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Modeling the trophic transfer of beta radioactivity in the marine food web of Enewetak atoll, Micronesia Dalsgaard, Anne Johanne Tang 1999

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M O D E L I N G T H E TROPHIC TRANSFER OF B E T A RADIOACTIVITY M A R I N E FOOD W E B OF E N E W E T A K A T O L L ,  IN THE  MICRONESIA  by ANNE JOHANNE TANG  DALSGAARD  B . S c , The U n i v e r s i t y o f C o p e n h a g e n ,  1995  A THESIS SUBMITTED IN PARTIAL F U L F I L M E N T OF THE REQUIREMENTS FOR THE D E G R E E OF M A S T E R OF  SCIENCE  in T H E F A C U L T Y OF G R A D U A T E  STUDIES  (Department o f R e s o u r c e M a n a g e m e n t and E n v i r o n m e n t a l Studies; Fisheries Centre) W e accept this thesis as c o n f o r m i n g to the^Fequ^ired^standard  T H E UNIVERSITY OF BRITISH C O L U M B I A January 1999 © A n n e Johanne T a n g D a l s g a a r d ,  1999  In  presenting  degree  this thesis  at the University  in partial fulfilment  or  by  his  requirements  for  an  I further agree that permission for  of this thesis for scholarly purposes  department  the  advanced  of British Columbia, I agree that the Library shall make it  freely available for reference and study. copying  of  or  her  representatives.  extensive  may be granted by the head of my It  is  understood  that  publication of this thesis for financial gain shall not be allowed without  copying  or  my written  permission.  Department of ^JZJQQTCC  Manaae/nerrL ctnct £noy'/-o'nmen-cjoU c&u.oLCeS  The University of British Columbia Vancouver, Canada  DE-6 (2/88)  Abstract A n approach for m o d e l i n g the t r o p h i c transfer o f beta radioactivity w i t h i n the marine f o o d w e b o f E n e w e t a k A t o l l , M i c r o n e s i a , C e n t r a l P a c i f i c is described. F r o m 1948 to 1958 this atoll w a s used b y the U S military for testing o f nuclear weapons w h i l e m o n i t o r i n g the impact o n the ecosystem. I n parallel to these military operations, a marine laboratory w a s operating o n the atoll, hosting a w e a l t h o f scientists p e r f o r m i n g basic research. P r o b a b l y the most r e n o w n e d study was carried out by H . T . O d u m and E . P . O d u m i n 1954, w h o examined the trophic structure o f the w i n d w a r d reef c o m m u n i t y and its p r o d u c t i v i t y per unit area. B a s e d o n this study and o n the vast amount o f scientific literature o n the atoll, a mass-balance t r o p h i c m o d e l o f the w i n d w a r d reef w a s  constructed,  based  o n the E c o p a t h  modeling  software. E c o p a t h uses as its basic inputs the biomass, production/biomass, and f o o d c o n s u m p t i o n rates o f the various functional groups i n the ecosystem, a l o n g w i t h a diet matrix. B a s e d o n these inputs it estimates the f l o w o f biomass between  the functional g r o u p s  and presents  the  c o r r e s p o n d i n g predation mortalities i n a matrix where the c o l u m n s represent the intake of, and the r o w s the losses of, biomass f r o m the groups. A set o f first-order differential equations, relating the intake and loss o f biomass to the amounts o f radioactivity i n the groups, was then set up. T h e equations w e r e integrated over time and calibrated b y m i n i m i z i n g the sum o f squared deviations between the observed and predicted levels o f radioactivity, thus m a p p i n g the transfer o f radioactivity onto the transfer o f biomass. T h e o r i g i n a l f o o d w e b / mass-balance model,  which  was  constructed  without  reference  to  the  data  on  radioactivity,  was  subsequently re-calibrated to achieve a m a t c h between the f o o d w e b and the radioactivity data. T h e results predict that there is a time lag between the observed m a x i m u m o f radioactivity and the t r o p h i c p o s i t i o n o f the groups, and that beta radioactivity is not b i o a c c u m u l a t e d  up  t h r o u g h the f o o d web. F i n a l l y , suggestions o n h o w to incorporate the approach as a general routine into the E c o p a t h software are given.  n  Table of Contents Abstract  ii  T a b l e o f Contents  iii  L i s t o f Tables  vi  List o f Figures  viii  Acknowledgments  '  1. I n t r o d u c t i o n  x  1  1.1 G e n e r a l i n t r o d u c t i o n and objectives  1  1.2 E n e w e t a k A t o l l , l o c a t i o n and description  2  1.3 A t o l l f o r m a t i o n and D a r w i n ' s theory o f subsidence  6  1.4 H i s t o r i c a l events o n E n e w e t a k A t o l l  7  2. B a c k g r o u n d theory  13  2.1 T h e o r y o f radioactivity  13  2.1.1 N a t u r a l and artificial radioactivity  13  2.1.2 R a d i o a c t i v e decay  :  13  2.1.3 T h e b i o l o g i c a l effects o f radiation  16  2.1.4 M e a s u r i n g radioactivity  17  2.1.5 U n i t s o f radioactivity  18  2.2 R a d i o a c t i v i t y f r o m nuclear explosions  18  2.2.1 T y p e s o f nuclear explosions  18  2.2.2 D e c a y o f m i x e d fission products  21  2.2.3 U p t a k e o f radioactivity b y marine organisms 2.3 C o m p a r t m e n t m o d e l i n g  21 24  2.3.1 E c o p a t h  24  2.3.2 E c o r a n g e r  26  3. M e t h o d s  2  3.1 D e f i n i n g the m o d e l e d area  8  28  3.1.1 F o r e r e e f 3.1.2 A l g a l ridge  3  0  30  3.1.3 R e e f  flat  3.1.4 C o r a l head z o n e 3.1.5 S a n d / s h i n g l e  3  1  3  1  >  3  3.2 V a l i d a t i n g the E c o p a t h m o d e l  31  3.2.1 N o n - f i s h groups  32  3.2.1.1 D e t r i t u s  3  3.2.1.2 B e n t h i c P r i m a r y P r o d u c e r s  3  2  2  3.2.1.3 P h y t o p l a n k t o n  3  3  3.2.1.4Zooplankton  3  3  3.2.1.5 C o r a l s and sea anemones (Class anthozoa)  34  3.2.1.6 Foraminiferans and other p r o t o z o a n s  34  iii  3.2.1.7 G a s t r o p o d s  35  3.2.1.8 B i v a l v e s  35  3.2.1.9 Shrimps and lobsters  36  3.2.1.10 S t o m a t o p o d s  36  3.2.1.11 M i s c e l l a n e o u s crustaceans  37  3.2.1.12 E c h i n o d e r m s - not i n c l u d i n g holothurians  37  3.2.1.13 H o l o t h u r i a n s  37  3.2.1.14 Polychaetes and other w o r m - l i k e invertebrates  38  3.2.1.15 Sessile invertebrates  38  3.2.1.16 C e p h a l o p o d s  38  3.2.2 B i o m a s s , P / B , and Q / B values o f non-fish groups 3.2.2.1 R e m a r k s to Table 3.3  39 39  3.2.3 F i s h g r o u p s  49  3.2.3.1 T h e distribution and abundance o f fish  49  3.3 T h e o r i g i n and i n c o r p o r a t i o n o f the radioactivity data  52  3.3.1 T h e o r i g i n o f the radioactivity data  52  3.3.2 O b s e r v e d trends i n radioactivity i n various organisms  53  3.3.3 R a d i o a c t i v i t y i n w h o l e organisms  55  3.3.4 S i m u l a t i n g the observed trends i n beta radioactivity  55  4. R e s u l t s  59  4.1 B a l a n c i n g the E c o p a t h m o d e l  59  4.1.1 F i r s t r u n w i t h E c o r a n g e r using initial input parameters 4.1.1.1 M o d i f y i n g the predation mortality experienced by surgeonfish  59 60  4.1.1.2 M o d i f y i n g the predation mortality experienced b y shrimps, miscellaneous crustaceans, and gastropods  60  4.1.2 S e c o n d r u n w i t h E c o r a n g e r using m o d i f i e d input parameters 4.2 T h e fate o f beta radioactivity  61 64  4.2.1 M a p p i n g the fate o f beta radioactivity  64  4.2.2 S i m u l a t i n g the fate o f beta radioactivity  64  4.2.3 R e - c a l i b r a t i n g the E c o p a t h m o d e l  68  4.2.4 B e t a radioactivity and trophic levels  70  4.3 Parameter estimation and n e t w o r k analysis  71  4.3.1 S u m m a r y statistics  71  4.3.2 Transfer efficiencies  71  4.3.3 M i x e d t r o p h i c impact  72  5. D i s c u s s i o n  74  5.1 M o d e l input parameters  74  5.1.1 T h e time span c o v e r e d by the m o d e l  74  5.1.2 F i s h biomass and abundance estimates  75  5.1.2.1 V i s u a l census and rotenone sampling  75  5.1.2.2 F i s h biomass estimates at E n e w e t a k A t o l l  76  5.1.2.3 C o m p a r i n g the standing stock o f c o r a l reef fish  77  5.1.2.4 T h e abundance and role o f herbivorous fish  77  5.1.2.5 T h e fish fauna and z o o p l a n k t o n o n the fore reef  80  iv  5.2 O u t p u t s o f the m o d e l  82  5.2.1 T h e role o f benthic primary producers  82  5.2.2 T h e role o f detritus  82  5.2.3 C o m p a r i n g w i t h other models  83  5.2.3.1 T r o p h i c transfer efficiencies  83  5.2.3.2 B i o m a s s by t r o p h i c level  84  5.2.3.3 E c o s y s t e m maturity  85  5.3 S i m u l a t i n g radioactivity  86  5.3.1 T h e re-calibrated E c o p a t h m o d e l  86  5.3.2 T r o p h i c transfer o f radioactivity and the ' f o o d w e b time l a g '  87  5.3.3 D i l u t i o n effects and the additional mortality (IvT)  87  5.3.4 B i o - d i m i n u t i o n o f beta radioactivity  88  5.3.5 Potentials o f the approach  89  References  91  Appendices  104  A p p e n d i x 1. D i e t matrix o f the seventeen non-fish groups i n c l u d e d i n the m o d e l  104  A p p e n d i x 2. D i e t matrix o f the fish species i n c l u d e d i n the m o d e l  105  A p p e n d i x 3. Scientific and c o m m o n names o f the fish species i n c l u d e d i n the m o d e l  112  A p p e n d i x 4. D e r i v i n g the Q / B values o f the ten fish groups  117  A p p e n d i x 5. F i s h biomass estimates o f O d u m and O d u m (1955)  123  A p p e n d i x 6. L i s t o f the ecosystem maturity attributes, defined by O d u m (1969), that are quantified i n E c o p a t h  125  List of Tables T a b l e 1.1. Stratigraphic subdivisions o f bore holes drilled at E n e w e t a k A t o l l  7  T a b l e 2.1. N a t u r a l l y o c c u r r i n g radioisotopes i n sea water  14  T a b l e 2.2. R a d i o a c t i v e decay f r o m a nuclear detonation  15  T a b l e 2.3. D a t e s and l o c a t i o n o f the military nuclear detonations at E n e w e t a k A t o l l  19  Table 2.4. A r t i f i c i a l radioisotopes originating f r o m a nuclear e x p l o s i o n  20  Table 2.5. R a d i o i s o t o p e s i n marine organisms at E n e w e t a k A t o l l  23  T a b l e 3.1. T h e areal extent o f the five zones across the w i n d w a r d reef.  29  T a b l e 3.2. M a r i n e benthic algae at E n e w e t a k A t o l l  33  Table 3.3. S u m m a r y table o f the biomass, P / B , and Q / B values o f the non-fish groups  39  Table 3.4. B i o m a s s estimates o f detritus  41  T a b l e 3.5. B i o m a s s estimates o f benthic p r i m a r y producers  41  T a b l e 3.6. C o r a l biomass estimates  42  T a b l e 3.7. T h e biomass o f foraminiferans  42  T a b l e 3.8. B i o m a s s estimates o f gastropods  43  Table 3.9. B i o m a s s estimates o f shrimps and lobsters  43  T a b l e 3.10. B i o m a s s estimates o f crabs and other crustaceans  44  T a b l e 3.11. B i o m a s s estimates o f echinoderms  44  T a b l e 3.12. B i o m a s s estimates o f holothurians  45  T a b l e 3.13. B i o m a s s estimates o f polychaetes and other w o r m - l i k e invertebrates  45  Table 3.14. R a t e constants for some holothurians at E n e w e t a k A t o l l  48  T a b l e 3.15. B i o m a s s , P / B and Q / B values for infaunal polychaetes  48  T a b l e 3.16. E x a m p l e o f the stomach contents o f Neoniphon  50  sammara  T a b l e 3.17. S u m m a r y table o f the biomass, P / B , and Q / B values o f the ten fish groups  51  Table 3.18. Sample sizes o n w h i c h the data o n beta radioactivity w e r e derived  54  T a b l e 3.19. R e l a t i v e weight o f the different b o d y parts o f fish, bivalves, holothurians, and gastropods  55  T a b l e 4.1. B a s i c estimates o f the 'best m o d e l '  62  Table 4.2. S c a l i n g factors generated b y S o l v e r  69  vi  T a b l e 4.3. ' A d d i t i o n a l mortalities' ( M )  70  Table 4.4. S u m m a r y statistics  72  T a b l e 4.5. Transfer efficiency (%) by t r o p h i c level  72  T a b l e 5-1. Standing stock o f fish o n c o r a l reefs i n different regions  78  T a b l e 5-2. T r o p h i c transfer efficiencies (%) for four c o r a l reef ecosystem m o d e l s  84  Table 5-3. B i o m a s s at discrete t r o p h i c levels  84  vii  List of Figures F i g u r e 1-1. W e s t e r n P a c i f i c and M i c r o n e s i a  3  F i g u r e 1-2. E n e w e t a k A t o l l , R e p u b l i c o f the M a r s h a l l Islands  5  F i g u r e 1-3. T i m e a r r o w s h o w i n g the major human events o n E n e w e t a k A t o l l  9  F i g u r e 1-4. T h e physiographic zones o f the reef i n surface and cross section v i e w  10  F i g u r e 2-1. T h e u r a n i u m series  15  F i g u r e 2-2. Processes t a k i n g place once radioactive fallout reaches the ocean surface  22  F i g u r e 2-3. Schematic representation o f an E c o p a t h m o d e l  27  F i g u r e 3-1. C r o s s - r e e f currents and channel currents  28  F i g u r e 3-2. Z o n a t i o n across the w i n d w a r d reef as defined i n the present study  29  F i g u r e 3-3. T o t a l beta radioactivity i n corals (Acropora)  54  after the ' N e c t a r ' shot  F i g u r e 3-4. Transfer o f radioactivity between compartments o f an e c o s y s t e m  56  F i g u r e 3-5. R a d i o a c t i v i t y i n the benthic primary producers  57  F i g u r e 4-1. Simplified t r o p h i c f l o w diagram o f the w i n d w a r d reef o f E n e w e t a k A t o l l  63  F i g u r e 4-2. M a p p i n g the fate o f radioactivity  65  F i g u r e 4-3. Trends i n beta radioactivity i n the functional groups  66  F i g u r e 4-4. M o d i f y i n g the columns or the r o w s o f the predation mortality matrix  68  F i g u r e 4-5. T r o p h i c levels and days required to reach m a x i m u m levels o f beta radioactivity.  71  F i g u r e 4-6. M a x i m u m level o f beta radioactivity and t r o p h i c levels  71  F i g u r e 4-7. M i x e d t r o p h i c impact diagram  73  F i g u r e 5-1. L e s l i e plots  76  F i g u r e 5-2. B i o m a s s pyramids  84  F i g u r e 5-3. N e t w o r k analysis  86  viii  Acknowledgments I w o u l d like to express m y sincere gratitude t o m y advisor and mentor, D r . D a n i e l P a u l y , f o r his unique guidance a n d never failing trust. F o r g i v i n g m e the o p p o r t u n i t y t o study at U B C and f o r his ideas a n d inputs w i t h o u t w h i c h this fruitful project w o u l d never have happened. A l s o a very special thanks t o D r . C a r l W a l t e r s f o r his invaluable inputs, t o D r . L e s s L a v k u l i c h for his tremendously w a r m and very helpful support t h r o u g h o u t m y time as a student i n R M E S , and t o D r . V i l l y Christensen f o r helpful discussions and pleasant interactions. I thank J . L . M u n r o o f I C L A R M , M . D u k e o f the U n i v e r s i t y o f W a s h i n g t o n , and R . E . F o r e m a n o f the U n i v e r s i t y o f B r i t i s h C o l u m b i a f o r k i n d l y lending m e hard t o access data and literature. I also w i s h t o thank D r . R E . F o r e m a n f o r helpful c o m m e n t s o n the manuscript. T h a n k s t o m y f e l l o w students a n d friends at the Fisheries Centre, a n d t o D r . T o n y Pitcher, A n n T a u t z , and I n g r i d R o s s w h o helped realize m y stay at the Fisheries Centre. A n d finally, thanks t o m y dear family and close friends f o r always being there f o r me.  ix  1. Introduction 1.1 General introduction and objectives. In D e c e m b e r  1942, w h e n Italian physicist E n r i c o F e r m i p r o d u c e d the first nuclear fission  reaction i n a secret u n d e r g r o u n d military laboratory i n C h i c a g o ( L e n s s e n 1991), artificial radioactivity became an environmental reality. Since the m i d 1940s, radioactivity has been released into the marine environment f r o m various anthropogenic sources i n c l u d i n g nuclear w e a p o n s testing, radioactive waste disposal (both c i v i l i a n and military sources), and effluent from power  and fuel reprocessing  plants as w e l l as accidental releases ( K e n n i s h  1998,  Osterberg et al. 1964, R o w a n and R a s m u s s e n 1994). O n c e i n the marine environment this radioactivity is o f serious human health c o n c e r n because o f its potential to distribute itself throughout diffuse f o o d w e b s ( C l a r k 1989, L e n s s e n 1991, K e n n i s h 1998). Essential to understanding the contaminant pathways and ultimate fate o f radioactivity i n marine ecosystems is the k n o w l e d g e o f t r o p h i c relationships (Jarman et al. 1996). H o w e v e r , incomplete or t h e r m o d y n a m i c a l l y unbalanced f o o d w e b s have often been used to describe the fate o f radioactivity. Indeed, laboratory experiments structured a r o u n d simplified f o o d chains are probably a m o n g the main reasons for contradictory reports c o n c e r n i n g the  relative  importance o f transfer w i t h i n f o o d w e b s versus direct u p t a k e ( a d s o r p t i o n and absorption) o f radioactivity by aquatic organisms ( O p h e l and J u d d 1966, P o l i k a r p o v 1966, T h o m a n n 1981). Similarly,  investigations  based  on  field  observations  have  suffered  from  difficulties  in  adequately representing and quantifying the t r o p h i c p o s i t i o n o f the organisms ( K i r i l u k et al. 1995, Z a n d e n and R a s m u s s e n 1996). T h i s p r o b l e m has i m p e d e d studies f r o m examining the importance and quantifying the effects o f t r o p h i c transfer and f o o d web dynamics i n explaining observed  patterns  of  contaminant  bioaccumulation  (Kiriluk  et  al.  1995,  Zanden  and  R a s m u s s e n 1996). R e c e n t l y , the study o f the enrichment o f stable isotopes (particularly 5 N / 5 N ratios) t h r o u g h 1 5  1 4  aquatic f o o d w e b s has s h o w n to be a p r o m i s i n g measure o f the o r g a n i s m ' s (fractional) t r o p h i c position, t a k i n g into account the importance o f o m n i v o r y and c o m p l e x i t y , characteristics o f aquatic f o o d w e b s ( C a b a n a and R a s m u s s e n 1994, K i r i l u k et al. 1995, Z a n d e n and R a s m u s s e n  1  1996). It has further been demonstrated that the enrichment o f 5 contaminant  levels  o f certain persistent  pollutants,  suggesting  1 5  N is correlated w i t h the  that  t r o p h i c transfer  of  contaminants can be significant ( K i r i l u k et al. 1995, Z a n d e n and R a s m u s s e n 1996). A n o t h e r approach for determining t r o p h i c positions o f organisms is t h r o u g h the use o f massbalance f o o d w e b models constructed w i t h the E c o p a t h a p p r o a c h and software, initiated by P o l o v i n a (1984) and further developed b y Christensen and P a u l y (1992a,  1995). Recently,  K l i n e and P a u l y (1998) examined the relation between t r o p h i c positions estimated by 5  1 5  N  enrichment and by E c o p a t h and f o u n d an extremely h i g h c o r r e l a t i o n (r = 0.986). In this study, the E c o p a t h approach is taken one step further and its potential for predicting the fate o f radioactivity w i t h i n a marine f o o d w e b is examined. T h e study proceeds  by  m a p p i n g the fate o f beta radioactivity onto an E c o p a t h generated f o o d w e b o f the marine ecosystem  o f Enewetak  Atoll,  M i c r o n e s i a , C e n t r a l Pacific.  