731

J. Phycol.

37,

731–737 (2001)

ROLE OF ULTRAVIOLET RADIATION IN MAINTAINING THE THREE-DIMENSIONAL STRUCTURE OF A CYANOBACTERIAL MAT COMMUNITY AND

FACILITATING NITROGEN FIXATION

1

Richard P. Sheridan

2

Division of Biological Sciences, University of Montana, Missoula, Montana 59812

Cyanobacterial mat communities were collectedin the mangrove forest bordering the Grand Cul deSac Marin, Guadeloupe, French West Indies, whichsupports a community of nitrogen fixing cyanobacte-rial mats established on the trunk and branches ofblack mangrove (

Avicennia germinans

L.). This studypresents results that are focused on the mat commu-nity and the physiological and morphological adapta-tions to UV radiation. The dominant surface speciesof the mat,

Nostoc

cf

commune Vaucher

and

Scytonema

sp., possessed the UV-shielding pigment scytonemin.Mats grown on medium D agar without nitrogen underphotosynthetically active radiation (PAR) only, rapidlybecame disorganized compared with those exposed to

PAR

�

UV-A (320–400 nm)

�

UV-B (280–320 nm) ir-radiation. Concurrent with disorganization, acetylene

reduction activity (ARA

�

one third of N

2

reduction)was severely reduced, whereas mats irradiated withPAR

�

UV-A

�

UV-B maintained high ARA activity.Mats incubated for 27 days under PAR

�

UV-A

�

UV-B then exposed to PAR only exhibited a 68% stimu-lation of ARA, whereas ARA values were 33% inhib-

ited in mats incubated with PAR only and thenexposed to PAR

�

UV-A

�

UV-B. This favorableequilibrium was facilitated by the mats’ three-dimensional structure in which the most UV-resistantspecies,

N. commune

, covers the surface with UV-sen-sitive species below this protective covering. The UVstressor was essential for the maintenance of matstructure and ARA.

Key index words:

Community structure; cyanobacteria;nitrogen fixation; ultraviolet

Abbreviations:

ARA, acetylene reduction activity; PAR,photosynthetically active radiation; UV-A, ultravioletA (320–400 nm); UV-B, ultraviolet B (280–320 nm);

UVR, ultraviolet radiation

Highly productive mangrove communities occupy75% of tropical coastlines (Zuberer and Silver 1978).These coastal lowlands are often nutrient limited(Ryther and Dunstan 1971). This apparent paradoxof high productivity and low nutrients can be ex-plained in part by facilitation between mangrove spe-cies and nitrogen fixing cyanobacteria. I reported the

occurrence of aerial nitrogen-fixing cyanobacterialmats established on black mangrove (

Avicennia germin-ans

) trunks and branches that potentially contributeabout 42 g N

�

m

�

2

�

y

�

1

to the Canal Perrin mangrovecommunity, Guadeloupe, French West Indies (Sheri-dan 1991). Studies concentrating on nitrogen fixationin mangal community substrate muds have also beenpresented (Gotto and Taylor 1976, Zuberer and Silver1978, Potts 1980, van der Valk and Attiwill 1984, Hicksand Silvester 1985).

The Canal Perrin receives high intensity photosyn-thetically active radiation (PAR) and UV radiation(UVR, 280–400 nm). Both UV-A and UV-B inhibitedalgal photosynthesis (Lorenzen 1979, Holm-Hansen1990). UV-B reduced the rate of chl synthesis andCO

2

fixing enzyme concentrations (Lesser et al. 1994).

Calothrix

exposed to natural UVR over a 3-month pe-riod maintained high levels of scytonemin, and thesecells resisted UV inhibition of photosynthesis (Bre-nowitz and Castenholz 1997). Bothwell et al. (1994)noted that communities of attached algae protectedfrom UVR had a reduced standing crop comparedwith those communities exposed to natural UV inten-sities. This paradox resulted from the inhibitory effectof UV on the larval chironomid consumers. The re-sults of this study emphasize the difficulty of predict-ing the impact of UVR and the importance of an eco-system approach to understanding the effects of futureUV increases.

