Pacific Science (1976), Vol. 30, No.2, p. 197-20 5

Printed in Great Brit ain

The Correlation of Soil Algae, Airborne Algae, and Fern Spores withMeteorological Conditions on the Island of Hawaii I

J OHNNY L. CARSON2 AND R. MALCOLM BROWN, JR.2

ABSTRACT : Cor relations of the generic diversity of soil and airborne algae withaltitude on the island of Hawaii are noted. Distribution of the soil algae was deter­mine d by culturing an aqueous soil extract fro m designated altitudes on agarizedinorganic growth media. Distribution of airborne algae and fern spores was deter­mined by investigations of viable particulate impactions on the surface of agarizedinorganic growth media identical to that used in culturing the soil samples.

Lit tle cor relation occurs between the generic dive rsity of the airborne and soilalgae at corresponding altitudes, which suggests a cosmopolitan mixing of air­borne propagules that have been released from different altitudes. However, strikingrelationships were noted in the quantitative determinations of airborne green andblue-gree n algae and of fern spore impactions with the varying meteorologicalconditions of rain, fog -mist, and clear, sunny conditions accompanying thealtitude change.

INTRODUCTION

THE H AWAllAN ISLANDS of the Pacific Oceanare ideal natural sites for many scientific in­quiries, particularly for studies of atmosphericdispersal both of microorganisms and higherplants (Brown 1965, 1971). The advantages ofthe islands for such investiga tions are twofold.First, the islands lie at least 2000 miles fromany major land mass, and the prevalent no rth­east trade winds carry few viab le disseminulesover the many miles of ocean and into theislands. The ability of the marine environmentto " scrub " particulates from the atmospherehas been observed and reported (Glynn 1933,Stepanov 1935, May 1958, Davies 1959, Brown1971, and personal communication). Viableairborne microorganisms have been collectedand cultured from air samples over the islands,suggesting that release and dispersal of theseparticulates is largely an activity of each indi­vidual island (Brown 1971). Secondl y, weatherconditions throughout the islands are highly

I This wo rk was supported in part by a grant fromthe Research Council of the Unive rsity of NorthCarolina to the junior auth or . Manuscript accepted 30No vember 1975.

2 University of North Carolin a, Department ofBotany, Chapel Hill , North Carolina 27514.

uniform and predictable (Jones 1939, Leopoldand Stidd 1949). Such conditions mo re readi lypermit analysis and modelling of dispersalmechanisms and patterns. The trade winds andthe barriers provided by th e topography of theislands con stitute the principle variations inweather conditions (Doty and Muel ler-Dorn­bois 1966). These factors at times result inextreme variations of climate within very shortdistances. Humidity can vary from 0 to 100percent within distances of severa l tens of miles,and temperatu res can vary from 90° F at sealevel to below zero at the summits of tallmountains (Carlquist 1970).

Stud ies of atmospheric dispersal of algaehave receive d greater acknowledgment in re­cent years with concurrent findin gs that air­borne algae and other airborne microbes arecausal agents in inhalant allergie s and otherrespiratory disorders (Hatch 1961; McElhenneyet al. 1962; McGovern, McElhenney, andBrown 1965; Bernstein and Safferman 1966,1970). Extensive studies of airborne fungal andbacterial particulates have been conducte d(Pady and Gregory 1963, Pathak and Pady1965, Pady and Kramer 1967). H owever, it hasbeen shown that algae may be predominantmembers of the aerial flora and that algae areimportant colonizers of isolated land areas

197

198 PA CIFIC SCIE N CE, Volume 30, Ap ril 1976

FIGURE 1. View of Mauna Loa and a portion of the Mauna Loa transect looking no rthwest at app rox imately4000 feet above sea level.

(Brown 1965) and bodies of water (Mag uire1963).

Schlichting's studies (1961, 1964, 1969, 1971)include the collection of viable airborne algaeand protozoa and the correlation of meteoro­logical conditions with th eir dispersal. He notedthe relationship of the aerial biota with themovement of air masses, bu t emphasized agreater correlation of the aerial flora with th emicrometeorological conditions within the airmass.