This mapping  calibration o f a preliminary m o d e l , initially constructed w i t h o u t reference radioactivity, and subsequent  involves  re-  to the data o n  m o d i f i c a t i o n o f some o f the m o d e l inputs, until a m a t c h is  achieved between the f o o d w e b and the pollutant data. T h e dissemination o f radioactivity is then simulated, using the t r o p h i c fluxes determined f r o m the m o d e l . T h u s the objectives o f this study are: •  T o simulate the t r o p h i c interactions a m o n g the functional g r o u p s o f the marine ecosystem o f E n e w e t a k A t o l l using the E c o p a t h m o d e l i n g software; and  •  T o m o d i f y the E c o p a t h m o d e l to simulate the fate o f beta radioactivity, originating f r o m a nuclear detonation, w i t h i n the marine ecosystem o f E n e w e t a k A t o l l .  1.2 Enewetak Atoll, location and description. E n e w e t a k A t o l l belongs to the R e p u b l i c o f the M a r s h a l l Islands. T h i s is a y o u n g republic f o r m e d i n 1987 as one o f the easternmost states o f M i c r o n e s i a i n the W e s t P a c i f i c O c e a n ( F i g u r e 1.1). T h e M a r s h a l l Islands are situated o n t w o subparallel chains o f extinct volcanoes (Henry  and  Wardlaw  1990),  the  Ratak  and  Ralik  meaning  "Sunrise"  and  "Sunset",  respectively, i n the M a r s h a l l e s e language ( K a r o l l e 1993). E n e w e t a k itself means " i s l a n d w h i c h points to the east" ( H e l f r i c h and R a y 1987), and is situated o n the northwestern extreme o f the R a l i k C h a i n at 1 1 ° 3 0 ' N latitude and 1 6 2 ° 1 5 ' E longitude. There has been some c o n f u s i o n  2  regarding place names o f the atoll. P r i o r to 1973  the E n g l i s h spelling o f E n e w e t a k  was  ' E n i w e t o k ' ( A n o n . 1979), but w i t h the gradual r e c o g n i t i o n o f the native people and the movement o f the M a r s h a l l Islands t o w a r d s independence (see F i g u r e 1.3), the spelling was changed to a c k n o w l e d g e the native p r o n u n c i a t i o n ( A n o n . 1979). I n the case o f island names, up to four different spellings might be f o u n d ( D a w s o n 1957) as b o t h native names and the E n g l i s h spelling has changed over time. O n top o f this are the military c o d e names that were assigned to the islands w h e n the atoll w a s used for nuclear testing ( H e n r y and W a r d l a w 1990). T h e atoll is oval-shaped and dominated b y a 4 0 k m l o n g n o r t h - s o u t h b y 3 2 k m w i d e east-west oriented l a g o o n w i t h a mean depth o f 48 m and a m a x i m u m depth o f 64 m ( A t k i n s o n et al. 1981). S u r r o u n d i n g the l a g o o n is a necklace o f small islands and submerged c o r a l reefs (Figure 1.2). " S u r p r i s i n g l y , it is difficult to determine the exact number o f islands. D u e to the effects o f storms, small islands are ephemeral, and t w o islands and part o f a third obliterated b y nuclear explosions. C u r r e n t l y [1987] there are 39 recognizable islands  were ..."  (Reese 1987). T h e atoll is situated w i t h i n the belt o f the northeast trade w i n d s and the N o r t h E q u a t o r i a l C u r r e n t w h i c h m o v e s w e s t w a r d at a speed o f 2 0 - 50 c m s " . F o r nine months o f the 1  year the w i n d w a r d side must therefore  withstand a constant w a v e attack  (Ladd  1973,  A t k i n s o n 1987), w h i c h i n t u r n brings about a fresh supply o f o x y g e n , nutrients and f o o d to the aquatic ecosystem. T h e w i n d w a r d side is thus the most v i t a l part o f the reef, concentrating l i v i n g organisms and i n d u c i n g active reef b u i l d i n g ( L a d d 1961, 1973). T h e islands consist o f reef debris that is f o r m e d o n the reef front and p i l e d up b y the currents, waves, and w i n d s ( L a d d 1973). H e n c e , the majority o f the islands are concentrated o n the w i n d w a r d side c o m p r i s i n g the northeastern and eastern reef perimeter. T h e remainder o f the reef may be d i v i d e d into three parts w i t h distinct m o r p h o l o g i e s related to their p o s i t i o n relative to the prevailing w i n d s . These are; the l e e w a r d reef o n the southwest, a transitional reef o n the northwest, and a transitional reef o n the southeast (Ristvet 1987) ( F i g u r e 1.2). T h e m a x i m u m elevation above sea level o f any island is a p p r o x i m a t e l y 4 meter. T h e total land area is 6.5 k m w h i l e the l a g o o n covers an area o f 932 k m ( A t k i n s o n et al. 1981). B e c a u s e o f 2  2  the l o w elevation and little land mass, the weather conditions o n the atoll are dictated b y the surrounding ocean ( C o l i n 1987b). T h e air temperatures range f r o m 2 8 . 5 ° C i n the dry season to 30.0°C i n the w e t season. T h e w e t season stretches f r o m A p r i l to m i d - N o v e m b e r and 4  162°10'  162°  162°30'  162°20' 1—  I  I  I  I  I  I  I  NAUTICAL MILES  I  I  FEET  I  I  I  I I  I I I I I  KILOMETERS  1  I  Figure 1-2. Enewetak A t o l l , Republic of the Marshall Islands, with locations relevant for the present study. Modified from Wardlaw et al. (1991). w i t h i n this p e r i o d , the atoll receives about 8 5 % o f an average yearly rainfall o f 1470 m m ( M e r r i l l and D u c e 1987). T h e atoll is traversed by three channels; the E a s t D e e p C h a n n e l w h i c h is 1.5 k m w i d e and 55 m deep, the S o u t h Passage w h i c h is 9.7 k m w i d e and 11-22 m deep, and the 4.2 k m w i d e and 2 m deep Southwest Passage consisting o f a n e t w o r k o f small passages rather than a single channel ( A t k i n s o n et al. 1981) ( F i g u r e 1.2).  5  W a v e s b r e a k i n g o n the w i n d w a r d reef constantly drive water across the reef flat into the l a g o o n m a k i n g this surf-driven i n f l o w the major water input. T h e speed o f the cross-reef current depends o n the height o f the s u r f and the tide a n d ranges between 10 t o 150 c m s "  1  ( A t k i n s o n et al. 1 9 8 1 , A t k i n s o n 1987). T h e tides are semi-diurnal w i t h a m a x i m u m range o f approximately 1.8 m ( W e l l s and Jenkins 1988). W a t e r also enters a n d leaves the l a g o o n across the leeward sections and t h r o u g h the three channels. T h e S o u t h Passage is the m a i n exit w h i l e the currents i n the D e e p C h a n n e l and the Southwest Passage reverse w i t h the tide (every 6.2 hours) ( A t k i n s o n 1987). Three current levels exist i n the l a g o o n w h i c h c a n be distinguished b y their speed and direction. A t the t o p is a w i n d - d r i v e n surface current, 5-15 m thick, m o v i n g southwest at a speed o f 10 cm-s" ( W a r d l a w et al. 1991). B e l o w this, at 10 t o 3 0 m depth, is a m i d - d e p t h 1  current f l o w i n g northeast at a speed o f 2 to 4 c m s " . F i n a l l y , at 3 0 to 50 m depth, a deep 1  current flows s o u t h w a r d at a speed o f 0.5 to 1.5 cm-s" . D e s p i t e this three-layer circulation 1  system, the water i n the l a g o o n is w e l l m i x e d w i t h an average salinity o f 3 4 . 4 % o a n d an average temperature o f 2 7 - 2 9 ° C ( W a r d l a w et al. 1991). T h e average residence time o f the w a t e r i n the l a g o o n is 33 days but m a y be u p t o f o u r times longer f o r w a t e r entering across the northern perimeter o f the atoll a n d somewhat shorter f o r water entering across the southern perimeter ( A t k i n s o n 1987).  1.3 Atoll formation  andDarwins  theory of  subsidence.  D u r i n g his v o y a g e w i t h the H.M.S. Beagle (1831 - 1836) Charles D a r w i n c o n c e i v e d his theory o f reef formation. H e h a d noticed the existence o f three basic types o f c o r a l reefs: fringing reefs along the shoreline, barrier reefs separated f r o m land b y a w i d e l a g o o n , a n d atolls w h i c h are reefs encircling a central l a g o o n ( B l a n c h o n 1997). A t o l l s , he hypothesized, are the last step i n a g e o l o g i c a l process o f a subsiding v o l c a n i c islands ( L a l l i a n d P a r s o n s 1994). A s a v o l c a n i c island fringed b y c o r a l reefs s l o w l y sinks (a process that m a y happen w h e n a ' n e w l y ' formed v o l c a n o presses d o w n o n a thin oceanic plate) the c o r a l organisms g r o w u p w a r d s t o w a r d the light and o u t w a r d s t o w a r d the fresh supply o f oxygen, organisms are successful  nutrients, a n d f o o d . I f the coral  i n k e e p i n g u p w i t h the speed o f subsidence,  a barrier reef w i l l  gradually f o r m as the corals closest t o the island suffocate i n the debris f o r m e d o n the front  6  reef. A s the subsidence continues the central island w i l l eventually disappear leaving a l a g o o n w i t h a perimeter o f c o r a l reefs (an atoll) ( M a r a g o s et al. 1996). In 1951, D a r w i n ' s theory w a s confirmed w h e n t w o holes w e r e drilled at E n e w e t a k  Atoll,  penetrating t h r o u g h the limestone cap and reaching the v o l c a n i c r o c k basement at depths o f 1267 m and 1405 m , respectively (see Table 1.1).  " T h e limestones recovered w e r e all o f  s h a l l o w water o r i g i n demonstrating b o t h subsidence o f the atoll and the u p w a r d g r o w t h o f shallow water corals since E o c e n e time, approximately 4 9 m i l l i o n years B . P . . . " ( G r i g g 1982). T h e limestone w a s characterized b y t h i c k intervals o f unleached aragonite-rich  carbonate  sediment w i t h w e l l preserved aragonitic fossils alternating w i t h layers w h e r e the aragonite had been dissolved. T h e latter represent periods w h e n the atoll s t o o d above w a t e r level and w a s subjected to the l o c a l weather conditions ( L a d d 1973, H e n r y and W a r d l a w 1990). Table 1.1. Stratigraphic subdivisions recognized in holes drilled at Enewetak A t o l l . Modified from Ladd (1973). Stratigraphic divisions  Depth (m)  Post-Miocene Upper Miocene Lower Miocene Upper Eocene  0 -200 200 - 3 0 0 300 - 9 0 0 900 - 1400  1.4 Historical events on Enewetak Atoll. E n e w e t a k A t o l l is no doubt one o f the most intensively studied and most abused atolls in the w o r l d . It w a s a major battle site at the end o f W o r l d W a r II between the U . S . armed forces and Japan w h o had o c c u p i e d the M a r s h a l l Islands (and the majority o f M i c r o n e s i a ) f r o m 1914 (see F i g u r e 1.3). T h e battle damage was augmented w i t h the g r o u n d i n g o f a fully loaded o i l tanker o n the w i n d w a r d reef d u r i n g the A m e r i c a n invasion, possibly causing the death o f l o n g sections o f the s u r f z o n e ( E m e r y et al. 1954, L a d d 1973). W h i l e Japan's interests i n M i c r o n e s i a had been mainly e c o n o m i c , the A m e r i c a n interests were purely strategic. T h e former Japanese areas w e r e placed under administration by the U n i t e d N a t i o n s and i n 1947  a Trusteeship  Agreement  was  signed b y President H . S . T r u m a n  establishing the T r u s t T e r r i t o r y o f the P a c i f i c Islands ( K a r o l l e 1993). In the same year, the native people o f E n e w e t a k A t o l l w e r e r e m o v e d , as officials i n W a s h i n g t o n D . C . announced that the atoll w a s g o i n g to be used for nuclear testing ( V a n D y k e 1991).  7  F r o m 1948 to 1958, the atoll was part o f the U . S . P a c i f i c P r o v i n g G r o u n d s and test site for 43 nuclear detonations ( F i g u r e 1.3 and T a b l e 2.3). T h e largest o f these w a s the M i k e test i n 1952 (part o f ' O p e r a t i o n I v y ' , F i g u r e 1.3 and Table 2.3). T h i s w a s the first h y d r o g e n devise ever to be tested, and the blast w a s estimated at 10.4 megatons or 7 5 0 times the H i r o s h i m a b o m b , resulting i n the v a p o r i z a t i o n o f an island ( A n o n . 1998). T h e testing o f nuclear devises Enewetak's  damaged  or destroyed the vegetation  o n all but t w o  of  islands ( L a d d 1973). T h e military activities o n the atoll also i n c l u d e d the  c o n s t r u c t i o n o f buildings, runways, and causeways,  the latter c o n n e c t i n g islets to facilitate  transportation. " T h e s e structures barred cross-reef c i r c u l a t i o n o f ocean w a t e r i n certain areas and radically changed e c o l o g i c a l conditions o n the reef and i n parts o f the l a g o o n " ( L a d d 1973). E n e w e t a k also received fallout f r o m the nuclear testing o n B i k i n i A t o l l . T h i s atoll, located u p w i n d and up-current f r o m E n e w e t a k (see F i g u r e 1.1), w a s part o f the U . S . P a c i f i c P r o v i n g G r o u n d s as w e l l , and w a s the first atoll used for nuclear testing ( O p e r a t i o n C r o s s r o a d s i n 1946, c o m p r i s i n g t w o tests). Meanwhile,  between  tests,  the  atoll was  studied  intensively b y  biologists,  geologists,  oceanographers, and geophysicists ( L a d d 1973). O n e o f the most remarkable, and probably the most cited study o n the atoll, w a s c o n d u c t e d b y H . T . O d u m and E . P . O d u m i n 1954 ( O d u m and O d u m 1955). Since this study also serves as an important b a c k g r o u n d for the present study, it is here briefly summarized. It w a s c o n d u c t e d a l o n g a transect o n a typical inter-island reef (Japtan, see F i g u r e 1.2) o n the w i n d w a r d side o f the atoll i n an area w h i c h , at that time, w a s yet not seriously affected b y the nuclear tests. T h e objectives o f the study w e r e t w o f o l d . T h e first objective was to determine the relationship between the standing stock o f organisms and their p r o d u c t i v i t y per area. T h i s w o u l d give the investigators a r o u g h idea o f the p r o p o r t i o n a l i t y between the p r o d u c t i v i t y o f the coral r e e f c o m m u n i t y and its standing crop (i.e., t u r n o v e r rate, or production/biomass ratio). T h e second objective w a s to p r o v i d e for a reference point that w o u l d " a i d future comparisons between the n o r m a l and the irradiated reef  8  'Nuclear events'  Historical events  1990 1987: The Republic of the Marshall Islands is formed. 1983: MPRL is closed down.  1 QSfl  1^80: Cleanup 'complete' - Enewetak officially returned to the people of Enewetak. M P M L changes to Mid-Pacific Research Laboratory (MPRL).  IVoU  1977: The US Defense Nuclear Agency (DNA) begins the cleanup of Enewetak. 1974: E M B L is renamed 'Mid-Pacific Marine Laboratory' (MPML).  1970  1963: Limited Test-Ban Treaty: All future testing should be underground.  1960  1958: Joint moratorium on atmospheric testing of nuclear weapons by the US and Soviet (violated in 1961 by the Soviet and by the US in 1962).  1958: Operation Hardtack; 22 detonations. 1956: Operation Redwing; 11 detonations.  1954: Establishment of Enewetak Marine Biological Laboratory (EMBL).  1954: Operation Castle; 1 detonation. 1952: Operation Ivy; 2 detonations. 1951: Operation Greenhouse; 4 detonations. 1948: Operation Sandstorm; 3 detonations._  _ 1950 < <  1948: The Pacific Proving Grounds are formed. 1947: Officials in Washington DC announces that Enewetak will be used for nuclear testing. The native people removed to Ujelang Atoll. 1944: American landing.  1940  }  1914 -1944: The Marshall Islands part of the Pacific Territories controlled by Japan.  1900 1890s  The Marshall Islands declared a German protectorate.  1790s  Europeans 're-visit' Enewetak.  1529: Enewetak 'discovered' by the Spanish explorer Alvaro de Saavedra.  Time o f Christ.  No archeological research has been conducted at Enewetak, but other area in the Marshall Islands were occupied at this time. According to the Enewetakese they "were there from the beginning" (Kiste, 1987).  Figure 1-3. Time arrow showing the major human events (civil and military) on Enewetak Atoll (Helfrich and Ray 1987, Kiste 1987, Wells and Jenkins 1988, Karolle 1993).  9  ecosystem...  Since nuclear e x p l o s i o n tests are being c o n d u c t e d i n the v i c i n i t y o f these  inherently stable reef communities, a unique o p p o r t u n i t y is p r o v i d e d for critical assays o f the effects o f radiations due to fission products o n w h o l e populations and entire  ecological  systems i n the f i e l d " ( O d u m and O d u m 1955). T h e transect w a s d i v i d e d into six zones, as illustrated i n F i g u r e 1.4: the w i n d w a r d buttress zone, coral-algal ridge, encrusting zone, zone o f small c o r a l heads, z o n e o f large c o r a l heads, and z o n e o f sand and shingle.  LARGE HEADS  SAND-SHINGLE  SMALL HEADS  1  1  ENCRUSTING ZONE RIDGE  1  BUTTRES E Z 0 N  r — i  LOW TIDE  100 M  M/SEC .16 '  • •32  •40  ...39  AVERAGE TIDE  .11  .01  •36  .02^S***^  .09  .15  .37  .26  LOW SPRING TIDE  Figure 1-4. Diagram showing the physiographic zones of the reef in surface and cross section view, and the average current velocities in m/sec. The approximate location of the 6 quadrats is indicated in the upper diagram. Redrawn from Odum and Odum (1955). D u r i n g a 6 w e e k p e r i o d the organisms w i t h i n each zone, ranging f r o m zooxanthellae w i t h i n c o r a l p o l y p s to sharks i n pelagic waters, w e r e described and g r o u p e d into discrete t r o p h i c levels c o m p r i s i n g p r i m a r y producers, herbivores, carnivores, and decomposers.  A  rough  estimate o f the biomass per area for each g r o u p w a s obtained u s i n g a variety o f methods. T h e 10  ambitiousness o f the study and the limited time available meant that " f e w e r replications w e r e made than w o u l d be required to obtain m a x i m u m accuracy f r o m each m e t h o d . Therefore it is the orders o f magnitude w h i c h emerge, but care is taken to base c o n c l u s i o n s only o n large, probably significant differences" ( O d u m and O d u m 1955). T h e results o f the g r o u p i n g s and quantification w a s presented as biomass pyramids, one f o r each zone. D e s p i t e the different t a x o n o m i c c o m p o s i t i o n s i n the six zones and the v a r i o u s errors a c c o m p a n y i n g the crude biomass estimates, the general shape o f the pyramids w a s the same and the ratio o f standing crop  between  trophic  levels  was  estimated  as:  herbivores/primary  producers  18.9%;  carnivores/herbivores 8 . 3 % (see F i g u r e 5.2). T h e study m o r e o v e r s h o w e d that the reef was highly p r o d u c t i v e c o m p a r e d to other systems ( w i t h m o r e than 24 g glucose-m^-day" g glucose-m" -year 2  _1  1  or 8760  (gross p r i m a r y production)). O n a yearly basis the p r o d u c t i o n o f the reef  seemed to m a t c h the respiration, indicating that the c o m m u n i t y w a s at e c o l o g i c a l climax. G i v e n a standing stock o f about 8 5 0 g dry weight-m" , the production/biomass ratio o f the reef 2  w a s approximately 12.5 year" . 