UV-absorbing pigments provide cyanobacteria withpartial protection from UV. The UV-absorbing pig-ment scytonemin has an

in vivo

absorption maximumat 370 nm and was shown to be part of a strategy foradaptation to short-wavelength radiation (Garcia-Picheland Castenholz 1991, Garcia-Pichel et al. 1992). An-other group of pigments, the mycosporine-like aminoacids, protect against UV-B (Garcia-Pichel and Casten-holz 1993, Neale et al. 1998). Carotenoid pigmentsmay also confer UV photoprotection to chl

a

biosyn-thesis (Asato 1972, Abeliovich et al. 1974, Buckley andHoughton 1976, Hirosawa and Miyachi 1983, Paerl1984, Tytler et al. 1984).

This article presents studies focused on the matcommunity and the physiological and morphologicaladaptations to UV that protect physiological functionsin a UV-stressed environment. Central to these studiesis the possible role of UV as an ecological forcingagent that controls the three-dimensional structure ofcyanobacterial mat communities and the resultantchemical and light quality gradients of the mat micro-

1

Received 13 August 1999. Accepted 22 May 2001.

2

Author for correspondence: e-mail sheridan@selway.umt.edu.

732

RICHARD P. SHERIDAN

environment. I hypothesize that long-term exposureto tropical UV fluence rates has resulted in physiolog-ical and mat structure adaptations that confer surviv-ability to the cyanobacterial constituents of the mat.The spatial orientation of UV-resistant species at themat’s surface provides protection to the UV-sensitivespecies located in the deeper mat layers. This commu-nity structure facilitates nitrogen fixation in a UV-stressed environment.

materials and methods

Biogeographical distribution of cyanobacterial mats in mangal com-munities.

I conducted a survey of nine islands in the CaribbeanArchipelago and identified four with coastal forests in whichblack mangrove (

A. germinans

) hosted epiphytic cyanobacterialmat communities. These were located in Guadeloupe (GrandeCul de Sac Marin, Pointe De La Saline, and Port d’Enfer), St.Martin (South Orient Bay), Tobago (Bon Accord Swamp), andTrinidad (Coroni Swamp).

Study site.

The Canal Perrin mangrove community is locatedon the French West Indian island of Guadeloupe (16

�

40

�

N,61

�

10

�

W). Red mangrove (

Rhizophora mangal

) fringes the openwater of the Grand Cul de Sac Marin. Between 150 and 375 minland, a mixed forest of red and black mangrove (

A. germin-ans

) is present. The trunks and fine branches of black man-grove are covered with a dense, gelatinous, dark olive-coloredmat of cyanobacteria (Sheridan 1991, 1992).

Mean values (

n

�

27) for subcanopy PAR (400–700 nm)and UVR (280–400 nm) from September through December1998 were as follows: PAR, 169 W

�

m

�

2

(range, 3.0–366); UV-A(320–400 nm), 7.50 W

�

m

�

2

(range, 0.21–17.2); and UV-B (280–320 nm), 0.37 W

�

m

�

2

(range, 0.041–0.87). Light intensity mea-surements were recorded between 1100 and 1300 h.

Sampling.

Mat samples were collected from 10 randomly se-lected black mangrove trees between 200 and 300 m along myestablished transect line (Sheridan 1991) in a mixed red andblack mangrove community. Mats were harvested intact by cut-ting the bark with a scalpel, air dried, and returned to the Uni-versity of Montana. Dried cyanobacteria retain their viability forlong periods of time (Potts 1994).

Laboratory culture.