Hawaii, the " Big Island ," is an excellent siteto investigate the variations among airbo rnealgae with altitude and changin g meteorologicalconditions within short geographical distances.Within a distance of 50 miles is an alti tudinalgradient from sea level to 6500 feet as well asmeteo rolog ical conditions that may vary fromextensive rain downpours at the lower eleva­tions to dry, sunny conditions at the hig heraltitudes. This is due to several features of themeteorological regime of th e island. First,Hawaii, like the other islands of the chain, isinfluenced by orographic rainfall. This is

particularly evident along the no rtheasternHamakua Coast of th e island. Secondly, hig hmo untain masses like Mauna Loa (Figures 1and 2), being very broad and wide, absorbgrea t quantities of heat during the day, form­ing updrafts toward the summit. During theafternoon, air surrounding th e mountains israpidly drawn upward and the moisture it con­tains can be condensed rapidly. This can resultin extensive rainfall on the low er slopes , taper­ing off to light showers higher up , and clearsunny conditions at higher altitudes (Carlquist1970). Finally, the two preceding featu res maybe influenc ed further by the inve rsion layer,which genera lly occurs from 5000 to 7000 feet.Such conditions result in a predictable varia­tion of the soil algal flora. This, in turn, medi­ates the dispersal of biologically significantmaterials with potentia l reproductive capacity.

It is important that inquiries be made intothe nature of dispersal in various geog rap hicaldistances under predictable and consistentmeteorol ogical condi tions. The transect des­cribed here is on the order to 50 miles th rough

Tran sect Route .,. ;;:.

Boundary Hawa ii Vo lcanoesNational Park - - --

MaunaKea 0

13, 7 96'

1000'

~-..... 6500' 2000' :/ .....····

Mauna r-;> ';.:. ,5000' .Lo~ 10 6000 .." 4000' :

13,677 / __I"~ ,"J ..... ·.... 3000

-~

N

I« , II I , ! I

5 0 5 10M i lE S

ISLAND OFHAWAII

FIG URE 2. Map of the island of Hawaii showing the transect route.

15

200

areas of pronounced meteorological changes(Figure 2). A similar scheme has been des­cribed by Brown (1963), which was on theorder of 15 miles and which also ran gedthrough zones of marked meteorologicalchanges.

MATE RIALS AND METH ODS

During the summer of 1971, a transect wasset up on the island of Hawaii from th ecoastal city of Hilo up to 6500 ft on theslopes of Mauna Loa. Soil sampl es werecollected aseptically in sterile plastic bagsfrom the top 1.0 inch of the substrate at1000-ft-altitude intervals and packaged andsent by air to our laboratory at the Uni­versity of North Carolina. There, 5 g of eachsoil sample were suspended in 30 ml of Bold 'sBasal Medi a (BBM) (Brown and Bold 1964),sonicated mildly, and 0.5 ml of the suspensionwas cultured on each of three Petri dishes ofagarized BBM. The cultures were inspectedfor algal generic diversity after bein g incu­bated for 1 mo nth on a continuous light cycleof approximately 7000 lux and 19° C. Duringthe autumn of 1973, the same transect wasmad e; sterile Petri dishes of agarized BBMwere exposed at 500-ft-altitude intervals for1 minute each from an automobile traveling at35 miles per hour from Hilo to 6500 ft onMauna Loa . The air-sampling transect wasmad e two tim es at different hours of the dayunder similar meteorological conditions. Theseplates were incubated for 1 month on a con­tinuous light cycle of approximately 3500 luxand 19° C. Determinations of algal genericdiversity were made as well as quantitativecolony counts of the different taxa of airbornealgae and fern spore impactions as a functionof viable fern gametophytes observed. Resultsare a total of the two exposures made at eachdesignated altitude.