1  F r o m 1954 to 1986, 1028 scientists visited E n e w e t a k , m a n y returning several times to f o l l o w up o n their field w o r k ( H e l f r i c h and R a y 1987). T h e scientists w e r e stationed at E n i w e t o k M a r i n e B i o l o g i c a l L a b o r a t o r y ( E M B L ) w h i c h w a s established i n 1954 and managed by the U n i v e r s i t y o f H a w a i i . T h e laboratory w a s initially sponsored b y the U . S . A t o m i c E n e r g y C o m m i s s i o n ( A E C ) and later by the U . S . Department o f E n e r g y ( D O E ) ( H e l f r i c h and R a y 1987, W e l l s and Jenkins 1988). It w a s r u n part-time until 1974 w i t h the research focusing o n increasing the k n o w l e d g e o f the atoll ecosystem.  I n 1974 it w a s u p g r a d e d to a full-time  laboratory and renamed the M i d - P a c i f i c M a r i n e L a b o r a t o r y ( M P M L ) . research  changed  to  include mainly l a g o o n  oceanography,  T h e focus  groundwater  o f the  dynamics,  ciguatera fish p o i s o n i n g . I n 1979 it was decided to phase d o w n the laboratory. A  and major  cleanup / rehabilitation p r o g r a m , initiated i n 1977 b y the U . S . Defense N u c l e a r A g e n c y ( D N A ) w i t h the objective o f preparing the atoll f o r the return o f its native people, w a s about to finish, and funding f o r the laboratory w a s running l o w . T h e name w a s changed for the second time to the M i d - P a c i f i c R e s e a r c h L a b o r a t o r y ( M P R L ) to reflect that the research no longer  was  confined t o the marine environment. I n 1982 the laboratory w a s finally terminated ( H e l f r i c h and R a y 1987). 11  O n e o f the results o f the research o n the atoll is a c o l l e c t i o n o f m o r e than 2 0 0 reprints o f scientific publications. T h e c o l l e c t i o n w a s issued as three v o l u m e s i n 1976  and a fourth  volume  two  in  1979  (Anon.  1976a-c,  Anon.  1979) . 1  Furthermore,  in  1987,  volumes  synthesizing the research o f the laboratory's entire history w a s published ( D e v a n e y et al. 1987, H e l f r i c h and R a y 1987). These t w o publications together w i t h the study by O d u m and O d u m (1955) and recently declassified material o n the level o f beta radioactivity i n the b i o t a o f the a t o l l f o r m the b u l k o f 2  material u p o n w h i c h this study is based.  The four volumes (Anon 1976a-c; Anon. 1979), which are hard to access, were kindly made available by J.L. Munroof ICLARM. Kindly provided by Marcus Duke from the University of Washington, Seattle. The material consisted of reports prepared by the Laboratory of Radiation Biology, University of Washington, in contract with the United States Atomic Energy Commission. 1  2  12  2. Background theory T h e f o l l o w i n g chapter provides the b a c k g r o u n d theory for the thesis, and is d i v i d e d into three main parts. T h e first part deals w i t h the theory o f radioactivity, describing the processes o f radioactive decay and the effects o f radioactivity o n l i v i n g organisms. T h e second part deals w i t h the different types o f nuclear explosions at E n e w e t a k A t o l l , the decay o f the radioactive material p r o d u c e d b y these tests, and the uptake o f radioisotopes b y marine organisms. Finally, the E c o p a t h compartment m o d e l i n g software, w h i c h a l l o w s f o r the construction, analysis, and c o m p a r i s o n o f mass-balance t r o p h i c models, is described.  2.1 Theory of radioactivity.  2.1.1  N a t u r a l and artificial radioactivity.  R a d i o a c t i v i t y has always been a natural component o f the environment. W h e n the E a r t h w a s formed, m u c h o f its constituent matter w a s radioactive. O v e r time, this radioactive material has decayed, l e a v i n g behind o n l y the isotopes w i t h the longest h a l f l i f e  3  a n d their decay  products. C o s m i c radiation is another source o f natural radioactivity that continuously adds small quantities o f C a r b o n , T r i t i u m , and other radioisotopes t o the u p p e r atmosphere (Table 1 4  2.1). F r o m here they reach the E a r t h ' s surface as part o f the rain ( M a u c h l i n e and T e m p l e t o n 1964, B a b l e t and Perrault 1987b, S m i t h 1994). R a d i o a c t i v i t y f r o m v a r i o u s anthropogenetic activities such as f r o m nuclear testing and nuclear waste is, o n the other hand, an artificial source o f radioactivity that has added m o r e a n d n e w radioisotopes t o the environment ( S e y m o r e 1960).  2.1.2  R a d i o a c t i v e decay.  R a d i o a c t i v i t y is the spontaneous emission o f excess energy f r o m atoms. A t o m s consist o f a nucleus o r b i t e d b y electrons. T h e nucleus contains p r o t o n s a n d neutrons, a n d w h i l e the number o f protons are fixed f o r every element i n the p e r i o d i c a l system, the number o f neutrons m a y vary. A t o m s w i t h the same number o f protons b u t a different number o f neutrons are k n o w n as isotopes. R a d i o i s o t o p e s are isotopes i n w h i c h the ratio o f neutrons t o  3  The time it takes for half of the radioisotopes to decay. See also section 2.1.2 on radioactive decay. 13  protons makes the nucleus unstable. T o b e c o m e stable the nucleus must give o f f energy, a process w h i c h is k n o w n as radioactive decay. Table 2.1. Naturally occurring radioisotopes in sea water. Modified from Seymore (1960) and Bablet and Perrault (1987b). H a l f life (years)  Amount  Terrestrial origin: Rubidium  4.70-10'°  3.4-10  232  Thorium  1.42-10  1.0-10  238  Uranium  4.50-10  ^Potassium  1.25-10  235  Uranium  234  230  Radioisotope  3  87  23  10  Activity (Bq-l')  b  0.2  -5  10  <0.1  3.0-10  s  0.1  9  4.7-IO"  5  12.3  7.13-10  8  2.1-10"  8  Uranium  2.48-10  5  1.9-10''°  Thorium  7.52-10  'Protactinium  3.43-10  9  2  1.0-10  13  <1.0-10  15  Radium  16.22-10  21.60-10° 19.40-10°  1.1-10"'  5  6  6.70-10°  1.4-10"'  210  Polonium  0.38-10°  2.2-IO '  234  Thorium  0.07-10°  4.3-10"'  228  Cosmic origin: Carbon  55.70-10  14  Tritium  -  12.26-10°  <0.1 -  7  -  7  14  <0.1  1.7-10"'  <0.1  (2to3)-10-  2  -  12  Actinium  <0.1  13  2.0-10'  4  227  '°Lead Radium  <3.0-10  4  226  2  (g-1" ) 1  8  a. The radioactive 'half live' is the time it takes for 5 0 % of the radioisotopes to decay; b. Becquerel-litef (becquerel (Bq) = disintegrations per second). Dashes indicate that the activity in 1  sea water is insignificant. Three types o f r a d i a t i o n products are typically generated i n a nuclear detonation: fissile n o n fission products, fission products, and activation products. F i s s i l e non-fission p r o d u c t s consist o f P l u t o n i u m a n d U r a n i u m atoms that d i d not undergo fission, i.e., d i d not split apart i n the detonation. T h e y are essentially alpha emitters (see Table 2.2). F i s s i o n products, o n the other hand, are the radioisotopes that are f o r m e d w h e n U r a n i u m and P l u t o n i u m atoms d o undergo fission. A c t i v a t i o n p r o d u c t s are f o r m e d w h e n elements f r o m the s u r r o u n d i n g environment, o r f r o m the nuclear b o m b itself, captures neutrons p r o d u c e d i n the detonation. F i s s i o n and activation p r o d u c t s mainly give o f f beta and g a m m a r a d i a t i o n (see T a b l e 2.2) (Bablet and Perrault 1987b).  14  Table 2.2. Types o f radioactive decay from a nuclear detonation and the processes that lead to them. Based on Smith (1994) and Skarsgard (1997). Radioactivity  Process  Alpha  Emission o f a Helium particle (2 H e ) from the nucleus: 2  ^U->  23  9  4  0  Th+^He +energy  Emission o f an ordinary electron (negatron) as a neutron transforms into a proton:  Beta  2° Co—^gNi* + negatron + uncharg ed particle or the emission o f an anti-electron (positron) as a proton transforms into a neutron: 22  Na—» ,Ne + positron + uncharg ed particle 22  The result o f beta decay is that the atomic number changes, and a new element is formed. Emission o f photons from a nucleus going from a high energy excited state to a low  Gamma  energy stable state, e.g., the N i atom produced i n the negatron emission example above, is marked by a star to indicate that it is i n an excited state, and w i l l emit gamma rays (y): 28 N i *  -> 2y  Formed during fission o f Uranium and Plutonium. W h e n the atoms split, excess neutrons are emitted that in turn may ionize other atoms.  Neutrons  234|J 2.45x1_q'y  230  90  2 2 6  2 2 2  2 1 8 0  85  210p  Q  "*  ..  2i°Bi  I£  b  w  2 1  80  22 3y  A.  P  2 0 6  214  T  r  1  234  T h  24.1 d  Ra  Rn 3.82 d  J  N t  /, 2 1 4  T n  8.0x10* y  a Decay  3.05 mir  Bi  Z™™  V  ' 210 |r  / 2x 10*%  min  ^  /  f^'^  >C r 206J| 4.20  /  A t omv.  /  ^  Pb 26.8  min  1 .3  p Decay  Denotes Major Branch  Hg  8.1  —i 125  min  130  135  140  145  N  Figure 2-1. The uranium series. Redrawn and modified from Skarsgaard (1997). N is the number o f neutrons in the nucleus, while Z is the atomic number equal to the number o f protons in the nucleus.  15  D e c a y p r o d u c t are themselves often radioactive, f o r m i n g so-called decay chains that ends w h e n a stable element is formed. A typical example is the U r a n i u m series s h o w n i n F i g u r e 2.1.  2.1.3  T h e b i o l o g i c a l effects o f radiation.  A s neutrons, photons, alpha and beta particles travel t h r o u g h l i v i n g tissue, they interact w i t h its constituent atoms. D u r i n g this interaction, energy is transferred f r o m the particles to the incident atoms, i n most cases to the orbiting electrons. I f the g a i n i n energy is large enough, the electrons w i l l be k n o c k e d away f r o m the atoms, i.e., the atoms are i o n i z e d . I f not enough energy is transferred the result w i l l be an excitation o f the atom. A l p h a particles are t o o large to penetrate the epidermis and do not constitute any serious external risk. O n c e inside the organism, however, they are extremely hazardous. T h e i r size and l o w v e l o c i t y means that f o r a g i v e n level o f energy, they are m o r e l i k e l y t o cause i o n i z a t i o n and excitation than, f o r example, beta particles. A l p h a particles are thus characterized b y a rapid loss o f energy and dense i o n i z a t i o n o f the nearby tissue. B e t a particles, o n the other hand, are smaller, faster, and travel further before they lose their energy, and are more penetrating than alpha particles. B e s i d e s internal damage, they c a n cause severe external damage to the lenses o f the eye and to the epidermis. P h o t o n s (gamma-rays), depending o n their energy, may either cause excitation o f atoms, k n o c k a w a y l o o s e l y b o u n d electrons, or convert into matter i n the f o r m o f a p o s i t r o n and a negatron that, i n turn, may ionize surrounding .atoms. G a m m a - r a y s are the most penetrating type o f r a d i a t i o n and may cause severe h a r m to the w h o l e body. I o n i z e d and excited atoms / molecules are thus the principal result o f absorbed radiation i n organic tissues. T h i s especially applies for water molecules w h i c h constitute the greater part o f the tissue. H e r e , the most important process is generally considered t o be: ionization  H 0 2  (2.1)  >H 0 +e 2  +  T h e i o n i z e d water m o l e c u l e just f o r m e d reacts w i t h another w a t e r m o l e c u l e to give a h y d r o x y l radical ( O H * ) : H O +H OH>H;O+OH* 2  +  (2.2)  2  16  T h e electron f o r m e d i n (2.1) readily reacts w i t h water molecules and h y d r o g e n ions to f o r m h y d r o g e n radicals  (FT):  e~+H 0->H CT - * O r T + H ' 2  (2.3)  e-+H H»H*  (2.4)  2  +  R a d i c a l s are extremely reactive. H y d r o x y l radicals are strong o x i d i z i n g agents and  hydrogen  radicals and electrons are strong r e d u c i n g agents. B e s i d e s the radiation i n d u c e d processes that affects the water molecules, and hence indirectly affects the other molecules i n the tissue, direct alterations o f molecules other than water also occur. A n example is the rupture o f the phosphate sugar b a c k b o n e i n D N A molecules, but many other alternations may also take place ( K i n n e 1984, S m i t h 1994, S k a r s g a r d 1997). A single or a f e w r a d i a t i o n events do not pose any risk to the health o f the o r g a n i s m as l o n g as its n o r m a l repair mechanisms can keep pace. It is the cumulative effect o f cellular damage that makes radioactivity dangerous. D i v i d i n g cells are particular prone to r a d i a t i o n damage and so fetuses are m o r e susceptible than fully developed organisms. B e s i d e s burns and skin ulcers, radiation  may  cause  cancer,  degenerative  diseases,  mental  retardation,  chromosome  aberrations, and genetic disorders (Lenssen 1991).  2.1.4  M e a s u r i n g radioactivity.  T h e radioisotopes originating f r o m a nuclear detonation do not decay immediately, but have a characteristic probability o f decay  per unit o f time. F o r a large  p o p u l a t i o n o f similar  radioisotopes, the number that decay per unit time (the activity) c a n be described as the p r o d u c t o f the number o f nuclei (N) and the decay constant (A,) ( K i n n e 1984): dN/dt = - A . - N  (2.5)  Integrating this equation results i n a negative exponential function o f the f o r m : N = N -e0  (2.6)  X t  where N is the number o f radioisotopes present at time zero. B e s i d e s X, radioactive decay is 0  often measured b y the physical h a l f life ( t  1 / 2  ) , w h i c h is the time it takes for h a l f o f the  radioisotopes to decay:  17  N /2 = N e 0  0  =>  1 / 2  t  1 / 2  =ln2/X  R a d i o a c t i v e h a l f lives may range f r o m fractions o f a second to trillions o f years  (2.7) (Seymore  1960).  2.1.5  U n i t s o f radioactivity.  R a d i o a c t i v i t y is measured i n number o f disintegrations per unit o f time. T h e S I unit is the becquerel ( B q ) , defined as disintegrations per second. A c t i v i t y is solely a measure o f the energy that is released f r o m the a t o m and does not distinguish between alpha or beta particles, g a m m a rays, or neutrons. N o r does it tell anything about the quantity o f energy that is absorbed i n the irradiated matter. T h i s quantity, however, is important w h e n determining the b i o l o g i c a l effects o f irradiation, because the different forms o f radioactivity differ i n their penetration p o w e r and their ability to i o n i z e matter (see section 2.1.3) ( S e y m o r e 1960). T h e SI unit for the absorbed dose or energy deposited i n matter is the gray ( G y ) , and is defined as an absorbed radiation dose o f one j o u l e per k g .  2.2 Radioactivity from nuclear  2.2.1  explosions.  T y p e s o f nuclear explosions.  F o r t y three nuclear devices w e r e detonated at E n e w e t a k A t o l l (see T a b l e 2.3). F o r t y one were detonated f r o m t o w e r s , barges, the ocean surface, or d r o p p e d f r o m aircraft's w h i l e t w o were detonated underwater. " E a c h o f the explosions exerted its o w n special effects o n the atolls. T h e underwater shots released large amounts o f radioactive materials into the water to be absorbed, retained, or passed o n i n the c o m p l e x marine b i o l o g i c a l w e b , but deposited only minimal amounts o f radioactive substances o n the land areas or i n the atmosphere. T h e t o w e r shots caused spectacular physical disturbance to the islets o f the atolls, often  completely  obliterating life i n the immediate area, and released radioactive material w h i c h contaminated nearby land and water areas. T h e third general type o f shot, the high-altitude detonation, probably had little or no effects o n the atolls. A n y radioactive materials released w o u l d have been q u i c k l y m o v e d out o f the area by w i n d s " ( W e l a n d e r et al. 1966).  18  Table 2.3. Dates and location o f the military nuclear detonations at Enewetak Atoll. Modified from Henry and Wardlaw (1991) and Helfrich and R a y (1987). The origin o f the beta radioactivity traced in this study is mainly from the Nectar shot (1954), which is marked in bold.  Military name of event X-RAY YOKE ZEBRA DOG EASY GEORGE ITEM MIKE KING NECTAR LACROSSE YUMA ERIE SEMINOLE BLACKFOOT KICKAPOO OSAGA INCA MOHAWK APACHE HURON CACTUS BUTTERNUT KOA WAHOO HOLLY YELLOWWOOD MAGNOLIA TOBACCO ROSE UMBRELLA WALNUT LINDEN ELDER OAK SEQUOIA DOGWOOD SCAEVOLA PISONIA OLIVE PINE QUINCE FIG 3  a  a  Date Apr. 14, 1948 Apr. 30, 1948 May 14, 1948 Apr. 7, 1951 Apr. 20, 1951 May 8, 1951 May 24, 1951 Oct. 31, 1952 Nov. 15, 1952 May 13, 1954 May 4, 1956 May 27, 1956 May 30, 1956 June 6, 1956 June 11, 1956 June 13, 1956 June 16, 1956 June 21, 1956 July 2, 1956 July 8, 1956 July 21, 1956 May 5, 1958 May 11, 1958 May 12, 1958 May 16, 1958 May 20, 1958 May 26, 1958 May 26, 1958 May 30, 1958 June 2, 1958 June 8, 1958 June 14, 1958 June 18, 1958 June 27, 1958 June 28, 1958 July 1, 1958 July 5, 1958 July 14, 1958 July 17, 1958 July 22, 1958 July 26, 1958 Aug. 6, 1958 Aug. 18, 1958  Burst type/height Tower, 63 m Tower, 63 m Tower, 63 m Tower, 94 m Tower, 94 m Tower, 63 m Tower, 63 m Surface Airdrop, 471 m Barge Surface Tower, 63 m Tower, 94 m Surface Tower, 63 m Tower, 94 m Airdrop Tower, 63 m Tower, 94 m Barge Barge Surface Barge Surface Underwater, 157 Barge Barge Barge Barge Barge Underwater Barge Barge Barge Barge Barge Barge Barge Barge Barge Barge Surface Surface  b  a. Thermonuclear bomb; b. O f f bottom in approximately 50 m o f water; c. kt = kiloton, Class. = classified.  19  Yield (ktf 37.0-10° 49.0-10° 18.0-10° Class. 47.0-10° Class. Class. 10.4-10 50.0-10 16.9-10 40.0-10° Class. Class. 13.7-10° Class. Class. Class. Class. Class. Class. Class. 18.0-10° Class. 13.7-10 Class. Class. Class. Class. Class. Class. Class. Class. Class. Class. 8.9-10 Class. Class. Class. Class. Class. Class. Class. Class. 3  1  2  2  3  Location Enjebi Aomon Runit Runit Enjebi Eleleron Enjebi Elugelab Runit Elugelab Runit Aomon Runit Boken Runit Aomon Runit Lujor Eleleron Elugelab Elugelab Runit Runit Teiteiripucchi Mut Runit Enjebi Runit Enjebi Runit Ikuren Enjebi Runit Enjebi Bokoluo Runit Enjebi Runit Runit Enjebi Enjebi Runit Runit  T h e nuclear detonations at E n e w e t a k A t o l l w e r e either fission o r f u s i o n (thermonuclear) types. * *  239  Fission bombs  contain  U r a n i u m and  P l u t o n i u m atoms that  split i n h a l f under the  detonation f o r m i n g t w o isotopes o f approximately h a l f the size o f the o r i g i n a l atom. Since the neutron t o p r o t o n ratio i n light elements is l o w e r than i n heavier elements, most o f the 'fission daughter elements' are unstable and give o f f radioactivity. A p p r o x i m a t e l y 2 0 0 isotopes o f 35 elements are created w i t h the detonation o f a fission b o m b (see T a b l e 2.4). M o s t have v e r y short h a l f lives, but a f e w have h a l f lives o f up t o 3 0 years ( S e y m o r e 1960), a n d U r a n i u m and P l u t o n i u m atoms that d i d not split i n the detonation (fissile non-fission products, see section 2.1.2) have h a l f lives o f up t o 4.5-10 years (see T a b l e 2.4). 