The Physiological Ecology of UV-Absorbing Compounds from the Mucus of Marine Fishes

122 Pages·2006·3.06 MB·English

UNIVERSITY OF HAWAI'1 LIBRARY
THE PHYSIOLOGICAL ECOLOGY OF UV-ABSORBING COMPOUNDS
FROM THE MUCUS OF MARINE FISHES
A DISSERTATIONSUBMITTED TO THE GRADUATEDIVISION OFTHE
UNIVERSITY OFHAWAI'IIN PARTIALFULFILLMENT OFTHE
REQUIREMENTS FOR THEDEGREE OF
DOCTOR OFPHILOSOPHY
IN
ZOOLOGY
AUGUST 2003
By
Jill P. Zamzow
Dissertation Committee:
George Losey, Chairperson
Paul Nachtigall
Andrew Taylor
TimothyTricas
DavidJameson
ACKNOWLEDGEMENTS
G. Losey, A. Taylor, T. Tricas, P. Nachtigall, D. Jameson, andP. Nelson
provided valuable discussions, insight and helpful comments that greatlyimproved
this dissertation. Equipment loans byE. G. Grau, P. Jokiel, R. Bidigare, M. Atkinson,
M. Hadfield, and H. and A. Zamzow are greatly appreciated. Many thanks for field
and technical assistance are due to G. Cailliet, S. Christensen, E. Conklin, D. Copson,
K. delCarmen, P. FitzGibbon, K. Jennings, G. Kaneko, W. Loeffler, J. Marshall, A.
May, A. Meyer, M. Okihoro, S. Shimoda, L. Smith, D. Strang, and R. Yoshiyama.
Staffmembers at Heron IslandResearch Station, LizardIslandResearch Station, and
Johnston Atoll National WildlifeRefuge were very helpful. This work was supported
by the National Science Foundation (Grant#OCE 9810387), SigmaXi Grants in Aid
ofResearch, the AchievementRewards for College Scientists (ARCS) Foundation,
and the University ofHawaii Arts and Sciences Advisory Council.
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ABSTRACT
This dissertation details myinvestigation into the physiological ecology of
UV-absorbing compounds found in the mucus ofmarine fishes. In a survey ofover
200 species offishes from aroundthe Pacific, I found that approximately 90% of
fishes possess mucus that absorbs stronglyin the UV. High-performance liquid
chromatography ofselectedmucus confirmedthat the UV-absorbing compounds in
the mucus are mycosporine-like amino acids, orMAAs.
I determined that the mucus ofexperimentally UV-exposed Thalassoma
duperrey absorbs more stronglyin the UV than the mucus ofthose protectedfrom
UV by UV-opaque (but visible light transparent) plastic. However, this difference in
mucus absorbance only occurs iffish are provided adietary source ofMAAs.
Furthermore, I found that males have highermucus absorbance than females, and
females exposedto UV sufferhigh rates ofskin damage. Females also sequester
MAAs in theireggs, and may suffer aconflict ofinterestbetween providing
sunscreen protection for theireggs vs. theirown skin.
Three coral reeffish species (Canthigasterjactator, Chaetodon multicinctus,
and Thalassoma duperrey) were sampled overa depth gradient, and shallow water
fish generally had superior sunscreen, both in terms ofmagnitude and short
wavelength spectral shifting, as compared with deeper waterindividuals ofthe same
species.
IV
Temperate tidepool sculpins (Family: Cottidae) showed a significant loss of
UV-absorbing compounds with increasingnorth latitude, and overall, fishes from
highertidepools had more sunscreen than fishes from low tidepools.
Behavioral experiments with Thalassoma duperrey showedno dietary orUV
induceddifferences in weight loss or swimming behavior, and the results on shade
seekingbehavior were equivocal.
Thus, sunscreening compounds seem to be ubiquitous among marine fishes.
The correlations Ihave found between the UV absorbance ofmucus and the depth,
latitude, orUV exposure ofthe sampledindividual leadme to believe that mucus UV
absorbance is an adaptive defense against UV for fishes.