Primavera tissue culture flasks (no. 3813,Falcon, Becton Dickinson Labware, Franklin Lakes, NJ) with avolume of 67 mL were used for the long-term incubation of themat samples. The 4

�

8.5-cm surface window was removedfrom the flasks and replaced with the following filters: 1) PAR

�

UV-A

�

UV-B passing cellulose diacetate (DIACETATE, Ca-dillac Plastic & Chemical Co., Spokane, WA); 2) UV-B absorb-

ing, PAR

�

UV-A transparent biaxially oriented polyester(CADCO A/S polyester, Cadillac Plastic & Chemical Co.); and3) UV-A

�

UV-B absorbing, PAR transmitting UF-5 styrene(Plexiglas MC #14B199, Atohaas, Philadelphia, PA) filters(Fig.1). Transmittance was monitored after each experimentalperiod using a Shimadzu MPS 50L recording spectrophotome-ter (Shimadzu Corp., Kyoto, Japan), and each experiment be-gan with new filter material. The exterior sides and bottom ofthe flasks were painted black to prevent the entrance of unfil-tered wavelengths of light.

Mats were first rehydrated with liquid medium D withoutcombined nitrogen and then placed on 1% agar plus mediumD (Castenholz 1988) minus combined nitrogen. Each flask con-tained four 7

�

30-mm mats. Acetylene reduction activity(ARA) was determined for three mats, whereas the fourth wasreserved for SEM analysis. Three separate replicates of fourmats each were incubated. There were three blocks of threelight treatments with each treatment tested for ARA from day17 to day 27, resulting in five consecutive ARA determinations.Flasks fitted with each of the three filter types (Fig. 1) were ex-posed for 27 days at 27

�

C to the illumination regime describedbelow. The photoperiod was 12:12-h light:dark, which was com-parable with that experienced at the latitude of Guadeloupe.ARA measurements were taken between 6 and 8 h after the on-set of illumination.

Laboratory PAR and UV sources.

The source of PAR was fromGeneral Electric Very High Output cool white fluorescentlamps (General Electric, Fairfield, CN), UV-A from Sylvaniablack light fluorescent lamps (peak output 365 nm, range 310–405 nm, Osram Sylvania, Danvers, MA), and UV-B radiation fromWestinghouse FS-40 fluorescent lamps (peak output 310 nm,range 280–360 nm, Westinghouse Electric Co., Columbia, SC).Irradiation sources were enclosed in a temperature-controlledchamber set to the mean Canal Perrin temperature of 27

�

C. PARand UV fluence rates were adjusted to ecologically relevant man-grove subcanopy values (PAR, 130 W

�

m

�

2

; UV-A, 5.8 W

�

m

�

2

;UV-B, 0.30 W

�

m

�

2

). PAR and UV measurements were taken withthe sensor placed at the level of the culture flask. Fluorescent UVsources used in laboratory experiments may not mimic the bal-ance of DNA and photosynthesis damaging natural solar radia-tion (Cullen and Neale 1997).

PAR, UV, and temperature detectors.

An International Light (New-buryport, MA) IL-1700 radiometer was used to measure UV.Detector selection and the calibration of that detector are twocritical parameters. UV-B detection used the InternationalLight UV-B detector SED 240/UVB-1/W (265–310 nm), whichwas calibrated using the preferred broad band SOL calibrationtechnique. SOL UV-B sensor calibration uses a calibrationsource from International Light that matches the solar spec-trum between 280 and 330 nm. This precise calibration source

Fig. 1. Percent transmittance vs.wavelength (nm) of the cellulose diac-etate, polyester, and UF-5 filters usedin the experimental treatments.

UV AND MAT STRUCTURE

733

replaces the less precise single point calibration procedure inwhich a single narrow wavelength band was used to calibrateUV-B sensors. UV-A detection used the International Light SED033/UVA/W (330–375 nm) detector calibrated by the singlepoint method. The single point calibration method is accept-able for the UV-A sensor because the band is relatively flat com-pared with the 10

4

-fold change in energy over the UV-B band.PAR photon flux density (400–700 nm) was recorded using aLi-Cor (Lincoln, NE) Quantum Sensor LI-190SA and a Li-Cor1000 datalogger. The datalogger was programmed for simulta-neous photon flux density and thermocouple temperature datalogging. The internal incubation flask temperature was re-corded hourly.

ARA.