9  In f u s i o n b o m b s , isotopes  o f H y d r o g e n ( D e u t e r i u m a n d T r i t i u m ) fuse 6  under v e r y  233  temperatures ( o n the order o f 10 ° C , triggered b y the fission o f  Uranium or  239  high *  Plutonium).  F u s i o n b o m b s have also been termed " c l e a n devices" o r " c l e a n b o m b s " since relatively f e w radioisotopes are f o r m e d ( S e y m o r e 1960). T h o s e that are f o r m e d include T r i t i u m , D e u t e r i u m and a variety o f i n d u c e d radioisotopes (activation products, see section 2.1.2 and T a b l e 2.4). Table 2.4. Artificial radioisotopes originating from a nuclear explosion. Modified from Seymore (1960) and Bablet and Perrault (1987b). Fission products Half life Radioisotopes (days) 11.0-10 Cesium Strontium- Yttrium 10.1-10 98.6-10 Antimony Promethium 91.3-10 62.1-10 Europium 36.5-10 Ruthenium- Rhodium Cesium- Praseodymium 8.4-10 Zirconium- Niobium 65.0-10° Yttrium 58.8-10° 52.7-10° Strontium 40.0-10° Ruthenium- Rhodium 32.5-10° Cesium- Praseodymium Barium 13.0-10 80.0-10" Iodine 45.7-10" Lanthanum 73.1-10" Yttrium 3  137  90  3  1  1 2 5  147  1  1  155  106  144  1  1  95  91  89  103  Activation products Half life Radioisotopes (days) 20.3-10 "Carbon 10.2-10 Bismuth 44.5-10 Tritium 19.3-10 °Cobalt 94.9-10 Iron 31.2-10 Manganese 27.1-10 Cobalt Silver 25.0-10 Zink 24.5-10 70.0-10° Cobalt 45.0-10° Iron 1  5  207  3  6  2  55  1  54  1  2  238  8  239  3  235  2  24  2  241  1  238  1  57  110m  Non-fission fissile isotopes Half life Radioisotopes (days) 45.0-10 Uranium 24.4-10 Plutonium 71.0-10 Uranium °Plutonium 66.0-10 45.8-10 Americium Plutonium 86.4-10°  a  1  65  1  58  59  141  140  3  1 3 1  1  140  4  90  4  a. T h e ' m ' indicates that the silver atom is an isomer, i.e., that it is i n a long-lived excited state but eventually w i l l give off gamma rays (usually gamma rays are emitted instantly following an alpha or beta decay).  20  In the largest nuclear devices a so-called fission-fusion-fission process takes place. H e r e , the h i g h temperatures f r o m a fission process triggers a fusion process that i n t u r n releases a flux o f neutrons that c a n fission m o r e material (Seymore 1960).  2.2.2  D e c a y o f m i x e d fission products.  T h e many radioisotopes created i n a nuclear detonation have different h a l f lives, some longer and some shorter than the average. T h e overall rate o f decay o f all fission p r o d u c t s c o m b i n e d therefore decreases over time (Seymore  1960): " F o r the m i x t u r e o f all fission products,  radioactivity decreases tenfold for each sevenfold increase i n time f o l l o w i n g the detonation i n w h i c h the isotopes w e r e p r o d u c e d . A t this rate the decrease i n activity f r o m one h o u r after t o 343 hours after (approximately t w o w e e k s ) is a t h o u s a n d f o l d . " The 2 3 5  theoretical  gross beta-decay  o f mixed  slow-neutron  initiated fission  products o f  U r a n i u m w a s estimated b y H u n t e r and B a l l o u (1951). O v e r a p e r i o d o f 1 t o 1000 days the  decay is a p p r o x i m a t e d b y a straight line o n a l o g - l o g scale, w i t h a n average slope o f -1.2 ( B o n h a m 1958). T h i s f o r m o f decay can b e described b y a p o w e r f u n c t i o n D = a • t " , where 1 2  D is the amount o f radioactivity at time t i n days after the detonation and a is the intercept. A distinction should be made between decay and decline. D e c a y refers t o the decrease i n activity determined f r o m a sample kept and measured repeatedly i n the laboratory. D e c l i n e , o n the other hand, refers t o the rate o f change i n activity determined f r o m samples collected over time i n the same locality. " I f decline is m o r e r a p i d than decay a r e d u c t i o n o f activity i n the environment b e y o n d that caused solely b y physical decay is suggested, a n d conversely, a steeper decay than decline suggests either an increase i n availability i n the environment o r a n a c c u m u l a t i o n o r concentration o f radioactivity b y the organism. E q u a l i t y o f decay and decline suggests that uptake and excretion o f radioisotopes have reached a n e q u i l i b r i u m w i t h the environment" ( B o n h a m 1958).  2.2.3  U p t a k e o f radioactivity b y marine organisms.  T h e most abundant naturally o c c u r r i n g radioisotopes i n sea w a t e r ( ' b a c k g r o u n d r a d i o a c t i v i t y ' ) are  40  P o t a s s i u m and  T a b l e 2.1). by  1 4  40  Carbon,  8 7  R u b i d i u m , c o m p r i s i n g approximately 9 0 % and 1 0 % , respectively (see  P o t a s s i u m is also the principal radioisotope f o u n d i n marine organisms, f o l l o w e d 2 3 2  Thorium,  2 3 4  T h o r i u m and  2 2 6  R a d i u m (Bablet and P e r r a u l t 1987b).  21  W i t h the nuclear explosions at E n e w e t a k A t o l l , a huge number o f artificial radioisotopes w e r e added t o the marine environment, initially i n the f o r m o f l o c a l fallout o n the o c e a n surface. F r o m here, the radioisotopes w e r e subjected t o oceanic d i l u t i o n , dispersion, concentration, and transport ( M a u c h l i n e and T e m p l e t o n 1964) as illustrated i n F i g u r e 2.2, w h e r e the t h i c k e r a r r o w indicates the route f o l l o w e d i n the present study.  Dilution and dispersion  Advection  Turbulent diffusion  Transport  Currents  Concentration  Moving organisms  Adsorption  Physicalchemical  Co-precipitation  Biological  Retentive processes  Deposition of silt  Static organisms  Ion-exchange  Flocculation and sedimentation  Figure 2-2. A schematic illustration o f the various processes taking place once the radioactive fallout reaches the ocean surface. The thicker arrows indicate the pathway followed in this study. Adapted and modified from Mauchline and Templeton (1964). Biological  concentration  refers  t o the uptake  o f radioisotopes  b y marine  organisms.  D e p e n d i n g o n the organism, this happens i n different ways. Single cell organisms m a y acquire the radioisotopes t h r o u g h passive diffusion, active uptake across membranes, adsorbed t o the surface, o r w i t h water engulfed d u r i n g the f o r m a t i o n o f f o o d v a c u o l e s (Sanders and G i l m o u r 1994). H i g h e r organisms m a y acquire t h e m t h r o u g h the f o o d f o l l o w e d b y a n absorption i n the gut, o r they m a y absorb t h e m directly f r o m the water t h r o u g h g i l l surfaces o r other external epithelia ( M a u c h l i n e and T e m p l e t o n 1964). O n c e w i t h i n the o r g a n i s m , the radioisotopes are treated the same w a y as their stable isotopes, o r other similar elements, a n d are accumulated  22  as non-radioactive elements. R a d i o i o d i n e , for example, is concentrated i n the t h y r o i d because it is similar t o stable Iodine. S t r o n t i u m is concentrated i n the skeleton o f vertebrates because o f its similarity w i t h C a l c i u m , and C e s i u m is concentrated i n muscles and flesh due to its similarity w i t h P o t a s s i u m (Bablet and Perrault 1987b). T h e first marine organisms to concentrate fallout material f o l l o w i n g a nuclear test are the p r i m a r y producers i n c l u d i n g p h y t o p l a n k t o n and algae. W i t h i n a f e w hours, these organisms can concentrate radioisotopes a thousand f o l d ( D o n a l d s o n 1959, S e y m o r e 1960, B a b l e t and Perrault 1987b). P l a n k t o n seems to have no preference but contains most o f the fallout radioisotopes f o u n d i n sea water ( S e y m o r e 1960). T h e most c o m m o n radioisotopes detected i n p r i m a r y producers w i t h i n a f e w w e e k s after a nuclear detonation at E n e w e t a k A t o l l are s h o w n i n T a b l e 2.5. F r o m p r i m a r y producers, the radioisotopes are disseminated to the rest o f the f o o d web as determined b y the prey / predator relationships and the selective uptake o f isotopes b y the organisms (see T a b l e 2.5). Table 2.5. Radioisotopes typically detected in marine organisms at Enewetak A t o l l following a nuclear detonation. Based on Bablet and Perrault (1987b), and Donaldson (1959). Type or organisms' Primary producers  Dominant radioisotopes Zirconium - Niobium, ' ' Cobalt, Zinc, ' Iron,  95  95  1 4 U 4 4  Herbivores (except  fish)  57  C e r i u m (rare earth),  58  103  60  65  55  59  ' R u f h e n i u m , Manganese 106  54  Cerium (rare earth), Ruthenium-Rhodium  Herbivorous fish (e.g., surgeonfish)  65  Zinc, ' ' Cobalt  First order carnivores (except fish)  144  57  58  60  Cerium, Ruthenium, ' Cobalt, Zinc, Zirconium - N i o b i u m , S i l v e r , Manganese, C e s i u m (only as trace element) 103,106  57,58  95  n 0 m  60  65  b  54  137  First order carnivorous fish  65  Second and higher order carnivores  65  Zinc, ' Iron, ' ' Cobalt, 55  59  57  58  137  Cesium  Zinc, C e r i u m (rare earth), ' Cobalt, R u t h e n i u m , traces of Manganese, Zirconium N i o b i u m , and C e s i u m 1 4 1 , 1 4 4  57,58  103,106  95  60  60  54  137  a. The organisms are arranged after trophic level with lower trophic level organisms mentioned first and higher trophic level organisms mentioned last in the column; b. T h e ' m ' indicates that the silver atom is an isomer, i.e., that it is in a long-lived excited state but eventually w i l l give off gamma rays (usually gamma rays are emitted instantly following an alpha or beta decay).  23  Strontium and  C e s i u m , w h i c h are b o t h considered hazardous t o humans because o f their  l o n g h a l f lives and similarity t o C a l c i u m and P o t a s s i u m , respectively, are not concentrated to any high extent i n marine organisms (Bablet and Perrault 1987b). In fish, the alimentary tract generally shows the greatest amount o f r a d i o a c t i v i t y f o l l o w e d b y the liver, skin, bone, and muscles ( D o n a l d s o n 1959).  2.3 Compartment  modeling.  A convenient w a y o f dealing w i t h w h o l e ecosystems and the transfer o f material amongst their components  is t h r o u g h  the use o f compartment  investigation is d i v i d e d into a number  models.  Here  the ecosystem  o f distinct functional g r o u p s  under  ('compartments')  c o m p r i s i n g either single species o r groups o f similar species, and the transport o f material between the g r o u p s is described as a flux per unit time. M a t h e m a t i c a l l y , the compartments are connected b y a set o f either linear o r non-linear equations, one f o r the balance o f each group ( O ' N e i l l 1979). F u r t h e r m o r e , depending o n whether the a p p r o a c h is d y n a m i c or static, the equations m a y be either differential or non-differential. C o m p a r t m e n t m o d e l s have been used extensively i n the study o f tracers dynamics (see f o r example the r e v i e w b y O ' N e i l l (1979)).  2.3.1  Ecopath.  O n e o f the latest approaches i n compartment m o d e l i n g is the E c o p a t h software based o n a concept originally p r o p o s e d b y P o l o v i n a and c o - w o r k e r s ( P o l o v i n a 1984, 1993). It has since been further developed b y V . Christensen and D . P a u l y (Christensen and P a u l y 1992a,  1992b,  1995) t o incorporate routines f o r n e t w o r k analysis and system maturity indices based o n the theory o f R E . U l a n o w i c z , H . T . O d u m and E . P . O d u m . It has furthermore been turned into an periodically updated software  distributed b y the International C e n t e r f o r L i v i n g  Aquatic  R e s o u r c e s M a n a g e m e n t ( I C L A R M ; see http://www.ecopath.org). E c o p a t h is a m o d e l i n g software that a l l o w s f o r the straightforward c o n s t r u c t i o n , analysis, and c o m p a r i s o n o f mass-balance t r o p h i c models ( V a s c o n c e l l o s et al. 1997) (see F i g u r e 2.3). It is applicable f o r w e l l defined ecosystems i n either 'steady-state' o r i n w h i c h biomass changes d o occur. A n important constraint i n E c o p a t h is that d u r i n g the time p e r i o d considered, the energy entering any functional g r o u p must balance the energy leaving the g r o u p plus whatever energy  24  is accumulated w i t h i n the g r o u p (the mass-balance concept). T h u s , E c o p a t h can be compared to a b o o k k e e p i n g system where every flux must be accounted for. Assuming  similar conditions over the time p e r i o d c o v e r e d  by the  m o d e l , the  trophic  interactions a m o n g the functional groups o f the ecosystem can be described by a set o f linear mass-balance equations w h e r e i n P r o d u c t i o n by (i) = all predation o n (i) + non-predation losses o f (i) + export o f (i)  (2.8)  w h i c h may also be w r i t t e n P -M2 -P (l-EE )-EX 1  i  I  1  1  = 0  (2.9)  where; P i is the p r o d u c t i o n o f i ; M 2 ; is the predation mortality o n i ; E E ; is the ecotrophic efficiency o f i , or the fraction o f the p r o d u c t i o n o f i that is c o n s u m e d w i t h i n the system and exported or harvested ( E E ; is usually left as the u n k n o w n to be estimated w h e n solving E q u a t i o n (2.9)); 1-EEj is the 'other m o r t a l i t y ' , i.e., the non-predation losses o f i , or the fraction o f the p r o d u c t i o n o f i that flows to detritus; and E X ; is the export o f i. E q u a t i o n (2.9) can be re-expressed as: B,  (P/B),-±B  1  • (Q/B)j • DCji - B , •(P/B)  i  (l-EE^-EX, = 0  (2.10)  J=I  or B , .(P/B). E E , - I B  J  (Q/BV  DCjj - E X , = 0  (2.11)  j=i  where; B ; is the biomass o f i during the p e r i o d considered; P / B ; is the production/biomass ratio o f i w h i c h , under the assumption o f equilibrium, is equal to the total mortality rate (Z;) (Christensen and P a u l y 1992b); Q/Bj is the consumption/biomass ratio o f i ; and D C j i is the fraction o f prey i i n the average diet o f predator j. B a s e d o n E q u a t i o n (2.11), for an ecosystem w i t h n functional groups, a system o f n linear equations can be set up:  25  B, (P/B)j EE, - B j (Q/B), DC;, - B , ( Q / B ) • D Q - . . . - B - ( Q / B ) DC;, - E X , =0 2  n  (2.12)  n  EL • (P/B) • EE, - f i , • (Q/EI), • DC, - E L • (Q/E!) • D C ^ - . - B , , • (Q/E!) • DC^ - E X , =0 2  2  2  n  B • (P/B) • E E , - B , • (Q/B), • DC, - B , • (Q/B) • DC,,,-. - B , • (Q/E!) • D C - E ^ , =0 n  n  n  2  n  m  T h i s system o f linear equations can be s o l v e d u s i n g standard m a t r i x algebra (Christensen and P a u l y 1992a, 1992b). O n l y one o f the input parameters: B , ( P / B ) ;  i;  ( Q / B ) ; o r E E ; , may i n  general be left u n k n o w n , w h i l e the diet c o m p o s i t i o n matrix, exports, and harvests always must be p r o v i d e d . The  solution o f  E q u a t i o n (2.11)  allows  calculation o f  the  energy  balance  of  each  compartment, u s i n g C o n s u m p t i o n b y (i) = p r o d u c t i o n by (i) + respiration by (i) + unassimilated f o o d b y (i) R e a r r a n g i n g the equation, respiration can be quantified g i v e n the other  (213) flows:  R e s p i r a t i o n b y (i) = c o n s u m p t i o n by (i) - p r o d u c t i o n b y (i) - unassimilated f o o d b y (i)  (214)  In E c o p a t h , the mass-balance concept implies that E q u a t i o n s (2.8) t h r o u g h (2.13) applies for all compartments o f the ecosystem, i.e., that the estimated E E ; range between 0 and 1 (a diagnostic for mass-balance).  2.3.2  Ecoranger  T h e majority o f E c o p a t h models so far have been created w i t h a single set o f mean input parameters for the p e r i o d under consideration, and the researchers w e r e unable to take into account the large uncertainties that tend to a c c o m p a n y b i o l o g i c a l data. T h i s rather critical point has n o w been s o l v e d w i t h the i n t r o d u c t i o n o f E c o r a n g e r (Christensen and P a u l y 1995), an E c o p a t h routine that a l l o w s one to enter, for each input parameter, a mean o r m o d e value, a range, and a distribution. T h e shape o f the distribution depends o n o n e ' s p r i o r k n o w l e d g e o f the data and may be either u n i f o r m , triangular o r n o r m a l . O n c e the routine is r u n n i n g , input variables f o r each parameter type are d r a w n r a n d o m l y f r o m the specified distributions and the resulting models are evaluated. O n l y models that pass the constraints o f mass-balance and  26  w h i c h are t h e r m o d y n a m i c a l l y possible are accepted. T h e process is repeated i n a M o n t e - C a r l o fashion where the user specifies the number o f realizations a n d desired successful  runs  (accepted models). O f the accepted m o d e l s the 'best m o d e l ' i n a least-square sense (i.e., that w i t h the least square d e v i a t i o n f r o m the modes o r means) is saved a n d used f o r further analysis.  I Apex predators B-2.5  Q.  O  Benthic producers B = 1,300  Detritus B = 2,000  Figure 2-3. Schematic representation o f an Ecopath model o f a coral reef i n the V i r g i n Islands, Caribbean (Opitz 1996). The functional groups are arranged along the vertical axis according to their trophic level. The area o f each box is proportional to the logarithm o f the biomass of the corresponding functional group. Flows exit a box from the upper half and enters a box in the bottom. Flows cannot be divided, but can merge with flows from other boxes.  27  3. Methods T h e f o l l o w i n g chapter describes the m e t h o d o l o g y applied i n the study and is d i v i d e d into three main parts. I n the first part, the m o d e l e d section o f the atoll perimeter is defined and the z o n a t i o n across the reef section is described. T h e second part is d e v o t e d to the process o f d e r i v i n g the m o d e l input parameters for the seventeen non-fish and ten fish g r o u p s included i n the m o d e l . L a s t l y , the o r i g i n and ' p r o c e s s i n g ' o f the radioactivity data is described, and the theory o f c o m b i n i n g the m o d e l outputs w i t h the radioactivity data to simulate the observed trends i n radioactivity over time is explained.  3.1  Defining  the modeled area.  A s mentioned i n section 1.2, E n e w e t a k atoll may be d i v i d e d into f o u r parts: the w i n d w a r d reef, the leeward reef, and t w o transitional reefs. T h e majority o f the b i o l o g i c a l research has been c o n d u c t e d o n the w i n d w a r d reef i n c l u d i n g the study by O d u m and O d u m (1955) s u m m a r i z e d i n section 1.4. T h e E c o p a t h m o d e l was therefore restricted t o this area stretching f r o m , but not i n c l u d i n g , E n e w e t a k Island i n the south up to, and i n c l u d i n g , B o g o n Island i n the north as s h o w n i n F i g u r e 3.1. BOGON is. TRADES  JAPTAN IS.  ENEWETAK IS.  Figure 3-1. Cross-reef currents and channel currents. Redrawn and modified from Atkinson et al. (1981).  