkages of the biotic chemical and physical factors at spa-tial scales from molecular to global

AcknowledgmentsThe authors thank the US Geological Survey the NationalAeronautics and Space Administration the US Embassy in theRepublic of Mali the Friends of Virgin Islands National Parkand the American International School of Bamako (MaliWest Africa) for providing funding and in-kind support forthis project Special thanks go to Ray Smith and Mark Ranneberger for sample collection and to Scott Carr and PatChavez for their innovative ideas We also thank our col-leagues for hours of stimulating discussions and the review-ers for their constructive comments

References citedAntonius A 1973 New observations on coral destruction in reefs 10th

Meeting of the Association of Island Marine Laboratories of the Caribbean10 3

Arimoto R Duce RA Ray BJ Ellis WG Jr Cullen JD Merrill JT 1995 Traceelements in the atmosphere over the North Atlantic Journal of Geo-physical Research 100 1199ndash1213

Arimoto R Snow JA Graustein WC Moody JL Ray BJ Duce RA TurekianKK Maring HB 1999 Influences of atmospheric transport pathways on

478 BioScience May 2003 Vol 53 No 5

Articles

contaminants For example burning of municipal or house-hold waste containing various chlorinated materials such aspolyvinyl chloride plastics is a major source of PCDDFemissions to the atmosphere (eg Lemieux et al 2000) Thesecombustion practices are believed to concentrate heavy met-als The primary source of PAHs in the atmosphere is com-bustion of fuels ranging from petroleum to woodAlthough low compared with the levels in some regions ofthe world pesticide use in the Sahel region of Africa is in-creasing in order to control disease vectors and protect cropsfrom plant and insect pests Organochlorine pesticides (egDDT) historically have been used but newer-generation pesticides (eg synthetic pyrethroids) are increasingly beingapplied in dust source regions (van der Valk and Diarra2000) Many of these pesticides are known to volatilize or sorbto small clay particles which can be transported over long dis-tancesAntibiotics and pharmaceuticals are widely used to treatthe numerous diseases and infections that occur in WestAfrica Basic sanitary facilities such as pit toilets and sewagetreatment are lacking and a large river (Niger) the primarydepository of waste floods annually in a country with less than2 cm of precipitation a year The result is a stew of excretedantibiotics pharmaceuticals microorganisms pesticidescombustion products other organic compounds contami-nant breakdown products and silt deposited on the floodplainChemical contaminants sorbed to the small dry soil particlescould be advected into the atmosphere by strong convectivestorms and transported thousands of kilometers Known orsuspected compounds that are toxic carcinogenic or muta-genic or that act as endocrine disruptors may be carriedsorbed on dust particles or in the gas phase in the dust air mass(Bidleman 1999) These chemical contaminants may ad-versely affect the marine and terrestrial ecosystems on whichthe contaminants are deposited (eg Solomon 1998Daughton and Ternes 1999) Similar source considerations exist in Asian dust regions In addition Asian dust air massesmove across areas especially China Korea and Japan wherechemical emissions have increased substantially in recentyears because of extensive construction of major chemical production facilities and increased use of industrial and agri-cultural chemicals

The aquatic toxicology of numerous chemical contami-nants such as PAHs organochlorines (eg DDT) and met-als has been studied extensively These compounds havebeen found to act as neurotoxins narcotics endocrine dis-ruptors mutagens carcinogens or disruptors of growth andreproductive processes (Rand 1995) Concentrations as lowas a few parts per trillion of some contaminants have beenshown to produce significant effects in marine organismsand humans The effects of atmospherically transported anddeposited chemical contaminants on coral reefs at the mol-ecular cellular organismal and system levels are essentiallyunknownWe propose four questions for investigation (1) Arechemical contaminants transported with African or Asian dustimpairing immune response or reproduction in coral reeforganisms (2) Are these contaminants interfering with the

ability of coral larvae to settle and grow or with the survivalof young corals (3) Are effects at the cellular or molecular levelaffecting metabolism reproduction calcification or im-munocompetency (4) What synergistic cumulative orthreshold effects are at work The implications of atmospherictransport and deposition of chemical contaminants on coralreefs and other ecosystems may be substantial