Quartz cuvettes (UV-B treatments, 8 mL, Beckman Co.,Fullerton, CA) or UV transmitting plastic fluorometric cuvettes(UV-A and PAR treatments, 8 mL, Whatman Co., Tewksbury,MA) sealed with a rubber septum were used to determine theARA. Mat samples were withdrawn from the incubation Primav-era flasks and placed in the cuvettes. The cuvettes were injectedwith 10% v/v acetylene (calcium carbide/H

2

O), placed in theculture cabinet, and covered with one of three UV filters (Fig. 1).Incubation time was 1 h at the PAR and UV fluence rates usedduring culture. ARA determinations used the acetylene reduc-tion technique (see Sheridan 1991, 1992; limitations and pre-cautions relevant to the application of this assay are discussed).

Data collection and preparation of mats for SEM.

After exposurefor 27 days to PAR, PAR

�

UV-A, or PAR

�

UV-A

�

UV-B, in-tact mats on bark were fixed in 3% glutaraldehyde (pH 7.1),rinsed in buffer (pH 7.1), and dehydrated in a series of solu-tions having increasing ethanol concentrations. Mats were criti-cal-point dried, mounted on aluminum stubs with double-stickcellophane tape, and sputter coated with gold-palladium. Pre-pared mats were viewed using a JOEL 35CS scanning electronmicroscope. Surface photographs were taken at random. Mat sur-face disruption by subsurface species was quantified by placinga grid on the SEM screen and counting filaments per 16-

m quad-rats from random sections of the mat (magnification

�

780).

Pigment absorption spectroscopy.

Mat species in unialgal culture(separated by serial streaking on agar

�

medium D) wereplaced between two quartz plates. The

in vivo

absorption spec-troscopy of these samples was determined over the range of300–400 nm using a Shimadzu MPS 50L spectrophotometer.

results

Cyanobacterial mat structure.

The mat surface layer iscomposed of

Nostoc cf. commune

Vaucher and

Scytonema

sp. Located beneath these in a gelatinous matrix are

Microcystis littoralis

(Hansg.) Forti along with

Gloeothece

sp.,

Chroococcus

sp., and two species of

Phormidium

(Desikachary 1959). The subsurface species are notarranged in distinct layers but are intermixed.

Alteration of mat morphology.

Mats incubated (Fig. 2)for 27 days in tissue culture flasks were exposed toPAR only, PAR

�

UV-A, and PAR

�

UV-A

�

UV-Bwavelengths. Mats were periodically tested for ARAin cuvettes irradiated with the same light regime asused during incubation or tested in darkness. Statis-tical comparisons used only ARA values for days 17through 27 during which time nitrogenase activityhad attained equilibrium (Fig. 2). Mats irradiated withPAR

�

UV-A

�

UV-B during long-term incubationhad illuminated ARA values that exceeded those forPAR

�

UV-A treatment by 4.7 and the PAR-only treat-ment by 3.0. Data were analyzed using block analysisof variance (ANOVA) with repeated measures of ARAthrough time. ARA values for mats treated with PAR

�

UV-A

�

UV-B were significantly different (

P

0.001)from those incubated with PAR

�

UV-A and PARonly. The PAR

�

UV-A ARA values were not signifi-cantly different from those treated with PAR-only.

Dark ARA values for PAR

�

UV-A

�

UV-B treatedmats were significantly different (

P

0.001) from thePAR-only treatments, but they were not significantlydifferent from PAR

�

UV-A irradiated mats (blockANOVA with repeated measures of ARA through time).When light versus dark ARA values within the sameUVR treatment set were compared, mats irradiatedwith PAR

�

UV-A

�

UV-B and PAR-only had valuessignificantly different from each other (

P

0.005),whereas the PAR � UV-A treated mats were not signif-icantly different (Mann-Whitney nonparametric test).

SEM micrographs of mat surface. SEM micrographsshow the crenulated polysaccharide mucilaginous nod-ules of N. commune (Fig. 3, A and B). The surfacestructure of mats irradiated for 27 days (Fig. 2) with

Fig. 2. Mean ARA (n � 9) for Ca-nal Perrin mats exposed for 27 days toPAR � UV-A � UV-B, PAR � UV-A,and PAR-only at 27� C. The photope-riod was 12:12-h light:dark.