28  T h e w i n d w a r d reef itself may be d i v i d e d into distinct zones, perpendicular t o the prevailing w e s t w a r d m o v i n g N o r t h E q u a t o r i a l Current, each z o n e w i t h a characteristic flora and fauna ( L a d d 1973). G d u m a n d O d u m (1955) distinguished between six zones o n their transect (see F i g u r e 1.4), a z o n a t i o n that is fairly t y p i c a l o f the central and southeastern w i n d w a r d reef ( C o l i n 1987a). I n this study, however,  part o f the  only five zones w e r e distinguished,  beginning f r o m the oceanic side: fore reef, algal ridge, r e e f flat, c o r a l head zone, and sand / shingle z o n e (Figure 3.2).  Sand / shingle zone  Coral head zone  Reef flat  Algal ridge  Fore reef zone  Figure 3-2. Zonation across the windward reef as defined in the present study. Redrawn and modified from Johannes and Gerber (1974).  T h e area o f each z o n e w a s determined f r o m a d i g i t i z e d bathymetric map o f the atoll (see Table 3.1). A short description o f the five zones f o l l o w s b e l o w .  Table 3.1. The area of the five zones across the windward reef as determined from a digitized map of the atoll (Anon. 1944). Islands were included under the reef flat area. Zone  Depth range (m) 0-20 0 0 0-4 4-20  Fore reef A l g a l ridge Reefflat Coral heads Sand / shingle a  b  a. b. c. d. e.  e  M e a n depth jm)  Area (km )  10.00 0.25 0.60 2.00 12.00  0.83 1.15 3.45 2.24 10.18  Defined as A of the 0 m depth zone; Defined as A of the 0 m depth zone; Defined as V of the area down to 100m depth; From Figure 2 in Buddemeier (1975), the depth at mean tide; A s identified from a bathymetric map (Anon. 1944). l  3  5  29  d  d  2  3.1.1  F o r e reef.  T h e fore reef area, w h i c h is located seaward o f the algal ridge, has never been accurately determined, but C o l i n (1987a) suggested that it is about 3 t o 4 times smaller than the reef flat. It ranges i n w i d t h f r o m about 3 0 0 m i n the south t o less than 100 m i n the n o r t h ( C o l i n 1987a). A t y p i c a l spur and g r o o v e system, f o r m e d b y encrusting coralline algae ( M a r s h 1970), characterizes the zone immediately seaward o f the algal ridge ( W i e n s 1962, C o l i n  1987a,  R i s t v e t 1987). Invertebrates such as sea urchins are abundant o n the sides o f the spurs w h i l e the grooves are f l o o r e d w i t h boulders and cobbles that are m o v e d b y the currents, preventing organisms f r o m settling. F i s h (including herbivores parrotfish a n d surgeonfish that m o v e onto the algal ridge a n d reef flat at h i g h tide, see section 5.1.2.4) are numerous ( C o l i n 1987a). S e a w a r d o f the spur and g r o o v e system, the b o t t o m slopes gently d o w n t o about 18-23 m depth where a sharp d r o p - o f f begins. A f e w corals (primarily the v a s i f o r m Acropora  cytherd)  can be f o u n d i n this area, however, the b o t t o m is m o s t l y c o v e r e d b y r o c k s , many w i t h signs o f b o r i n g c l i n o i d sponges ( S m i t h and H a r r i s o n 1977, C o l i n 1987a).  3.1.2  A l g a l ridge.  T h e spur a n d g r o o v e system leads u p to a marginal algal ridge l o c a t e d w i t h i n the surf zone. S o m e o f the g r o o v e s  continue beneath the algal ridge a n d reef flat, f o r m i n g large  surge  channels. L o n g sections o f the algal ridge are d e a d , w h i c h is l i k e l y a result o f w a r t i m e o i l 4  p o l l u t i o n ( L a d d 1973) (see section 1.4). I n general, the algal ridge is p o o r l y  developed,  consisting o f a n a r r o w band o f corals and (mostly soft) algae. O d u m and O d u m (1955) found that the encrusting y e l l o w c o r a l Acropora  palmerae,  P o c i l l o p o r a , and Millepora  platyphylla  c o v e r e d u p t o 5 0 % o f the area, w h i l e S m i t h and M a r s h (1973), o n a transect close to O d u m s ' , found that the c o r a l c o v e r w a s m u c h less. D o m i n a n t algae o n the algal ridge are the fleshy algae Dictyosphaeria  intermedia,  Zonaria  variegate,  D i c t y o t a as w e l l as the calcareous r e d algae Porolithon  Caulerpa  Assumed to be the situation throughout the.period covered by the model. 30  C e r a m i u m , and  onkodes ( O d u m a n d O d u m 1955,  S m i t h and M a r s h 1973).  4  elongata,  3.1.3  R e e f flat.  T h e r e e f flat varies i n w i d t h f r o m 9 0 - 160 m , and is m o s t l y c o v e r e d b y water. It consist o f sandy areas and s m o o t h r o c k s that slope gradually t o w a r d s the l a g o o n ( L a d d 1973). T h e zone is paved w i t h coralline algae such as Jania  capillacea  a n d P o r o l i t h o n ( S m i t h 1973b, S m i t h  and M a r s h 1973). C o r a l s are sparse a n d c o v e r m u c h less than h a l f o f the area. T h e most conspicuous corals are Acropora  and Millepora.  F i l a m e n t o u s red, - b r o w n , - a n d green algae,  cyanobacteria a n d foraminiferans f o r m heavy mats throughout the area ( O d u m a n d O d u m 1955, L a d d 1973).  3.1.4  C o r a l head zone.  T h e c o r a l head z o n e is strictly subtidal and located t o w a r d s the l a g o o n . It is r i c h o n corals such as r o u n d e d heads o f Favia pallida  and Cyphastrea serailia,  m i c r o a t o l l s (colonies where  the central part is dead but the sides are still thriving) o f Porites lutea, branching forms o f A.  cymbicyathus,  Pocillopora,  Stylophora,  a n d the blue  coral  Acropora  gemmifera,  Turbinaria  mesenterina. Strips o f sand, shingle, and cobble runs b e t w e e n the corals. T h e area  varies i n w i d t h f r o m about 2 0 0 m i n O d u m s ' study area t o about 1 k m i n the north. F i s h are abundant ( O d u m and O d u m 1955, S m i t h and M a r s h 1973, Johannes and. G e r b e r 1974, C o l i n 1987a).  3.1.5  S a n d / shingle.  T h e central l a g o o n is b o r d e r e d b y a terrace dotted w i t h n u m e r o u s p a t c h reefs. T h e terrace varies i n w i d t h f r o m a f e w hundred meters i n the south t o m o r e than 1 k m i n the n o r t h (Ristvet 1987). T h e depth at the outer edge o f the terrace is about 15-22 m ( W a r d l a w et al. 1991). T h e patch reefs w e r e i g n o r e d i n this study. Instead the area w a s considered t o be u n i f o r m l y c o v e r e d b y sand and shingle ( p r o d u c e d upstream). Foraminiferans a n d filamentous algae, the latter l i v i n g w i t h i n the c o r a l shingle, are very abundant ( O d u m and O d u m 1955).  3.2 Validating the Ecopath model. T h e data used f o r the c o n s t r u c t i o n o f the E c o p a t h m o d e l w e r e a l l f r o m the published literature. T h e y represent m o r e than 3 0 years o f research, ranging f r o m the study b y O d u m and O d u m (1955) i n 1954 t o studies w e l l into the 1980s. T h i s rather large time span w a s  31  justified as c o r a l reefs are k n o w n t o be v e r y stable systems changing little over time ( O d u m and O d u m 1955). I n a f e w cases, data were i m p o r t e d f r o m similar systems i n other parts o f the w o r l d . Seventeen non-fish and ten fish groups w e r e identified, and biomass estimates f o r each group and f o r each z o n e w e r e obtained. T h e estimates w e r e subsequently averaged into a single w e i g h t e d biomass estimate f o r each group.  3.2.1  N o n - f i s h groups.  A qualitative d e s c r i p t i o n o f the non-fish groups is g i v e n b e l o w , w h i l e the E c o p a t h parameters ( B , P / B , a n d Q / B ) are explained i n Table 3.3 a n d the remarks f o l l o w i n g the table. A diet matrix can be f o u n d i n A p p e n d i x 1.  3.2.1.1  Detritus.  D e t r i t u s consist o f dissolved a n d particulate organic matter ( D O M a n d P O M ) . D O M stems f r o m p h y t o p l a n k t o n , benthic algae, and corals that excrete large fractions o f their primary p r o d u c t i o n directly into the water. It is an important source o f energy f o r filter feeding organisms i n c l u d i n g bacteria, z o o p l a n t k o n , bivalves,  sponges,  polychaetes,  tunicates and  corals. P O M consist o f dead organic matter i n c l u d i n g excrements, feces, non-assimilated f o o d , etc. It is c o l o n i z e d b y bacteria and algae, and is c o n s u m e d b y a variety o f filter-feeders a n d fish ( S o r o k i n 1990).  3.2.1.2 Benthic Primary  Producers.  T h i s g r o u p consist o f all p r i m a r y producers associated w i t h the benthic environment such as encrusting, matted, a n d fleshy green algae,  calcareous  r e d algae,  attached t o dead c o r a l fragments / heads (mainly Halimedd),  large branching algae  free-living small algae, b o r i n g  red a n d green algae, a n d cyanobacteria. A l l i n all, 2 3 8 species o f benthic algae have been identified at E n e w e t a k A t o l l (see T a b l e 3.2). B e n t h i c algae fragments f r o m the reef front constitute a large fraction o f the p l a n k t o n over the reef and is u t i l i z e d b y many herbivores and detritivores ( W i e b e et al. 1975).  32  Table 3.2. Marine benthic algae at Enewetak Atoll. From Tsuda (1987). Number o f species  Division  16 89 24 109  Cyanophyta (cyanobacteria) Chlorophyta (green algae) Phaeophyta (brown algae) Rhodophyta (red algae)  3.2.1.3  Phytoplankton.  Sargent and A u s t i n (1949) measured an extremely l o w concentration o f p h y t o p l a n k t o n i n the lagoon o f Enewetak  Atoll,  supporting the general b e l i e f that  p h y t o p l a n k t o n is o f no  significance i n c o r a l reef ecosystems. S o r o k i n (1993), h o w e v e r , has recently p r o v i d e d several examples o f p h y t o p l a n k t o n b l o o m s i n atoll lagoons,  a n d C o l i n (1987a) has o n several  occasions observed large p h y t o p l a n k t o n b l o o m s i n the l a g o o n o f E n e w e t a k A t o l l (perhaps an artifact o f the nuclear testing). T h i s inconsistency b e t w e e n observations, a n d a general lack o f data f r o m reef zones other than the l a g o o n , meant that the biomass o f p h y t o p l a n k t o n w a s left as the u n k n o w n t o be estimated b y E c o p a t h (see section 2.3.1).  3.2.1.4  Zooplankton.  T h i s g r o u p consist o f m e r o p l a n k t o n ('temporary' z o o p l a n k t o n such as fish - a n d invertebrate larvae) and h o l o p l a n k t o n ('full-time' z o o p l a n k t o n ) . I n a study o f the fish and z o o p l a n k t o n at E n e w e t a k A t o l l , H o b s o n a n d Chess (1978) discovered that p l a n k t i v o r o u s fish concentrate i n areas o f strong current d u r i n g the day, where they feed o n z o o p l a n k t o n o f oceanic origin. I n contrast, n o c t u r n a l p l a n k t i v o r o u s fish concentrate i n areas o f w e a k currents where they feed o n resident z o o p l a n k t o n that enter the water c o l u m n at night i n concentrations 2-3 times higher than the day time concentrations. " . . . z o o p l a n k t o n is extremely abundant i n reef waters and so is an important component o f the c o r a l reef e c o s y s t e m . . .  S u c h i n f o r m a t i o n as is  available shows that the largest z o o p l a n k t o n biomass c o u l d be f o u n d at night u p the shallow reef areas w i t h patch reefs c o v e r e d w i t h l i v i n g corals o r w i t h r u b b l e . . . , i.e., i n places where i n accordance w i t h earlier d a t a . . . it ought to be lowest, b e i n g depleted b y b o t t o m sessile predators, and especially c o r a l s " ( S o r o k i n 1993). There is a general lack o f z o o p l a n k t o n data (and other data) f r o m the fore reef w h i c h is physically v e r y difficult t o monitor. H a m n e r et al. (1988), h o w e v e r , w a s able t o sample the w i n d w a r d side o f D a v i e s Reef, A u s t r a l i a , a n d f o u n d that z o o p l a n k t o n is a major source o f  33  energy to the reef. P l a n k t i v o r o u s fish l i v i n g o n the fore reef f o r m a " w a l l o f m o u t h s " that effectively removes the z o o p l a n k t o n before the water hits the reef. A s most investigations thus have underestimated the biomass o f z o o p l a n k t o n , it w a s left to be estimated b y E c o p a t h .  3.2.1.5 Corals and sea anemones (Class anthozoa). T h i r t y eight species o f o c t o c o r a l s ( O c t o c o r a l l i a ) and 169 species o f stony corals (Scleractinia) have been identified at E n e w e t a k A t o l l ( B u r c h 1987, D e v a n e y and L a n g 1987). Sea anemones are m u c h less abundant than corals, and no t a x o n o m i c w o r k has been published (Cutress and A r n e s o n 1987). It has been estimated that there is about three times as m u c h p r i m a r y p r o d u c e r biomass i n corals as there is animal biomass ( O d u m and O d u m 1955). T h e p r i m a r y p r o d u c e r s consisted o f b o r i n g filamentous algae and zooxanthellae (in the ratio 16:1). I n this study,  however,  zooxanthellae w e r e i n c l u d e d i n the c o r a l biomass. Since the plant b i o m a s s is l o c a t e d w i t h i n the c o r a l skeleton, it does not receive e n o u g h light to contribute significantly to the reefs primary p r o d u c t i o n ( L e w i s 1981, M a r s h 1987). A l t h o u g h some corals are capable o f obtaining all their energy f r o m the zooxanthellae ( M a r s h 1987), most hermatypic corals feed autotrophically, as predators, and as filter feeders all at the same time. C o r a l s primarily feed at night, but some also feed d u r i n g day o r at d u s k and d a w n ( S o r o k i n 1990, 1993). Scleractinian corals have been s h o w n t o feed o n " c o p e p o d s , ostracods, mysids, chaetognaths, appendicularians, nematods, polychaetes, small j e l l y fish and salps. T h e d o m i n a t i n g c o m p o n e n t s i n the gut contents w e r e z o e a and c o p e p o d s . T h e suspended organic material ingested b y c o r a l s . . . i n c l u d e d bacteria, p r o t o z o a , detritus, and dead z o o p l a n k t e r s . . . " ( S o r o k i n 1993).  3.2.1.6 Foraminiferans  and other protozoans.  A p p r o x i m a t e l y 2 8 0 species o f foraminifera and n o n p l a n k t o n i c p r o t o z o a n s have been identified at E n e w e t a k A t o l l ( C h a v e and D e v a n e y 1987). T h e p r o t o z o a n fauna is fairly t y p i c a l o f the W e s t e r n P a c i f i c t h o u g h they are particular scarce o n some o f the n o r t h e r n islands. T h i s , h o w e v e r , m a y v e r y w e l l be a result o f the nuclear testing that t o o k place i n the area (Hirshfield et al. 1968).  34  Foraminiferans are an important f o o d  source  f o r many benthic invertebrates i n c l u d i n g  holothurians, sea urchins, polychaetes and shrimps as w e l l as f o r fish that graze and scrape the c o r a l surfaces a n d sandy substrates ( S o r o k i n 1993). L i p p s a n d D e l a c a (1980) identified approximately  2 0 0 shallow  water  species.  A  large  number  o f suspension  feeding  foraminiferans, many containing zooxanthellae, w e r e f o u n d i n c r y p t i c habitats w h e r e they live protected f r o m their predators. F i l a m e n t o u s a n d mat-like types, o n the other hand, have adapted t o the h i g h predation pressure t h r o u g h a h i g h turnover rate. S y m b i o t i c foraminiferans are amongst the most important p r i m a r y p r o d u c e r s i n the sand / shingle zone ( S o r o k i n 1993). Foraminiferans feed either autotrophically o r o n bacteria, algae, other benthic protozoans, and eggs and larvae o f meiobenthic organisms ( S o r o k i n 1993).  3.2.1.7  Gastropods.  A total o f 1116 species o f marine m o l l u s k s have been identified at E n e w e t a k A t o l l , 9 9 4 o f w h i c h are gastropods ( K a y a n d J o h n s o n 1987). C o n u s , M o u r l a , D r u p a , Thais, a n d C y p r a e a are particular abundant o n the reef flat ( R e n a u d 1976, K o h n 1980, M i l l e r 1982). " G a s t r o p o d s are m u c h m o r e abundant o n intertidal benches than o n m o r e c o m p l e x a n d benign subtidal c o r a l reefs i n the same regions, although species diversity is considerably lower... w i t h particular attention t o the genus C o n u s " ( K o h n and L e v i t e n 1976). M a n y gastropods are important predators o n other gastropods and o n polychaetes. T h e diet o f Drupa morum, e.g., consisted o f 4 4 % vermetids, 4 2 % nereids, 5 % other polychaetes, and 9 % crustaceans ( K o h n 1987).  3.2.1.8  Bivalves.  O n e hundred and fifteen different species o f bivalves have been identified at E n e w e t a k A t o l l ( K a y and J o h n s o n 1987), and t w o groups w e r e distinguished i n the E c o p a t h m o d e l : tridacnids (giant clams) and 'other bivalves'. G i a n t clams, like 'other b i v a l v e s ' , are filter feeders but, i n addition, contain symbiotic zooxanthellae w h i c h under favorable conditions m a y supply u p t o 1 0 0 % o f the giant clams energy requirement ( H e s l i n g a and Fitt 1987). I assumed that giant  35  clams, as a g r o u p , obtain 7 5 % o f their energy f r o m symbiotic zooxanthellae and the remaining 2 5 % f r o m feeding o n p h y t o p l a n k t o n . 5  F e w records o f bivalves other than giant clams w e r e f o u n d i n the literature, but S o r o k i n (1993) mentioned that bivalves (including giant clams) " c o m p r i s e 1 0 - 3 0 % o f the malacofauna  reefs  and about the same part o f its total biomass". M a n y bivalves bore into corals  and r o c k s w h i c h might explain that they have been somewhat  o v e r l o o k e d . B i v a l v e s are  numerous i n the sand / shingle zone ( R i d d l e et al. 1990).  3.2.1.9 Shrimps and lobsters. Approximately  150  species  of  decapod  shrimps and  lobsters  (infraorders:  Penaeidea,  Stenopodidea, C a r i d e a , and Palinura) have been identified at E n e w e t a k A t o l l ( D e v a n e y and B r u c e 1987). N o t i n c l u d e d i n this number are the callianassid shrimp (ghost / b u r r o w i n g shrimp) l i v i n g i n the sand / shingle zone. T h o u g h they represent some o f the most abundant infauna i n this area, no biomass estimate has been derived ( S u c h a n e k and C o l i n  1986,  Suchanek et al. 1986). "Callianassids are amongst the most elusive o f c o r a l reef animals. T h e i r high density (indicated b y the frequency o f their feeding m o u n d s ) and h i g h sediment-turnover rates... suggest they are major consumers. N o satisfactory technique has yet been developed to quantify these animals o r their c o n t r i b u t i o n to total c o m m u n i t y m e t a b o l i s m " ( R i d d l e et al. 1990). D e v a n e y and B r u c e (1987) discovered four species o f lobster o n the w i n d w a r d reef. penicillatus,  Panulirus  w h i c h lives o n the outer reef slope d u r i n g day and m o v e s onto the reef flat at  night, w a s particularly c o m m o n (Ebert and F o r d 1986).  3.2.1.10  Stomatopods.  S t o m a t o p o d s w e r e i n c l u d e d as a g r o u p because they often o c c u r i n the diet o f other groups. T w e l v e species o f stomatopods, considerably smaller than the same o r related species f o u n d i n other parts o f the I n d o - W e s t P a c i f i c area, have been identified at E n e w e t a k A t o l l ( R e a k a and M a n n i n g 1987). T h e biomass o f the g r o u p w a s left to be estimated b y E c o p a t h .  