ConclusionsWe suggest that African and Asian dust air masses transportchemical and viable microbial contaminants to downwindecosystems in the Americas the Caribbean and the northernPacific and may be adversely affecting those ecosystemsAtmospheric flux of pathogenic microorganisms may be responsible for the widespread distribution of some diseasesoccurring on coral reefs and associated habitats Chemical con-taminants in dust air masses may alter the resistance of coralreef organisms to disease pathogens affect reproduction orsurvival of larvae interfere with calcification or act as toxinsinitiating a cascade of effects Episodic pulses of micro- andmacronutrients are known to initiate phytoplankton bloomsand may similarly trigger pathogen reservoirs or act to sustain the shift from coral- to algae-dominated reefs Thresh-old effects may be at work Human health may also be ad-versely affected primarily by inhalation of known or suspectedcomponents in dust events including nonpathogenic andpathogenic viable microorganisms chemical contaminantssuch as carcinogens toxins endocrine disruptors and toxicmetals and small particles that may trigger other physiolog-ical reactions (eg asthma cardiovascular events) To un-derstand the effects of these global-scale transport systems onecosystems and their organisms collaborative teams of re-searchers from diverse disciplines will be needed to elucidatethe linkages of the biotic chemical and physical factors at spa-tial scales from molecular to global

AcknowledgmentsThe authors thank the US Geological Survey the NationalAeronautics and Space Administration the US Embassy in theRepublic of Mali the Friends of Virgin Islands National Parkand the American International School of Bamako (MaliWest Africa) for providing funding and in-kind support forthis project Special thanks go to Ray Smith and Mark Ranneberger for sample collection and to Scott Carr and PatChavez for their innovative ideas We also thank our col-leagues for hours of stimulating discussions and the review-ers for their constructive comments

References citedAntonius A 1973 New observations on coral destruction in reefs 10th

Meeting of the Association of Island Marine Laboratories of the Caribbean10 3

Arimoto R Duce RA Ray BJ Ellis WG Jr Cullen JD Merrill JT 1995 Traceelements in the atmosphere over the North Atlantic Journal of Geo-physical Research 100 1199ndash1213

Arimoto R Snow JA Graustein WC Moody JL Ray BJ Duce RA TurekianKK Maring HB 1999 Influences of atmospheric transport pathways on

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Long Range Transport of Pesticides Chelsea (MI) Lewis PublishersBarnard LA MacIntyre IG Pierce JW 1974 Possible environmental index

in tropical coral reefs Nature 252 219ndash220Behrenfeld MJ Kolber ZS 1999 Widespread iron limitation of phyto-

plankton in the South Pacific Ocean Science 283 840ndash843

Bidleman TF 1999 Atmospheric transport and air-surface exchange of pes-ticides Water Air and Soil Pollution 115 115ndash166

Bidleman TF Patton GWWalla MDHargrave BTVass WP Erickson P FowlerB Scott V Gregor DJ 1989 Toxaphene and other organochlorines in Arc-tic Ocean fauna Evidence for atmospheric delivery Arctic 42 307ndash313

Bishop JKB Davis RE Sherman JT 2002 Robotic observations of duststorm enhancement of carbon biomass in the North Pacific Science 298

817ndash821Blanchard DC Syzdek L 1970 Mechanism for the water-to-air transfer

and concentration of bacteria Science 170 626ndash628

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croscopy Applied and Environmental Microbiology 56 352ndash356Brown JKM Hovmoslashller MS 2002 Aerial dispersal of pathogens on the

global and continental scales and its impact on plant disease Science 297

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ing sources of nutrients during four million years of ecosystem devel-

opment Nature 397 491ndash497Christensen LS Mortensen S Botner A Strandbygaard BS Ronsholt L

Henriksen CA Anderson JB 1993 Further evidence of long distance air-borne transmission of Aujeszkyrsquos disease (pseudorabies) virusVeterinaryRecord 132 317ndash321