734 RICHARD P. SHERIDAN

PAR � UV-A � UV-B wavelengths (Fig. 3B) retainedthe surface structure characteristics of mats that devel-oped under field conditions in the Canal Perrin man-grove community (Fig. 3A). Mats irradiated with PARonly rapidly exhibited changes in structure (Fig. 3D).Mats irradiated with PAR � UV-A also exhibited mod-ification of their surface structure (Fig. 3C). Nostoccommune, which dominates the surface of mats adaptedto field PAR and UV fluence levels, was rapidly (3–8days) displaced by trichomes of Phormidium cf. tenueerupting through the surface mucilage of N. commune(SEM micrographs, Fig. 3, C and D). Table 1 showsthe degree of mat surface disruption for each of thethree irradiance treatments and presents a compari-

son of these with control mats collected in the CanalPerrin mangrove community. Laboratory cultures ex-posed for 27 days to PAR � UV-A � UV-B and field-collected controls exhibited intact mat surfaces. One-way ANOVA showed that these had statistically similar(P 0.001) numbers of eruptive filaments (Table 1).In contrast, mats grown under PAR-only and PAR �UV-A had surfaces highly disrupted by emergent fila-ments. The number of erupted filaments (Table 1)for each were statistically different (P 0.001; one-way ANOVA) from each other and from the PAR �UV-A � UV-B irradiated mats and field sampled con-trol mats.

Physiological effects of mat disorganization. ARA valuesfor mats irradiated with PAR only, PAR � UV-A, andPAR � UV-A � UV-B were measured periodically overa 27-day period (Fig. 2). ARA values were determinedfor mats incubated beneath each of the three filtersand then exposed for 1 h to the following UV wave-lengths. Mats having received long-term (27-day) ex-posure to PAR � UV-A � UV-B and then exposed toPAR-only were stimulated 68% (Table 2). The ARAvalues for mats conditioned with PAR � UV-A were re-measured after incubation with PAR-only and exhib-ited a 62% stimulation. ARA values for mats previously

Fig. 3. Scanning electron microscope (�780) photomicrographs of intact Canal Perrin mats cultured under three UV conditions(A, field conditions Canal Perrin; B, PAR � UV-A � UV-B; C, PAR � UV-A; D, PAR-only). Reference line on micrograph D � 10 m.

Table 1. Mean (n � 40) values for the number of filaments per16-m grid (�780) erupting through the surface of cyanobacterialmats grown for 27 days under several light regimes.

Treatment PAR PAR � UV-APAR � UV-A

� UV-BControl(field)

Number of filaments 4.02 8.35 0.20 0.35SE 0.266 0.308 0.091 0.150

Control field samples were collected in the Canal Perrinmangrove community.

UV AND MAT STRUCTURE 735

exposed to PAR-only were inhibited by 33% when ex-posed to PAR � UV-A � UV-B.

Cyanobacterial mats may become anaerobic aftersun down. Non-heterocystous cyanobacterial speciesmay be induced to fix nitrogen by anaerobic incuba-tion (Stal 1995). To test for inducible nitrogen fixa-tion, dark ARA values were determined for mats afterincubation for 3 h in an atmosphere of air or nitrogen(Table 3). Mats previously irradiated with PAR �UV-A � UV-B for 27 days (Fig. 2) had the highestdark ARA values in N2, followed by those irradiatedwith PAR � UV-A and PAR-only, respectively. The dif-ference between sets was significant at the P 0.001level (one-way ANOVA) except between those matsthat had previously been exposed to PAR � UV-A andPAR-only. The dark aerobic ARA values for matsincubated with PAR-only, PAR � UV-A, and PAR �UV-A � UV-B were significantly different (P 0.005;one-way ANOVA), but ARA values for the PAR �UV-A � UV-B versus PAR-only irradiated mats werenot significantly different. The percent difference be-tween dark aerobic and anaerobic ARA values was low-est for the PAR � UV-A � UV-B incubated mats,higher for PAR � UV-A, and highest for the PAR mats.