After completion of this study, Dr. R.E. Foreman (pers. com.) has later noted that giant clams also feed extensively on DOM. 5  36  3.2.1.11 Miscellaneous  crustaceans.  T h i s g r o u p consist p r i m a r i l y o f crabs f r o m the infraorders B r a c h y u r a and A n o m u r a , but also includes other similar sized crustaceans, as w e l l as amphipods and isopods. Seventy six species o f A n o m u r a n crabs and 291 species o f B r a c h y u r a n crabs ( 5 3 % xanthid) have been identified at E n e w e t a k A t o l l ( G a r t h et al. 1987). A c c o r d i n g to K o h n (1987), seven out o f eight o f the most c o m m o n xanthid species studied w e r e herbivores. O n the r e e f flat, h o w e v e r , several xanthid species have been f o u n d to be important carnivores.  3.2.1.12 Echinoderms - not including This group  holothurians.  consist o f O p h i u r o i d e a (basket  stars / brittle stars), A s t e r o i d e a (sea  stars),  E c h i n o i d e a (sea urchins and heart urchins), and C r i n o i d e a (sea lilies). N i n e t y seven species have been identified at E n e w e t a k A t o l l (Devaney 1987a). B r i t t l e stars o f the genus Ophiocoma  can be found i n all zones ( C h a r t o c k 1983a),  o p e n sandy areas are dominated b y irregular herbivores sea urchins ( C o l i n 1987a).  however, Ophiocoma  are suspension and deposit feeders eating algae, and detritus. S o m e "specimens inhabiting the reef floor occasionally contained foraminiferans, sponge spicules, crustacean (e.g., isopod) skeletal parts, nematodes, and juvenile snail s h e l l s . . . " ( C h a r t o c k 1983a).  3.2.1.13  Holothurians.  Sea cucumbers have few i f any predators and are very abundant i n the atoll environment. Holothuria  atra  is, a c c o r d i n g to K o h n (1987), "the  most  conspicuous  deposit-feeding  invertebrate o n interisland platforms." T w e n t y species o f sea cucumbers f r o m five genera have been identified at E n e w e t a k A t o l l ( B u r c h 1987, Cutress and R o w e 1987). L a w r e n c e  (1980)  studied eight o f the most conspicuous species and f o u n d a distinct d i s t r i b u t i o n o n the reef flat, w i t h only t w o c o - o c c u r r i n g species. B a k u s (1968) reported an average density o f difficilis  Holothuria  o f 1 t o 32 individuals per 9 0 0 c m i n daytime, but up to 2 0 0 individuals per 9 0 0 c m 2  2  at night o n the tops o f slab r o c k s i n certain areas. B a c t e r i a and foraminiferans are major sources o f f o o d for holothurians ( B a k u s 1973), t h o u g h the foraminiferans probably pass t h r o u g h the digestive tract w i t h o u t m u c h effect, leaving bacteria and organic detritus as the m a i n sources o f energy. A n o t h e r important source energy is dissolved organic matter that the holothurians obtain directly f r o m the water.  37  of The  feces o f H. difficilis  contains " l i v i n g and dead filamentous blue-green a n d r e d algae, fish eggs,  unidentified detritus, sponge spicules, c o p e p o d exuvia, foraminiferans, fragments o f sea u r c h i n spines, h o l o t h u r i a n ossicles, gastropods, fish teeth and calcareous fragments" ( B a k u s 1968). W e b b et al. ( 1 9 7 7 ) estimated an assimilation efficiency f o r / / , atra o f 4 0 % .  3.2.1.14 Polychaetes and other worm like invertebrates. A total o f 132 species o f polychaetes f r o m 34 families have been identified at E n e w e t a k A t o l l ( D e v a n e y and B a i l e y - B r o c k 1987). Polychaetes play an important role as bioeroders and as f o o d f o r a variety o f fish and invertebrates, particularly m o l l u s k s ( S o r o k i n 1993). T h e algal ridge is d o m i n a t e d b y c a r n i v o r o u s nereid type annelids, the r e e f flat b y sedentary annelids and nereid type annelids, and the c o r a l head zone b y sedentary species l i v i n g w i t h i n the c o r a l heads ( O d u m and O d u m 1955). Polychaetes are suspension feeders, deposit feeders and carnivores, p r e y i n g o n encrusting invertebrates such as corals ( K o h n 1987). A c c o r d i n g t o S o r o k i n (1993), the s h a l l o w parts o f a c o r a l reef contains approximately 3 0 % filter feeding polychaetes, 4 0 % detritophages and o m n i v o r o u s polychaetes, and 3 0 % predatory polychaetes.  3.2.1.15 Sessile  invertebrates.  B e s i d e s sponges, this g r o u p comprises h y d r o z o a , chordates, hemichordates, and other sessile invertebrates. F o r t y species o f sponges  have been identified at E n e w e t a k A t o l l . B o r i n g  sponges are "the most c o m m o n infaunal associates o f the corals studied, w i t h 8 6 % o f the corals s h o w i n g sponge b i o e r o s i o n effects" ( D e v a n e y 1987b). " B o r i n g sponges c a n contribute up t o 2 5 % o f the total e r o s i o n o f the substratum o n E n e w e t a k . . . and are considered major eroders o n most c o r a l r e e f s . . . " ( R u s s o 1980).  3.2.1.16  Cephalopods.  C e p h a l o p o d s w e r e i n c l u d e d as a g r o u p because they often o c c u r i n the diet o f other groups. N o parameters pertaining particularly t o cephalopods f r o m E n e w e t a k A t o l l w e r e f o u n d i n the literature.  38  3.2.2 B i o m a s s , P / B , and Q / B values o f non-fish groups. Table 3.3 summarizes the biomass, production/biomass ( P / B ) , a n d consumption/biomass ( Q / B ) values f o r the seventeen non-fish groups i n c l u d e d i n the E c o p a t h m o d e l . Table 3.3. Summary table o f the biomass , P/B, and Q/B values o f the non-fish groups included in the 6  Ecopath model.  3  Functional group  Biomass (t wwkm" -year" )  Remark  185 3255  1 2  ? ?  -  212 33 16 6 21 3 ?  3 4 5 6 7 8  6 93 42 29 37 ?  9 10 11 12 13  2  Detritus Benthic primary prod. Phytoplankton Zooplankton Corals Foraminiferans Gastropods Giant clams Bivalves Shrimp and lobster Stomatopods M i s c . crustaceans Echinoderms Holothurians Polychaetes Sessile invertebrates Cephalopods  P/B (year" )  Remark  n.a. 2.0 593.0 55.0 2.0 14.0 2.2 0.2 2.3 4.6  -  -  1.8 4.3 1.2 0.2 5.8 2.3 2.1  Q/B (year" )  Remark  n.a. n.a. n.a. 165 4 21 9 3 10 27 27 30 4 4 24 29 7  -  1  1  !  14 15 16 18 20 22 24 22 26 28 29 17 31 32 33 33  17 19 21 23 25 17 27 28 29 30 30 32 33 33  a. The remarks are explained in the text that follows the table. Dashes indicate that no source was found, and question marks indsicate that the value was estimated by Ecopath. n.a. = not applicable.  3.2.2.1 Remarks to Table 3.3. 1) Table 3.4 summarizes the biomass estimates o f detritus ( P O M a n d D O M ) i n the different reef zones. T h e w e i g h t e d mean f o r the reef as a w h o l e w a s 185 t w w - k m "  2  2) O d u m and O d u m (1955) estimated the biomass o f benthic p r i m a r y producers, i n c l u d i n g zooxanthellae, i n all o f their zones. I g r o u p e d zooxanthellae w i t h their s y m b i o t i c counterparts (corals,  foraminiferans, and giant  clams)  and used  a ratio o f 16:1  plant biomass  to  zooxanthellae ( O d u m and O d u m 1955) t o derive the zooxanthellae biomass i n corals (see section 3.2.1.5) and subtract it f r o m the O d u m s ' benthic p r i m a r y p r o d u c e r estimate.  Wet weight was used as the model 'currency', however, Dr. R.E. Foreman (pers.com.) has later noted that organic weights (C), especially when working with radioisotopes, are preferrable. 6  39  T a b l e 3.5 summarizes the benthic primary p r o d u c e r estimates i n the different reef zones. T h e w e i g h t e d mean for the reef as a w h o l e w a s 3255 t w w - k m " . 2  3) T a b l e 3.6 summarizes the c o r a l biomass estimates i n the different r e e f zones. T h e w e i g h t e d mean for the r e e f as a w h o l e w a s 212 t w w - k m " . 2  4) T a b l e 3.7 summarizes the foraminiferan biomass estimates i n the different r e e f zones. T h e w e i g h t e d mean f o r the reef as a w h o l e w a s 33 t w w - k m " . 2  5) T a b l e 3.8 summarizes the g a s t r o p o d biomass estimates for the different reef zones. T h e w e i g h t e d mean for the reef was 16 t w w - k m " . T h i s is a v e r y conservative estimate. M i l l e r 2  (1982) f o u n d a density o f detritus-feeding vermetids (sessile w o r m snails) o n the reef flat o f 151-1084 per m w h i l e the biomass estimate i n Table 3.8 o n l y includes species o f the genus 2  Thais. 6) O d u m and O d u m (1955) estimated the biomass o f small giant clams and small herbivorous m o l l u s k s (gastropods) i n the c o r a l head zone. B a s e d o n their c o m m e n t s , I assumed that the small h e r b i v o r o u s m o l l u s k s consisted o f 1/3 giant clams and 2/3 gastropods. T h i s resulted i n a biomass estimate o f giant clams o f 35.94 t w w - k m " i n the c o r a l head z o n e (conversion: d w = 2  1 0 % w w ( O p i t z 1996)), and a w e i g h t e d mean for the reef as a w h o l e o f 6.2 t w w - k m " . 2  7) R i d d l e et al. (1990) estimated a biomass o f bivalves o f 37 t w w - k m " i n the l a g o o n o f 2  D a v i e s Reef, A u s t r a l i a (conversion: 1 g C = 2 g organic matter (ash) ( R i d d l e et al. 1990), and ash = 8 % w w (Sambilay 1993)). A s s u m i n g that this estimate also applies for the l a g o o n o f E n e w e t a k A t o l l , a w e i g h t e d mean o f 2 1 . 1 1 w w - k m " for the reef as a w h o l e w a s derived. 2  8) E b e r t and F o r d (1986) estimated a total p o p u l a t i o n o f 7 8 0 0 lobsters o n the w i n d w a r d reef (reef flat and fore reef zone). W i t h a mean carapace length o f 91.6 m m for males and 81.2 m m for females, assuming a sex ration o f 1:1, and a p p l y i n g a w e i g h t - l e n g t h relationship o f W = 0.0021-L  2 7 7 3  , a total biomass o f 0.716 t w w - k m " w a s derived (for the fore reef, algal ridge 2  and reef flat). O d u m and O d u m (1955) estimated a biomass o f shrimps o f ~1 g d w - m " i n the 2  c o r a l head zone. T a b l e 3.9 summarizes the biomass estimates o f shrimps and lobsters. T h e w e i g h t e d mean for the reef as a w h o l e w a s 3.1 w w t-km" . 2  9) H e r m i t crabs have been f o u n d o n the reef flat i n densities r a n g i n g f r o m 3 to 65 m " ( K o h n 2  1987). T a b l e 3.10 summarizes the biomass estimates for the g r o u p . T h e w e i g h t e d mean for the reef as a w h o l e w a s 6 t w w - k m " . 2  40  Table 3.4. Biomass estimates of detritus ( P O M and D O M ) in the different reef zones. POM  (g ww-m" )  (g ww-m' )  (g ww-m" )  Biomass (t ww-km" )  0.12 0.28 0.25 0.28 0.26 0.28 0.26 0.24 0.36 0.34 0.20  21.6  21.60  216.0  -  -  -  26.2 22.0  26.45 22.27  6.6 13.4  -  -  -  22.0  22.35  44.7  _  _  _  _  -  -  24.0  24.30  291.6  _  _  _  -  -  -  185.0  Zone  DOM  a  3  Fore reef II  Algal ridge Reef flat 0  II  Coral heads II  Sand / shingle it  Weighted mean  POM+DOM  a b  3  3  d  Source  6  2  Marshall et al. (1975) Johannes (1967) Marshall et al. (1975) Marshall et al. (1975) Gerber and Marshall (1974) Marshall et al. (1975) Gerber and Marshall (1974) Gerber and Marshall (1982) Marshall etal. (1975) Johannes (1967) Gerber and Marshall (1974)  -  -  a. Assuming C = 10% ww; b. The estimates were derived by wet combustion (Marshall et al. 1975) and therefore, according to Sorokin (1993), were underestimated 1 . 5 - 2 times. T o account for this all values were multiplied by 2; c. Biomass assumed equal to the coral head zone; d. Calculated as the average of the P O M estimates plus the D O M estimate; e. Estimated using Table 3.1.  Table 3.5. Biomass estimates of benthic primary producers (free living algae and boring filamentous algae) in the different reef zones. Modified from Odum and Odum (1955). Zone / group  Benthic primary producers (t ww-km" ) 2  Fore reef Algal ridge Reef flat Coral head zone Sand / shingle zone Weighted mean  3869 3520 5640 3869 2233 3255  c  b  a. Conversion: 1 g dw = 5.71 g w w (Opitz 1996); b. Average between the Odums' zone of small and large coral heads; c. Biomass assumed equal to the coral head zone.  41  a  Table 3.6. Coral biomass estimates (not including inorganic skeleton). F r o m Odum and Odum (1955). Zone  Zooxanthellae  A n i m a l polyps  (t ww-km" )  (t ww-km" )  (t ww-km" )  37 106 47 37 0 22  467 700 333 467 0 190  504 806 380 504 0 212  2  Fore reef Algal-coral ridge Reef flat Coral heads Sand / shingle Weighted mean  Total biomass  3  2  2  b  a. Conversion: dw = 15% w w (Vinogradov 1953, Odum and Odum 1955); b. This is the only zone where sea anemones were mentioned (4.3 gm" ) (Odum and Odum 1955); c. Biomass assumed equal to the coral head zone. 2  Table 3.7. The biomass of foraminiferans in the different reef zones. Modified from Odum and Odum (1955). Zone  Fore reef Algal ridge Reef flat Coral heads Sand / shingle Weighted mean  Coverage of sand / mats containing foraminifera (%) -  Counts-cm" of small forams (0.01 cm) -  Counts-cm" of large forams (0.1 cm)  70 34 67  -  0 19 54  -  2  25 2 3 -  2  Biomass  3  (t ww-km" ) 2  -  9.70 0.03 0.03 9.70 55.63 33.40  -  b  c  a. Odum and Odum (1955) estimated an ash-free dry weight ( A F D W ) o f large foraminiferans of 1.33-10" g. Assuming that foraminiferans are spherical, their volume is equal to / 7tr and the 4  4  3  3  volume-ratio o f a small foraminiferan with a diameter of 0.01 cm to a large foraminiferan with a diameter of 0.1 cm is 1:1000. This gives an A F D W of small foraminiferans of 1.33- 10" g 7  (conversion: A F D W = 8 6 . 5 % w w (Odum and Odum 1955)); b. Biomass assumed equal to the coral head zone; c. Biomass assumed equal to the reef flat.  42  Table 3.8. Biomass estimates of gastropods in the different reef zones/ Source  Biomass (t ww-km" )  Zone  2  Fore reef Algal ridge Reef flat Coral heads Sand / shingle Weighted mean  25.3  Odum and Odum (1955)  a  -  -  Odum and Odum (1955) Odum and Odum (1955) Riddle et al. (1990)  5.5 ' 25.3 19.0 16.0  b c  M  e  -  a. b. c. d. e.  Biomass assumed equal to the coral head zone; Conversion: dw = 18% w w (Arias-Gonzales et al. 1993); The estimate only includes species of the genus Thais; The estimate includes species of the genera Thais, Coury, and Conus; From Davies Reef lagoon, Australia, where Riddle et al. (1990) estimated a biomass of 765 mg C-m" (conversion: 1 g C = 2 g ash (Riddle et al. 1990), and ash = 8 % w w (Sambilay 1993)); f. Dashes indicate that no biomass estimate was found and that gastropods probably do not occur in the zone. 2  Table 3.9. Biomass estimates of shrimps and lobsters in the different reef zones. Zone  Biomass (t ww-km" )  Source  2  Fore reef  4.65°  Algal ridge Reef flat Coral heads Sand / shingle Weighted mean  0.72 0.72 3.93 3.93 3.10  a  b  Ebert and Ford (1986) Odum and Odum (1955) Ebert and Ford (1986) Ebert and Ford (1986) Odum and Odum (1955)  -  a. Conversion: dw = 2 6 . 7 % w w (Opitz 1996); b. Biomass assumed equal to the coral head zone; c. Assuming that both lobsters and shrimps occur in this zone in densities similar to the reef flat and coral head zone.  43  Table 3.10. Biomass o f crabs and other crustaceans in different reef zones. Source  Biomass (t ww-km" )  Zone  2  9.6 46.8 2.0 9.6 1.7 6.0  Fore reef A l g a l ridge Reef flat Coral heads Sand / shingle Weighted mean  -  a  Odum and Odum (1955) Odum and Odum (1955) Odum and Odum (1955) Riddle e t a l . (1990)  b  b  b  C  -  a. Biomass assumed equal to the coral head zone; b. Conversions: dw = 2 5 % ww (Opitz 1996); c. The crustacean infauna biomass from Davies Reef lagoon, Australia. Conversion: 1 g C = 2.2 g dw.  Table 3.11. Biomass of echinoderms in the different reef zones. Biomass  Zone  Source  3  (t ww-km" ) 2  53.6 157.6 240.0 13.6 53.6 120.0 93.1  Fore reef Algal ridge Reef flat Coral heads Sand / shingle Weighted mean  Odum and Odum (1955) Odum and Odum (1955) Chartock (1983a) Odum and Odum (1955) Odum and Odum (1955) Colin (1987a)  b  C  d  -  a. Conversion: dw = 2 5 % w w (Vinogradov 1953, Arias-Gonzales 1993); b. Biomass assumed equal to the coral head zone; c. Biomass o f Ophiocoma anaglyptica, the dominant benthic invertebrate in this zone according to Chartock (1983a); d. A density o f >50 urchins-m" (Colin 1987a) was converted into a biomass estimate assuming an 2  average wet weight o f irregular sea urchins of 2.4 g-ind" (Odum and Odum 1955). 1  44  Table 3.12. Biomass estimates o f holothurians in the different reef zones. Zone  Biomass (t ww-km" )  Source  233.5  -  2  Fore reef A l g a l ridge Reef flat Coral heads Sand / shingle Weighted mean  1.4 1.4 204.3 262.7 2.6 42.0  b  c  Odum and Odum (1955) Odum and Odum (1955) W e b b e t a l . (1977) Riddle e t a l . (1990)  a  a  -  a. Conversion: dw = 14% w w ((Bakus 1968) based on specimens o f Holothuria b. Biomass assumed equal to the mean of the coral head zone; c. Biomass assumed equal to the reef flat.  difficilis);  Table 3.13. Biomass o f polychaetes and other worm-like invertebrates in the different reef zones. Zone  Biomass  a  Source  (t ww-km" ) 2  Fore reef A l g a l ridge M  Reef flat II  Coral heads Sand / shingle Weighted mean  65 81 105 40 41 65 7° 29  b  Odum and Odum (1955) Odum and Odum (1955) Bailey-Brock et al. (1980) Odum and Odum (1955) Bailey-Brock et al. (1980) Odum and Odum (1955) Riddle e t a l . (1990)  a. Conversion: dw = 2 0 % w w (Arias-Gonzales 1993); b. Biomass assumed equal to the coral head zone; c. From Table 3.15, conversion: 1 g C = 11 g w w (Riddle et al. 1990, Opitz 1996).  45  -  10) Table 3.11 summarizes the biomass estimates f o r echinoderms other than holothurians i n the different zones. T h e w e i g h t e d mean for the reef as a w h o l e w a s 93.1 t w w - k m " . 2  11) W e b b et al. (1977) observed an average density o f Holothuria  atra o f 3.03 p e r m i n an 2  area similar t o O d u m s ' c o r a l head zone. O d u m and O d u m (1955) further estimated the density o f holothurians o n the reef flat and i n the c o r a l head zone. T a b l e 3.12 summarizes the v a r i o u s biomass estimates. T h e w e i g h t e d mean for the reef as a w h o l e w a s 4 2 t w w - k m " . 2  12) T a b l e 3.13 summarizes the biomass o f polychaetes and other w o r m l i k e invertebrates i n the different zones. T h e w e i g h t e d mean for the reef as a w h o l e w a s 2 9 t w w - k m " . 2  13) V e r y f e w biomass estimates w e r e f o u n d f o r the sessile invertebrate group. B a s i l e et al. (1984) f o u n d that sponges o c c u r i n the fore reef zone, and K o h n ( 1 9 8 7 ) f o u n d them o n the reef flat as w e l l : " C l i n o i d sponges that excavate chambers i n the hermatypic c o r a l Porites lutea o n interisland platforms are e c o l o g i c a l l y the most important P o r i f e r a o f the E n e w e t a k intertidal and s h a l l o w subtidal z o n e s . . . " O d u m and O d u m (1955) estimated a biomass o f 34 g dw-m" i n the c o r a l head zone. E x c e p t for the sand-shingle zone, I a p p l i e d this estimate f o r all 2  zones, w h i c h lead t o a w e i g h t e d mean o f 3 7 t w w - k m " ( c o n v e r s i o n : d w = 3 9 % organic w w 2  ( O p i t z 1996)). 