Marine biology

Transmission of solar ultraviolet radiation throughinvertebrate exteriors

DENEB KARENTZ and THOMAS GAST, Department of Biology, University of San Francisco, San Francisco, California 94117-1080

The occurrence of springtime ozone depletion over theAntarctic has created concern about the effects of

increased ultraviolet-B [UV-B, 280-320 nanometers (nm)] onmarine organisms (Karentz 1991, 1992). It is not known, how-ever, how much UV-B antarctic marine organisms areexposed to, nor how much irreparable damage UV-B expo-sure can cause. One area of research associated with thesequestions is directed toward identifying ways in which marineinvertebrate species are naturally protected from UV expo-sure. The obvious first line of defense that an animal has tosolar radiation exposure is its outer covering. Although someantarctic invertebrates live under rocks, in deep water, or inother low-light environments, many individuals in benthichabitats are exposed to UV-B radiation for extended periodsof time. UV-B wavelengths have been detected to at least 60meters (m) in antarctic waters (Smith et al. 1992), and biologi-cal effects have been monitored to 20 m (Karentz and Lutze1990; Heibling et al. 1992; Smith et al. 1992). Therefore, inter-tidal and subtidal populations are potentially exposed to bio-logically significant levels of UV-B.

Four species of antarctic invertebrates have been evaluat-ed to determine the amount of UV protection provided bytheir external covering. These taxa are common in intertidaland subtidal regions of the Antarctic Peninsula. Animals werecollected in Arthur Harbor (Antarctic Peninsula) and immedi-ately dissected for use. The four species examined were thesea urchin Sterechinus neumayeri, the sea star Odontastervalidus, the limpet Nacella concinna, and the tunicate Cnemi-docarpa verrucosa. Both the sea urchin S. neumayeri and thesea star 0. validus have a thin epidermal layer that is externalto a calcareous skeleton and the body wall. The epidermalcells of these echinoderms have no protective covering toreduce IJV exposure. The body of the limpet N. concinna iscompletely covered by a dorsal shell that has a structure typi-cal of other limpets, consisting of a complex layering of pro-teinaceous and calcareous compounds. The body of the tuni-cate C. verrucosa is enclosed by a thick outer layer of fibrouscellulosic material known as the tunic.

UV transmission was monitored using a biologicaldosimeter based on a DNA-repair-deficient strain ofEscherichia coli (CSR06) (Karentz and Lutze 1990). Thedosimeter consists of a liquid culture of E. coli cells packagedin JJV transparent polyethylene bags (Whiripak). Half of the

dosimeters were wrapped in one layer of polyester film (MylarD), which filters out wavelengths in the UV-B region. Pairs ofdosimeters, with and without Mylar filters, were incubatedunder sections of shell, tunic, or body wall for 6 hours on 4December 1991 (1130 to 1730 Greenwich mean time). Therewere three replicate samples for each species and triplicateplate counts for each dosimeter. The dosimeters and animalcovers were held in the same plane on an opaque surface andsubmerged a few centimeters in an outdoor flowing sea-watertank at Palmer Station. Water was pumped directly fromArthur Harbor. Survival of the dosimeter cells was calculatedrelative to a dark control (= 100 percent survival). When theUV-B portion of the solar spectrum is removed, survival isenhanced (figure 1). By comparing cell survival under totalsunlight exposure to survival under the minus UV-B (withMylar) treatment, the contribution of UV-B to the killing ofcells can be quantified. With no penetration of harmful solarradiation, cells would have 100 percent survival (same num-ber of viable cells as the dark control).

Analysis of dosimetry results indicated that the externalcoverings of all four species transmit biologically harmfulwavelengths of solar radiation (figure 2). Differences wereobserved between individuals and between species. Theremoval of UV-B wavelengths with Mylar filters increased sur-vival, indicating that LW-B wavelengths do penetrate the exte-rior surfaces of these organisms and that internal organs andcells are subjected to UV-B exposure.

Incident solar radiation data were obtained from theNational Science Foundation UV Monitoring Network (figure3). The scanning spectroradiometer at Palmer Station per-forms one wavelength scan per hour. To provide a standardmeasure of the biological effects of the incident solar radia-tion field, one pair of dosimeters (with and without a Mylarfilter) was exposed to ambient sunlight while shielded by fivelayers of neutral-density screen (figure 2). The layers ofscreening reduced the exposure fluence to 3 percent of theincident radiation. This was necessary because of the highsensitivity of the CSR06 cells to UV-B.

The transmission of IJV-B through the outer coverings ofthese invertebrate species is relatively low, generally less 3percent of incident radiation fluences. However, the damagecaused by prolonged exposures during 24-hour antarctic daylengths is unknown. This study has established that UV-B

ANTARCTIC JOURNAL - REVIEW 1993113

( full solar radiationdiation minus UV-B

10-600 nm

0-400 nm

)0-320 nm

100-) =noUVtranmission 21 f II

UV-B

123time (h)

100

80

-60>2:U)

40

20

100000

- 10000EC-)

-,10000)C-)C0)-100

101000 1200 1400 1600 1800

time (GMT)

Figure 1. Survival characteristics of Escherichia coil (strain CSR06)under ambient antarctic radiation: full solar radiation and solarradiation minus UV-B wavelengths.

(

a)C1

123123123123

CnemidocarpaNacellaOdonlacierSterechinus3%vetnicosaconcinnavalidusneumayeri

incidenttunicatelimpetsea starsea urchinradiation

Figure 2. UV transmission through the exteriors of four antarcticinvertebrate species as determined by biological dosimetry. Eachpair of bars represents one animal (three animals tested for eachspecies). Absence of bars indicates 100 percent killing of dosimetercells (that is, Cnemidocarpa verrucosa 1). The two bars at the farright represent the lethality of 3 percent incident radiation on thedosimeter cells during the course of the experiment.

Figure 3. Instantaneous hourly values of solar fluence during thecourse of the incubations (data for 1400 to 1600 are missing). Datawere obtained from the National Science Foundation UV MonitoringNetwork. Values reflect broad-band integrations of scanned data.(iW cm-2 denotes microwatts per square centimeter.)

wavelengths do penetrate the outer layers of adult inverte-brates. Subsequent investigations need to be conducted todetermine the extent of internal photodamage.

I. Bosch and M. Slattery assisted in this work. Researchwas supported by National Science Foundation grant OPP 90-17664.

References

Heibling, E.W., V. Villafahe, M. Ferrario, and 0. Holm-Hansen. 1992.Impact of natural ultraviolet radiation on rates of photosynthesisand on specific marine phytoplankton species. Marine EcologyProgress Series, 80, 89-100.

Karentz, D. 1991. Ecological considerations of antarctic ozone deple-tion. Antarctic Science, 3, 3-11.

Karentz, D. 1992. Ozone depletion and UV-B radiation in the Antarc-tic—Limitations to ecological assessment. Marine Pollution Bul-letin, 25, 231-232.

Karentz, D., and L.H. Lutze. 1990. Evaluation of biologically harmfulultraviolet radiation in Antarctica with a biological dosimeterdesigned for aquatic environments. Limnology and Oceanography,35,549-561.

Smith, R.C., B.B. Prézelin, K.S. Baker, R.R. Bidigare, N.P. Boucher, T.Coley, D. Karentz, S. Maclntyre, H.A. Matlick, D. Menzies, M.Ondrusek, Z. Wan, and K.J. Waters. 1992. Ozone depletion: Ultra-violet radiation and phytoplankton biology in antarctic waters.Science, 255, 952-959

ANTARCTIC JOURNAL - REVIEW 1993

114