UVR absorbing pigments. Unialgal cultures of mat spe-cies grown at 29� C and 130 W�m�2 cool white fluores-cent in medium D plus N were tested for UV absorb-ing pigments. The gold-colored pigment in N. communeand Scytonema sp. had the characteristic scytonemin invivo absorption peak (Fig. 4) at 374 nm (Garcia-Picheland Castenholz 1991). The remaining five mat specieslacked the identifying peak.

discussionAn ecosystem level UV impact study (Bothwell et

al. 1993) used the experimental protocol of allowingnatural recruitment of river diatoms onto artificialstream substrates. Reduced growth by UV-B sensitiveherbivorous species resulted in the alteration of com-munity structure (Bothwell et al. 1993). Mats com-posed of Lyngbya cf. aestuarii and Microcoleus chthono-plastes were described for an Australian intertidal matcommunity. Scytonemin, mycosporine-like amino ac-ids, and pterins were present in the sheath of L. cf. aes-tuarii, which protected the benthic community below(Karsten et al. 1998). No studies have been publishedconcerning the role of UVR as a stressor in control-ling the long-term three-dimensional structure ofcomplex mat communities.

The results of ARA studies presented here showedthat the potential nitrogen contribution to the cyano-bacterial mat and, in turn, to the mangal community(Sheridan 1991) was directly related to the structureof the cyanobacterial community. Intact Canal Perrincyanobacterial mats were irradiated with PAR, PAR �UV-A, and PAR � UV-A � UV-B radiation. Nitrogenfixation remained high in mats irradiated with PAR �UV-A � UV-B. Compared with these, PAR � UV-A ir-radiated mats exhibited reduced rates of nitrogen fix-ation, and mats protected from UVR had the lowestrates.

SEM micrographs showed that the uniform muci-laginous surface layer formed by N. commune for matsirradiated with PAR � UV-A � UV-B was severely dis-rupted by the filaments of Phormidium sp. A when themat was irradiated with PAR-only and PAR � UV-A.Accelerated growth by the UV-sensitive species Phor-midium sp. A in the absence of UVR or UV-B wasnoted as one mechanism resulting in the alteration ofthe mat’s three-dimensional organization. I speculatethat motility (Häder and Liu 1990) and growth (Calkinsand Thordardottir 1980, Ekelund 1990, Häder andLiu 1990, Ekelund and Bjorn 1990, Vernet 1990, Häderand Worrest 1991, Grobe and Murphy 1994) were im-paired by UVR in the Canal Perrin mats. Negativephototaxis responses to UV-A (Garcia-Pichel and Cas-tenholz 1994) and UV-B (Donker and Häder 1991,Donker et al. 1993) have been described. Upward mi-gration by Oscillatoria cf. laetevirens and Spirulina cf. sub-salsa occurred under low intensity illumination anddarkness, but upward motility was inhibited by UV-Aabove �1.5 W�m�2, UV-B as low as 0.1 W�m�2, and vis-ible light above �100 W�m�2 (Kruschel and Casten-holz 1998).

Nostoc commune dominates the surface of the CanalPerrin mat along with Scytonema sp. These two spe-cies have the UV photo-protecting pigment scytone-min (Garcia-Pichel and Castenholz 1991, Proteau etal. 1993). Aerobic (air) nitrogenase activity measuredunder laboratory conditions in darkness was lowestfor the Canal Perrin mats incubated 27 days with PAR �UV-A illumination, higher in PAR, and highest in

Table 2. Mean (n � 4) ARA as ppm C2H4�cm�2�h�1 for intactmats exposed to three different light regimes for 27 days (Fig. 2experiments) and then transferred to experimental treatmentsand incubated for 1 h.

Treatment Fig. 2,27 days

Experimentaltreatments % Change P values

PAR � UV-A � UV-B, 1234

PAR only, 2072 68% stimulation �0.001

PAR � UV-A, 173 PAR only, 277 62% stimulation �0.001PAR only, 126 PAR � UV-A �

UV-B, 10433% inhibition �0.05

P values are paired t test.