14) M a r s h (1970) estimated a p r o d u c t i v i t y o f reef-building calcareous red algae o n the algal ridge and i n the spur and g r o o v e system o f 4 0 0 8 g ww-m^-yr" ( c o n v e r s i o n : 1 g C = 16.7 g 1  w w ( O p i t z 1996)). U s i n g the biomass estimate f r o m the algal ridge ( T a b l e 3.5), a P / B ratio o f 2.2 year"  1  w a s derived. B a k u s (1967), u s i n g exclosure experiments, measured the primary  p r o d u c t i v i t y o f cyanobacteria o n the reef flat and f o u n d that it ranged b e t w e e n 0.65 - 2.15 gC-m^-day" o r 3 9 5 8 - 13111 g w w - m ^ y r " (conversion: 1 g C = 16.7 g w w ( O p i t z 1996)). 1  1  A p p l y i n g the biomass estimate f o r this zone (Table 3.5) lead t o a P / B value ranging f r o m 0.8 to 2.7 year" . C o m b i n i n g the t w o P / B estimates resulted i n a mean P / B value f o r the g r o u p as a 1  w h o l e o f 2 year" . 1  15) G e r b e r and M a r s h a l l (1982) measured a p h y t o p l a n k t o n c o n c e n t r a t i o n behind the reef o f 1.23 m g C-m" , and Sargent and A u s t i n (1949) measured a p r i m a r y p r o d u c t i o n o f 2 m g C-m" 3  3  -day"\ F r o m here a P / B ratio o f 593 year" w a s derived. 1  16) F r o m S o r o k i n (1993). 17) F r o m O p i t z (1996).  46  18) A P / B ratio o f 9.1 year" f o r zooxanthellae and 1.1 year" f o r c o r a l animal p o l y p s ( S o r o k i n 1  1  1993) w a s c o m b i n e d w i t h the biomass estimates f r o m T a b l e 3.6 t o give a w e i g h t e d P / B value o f 2 year" . 1  19) C o r a l s obtain approximately 7 0 % o f their energy f r o m s y m b i o t i c zooxanthellae and 30%> f r o m other external sources ( S o r o k i n 1993, example f r o m H e r o n Island, A u s t r a l i a ) . A s s u m i n g that corals consume 2993 t ww-km^-year" ( O p i t z 1996) ( c o n v e r s i o n : 1 k c a l = 1 g w w ) , and 1  using the w e i g h t e d mean c o r a l biomass estimate f r o m Table 3.6, a Q / B value o f 14 year" w a s 1  derived. T h e value w a s reduced t o 4 year" t o take into account the 70%> internal feeding o n 1  zooxanthellae. 20) H a l l o c k (1981) estimated a t u r n o v e r rate ( P / B ratio) o f 11-16 year" f o r three species o f 1  foraminifereans  (Amphistegine  lessoni,  A.  and Calcarina  lobifera,  i n the  spengleri)  Philippines. Since the same species o c c u r at E n e w e t a k A t o l l ( C h a v e and D e v a n e y 1987), an average P / B value o f 14 year" w a s applied f o r the g r o u p as a w h o l e . 1  21) A Q / B value o f 3 0 year" ( O p i t z 1996) f o r foraminiferans w a s l o w e r e d t o 21 year" to take 1  1  into account that 30%> o f the diet comes f r o m internal feeding o n zooxanthellae (see A p p e n d i x 1). 22) F r o m R i d d l e et al. (1990) . 23) R i d d l e et al. (1990) estimated a yearly c o n s u m p t i o n rate f o r large gastropods (> 2 m m ) o f 2 7 7 k J m" . T h e y also estimated a biomass o f 31 k J - m " ( c o n v e r s i o n : 1 g C = 4 2 k J , R i d d l e et 2  2  al. (1990)). T h i s lead t o a Q / B value o f 9 year" . 1  24) F r o m L e w i s (1981). 25) A r i a s - G o n z a l e s (1993) used a Q / B value o f 10 year" f o r a g r o u p o f bivalves i n c l u d i n g 1  Tridacna maxima. I l o w e r e d the value t o 3 year" t o take into account 7 5 % internal feeding o n 1  zooxanthellae (based o n H e s l i n g a and Fitt (1987)). 26) E b e r t and F o r d (1986) estimated a natural mortality ( M ) f o r Panulirus penicillatus  (spiny  lobster) o f 0.284 year" f o r males and 0.244 year" f o r females. W i t h n o fishing, and w i t h a 1  1  seemingly stable age structured p o p u l a t i o n , M can be assumed t o equal the total mortality ( Z ) w h i c h again equals P / B (Christensen and P a u l y 1992b). A sex ratio o f 1:1, therefore, resulted in an average P / B value o f 0.264 year" . A P / B value o f 5.34 year" f o r shrimps w a s obtained 1  1  47  f r o m A r i a s - G o n z a l e s (1993). A p p l y i n g the biomass estimates f r o m T a b l e 3.9, a w e i g h t e d P / B value o f 4.6 year" , f o r the g r o u p as a w h o l e , w a s derived. 1  27) P a u l y et al. (1993) estimated a Q / B value o f 2 9 year" f o r t w o penaid shrimps, and O p i t z 1  (1996) estimated a Q / B value f o r spiny lobsters o f 7.4 year" . A p p l y i n g the biomass estimates 1  f r o m T a b l e 3.9, a w e i g h t e d Q / B value o f 27 year" , f o r the g r o u p as a w h o l e , w a s derived. 1  28) F r o m O p i t z (1996), f r o m a group c o m p r i s i n g shrimps, hermit crabs, a n d stomatopods. 29) F r o m A r i a s - G o n z a l e s (1993), f r o m a g r o u p dominated b y x a n t h i d crabs. 30) F r o m P a u l y et al. (1993). 31)  A c c o r d i n g t o P a u l y et al. (1993),  the natural m o r t a l i t y ( M ) f o r l o w - m e t a b o l i s m  echinoderms is approximately equal to the rate constant K (time" ) o f the v o n Bertalanffy 1  g r o w t h function. K - v a l u e s f o r some holothurians at E n e w e t a k A t o l l are presented i n Table 3.14. Since there w a s n o harvest o f holothurians i n the p e r i o d considered f o r the m o d e l , the total mortality ( Z ) c a n be expressed i n terms o f M . Z , however, also equals P / B (Christensen and P a u l y 1992b), and hence a P / B value o f 0.227 year" w a s derived f r o m T a b l e 3.14. 1  32) R i d d l e et al. (1990) f o u n d that the infauna o f the D a v i e s R e e f l a g o o n , A u s t r a l i a , w a s dominated b y polychaetes (Table 3.13). A P / B value o f 5.8 year" a n d a Q / B value o f 24 year" 1  1  w a s derived f r o m T a b l e 3.15. 33) F r o m A r i a s - G o n z a l e s (1993). Table 3.14. Rate constants for some holothurians at Enewetak Atoll. Modified from Pauly et al. (1993). K (year )  Species  1  0.110 0.120 0.450 0.227  Holothuria atra Actinopyga mauritana Stichopus chloronotus Mean  Table 3.15. Bimass, P/B and Q/B values for infaunal polychaetes in the lagoon sediments of Davies Reef, Australia. Modified from Riddle et al. (1990). Biomass values are ± 9 5 % confidence limits. Feeding type Macrophagous Microphagous Macrophagous Microphagous  Size class (mm) > 2.0 > 2.0 0.5 - 2.0 0.5 - 2.0  Biomass (mg C-m" ) 2  124 217 71 224  ±55 ± 80 ± 16 ± 24  a. Average value from Table 5 in Riddle et al. (1990); b. Conversion: 1 g C = 48 k J (Opitz 1996).  48  P/B (year )  Q/B  2.6 3.3 10.3 8.5  12 15 37 35  a  1  b  3.2.3  F i s h groups.  3.2.3.1 The distribution and abundance of fish. F i s h are v e r y abundant i n a l l o f the M a r s h a l l Islands. F r o m  1953 t o 1966 Schultz and  collaborators (1953, 1960, 1966) identified and described 543 species, and a checklist o f 817 species (338 genera and 9 7 families) w a s recently assembled b y R a n d a l l and R a n d a l l (1987). In a comprehensive study, H i a t t and Strasburg (1960) examined the f o o d and feeding habits and e c o l o g i c a l relationship o f 223 fish species (56 families and 127 genera) o f the M a r s h a l l Islands. B y c o m p a r i n g this w o r k w i t h that o f S c h u l t z and collaborators ( 1 9 5 3 , 1960, 1966) and R a n d a l l and R a n d a l l (1987), 190 o f H i a t t and Strasburgs 223 species w e r e f o u n d t o o c c u r at E n e w e t a k A t o l l . I g r o u p e d the 190 species into t e n functional g r o u p s based on: 1) size: small < 3 0 c m T L a n d large > 3 0 c m T L ; 2 ) feeding type: h e r b i v o r o u s (parrotfish a n d 7  surgeonfish),  omnivorous  (> 1 0 % o f diet  consist  o f plant  material),  carnivorous o r  p i s c i v o r o u s ; 3) a data set o n the radioactivity i n reef fishes o f B e l l e Island ( F i g u r e 1.3), E n e w e t a k A t o l l ( W e l a n d e r 1957) (see section 3.3.1); and 4 ) t w o E c o p a t h m o d e l s b y A r i a s G o n z a l e s (1993). T h e ten fish groups were: miscellaneous p i s c i v o r o u s fish (mainly sharks and j a c k s ) , small c a r n i v o r o u s fish, large carnivorous fish, small o m n i v o r o u s fish, large o m n i v o r o u s fish,  snappers / groupers, butterflyfish, surgeonfish, parrotfish, and h e r r i n g (see A p p e n d i x 2  and 3). T h e diet c o m p o s i t i o n s ( A p p e n d i x 2 ) were, i n most cases, derived f r o m H i a t t and Strasburg (1960), w h o examined 2051 fish stomachs, and identified the types o f f o o d consumed. Table 3.16  shows  an example  o f the stomach context  o f Neoniphon  sammara  (Holocentrus  sammara i n H i a t t and Strassburg ( I 9 6 0 ) ) as presented b y H i a t t and Strasburg (1960). T o convert the percent c o l u m n i n T a b l e 3.16 into a diet c o m p o s i t i o n as required i n E c o p a t h , I c o u n t e d the number o f different f o o d items a n d assigned an equal w e i g h t t o each. I n the example f r o m T a b l e 3.16, 12 different items w e r e c o n s u m e d and thus, w e r e assigned a weight o f 100/12 = 8.3%o each. T h e items w e r e then g r o u p e d into the appropriate functional g r o u p (as identified i n the E c o p a t h model) and the ' w e i g h t s ' added t o derive the diet c o m p o s i t i o n .  "The length of a fish measured from the front of the jaw which is most anterior to the end of the longest caudal ray, but excluding the caudal filaments" (FishBase 1998). 7  49  Table 3.16. Example of the stomach context of Neoniphon sammara as presented by Hiatt and Strasburg (1960). Food item  Percentage o f fish containing the item  Crustacea Crab fragments Parthenopiid crab Thalamita sp. Pachygrapsus plicatus Portunic crab M a i i d crab Unidentified crustacean fragments Copepods Coelenterata Pieces of unidentified coral, partly digested Polychaeta Unidentified polychaetes Gastropods Cerithium sp. Algae A l g a l frond, bitten off In this example, the 12 f o o d items w e r e miscellaneous crustaceans  36 27 18 9 9 9 18 9 18 9 9 9  g r o u p e d into the f o l l o w i n g diet c o m p o s i t i o n :  6 6 . 7 % , corals 8 . 3 % , polychaetes  8.3%>, gastropods  8.3%>, and  benthic p r i m a r y producers 8 . 3 % . I n a f e w cases, the diet c o m p o s i t i o n s w e r e obtained directly f r o m A r i a s - G o n z a l e s (1993) and H o b s o n and Chess (1978). D e s p i t e numerous studies o f fish at E n e w e t a k A t o l l , f e w have been quantitative and then mostly concentrating o n a f e w species o r families o c c u r r i n g i n a specific habitat ( B a k u s 1967, M i l l e r 1982). O d u m and O d u m (1955) used visual census t o r o u g h l y estimate the biomass o f small and large herbivorous and carnivorous fish i n each o f their six r e e f zones (see A p p e n d i x 5). S m a l l fish were counted i n 3 6 m quadrates, a n d their numbers converted into biomass 2  assuming a mean d r y weight ( d w ) o f 2.42 g p e r i n d i v i d u a l , as determined f r o m a rotenone sample. L a r g e fish w e r e " r a p i d l y counted w i t h 360° underwater v i s i o n " , and converted t o d r y weight based o n a sample o f 12 speared fish o f the same size (120 g d w per individual). Table 3.17  summarizes the biomass estimates that w e r e converted f r o m d r y weight ( d w ) t o w e t  weight ( w w ) assuming that f o r fish except sharks, d w = 26%> w w (based o n Sambilay (1993)). T h e c o n v e r s i o n factor used f o r sharks and derived f r o m O d u m and O d u m (1955) w a s d w = 20% ww  50  T h e P / B values for the 10 fish groups (Table 3.17) w e r e obtained f r o m published E c o p a t h models ( A l i n o et al. 1993, A r i a s - G o n z a l e s 1993, Silvestre et al. 1993, O p i t z 1996), w h i l e the Q / B values w e r e estimated u s i n g the empirical regression b y P a u l y et al. ( P a u l y et al. 1990, Christensen and P a u l y 1992b, T a b l e 3.17, and A p p e n d i x 4): Q / B = 10  6 3 7  • 0.0313^ • W  ,  -  0  1  6  • 1.38 • 1.89 pf  8  (3.1)  Hd  where; W o o is the asymptotic or m a x i m u m weight o f the fish i n g r a m w e t weight; T k is the mean  annual habitat  temperature  expressed  as  1000/(T°C  +  273.1)  (an  annual  mean  temperature o f 27.5 w a s used i n all cases based o n A t k i n s o n (1987)); P f is one for apex predators, pelagic predators, and z o o p l a n k t o n feeders, and z e r o for all other feeding types; and H d characterizes the f o o d type and is set to one for herbivores and z e r o for carnivores. Table 3.17. Parameter estimates of the ten fish groups in the Ecopath model. Biomass  Functional group  (t ww-km" -year"')  Q/B (year" )  0.3 3.5 2.4 0.6 2.5 2.2 0.8 2.6 1.2 2.1  6 30 14 6 24 9 6 14 13 13  1  2  M i s c . piscivorous fish Herring Small carnivorous fish Large carnivorous fish Small omnivorous fish Large omnivorous fish Snappers / groupers Butterflyfish Surgeonfish Parrotfish  P/B (year" ) 8  3  6.3 0.4  C  d  -  f  d  d  5.7 9.4 3.9  e  C  C  C  c  b  1  a. Derived from Odum and Odum (1955) assuming that all large fish, other than sharks, in the sand / shingle zone could be grouped as miscellaneous piscivorous fish. Conversion: dw = 2 6 % ww (Sambilay 1993), except for sharks where dw = 2 0 % w w (Odum and Odum 1955). Dashes indicate that no biomass estimate was derived, but was left to be estimated by Ecopath; b. Q/B = consumption/biomass. Estimated using the empirical equation derived by Pauly et al. (1990) (see Equation (3.1) and Appendix 4); c. d. e. f.  Derived Derived Derived Derived  from from from from  Arias-Gonzales (1993); Opitz (1996); Silvestre et al. (1993); Alino et al. (1993);  g. P/B = production / biomass ratio.  51  3.3  3.3.1  The origin  and incorporation  of the radioactivity  data.  T h e o r i g i n o f the radioactivity data.  F r o m shortly before and u p to t w o years after the ' N e c t a r ' shot o n M a y 14, 1954 at E n e w e t a k A t o l l (Table 2.3), the level o f beta radioactivity i n the most c o m m o n aquatic organisms w a s measured, a n d the results prepared i n three reports b y the A p p l i e d Fisheries L a b o r a t o r y , University o f Washington,  Seattle  ( i n contract  w i t h the U n i t e d States A t o m i c  Energy  C o m m i s s i o n ) : B o n h a m (1958) studied the radioactivity i n invertebrates; P a l u m b o  (1959)  reported o n the level o f radioactivity i n algae; and W e l a n d e r (1957) l o o k e d at the radioactivity in reef fish. T h e ' N e c t a r ' shot t o o k place about 4.3 k m east-northeast  o f B e l l e Island (see F i g u r e 3.1),  w h i c h received a greater amount o f fallout than the rest o f the islands ( W e l a n d e r 1957). It therefore became center f o r subsequent investigations (as w e l l as the focus o f this study). Invertebrates, gastropods  i n c l u d i n g bivalves  (Lambis),  (Tridacna  a n d corals (Acropora,  crocea),  sea c u c u m b e r s  Porites,  Pocillopora,  (Holothuria  a n d Heliopora),  atra), were  collected a l o n g the seaward side o f B e l l e Island. A total o f 693 specimens o f fish, representing 57 species and 2 2 families, w e r e collected i n the same area u s i n g rotenone, h o o k and line, o r spear i n water f r o m about 5 c m t o about 4 m depth. A l g a e w e r e collected f r o m the intertidal zone a l l a r o u n d the island, w h i l e p l a n k t o n a n d water samples w e r e collected o n the l a g o o n side. A l l samples, except f o r p l a n k t o n and water, w e r e immediately put o n ice a n d kept i n freezers at the E n e w e t a k field laboratory until further processed. F i s h and invertebrates w e r e dissected as t o tissue ( W e l a n d e r 1957, B o n h a m 1958): bivalves w e r e dissected into mantle, adductor muscle, g i l l , kidney, visceral mass, a n d shell; gastropods w e r e dissected into mantle, foot muscle, terminal portions o f liver and gut, v i c e r a l mass, a n d shell; sea cucumbers into gonads, gut w i t h context, a n d b o d y w a l l ( B o n h a m 1958); a n d fish w e r e dissected into skin, muscle, bone, liver a n d viscera (Welander 1957). Similar tissues f r o m small fish w e r e p o o l e d , o r i n some cases the entire fish w a s used (Welander 1957). T h e samples w e r e sent t o the U n i v e r s i t y o f W a s h i n g t o n laboratory, Seattle, i n insulated containers w i t h dry ice.  52  F i v e milliliter water samples and filtered p l a n k t o n samples w e r e p l a c e d o n 3.8 c m stainless steel plates and dried and ashed before they w e r e sent to Seattle ( B o n h a m 1958). A t the U n i v e r s i t y o f W a s h i n g t o n laboratory, samples o f a p p r o x i m a t e l y one g r a m w e r e placed o n pre-weighed 3.8 c m stainless steel plates, w e i g h e d and d r i e d at 9 7 ° - 9 9 ° C for 12 to 24 hours. T h e y w e r e subsequently ashed overnight at 500°-550°C. A f t e r c o o l i n g and w e i g h i n g , they w e r e slurried w i t h ethyl a l c o h o l , spread evenly o n the plates w i t h a glass r o d , dried, and affixed to the plates w i t h a f e w drops o f 0.5 per cent F o r m v a r i n ethylene dichloride. T h e samples w e r e counted i n N u c l e o m e t e r internal gas-flow (methane) c o u n t i n g chambers, and were corrected b a c k to the date o f c o l l e c t i o n based o n the decay o f a soil sample collected at B e l l e Island o n M a y 15, 1954 ( D o n a l d s o n 1953, W e l a n d e r 1957, B o n h a m 1958, 1959).  3.3.2  O b s e r v e d trends i n radioactivity i n various organisms.  V a r y i n g w i t h the organisms, the field samples indicated that a m a x i m u m level o f radioactivity, in the organisms, w a s obtained between 1 - 1 0  days after the detonation, f o l l o w e d by an  approximately linear decline o n a l o g - l o g scale o f beta decay versus time (up to t w o years) after the detonation ( B o n h a m 1958, P a l u m b o 1959, W e l a n d e r 1957). F i g u r e 3.3 shows an example o f the observed beta radioactivity i n corals (Acropora) f r o m B e l l e Island as presented by B o n h a m (1958).  T h e figure shows that f r o m day 36 to day 710  after the  nuclear  detonation, the decline was approximately linear, w i t h a c o r r e l a t i o n o f - 0 . 9 7 6 , a c c o r d i n g to the (anti-logged) regression Y = 2.7 • 10 - T 8  2  2 3  .  T h e ' N e c t a r ' shot was not the first nuclear detonation i n the area, and residual l o n g - l i v e d radioisotopes f r o m earlier explosions rendered the decline curves less steep than i f they had been a result o f the ' N e c t a r ' shot alone ( B o n h a m 1958). T h e observed data o n beta radioactivity i n the v a r i o u s organisms w e r e based o n variable sample sizes as s h o w n i n T a b l e 3.18.  53  1000 ° N o t used i n regression • Used i n regression 100 oTt  10 >  1  1  3  o.i  O  6 pre-detonation level  1  10  100  1000  Days after nuclear detonation on M a y 14, 1954  Figure 3-3. Total beta radioactivity in corals (Acropora) in disintegrations-mm^g'wet-lO after the 'Nectar' shot on M a y 14, 1954 (Bonham 1958). From day 36 to 710 the decline approximates a straight line. 3  Table 3.18. M e a n number o f specimens from which the observed data on beta radioactivity were derived. Based on Bonham (1958), Palumbo (1959), and Welander (1957). Functional group  M e a n number of specimens  Dominant organisms  3  Giant clams  Halimeda, Dictyota, Caulerpa, Lyngbya, Spyridia, Udotea, 17.0 Codium, Microdictyon Acropora 3.6±0.5 Tridacna crocea 2.1 ± 0 . 