The collecti on sites can be described brieflyby altitude as follows: 0-2000 feet, urban­agricultural (suga rcane); 2000-4000 feet, wetupland forest (Metrosideros-Cibotium); 4000­6500 feet, dry upland forest (Metrosideros­Acacia).

PACI FIC SCIENCE, Volume 30, April 1976

RESUL TS AND DISCU SSIO N

Cultures made from soil samples indicatedthat the greatest generic diversity of the soilalgae occurs at an altitude of 4000 ft (Figure 3).Concurrently with these data, Figure 4 indi­cates that th e generic diversity of airbo rnealgae is also quite high at these altitudes. Thisarea may be considered wet upland forest, andrainfall is sufficient to support a lush growthof many plants (Carlquist 1970). The persis­tence of the orograph ic cloud cover at thisaltitude further enhances the effect of the rain,as little evaporation occurs.

Relatively little correlation is apparent be­tween the generic diversity of the soil algaeand the airbo rne algae at the same altitude. Thegreatest coincidence of generic similarity ofsoil and airborne algae occurs at th e 3000-ftlevel, an area permeated by fog-mist conditions,which may assist in the redepositio n of viableparticulates on a small scale. It seems apparent ,however, that dispe rsal at other altitudes islittle related to the soil flora at that alti tudeand, in fact, that some generic exchange of th eair spo ra between altitudes may occur. Suchan interaltitude exchange of particulates maybe derived from daytime updrafts and convec­tion. The released airborne particles may thenbe washed out or depos ited by other mech­anisms such as gravitation or turbulentdeposition.

An extensi ve downpour occurred at th elower altitudes (1000- 2000 ft) at the time of theair-sampling experiments. However, at alti­tudes of 2500-3000 ft, weather conditions werethose of the fog-mist charact eristic of thisarea. At thos e sampling stations 4000-6500 ftin altitude, conditions ranged from partlycloudy with in termittent sunshine to an almostperfectly clear atmosphere with visibility upto 20 miles.

Quantitativ e counts of the colonies of th eChlorophyceae, Cyanophyceae, and of viablefern spore impactions showed sharp contrastwith changin g meteorological conditions mov­ing up the gradient. Data from the air samples(Figure 5) taken at the lower altitudes (1000­2000 ft) suggest that a fairly quantitative wash­out of viable airborne algae and fern sporesoccurs due to the extensive rainfall. This

Correlation of Algae with Meteorological Conditions- CARSON AND BROWN 201

Alga lGeneraIsol atedf r om t heSoi l

Al ti tude f t

I I I I) 1000 2000 3000 4000 5000 6000

Characium sp

j: rI ': i'[1llllllli':i'lilChl ore lla s p ==_:'k0_=Chl oroeoeeum s p

Gl oe 0 eys ti s spHormi di um s pNannoeh l oris spP_haeo tus s p ~~~Itttttt~~~Pro t oe oe eus s p ~tt~:t~ttt~f ttt~:t~t:~:~:~t r~ttttt~:~:~:~ :~:~:~:fr}~:~:~:~:~:t~

Sti eh oeoee us s p tttt~tt1tt ~~t~tf)j~~tt~;;~Treb ouxi a s p ~tt~~ttttt~~Anabaen a s pHydroeo Ie um spLyngbya s p

~::;:~:~~~:~:~:~:::::~~~~::::...Nos t oe s p ~~~~;~~~ ~~~?~~ttt~~~;~

Phormi di um s p tttt~~ttt~~ tttt~~ttttPie e t one ma s p ttItttr~~rPo l yeys tis s p f~:~:~:~:~:;:r;t:;:~:~:;: ~tttt;~tt~;;~ .;;~tt~;tt~rt~;~Rivulari a s p ttttJtrt~Sey t onema s p ~tt~~t~t~tttTolypo th r i x s p ~:t~~ttt~~tt~:~B0 t r ydi ops is s pMona l l an tus ~tt;t~~t~ttt~spNav i eula s p )rt~tttitTotal Numbe rGene r a 0 f 2 5 4 8 5 4Chl orophy ee aeTotal Numbe rGene ra 0 f 2 2 2 7 4 4Cy an ophy ee aeTot al Numbe rGene ra of 1 1 1 2 1 0Xan th Q£hyee aeTot al Numbe rGene r a of