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TABLE OF CONTENTS
ACKNOWlEDGEMENTS iii
ABSTRACT iv
LIST OFTABLES viii
LIST OFFIGURES ix
CHAPTER 1: GENERAL INTRODUCTION 1
CHAPTER 2: BROAD SURVEY AND EFFECTS OFUV REGIME 6
Abstract 7
Introduction 7
Materials andMethods 9
Results 14
Discussion 22
CHAPTER 3: EFFECTS OFDIET, UV AND GENDER 27
Abstract 28
Introduction 28
Materials and Methods 30
Results 38
Discussion 45
CHAPTER4: ONTOGENETIC AND ENVIRONMENTALEFFECTS 52
Introduction 53
Materials and Methods 54
VI
TABLE OF CONTENTS (continued)
Results 56
Canthigasterjactator 56
Chaetodon multicinctus 58
Thalassoma duperrey 60
General trends 62
Discussion 64
CHAPTER 5: TEMPERATETIDEPOOLFISHES 67
Abstract 68
Introduction 69
Materials and Methods 70
Results 73
Discussion 76
CHAPTER 6: BEHAVIORALRESPONSES 79
Introduction 80
Materials and Methods 82
Results 84
Discussion 88
CHAPTER 7: SUMMARY AND CONCLUSIONS 90
Future directions 92
REFERENCES 94
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LIST OF TABLES
2.1 List ofSpecies Sampledfor Mucus Transmission 15
2.2 Mucus Transmission Cutoffs for Initial Six-WeekExperiment.. 21
3.1 Statistical Results, Change in Integrated Absorbance 38
3.2 Statistical Results, Change in CenterofAbsorbance 39
3.3 Statistical Results, Change in Damage Score 40
3.4 Statistical Results, Whole Eye Transmission Value .42
3.5 Statistical Results, Change in Skin Reflectance 44
5.1 CottidSpecies Usedin Statistical Analyses 71
5.2 Lens Transmission Values for Temperate Species 75
5.3 Additional Temperate Species Sampled 75
V111
LIST OFFIGURES
Figure Page
2.1 Absorbance Spectra ofMucus from SelectedHawaiian Fishes 12
2.2 Irradiance Measurements from Kaneohe Bay, Oahu 13
2.3 Absorbance Spectra ofAustralian Parrotfish Mucus 19
2.4 Mucus Transmission ofExperimental Thalassoma duperrey 20
2.5 CanthigasterjactatorSeen Through UV-sensitive Videocamera 23
3.1 Transmission spectraofexperimental acrylics 32
3.2 Total DailyUV Doses from Eppley Cell Radiometer 33
3.3 Mucus Absorbance Spectra ofExperimental T. duperrey 36
3.4 Changes ShownbyExperimental Fish 37
3.5 Change in Damage Score by Gender and UV Treatment 41
3.6 OcularTransmission vs. StandardLength 43
3.7 Change in Reflectance v. StandardLength 44
4.1 CanthigasterjactatorIntegratedAbsorbanceData 56
4.2 CanthigasterjactatorCenterofAbsorbance Data 57
4.3 Chaetodon multicinctus IntegratedAbsorbanceData 58
4.4 Chaetodon multicinctus CenterofAbsorbance Data 59
4.5 Thalassoma duperrey IntegratedAbsorbanceData 60
4.6 Thalassoma duperrey CenterofAbsorbanceData 61
4.7 Mean Absorbance Values by Species 62
4.8 Example Absorbance Spectrafor each Species 63
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LIST OFFIGURES (continued)
Figure Page
5.1 Example Absorbance Spectrafor Intertidal Fishes 73
5.2 Mean Absorbance by Site and Intertidal Height 74
6.1 Loss ofBodyWeightbyExperimental Fish 85
6.2 Swimming Behaviorvs. Time forExperimental Fish 86
6.3 Shade-seeking Behaviorvs. Time for Experimental Fish 87
6.4 Shade-seeking Behaviorvs. UV Dose 87
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CHAPTER 1:
GENERAL INTRODUCTION
Ultravioletradiation (UV, =280-400 nm) is damaging to organisms, from
cyanobacteria (Garcia-Pichel et al. 1993) to humans (Marks 1989). SolarUV can
damage DNA directly viaformation ofcyclobutane pyrimidine dimers (Setlow 1968)
and6-4 photoproducts (Vincent andNeale 2000). Solar UVcan also induce cellular
damage due to the formation ofreactive oxygen species such as singlet oxygen and
superoxide radicals (Dunlap et al. 2000). Anotherconsequence ofUV is the
formation of"sunburn cells", damagedcells "possessing a densely staining, glassy,
homogeneous cytoplasm and apyknotic nucleus most often in association with a
perinuclearorpericellular oedematous halo" (Bullock 1988).
SolarUV radiation penetrates clearwaterin quantities sufficientto be
biologicallyharmful, and negatively affects aquatic organisms such as dinoflagellates
(Jeffrey et al. 1999), phyto- andbacterio-plankton (Burnaet al. 2001), zooplankton
(Browman et al. 2000), amphibians (e.g., Fite et al. 1998, Kieseckeret al. 2001) and
larval (e.g., Vetteret al. 1999,Lesseret al. 2001) andadult fishes (e.g., Ahmed &
Setlow 1993, Bullock 1981). In Antarctica, Karentz andLutze (1990) found
biological effects ofUVB (280-320 nm) at 30 m depths. Utilizing a deep submersible,
Frank and Widder (1996) measured 380 nmirradiance, in the UVA (321-400 nm)
range ofthe spectrum, sufficientfor detection by crustacean visual systems at 500
600 m depth. Tropical marine fishes living in shallow waterare exposedto extremely
high and variable levels ofUV -- much higherlevels than are experiencedby animals
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