Table 3. ARA for Canal Perrin mats previously exposed tothree irradiation regimes for 27 days (Fig. 2 experiments)before the ARA measurements shown.

Treatment PAR � UV-A � UV-B PAR � UV-A PAR

Dark-N2 456 (37.26) 68.3 (12.81) 56.5 (6.61)Dark-air 1080 (51.5) 317 (26.5) 865 (87.33)% difference

(air to N2) �51.4 �73.5 �93.4

Mats were incubated in darkness with an air or nitrogenatmosphere. Mean (n � 4), SE in parentheses.

736 RICHARD P. SHERIDAN

PAR � UV-A � UV-B incubated mats. Reduced darkaerobic nitrogen fixation rates for PAR and PAR �UV-A irradiated mats did correlate in a general waywith the disruption of the mat’s surface and subse-quent loss of the heterocystous species N. commune tocompetition by UV-sensitive species.

Heterocystous species usually decrease or ceasenitrogenase activity in the dark (Mullineaux et al.1981, Stal and Krumbein 1985a,b, Griffiths et al.1987). Non-heterocystous species fix nitrogen in dark-ness, which avoids photosynthetically generated oxy-gen (Mullineaux et al. 1981, Stal and Krumbein1985a). However, during field studies at the CanalPerrin study site, the cyanobacterial mats exhibitedappreciable dark nitrogenase activity (Sheridan 1991).In experiments designed to restore the effect ofanaerobic compartments, the mats previously con-ditioned for 27 days with PAR, PAR � UV-A, andPAR � UV-A � UV-B were incubated in darkness witha nitrogen atmosphere for 3 h. However, the highestanaerobic (N2) ARA was measured for the PAR �UV-A � UV-B irradiated mats, with lower ARA valuesfor PAR � UV-A and PAR-only irradiated mats. ARAvalues correlated with mat disruption by competingspecies. I interpreted the dark anaerobic ARA resultsas an increased dependence by nitrogenase on aero-bic metabolism in those mats exhibiting disruptedthree-dimensional architecture. Long-term adapta-tion to UVR by the mat community provides a stablesurface layer of N. commune that confers protectionto UV-sensitive species deep within the mat. The in-tact mat may also facilitate nitrogen fixation by non-heterocystous cyanobacteria within anoxic compart-ments.

Bothwell et al. (1993) reported that paradoxically aUV irradiated experimental benthic algal communityexhibited a higher biomass than those protected fromUVR due to UV inhibition of chironomid consumeractivity. Here, I report another paradoxical effect ofUV in that those cyanobacterial mats exposed to UVRmaintained greater ARA activity than those protectedfrom UV-A and UV-A � UV-B.

Conclusions. The architecture of mats grown underPAR-only and PAR � UV-A were rapidly altered ascompared with those exposed to PAR � UV-A � UV-Birradiation. Concurrent with disorganization, nitro-gen fixation was severely reduced, whereas mats irra-diated with PAR � UV-A � UV-B maintained high lev-els of nitrogenase activity. The structure of the matunder PAR � UV-A � UV-B limits the extent of dam-age and probably favors repair mechanisms. There ap-pears to be an equilibrium between UV tolerance con-ferred by maintaining mat infrastructure and damageto cell processes. The net result of this equilibrium fa-vors survival of the mats and their nitrogen contribu-tion to the Canal Perrin mangal community. The re-sults raise the broader question concerning the roleof UVR as a stressor controlling the structure of othermicrobial and higher plant communities.

Supported by a National Science Foundation grant no. IBN-9709033. Appreciation is expressed to Professor Bill Granathfor SEM preparations and to Michelle Brown for expert field as-sistance. My host at the Laboratoire de Biologie et Végétales,Université des Antilles et de la Guyane, Guadeloupe, FrenchWest Indies, Professeur Jacques Portécop, and colleague Pro-fesseur Daniel Imbert played important roles during the courseof this study.

Fig. 4. In vivo absorption spectra ofunialgal preparations showing character-istic peaks of scytonemin in Nostoc com-mune (upper) and Scytonema sp. (lower).

UV AND MAT STRUCTURE 737

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