0 0 0 1 0 0Ba d llari ophy ee ae

F IGURE 3. Variation of generic diversity of soil algae by altitude.

washout has also been demonstrated by arainwater culture on BBM, where quantitativecolony counts of the Chlorophyceae sometimesreached 2000 per ml of cultured rainwater(Carson, unpublished data) .

At altitudes of 2500-3000 ft, viable impac­tions were, in some cases, quite extensive. It isat this altit ude that the orographic fog-mist isso prevalent. Nonlocal viable airborne dis­seminules may be trapped in this fog-misteither by collision or electrostatic attraction tothe water droplets and subse quently deposited.Loca l release of particles is also likely to be

due to splash dispersal from both precipitationand rainw ater dripping from vegetation. Atthis altitude, it is also likely that fern sporescould be deposited easily due to combinedwashing out and gravitation ; but algal dis­seminules under such conditions are morelikely to be released, dispersed, and then re­deposited. These findings coincide with thoseof May (1958), who found that smaller andmore variable droplets of frontal rain removedparticulates more readily than had been previ­ously thought.

At higher elevations (4500-6500 ft), however,

202 PACIFIC SCIENCE, Volume 30, April 1976

Alga lGe ne raCollecte df rom t heAtmo sph e re

Altitude ( ft .))

O1lo re l la s p ,

O1loro co c cum s p .

Oocys ti~ s p .

Pro toco c cus sp .

Hormi dium sp .

Calothrix s p ,

Os ci l l a t o r ia s p ,

Lyngbya s p .

En tophys a l is sp .

Synech ocy s tis sp .

Hona l lan tus s p .

Hon oci li a s p .

000000If"\ 0 If"\If"\ '!> <o

To t al Numbe rGe ne ra ofChLor ophy ce aeTo ta l Numb e rGe ne ra o fCy anophy ceaeTo tal Numbe rGen era o fXan thophy ceae

4

o

o 2 3

032 4

o 0 0 0

2 3 2 0 0 0

4 0 0 0 0 0

0200000

F IGURE 4. Varia tion of generic diversity of airborne algae by altitude.

the potential for release of algal dissemi­nu les decreases with the decreasing mois­ture factor. Furthermore, viable algal impac­tions are correspondingly lower. H owever,it is at this altitude that the greatest numbersof fern spore impactions occur. Furthermore,the fern spore impactions in many cases tookthe form of "clumps," suggesting that suffi­cient moisture was present after release to causesome cohesion among the spores and tha t theirrelease had been recent and local. Thus, thepotential for fern spore release increases atthese altit udes due to the drying of the sporan­gial wall of ferns from the more intense long­wave radiation regime and the resulting warmertemperatures.

In summary, it is clear that distinct systemsof aerial dispersal operate in thi s locality. Tworelease mechanisms function, one which isbasically passive and one which is active. Therelease of algae, some fun gi, and other micro­organisms to the air from the surface of thesoil or vegetation is generally passive, withparticles becoming airborne when the windblowing acro ss the substrate causes desiccationand subsequent release of substrate particlescarrying viable particulates. The splashing byprecipitation droplets of microbial-laden soilparticles is also basically a passive form of dis­pers al. An active release of the biota is mani ­fested by the ferns and pos sibly other crypto­gams such as the Bryophyta, whose spore

Cor relation of Algae with Meteorological Conditions-i-Ca nsox AN D BROW N

Chlorophyceae _ . _ ._ . - . - . -Cyanophyceae .

Xanthophyceae ®Fe rns

40VI

ca

~350Q.