Coale KH et al 1996 A massive phytoplankton bloom induced by anecosystem-scale iron fertilization experiment in the equatorial Pacific

Ocean Nature 383 495ndash501Darwin C 1846 An account of the fine dust which often falls on vessels in

the Atlantic Ocean Quarterly Journal of the Geological Society of Lon-don 2 26ndash30

Daughton CG Ternes TA 1999 Pharmaceuticals and personal care prod-

ucts in the environment Agents of subtle change Environmental HealthPerspectives 107 907ndash938

Delaney AC Parkin DW Griffin JJ Goldberg ED Reimann BEF 1967 Air-borne dust collected at BarbadosGeochimica et Cosmochimica Acta 31885ndash909

Denner EBM Smith G Busse HJ Schumann P Narzt T Polson SW LubitzW Richardson LL 2002 Aurantimonas coralicida gen nov sp nov the

causative agent of white plague type II on Caribbean scleractinian coralsInternational Journal of Systematic and Evolutionary Microbiology (1April 2003 httpdxdoiorg101099ijs002359-0)

Duce RA Tindale NW 1991 Atmospheric transport of iron and its depo-sition in the ocean Limnology and Oceanography 36 1715ndash1726

Duce RA Ray BJ Hoffman JL Walsh PR 1976 Trace metal concentrationas a function of particle size in marine aerosols from Bermuda Geo-physical Research Letters 23 339ndash342

Duce RA Unni CK Ray BJ Prospero JM Merrill JT 1980 Long-range at-mospheric transport of soil dust from Asia to the tropical North Pacific

Temporal variability Science 209 1522ndash1524Duce RA et al 1991 The atmospheric input of trace species to the world

ocean Global Biogeochemical Cycles 5 193ndash259

Edmunds PJ1991 Extent and effect of black band disease on Caribbean reefsCoral Reefs 10 161ndash165

mdashmdashmdash 2000 Recruitment of scleractinians onto the skeletons of corals killedby black band disease Coral Reefs 19 69ndash74

Eilers H Pernthaler J Glockner FO Amann R 2000 Culturability and in situabundance of pelagic bacteria from the North Sea Applied and Envi-ronmental Microbiology 66 3044ndash3051

Fiser A Lanikova A Novak P 1994 Mold and microbial contamination ofdust deposition in cowsheds for heifers and dairy cows Veterinary MedicinendashCzech 39 245ndash253

Geiser DM Taylor JW Ritchie KB Smith GW 1998 Cause of sea fan deathin the West Indies Nature 394 137ndash138

Giesy JP Kannan K 2001 Global distribution of perfluorooctane sulfonatein wildlife Environmental Science and Technology 35 1339ndash1342

Gillies JA Nickling WG 1996 Dust concentrations and particle-size char-acteristics of an intense dust haze event Inland delta region MaliWestAfrica Atmospheric Environment 30 1081ndash1090

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Hayes ML Bonaventura J Mitchell TP Prospero JM Shinn EA Van DolahF Barber RT 2001 How are climate and marine biological outbreaks func-tionally linked Hydrobiologia 460 213ndash220

Herman JR Krotkov N Celarier E Larko D Labow G 1999 The distribu-tion of UV radiation at the Earthrsquos surface from TOMS measured UV-backscattered radiances Journal of Geophysical Research 10412059ndash12076

Husar R et al 2001 Asian dust events of 1998 Journal of Geophysical Re-search 106 18317ndash18330

Jickells TD 1999 The inputs of dust derived elements to the Sargasso SeaA synthesis Marine Chemistry 68 5ndash14

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Lenes JM et al 2001 Iron fertilization and the Trichodesmium response onthe West Florida shelf Limnology and Oceanography 46 1261ndash1277

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Perry KD Cahill TA Eldred RA Dutcher DD 1997 Long-range transportof North African dust to the eastern United States Journal of Geophys-ical Research 102 11225ndash11238

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Rand GM ed 1995 Fundamentals of Aquatic Toxicology Effects Envi-ronmental Fate and Risk Assessment 2nd ed Washington (DC) Taylorand Francis