E .a>30L-

aQ.

l/)

c 25L-

a>LL

"tl

520

0OJ

:;( 15

.....a

:U10..cE:;:)

Z5

0....a / .~

2 3 4 5 6

Alt itude (feet x 1000)

203

FIGUR E 5. Total Chlorophyceae, Cyanophyceae, and fern spore impactions by altitude from air samples (to tal oftwo exposed plates).

release may be dependent upon desiccation of asporangium and a concurrent active dehiscence.

The passive dispersal of biological entitiesby splash dispersal obviously requires condi­tions of precipitation for release to occur.However, the release of viable particulatesfrom the surface of soil and vegetation bydesiccation requires the coordinate events ofsubstrate desiccation and pickup by windcurrents . These events clearly occur under clearatmospheric conditions but may also occurunder overcast conditions , provided no pre­cipitation occurs, in which case splash dis­persal is operative . The active dispersal of

fern spores is clearly a function of increasedlocal temperatures, resulting in the desiccationof the sporangial wall with the subsequentexplosive discharge of the sp ores fro m thespo rangium (Figure 6).

It is unlikely that there are differential po int,area, or line sources of airborne algae and otherpassively released biological particles to anysignificant degr ee up to 6000 ft . There is, how­ever, a likelihood of source differentiation interms of the fern flora, as the lower altitudesare dominated by agriculture. One only beginsto note a significant fern flora at approximately2500 ft . The ferns are conspicuous members of

204 PACIFIC SCIENCE, Volume 30, April 1976

FLOW CHART OF DISPERSAL OF AIR-BORNE ALGAE ANDFERN SPORES ON THE I SLAND OF HAWAI I

I SO~CEI- B - _

So i l an d Vege ta t ion(Al gae)

De s icca t i on o f s o ur ces ubstra tes withs ubsequen t re l eas e ofpropag ul e c on ta i ni ngs ubs t ra t e par t i c l es

Desi cc at i on o f sp o rangia lwal ls and ballis t icdisc harge of s por e s

De pos it io n due t omtc rome t e or o l ogi calparamet e rs

FIGURE 6. Flow chart of the dispersal of airborne algae and fern spores on the Mauna Loa transect.

the flora on the upper reaches of the transect,although this may not be true for the island as awhole.

The consistent local meteorological condi­tions of the tropics make models such as thispredictable with reproducible results as indi­cated in studies by Brown (personal communi­cation) on Haleakala, Maui, and by Carson(unpublished data) on the Nuuanu Pali,Oahu. The transect of this study is dominatedthroughout the year by the meteorologicalscheme previously outlined except during someperiods of frontal weather, which generallyoccur during the winter months (Daingerfield1921). It should be noted that the data pres­ented here do not constitute an absolutequalitative or quantitative value but ratherprovide a representation from both soil andair samples which indirectly reflects the biota inthe soil, the airborne flora, and the mechanismsby which dispersal may occur.

I t is the goal of aerobiological studie s suchas these to design both conceptual and mathe­matical models which illustrate the entire scopeof dispe rsal and coloni zation of biologicallysignificant materials in a given area. Figure 6 isgiven as such a conceptual model of the aero­biological features on thi s particular transect .

ACKNOWLEDGMENTS

The authors wish to convey their sincereappreciation to D rs. Maxwell D oty and GladysBaker of the D epartment of Botany, Universityof Hawaii, who graciously provided laboratoryspace, facilities, funds, and thei r time for thisresearch . The authors are also deeply gratefulto those private individuals who helped financethis research and to the First Baptist Church ofBlack Mountain, North Carolina, which sup­ported this research through a scholarship.The authors are also indebted to the followingpersons for their help in many ways: Mrs.Shirley Carson, Ms. Chris Hanson, Ms. EstherHsiao, and Mr. and Mrs . Walter Quensell.

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- - - . 1964. Meteorological conditions affect­ing the dispersal of airborne algae and pro­tozoa. Lloydia 27(1): 64-78.

---. 1969. The imp ortance of airborne algaeand protozoa. Air Pollu t. Con trol Asso c. J.19 (12): 946-951.

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