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Richardson LL Aronson R 2002 Infectious diseases of reef corals Pages1225ndash1230 in Kasim Moosa MK Soemodihardjo S Nontji A SoegiartoARomimohtarto K Sukarno Suharsono eds Proceedings of the NinthInternational Coral Reef Symposium 23ndash27 October Bali IndonesiaBali(Indonesia) Indonesian Institute of Sciences and State Ministry of Ed-ucation

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Ritchie MPedgley D 1989 Desert locusts cross the AtlanticAtenna 13 10ndash12Rosenfeld D Rudich Y Lahav R 2001 Desert dust suppressing precipitation

A possible desertification feedback loopProceedings of the National Acad-emy of Sciences 98 5975ndash5980

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Shen GT Boyle EA1987 Lead in corals Reconstruction of historical industrialfluxes to the surface ocean Earth and Planetary Science Letters 82289ndash304

Shinn EA Smith GW Prospero JM Betzer P Hayes ML Garrison VHBarber RT 2000 African dust and the demise of Caribbean coral reefsGeological Research Letters 27 3029ndash3032

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Smith GW Ives LD Nagelkerken IARitchie KB 1996 Caribbean sea-fan mor-talities Nature 383 487

Solomon KR 1998 Endocrine-modulating substances in the environmentThe wildlife connection International Journal of Toxicology 17 159ndash171

Swap R Garstang S Greco S Talbot R Kallberg P 1992 Saharan dust in theAmazon basin Tellus 44 133ndash149

Swap R Ulanski S Cobbett MGarstang M1996 Temporal and spatial char-acteristics of Saharan dust outbreaks Journal of Geophysical Research101 4205ndash4220

Syvitski JPM Lewis AG 1980 Sediment ingestion by Tigriopus californicusand other zooplankton Mineral transformation and sedimentologicalconsiderations Journal of Sedimentary Petrology 50 869ndash880

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Torsvik V Goksoyr J Daae FL 1990 High diversity in DNA of soil bacteriaApplied and Environmental Microbiology 56 782ndash787

Turner SM Nightingale PD Spokes LJ Liddicoat MI Liss PS 1996 In-creased dimethyl sulphide concentrations in sea water from in situ ironenrichment Nature 383 513ndash517

Uematsu M Sugita T Anikiev VV Medvedev AN 1992 Large-scale trans-port of pollution aerosol over the east coast of Asia Geophysical ResearchLetters 19 2219ndash2221

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van Dijk HFG Guicherit R 1999Atmospheric dispersion of current-use pes-ticides A review of the evidence from monitoring studies WaterAir andSoil Pollution 115 21ndash70

van Pul WAJ Bidleman TF Brorstrom-Lunden E Builtjes PJH Dutchak SDuyzer JH Gryning SE Jones KC van Dijk HFG van Jaarsveld JA1999 Atmospheric transport and deposition of pesticides An assessmentof current knowledge Water Air and Soil Pollution 115 245ndash256

Venkatesh MV Joshi KR Harjai SC Ramdeo IN 1975 Aspergillosis indesert locust (Schistocerca gregaria Forsk) Mycopathologia 57 135ndash138

Walsh JJ Steidinger KA 2001 Saharan dust and Florida red tides Thecyanophyte connection Journal of Geophysical Research 10611597ndash11612

Weinberg ED 1996 Acquisition of iron and other nutrients in vivo Pages79ndash94 in Roth J et al eds Virulence Mechanisms of Bacterial PathogensWashington (DC) American Society for Microbiology

Weir JR Garrison VH Shinn EA Smith GW 2000 The relationship betweenGorgonian coral (Cnidaria Gorgonacea) diseases and African dustevents Abstracts of the Ninth International Coral Reef SymposiumBali Indonesia October 23ndash27 2000 78

Young RW et al 1991 Atmospheric iron inputs and primary productivityPhytoplankton responses in the north Pacific Global Biochemical Cycles 5 119ndash134

480 BioScience May 2003 Vol 53 No 5

Articles