2  Gastropods  Lambis  Holothurians Parrotfish  Holothuria atra Scarus purpureus  3.0 2.9 ± 2.1  Bent. prim. prod. Corals  b  2.3 ± 0.5  Surgeonfish  Acanthurus triostegus  2.8 ± 1.6  Butterflyfish  Chaetodon auriga  2.1 ± 1.4  Small omniv. fish  Damseffish (Abudefdufbiocellatus), blennies  Herring  Snappers / groupers  Cardinalfish, squirrefish (Holocentrus sp.), wrasses (Halichoeres trimaculatus) Mullet (Neomyxis chaptalli), triggerfish, goatfish (Mulloidichthys samoensis) Epinephelus merra  M i s c . pisciv. fish  Jacks, sharks  Small carniv. fish Large carniv. fish  3.9 ± 2.5 30.0 3.0 ± 1.7 5.4 + 5.7 2.8 ± 1.7 1.7 + 0.8  a. M e a n values ± standard deviation; b. The value refers to the number of plates counted in the gas-flow counting chamber.  54  3.3.3  R a d i o a c t i v i t y i n w h o l e organisms.  T h e data o n r a d i o a c t i v i t y i n bivalves, gastropods, holothurians and fish w e r e reported as the activity i n v a r i o u s tissues (section 3.3.1) and n o t as the activity i n the organisms as a w h o l e . T h e relative weight o f the different b o d y parts o f bivalves, gastropods, holothurans, a n d fish was therefore obtained f r o m the literature (see T a b l e 3.19), a n d the activity f o r w h o l e organisms derived. Table 3.19. Relative weight o f the different body parts o f fish, bivalves, holothurians, and gastropods as determined from the literature. Organism Fish  Relative weight of various tissues 8 % skin, 6 3 % muscle, 18% bone, 2 % liver, 9 % viscera . 3  Bivalves {Tridacna crocedf  9 5 % shell, 0.75% adductor muscle (or 15% o f the tissue excluding shell, based on Heslinga and Watson (1985)), and the remaining 4 . 2 5 % equally divided into gills, viscera, mantle, and kidney.  Holothurians (Parastichopus calufornicus)  19% gut, 10% gonads, 17% muscle, 5 4 % body wall / integument (excluding body fluids and respiratory tree) . c  Gastropods  7 0 % shell and the remaining 3 0 % equally divided between liver, gut, mantle and muscle . d  a. b. c. d.  Based on Welander (1957); Reaches about 20 cm (Sorokin 1993); Based on Giese (1966); Based on Hammen (1980).  3.3.4  S i m u l a t i n g the observed trends i n beta radioactivity.  O n e o f the outputs o f a balanced E c o p a t h m o d e l is the estimated fluxes o f biomass a m o n g the functional g r o u p s as presented i n the ' f o o d intake m a t r i x ' . These fluxes w e r e used t o simulate the fate o f beta radioactivity w i t h i n the marine ecosystem o f E n e w e t a k A t o l l . A s s u m i n g that the radioactivity is m i x e d evenly w i t h i n a functional g r o u p , one m a y think o f it as ' t a g g e d ' biomass ( T ) that flows f r o m one functional g r o u p to another a c c o r d i n g t o the overall flux o f biomass between the groups as illustrated i n F i g u r e 3.4, where; B ; and B j are the biomasses (t-km" ) o f g r o u p i a n d j , respectively; T ; and Tj are the tagged biomasses (t-km" ) i n g r o u p i 2  2  and j , respectively; and Q is the flux o f biomass (t-km" -year"') f r o m g r o u p i to j . 2  y  55  Group j  Group i  Figure 3-4. A schematic representation o f the transfer of radioactivity between compartments of an ecosystem. The radioactivity can be thought o f as 'tagged' biomass (T) that flows from group i to j according to the flux o f biomass (Qy) where Bj and Bj are the biomasses o f group i and j , respectively. T h e transfer o f radioactivity per unit time f r o m g r o u p i t o j , p -, is p r o p o r t i o n a l t o the fraction y  o f ' t a g g e d ' biomass t o total biomass i n g r o u p i , T / B ; , and the flux ( Q ) o f biomass f r o m group y  i to j : T  where; M  <=>  Pij  = V  (3.2)  B;  = Qy/B;. M y is the transfer coefficient (year" ) f r o m g r o u p i t o g r o u p j , i.e., that part 1  y  o f the natural mortality o f i that is due t o j . T h e M s are calculated i n E c o p a t h and presented i n a predation mortality matrix. W h e n dealing w i t h radioactivity, there is an additional loss besides predation, 8, w i t h i n each g r o u p , resulting f r o m the physical decay o f the radioisotopes. T h e total o r gross beta radiation emitted b y fission products, p r o d u c e d i n a process where a number o f  2 3 5  U r a m i u m atoms  undergo fission simultaneous, e.g., i n a nuclear detonation, w a s presented b y H u n t e r and B a l l o u (1951) (see also section 2.2.2). T h e y f o u n d that the gross decay curve o f the fission products  c a n be described by a p o w e r  function  D = a • t , where b  D  is the amount  of  radioactivity at time t i n days after the detonation; a is the intercept; a n d b is the slope / decay rate (equal t o -1.2). W h e n differentiated, the equation m a y be re-expressed as: dD  = a-b-t -' = b-(a-t )-t b  dt  b  _ 1  = b-D-t  _ 1  = (b/t)-D = 5 - D  (3.3)  where; 5 = (b/t). C o m b i n i n g the income, loss and decay terms, the trend i n radioactivity i n the functional groups m a y be described by a linear differential equation system o f the f o r m : loss  dT = ZT .M dt .  decay  ;  L  1  i=  1 J  -T .XM J  J I  -5.T  (3.4)  J  i=l  w h i c h c a n be integrated over time.  56  T h e S o l v e r routine i n M i c r o s o f t E x c e l w a s applied to m i n i m i z e the total sum o f squared deviations between the observed and predicted levels o f beta radioactivity  [__(ln(obs/pred) )] 2  by m o d i f y i n g the predation mortality matrix f r o m the original E c o p a t h m o d e l , thus simulating a trend that w a s m o r e consistent w i t h the observed  data: the c o l u m n s o f the  predation  mortality matrix (i.e., the mortalities exerted by a predator o n its v a r i o u s prey groups) w e r e scaled up / d o w n by m u l t i p l y i n g t h e m w i t h a factor that S o l v e r w a s p r e p r o g r a m m e d to vary w i t h i n a certain range (0.25-1.75), w h i l e m i n i m i z i n g the residuals defined above. T h e r o w s o f the predation mortality matrix (i.e., the mortalities experienced by a g i v e n group) w e r e also modified, by a l l o w i n g S o l v e r to add an additional mortality ( M ) to the sum o f the mortalities +  (sum o f the r o w s ) . T h e coefficient  o f determination, R  (= l - S S  2  r e s  /SS  t o t  ),  w a s used  to  evaluate the fit o f different runs. T h e m o d i f i e d predation mortality matrix w a s subsequently used to re-calibrate the original E c o p a t h m o d e l by m o d i f y i n g the input biomass, i.e., the inputs directly p r o p o r t i o n a l to the predation mortalities, used for the next iteration (see E q u a t i o n (2.11)). T o initiate the simulation it was necessary to k n o w the levels o f beta radioactivity at the ' b o t t o m ' o f the f o o d web, i.e., at t r o p h i c level one, w h i c h comprises the benthic primary producers, p h y t o p l a n k t o n and detritus. T o derive the radioactivity i n the benthic primary producers,  a linear regression  was  performed  o n the  observed  concentrations  of  beta  radioactivity over time ( P a l u m b o 1959) (Figure 3.5), and the result used i n the simulation.  Benthic primary producers S  cr  m o  8  0  1  2  3  4  Time after detonation (log day) Figure 3-5. Regression of the observed concentrations of beta radioactivity over time in the benthic primary producers. Based on Palumbo (1959).  57  There w a s no observations o f the levels o f beta radioactivity i n p h y t o p l a n k t o n and detritus. It w a s therefore assumed that p h y t o p l a n k t o n incorporates beta r a d i o a c t i v i t y similar to benthic primary producers,  and l i k e w i s e that detritus contains levels  similar to benthic primary  producers w h i c h are the m a i n contributors to detritus (see section 4.2.1). R a d i o a c t i v i t y f r o m earlier nuclear tests i n the area w a s i g n o r e d under the assumption that it had no influence o n the overall trends. It was further assumed that the organisms do not take up radioisotopes selectively.  58  4.  Results  T h e f o l l o w i n g chapter is d i v i d e d into three m a i n parts later to be discussed i n Chapter 5. First the process o f balancing the E c o p a t h m o d e l using E c o r a n g e r is explained, i n c l u d i n g some necessary modifications o f the initial input parameters. T h e results are presented i n f o r m o f a table o f the basic estimates and as a f o o d w e b diagram. N e x t , the radioactivity data are m a p p e d onto the f o o d w e b diagram, and the simulation process i n c l u d i n g the modifications o f the predation mortality matrix and re-calibration o f the o r i g i n a l E c o p a t h m o d e l is explained. T h e results are s h o w n graphically and i n t w o tables. F i n a l l y , the summary statistics o f the m o d e l are presented together w i t h the results o f the n e t w o r k analysis, i n c l u d i n g the trophic transfer efficiencies estimated by E c o p a t h and a m i x e d t r o p h i c impact diagram.  4.1 Balancing  4.1.1  the Ecopath model.  First r u n w i t h E c o r a n g e r using initial input parameters.  T h e E c o p a t h m o d e l w a s balanced w i t h E c o r a n g e r using u n i f o r m distributions and a variability o f 9 9 % a r o u n d the initial input parameters (see T a b l e 3.3, 3.17, A p p e n d i x 1, 2, and 4). T h e majority o f the data came f r o m the O d u m s ' study (1955) and the h i g h variability assumed for the data w a s based o n their comment that t o o few replicates w e r e made to obtain m a x i m u m accuracy  f r o m the  methods  applied, and therefore,  all they  estimated  were  orders  of  magnitude (see also section 1.4). E c o r a n g e r w i l l not balance a m o d e l i f the input are grossly erroneous. In the present case, g i v e n the initial input parameters, E c o r a n g e r failed to find any solutions (balanced models, see section 2.3.2), and instead displayed a list o f the first 50 runs that failed. I n all cases the problem  was  the  ecotrophic  efficiency  (EE)  of  surgeonfish,  shrimps,  miscellaneous  crustaceans, and gastropods. T h e i r E E values w e r e m u c h higher than one, suggesting that they c o u l d not sustain the predation pressure. T h e initial E c o p a t h input parameters w e r e therefore m o d i f i e d , w i t h i n the ranges g i v e n i n the literature (see b e l o w ) , u n t i l E c o r a n g e r w a s able to balance the m o d e l .  59  4.1.1.1 Modifying  the predation mortality experienced by surgeonfish.  Surgeonfish initially accounted f o r more than 5 0 % o f the diet o f miscellaneous  piscivorous  fish. T h e particular diet c o m p o s i t i o n , however, h a d been derived f r o m just nine species w i t h detailed diet i n f o r m a t i o n (see A p p e n d i x 2 ) . B y i n c o r p o r a t i n g less detailed i n f o r m a t i o n f r o m species such as Triaenodon  obesus (Whitetip reef shark), Nebrius ferrugineus  qenie ( B l a c k f i n barracuda),  Sphyraena Gymnosarda  unicolor  (Dogtooth  Carangoides  tuna)  orthogrammus  all k n o w n  to consume  ( N u r s e shark),  (Island trevally), a n d (small)  reef  fish a n d  p l a n k t i v o r o u s fish ( L i e s k e and M y e r s 1994), and b y consulting other models ( P o l o v i n a 1984, O p i t z 1993), the f o l l o w i n g modified diet c o m p o s i t i o n f o r miscellaneous p i s c i v o r o u s fish w a s derived,  reducing  their  consumption  o f surgeonfish:  20%> surgeonfish,  1 9 . 1 % small  carnivorous fish, 1 2 . 5 % butterflyfish, 1 2 . 5 % parrotfish, 1 2 . 5 % large o m n i v o r o u s fish, 4 . 6 % small o m n i v o r o u s fish, 2 . 8 % large carnivorous fish, 1%> snappers / groupers, 1%> herring, 6%> miscellaneous  crustaceans,  4.6%> shrimps,  0.5%> cephalopods,  a n d 0.4%> stomatopods.  M o r e o v e r , t o make the diet c o m p o s i t i o n a d d u p t o one, cannibalism w a s increased t o 2 . 5 % .  4.1.1.2 Modifying  the predation  mortality  experienced  by  shrimps,  miscellaneous  crustaceans, and gastropods. S m a l l o m n i v o r o u s a n d carnivorous fish i n particular, caused a h i g h mortality o f shrimps, miscellaneous crustaceans, and gastropods. A f t e r c o m p a r i n g the Q / B values o f these t w o fish groups (estimated as arithmetic means rather than w e i g h t e d arithmetic means as n o biomass information w a s available, see A p p e n d i x 4 ) , w i t h other models ( A l i n o et al. 1 9 9 3 , O p i t z 1996), the Q / B value w a s l o w e r e d f r o m 14 t o 10 year" f o r small c a r n i v o r o u s fish and f r o m 24 1  to 15 year" f o r small o m n i v o r o u s fish. 1  T o reduce the mortality o f the three invertebrate groups even further, the diet o f butterflyfish w a s m o d i f i e d t o include 6 instead o f 12%> shrimps w i t h the difference assigned t o corals w h i c h are the only f o o d source f o r some butterflyfish ( S o r o k i n 1993, L i e s k e and M y e r s 1994). T h e diet o f echinoderms w a s m o d i f i e d t o include less miscellaneous crustaceans (1 instead o f 2%>) and m o r e benthic primary producers w h i c h are the most important f o o d i t e m f o r sea urchins  60  ( R u p p e r t and B a r n e s 1994) . C a n n i b a l i s m b y miscellaneous crustaceans w a s l o w e r e d f r o m 10 to 1% b y transferring the difference to detritus, as many crabs are scavengers and detritus feeders ( R u p p e r t and B a r n e s 1994). F i n a l l y , cannibalism b y small carnivorous fish w a s completely r e m o v e d , w h i l e it w a s reduced to  1%  and 3 %  for z o o p l a n k t o n and cephalopods,  respectively,  by rescaling their diet  c o m p o s i t i o n s to one. 4.1.2  S e c o n d r u n w i t h E c o r a n g e r u s i n g m o d i f i e d input parameters.  U s i n g the m o d i f i e d input parameters, E c o r a n g e r ( w i t h similar constraints as outlined i n section 4.1.1  and a l l o w i n g a m a x i m u m number o f total runs o f 100,000) w a s n o w able to  find  balanced models. O f 50 successful runs (restricted b y limited c o m p u t e r capacity) the basic estimates o f the 'best m o d e l ' are s h o w n i n T a b l e 4.1 and graphically i n F i g u r e 4.1.  After completion of this study, Dr. R.E. Foreman (pers. com.) has later noted that many echinoderms, including sea urchins, can survive solely on DOM. 8  61  b"  II r—< < N oo r o oo r o - - " t t s c ^ o o ^ o c N ^ I s o o r s T r i s r s r H  TJ  s  OOOOO°HHr-H,-Hr-Hcslr0V0in'-»'q-v0inv0Oi— o o o o o o o o o o o o o o o o  3 O li  S TJ 03 >  i n 00 V O oo C O C N 00 m o i n os i n 00  s  a'I  ON  O  CO OS CsJ OS cu  s o  > o a  -rt  c\3  m vo 5 vd as vd 00  9  3  1  Os o ro ro ro  CN VO  VO  r—i  CN VO VO  8  HH  ro i n vo in S  I/-I o CN Os r-- VO o Os o in rCN i n i n 00 vd vd 00 v d OS r- 5r n CN VO rCN  CN CN  CN o CN m  o  <%l C N C O &J l-l > • « > lH o © CO . rH CD  os r « C N in O o m 00 •«T ro Os C N r—i o i n o C N C N o  5  s° CN  .i=  VO  l-H OS O vo o i r~ o o os o  o Os CN  o  TJ  CD CD  o  o  o  o  o  o  o  o  o  o  o  o  i  16  S  —' O  CD  8 a—  o  WVDtsMcslrOcnOSrHH-o^rs — r m m H HHOSOscNOsr-OO^H-OSCNVO Os cn o cN o o o o o o o o o o o o o o o o o o o o o o o o  £9'53  O O O ^ f ^ ] r S ^ ^ ^ n ^ 0 0 Q ^ 0 ^ 0 0 O ^ ^ ) 0 0 v 0 ^ ^ 0 ^ O ^ t C 0 0 0 v n ^ c o i n3 r H ^ -i ^x ri i^S oc o N rs ^ d rq^c^prO v bTor^^r n o s ^ i / i"" i / i~~ odrn 0\ fN r i Q ~"" ~ '" ~ ^ S v d c1Hr-H ^ CN CN HH c-t •—i <N :  ;  ,  X  <  ,  J3  3  &  vo r - , , O co OS S vd ' CN  TJ +3  1  1 If  OS O o in  m vo O cil  i n r - Os o vd 00 Os in  CO CO CN  3  00 00 M" o vd o m CN  OS OS — ro CO  o  CO  r  o  CO  r-H  o o 00 •n ( N C N r - o 00 C O O0 r-H i n o «n" o C N o r—i Os O C N i n CO 00  <D  ,3 H  3  CD  I i  B 2 +3  •° s co"  «  II  m 00 !0 CO CO CO o vd 00 Os CN 00 vd o CN CN in  r-H V O i-H O  CN  H V O c s r - c i c n r j o r o i n r o o o v o c N O O O ro o O m o i n i n  <D  o  t  -3 CO  O O O O O r - H r - H r - H r - H ^ ^ i n r ^ l ^ l ^ M M O S i - H C N r O r O ' ^ ^ O q HHHcNCNCNCNCNHHtNHcNCNCNCNCNH  ^e  ^ 3 u to CD 3 CD  CD  CD  3 & S TJ +3 C  co c j  <D  o " oo g '—  1  VH  ^ a. CD  W  H  ^  &  .a  T3  CO  CD  a  -1  CO  . csi  o a  « o  d  CD  II  "fe  <D  a, 00 CN CO vo o ro CO vo V0 i n OS S 00 o OS 1 CN CO —1 CN  cB  c3 O TJ  11  cn  O co  S  3 TJ •§  CD  CD  § -a  o  O  2 °  CD  .>; oi5 H  '  oo .-I -^f r - i r-H i n m ^ r c s \ < N r ~ - r - o o c N m r < - i o o o 3 ^-OscOi-HCNOOOs^rcNOsoOiqCN — H - o — i O O c*l SO CN O r-H \o VO W-l r-H r-H C*-, r-H r—  „s  a.  "  3  o > o W o e9" M r3 So  o  3  a a a  .a  > JCD 3 03  --3  o  jo  (N o o  v X i r ^ ^ ^ o ^ v n « n r o ( N C O r v i r n ^ a \ ^ ^ o o ^ \ t ^ ^ ( > D ^  CD  (D  3  CN 3  CS  o o o o o o o o o o o o o o o o o o  TJ  s  II 03  TJ  (D  f  CD  Oi-iOHHTrrOCNOHHOmOcncNHHCNCNOHHCN-HOOO  ts  co  rH  oot^c^voost^cNoocosr^inoscsJ<^rncocNvpvoc»voosc>ooo  •a o >  3  ro rr - ro os Os r ^ S S o ' VO r ro ON ON  C N c N C N C ^ r S C s l r s l T r c N V O C N C N C N C N C N C N C N C N C N C N C N sf o o o o o o o o o o o o o o o o o o  CU _3  3  .3  ON  3  O HH o o o  -3  VH HH  O O  O  O O OO O O  O O O O O O O O O O O C N  CD  M  .tin CO  o 3 CD  ^  3 O  ^  II  «S 03 S O' TJ co O c3  g  M  S  sD  a a'a ;§ o .2 OH d  o 2 .2 3 TJ  o  °I  3  U  co "rrt  a 3  > O  M  II  .a o  Cs] VO  _  Ml  : II : II: :  ditL  CO. QO; : • I ; ; •» :  H  m S-2  ill: : I*  a.  m  ft  «  8  s *  - i  T3 ::£:::C0:::iO::  -3  3  ::: _V  Oi:0i:  Io  1 5 X _ _  111111111 ^ |9A9|  T3 *- —' o  r2  S  S  OjLjCJOJJ,  4.2 The fate of beta  4.2.1  radioactivity.  M a p p i n g the fate o f beta radioactivity.  In F i g u r e 4 . 2 the fate o f beta radioactivity has been m a p p e d onto the f l o w chart f r o m F i g u r e 4.1, o m i t t i n g the f l o w s f o r simplicity o f presentation. T h e level o f beta radioactivity w a s m o n i t o r e d i n 15 o f the 2 7 functional groups defined i n the m o d e l . T h e r a d i o a c t i v i t y in detritus was assumed to be equal to the level i n benthic p r i m a r y p r o d u c e r s (taking the biomass into account)  as the latter  is the m a i n source  o f detritus  (see T a b l e  4.1).  T h e level i n  p h y t o p l a n k t o n , the other, but less important p r i m a r y p r o d u c e r g r o u p i n the system, w a s derived i n a similar manner.  4.2.2  S i m u l a t i n g the fate o f beta radioactivity.  T h e results o f the simulations are s h o w n i n F i g u r e 4.3 and 4.4. F i g u r e 4.3 illustrates the simulated trends o f beta radioactivity predicted f r o m the original and the re-calibrated E c o p a t h m o d e l , respectively, w h i l e F i g u r e 4.4 features the results o f m o d i f y i n g o n l y the c o l u m n s or the r o w s o f the predation mortality matrix i n the m i n i m i z a t i o n process  (see section  3.3.4).  M o d i f y i n g the c o l u m n s thus moves the curves vertically u p o r d o w n ( F i g u r e 4.4a), w h i l e m o d i f y i n g the r o w s changes the slope o f the curves ( F i g u r e 4.4b). T o simulate the uptake o f beta radioactivity b y the organisms i n the first f e w days after the nuclear detonation, E q u a t i o n (3.4) w a s integrated over time steps o f 0.1 days. A f t e r day nine, daily time steps w e r e used. In the m i n i m i z a t i o n process,  S o l v e r w a s p r e p r o g r a m m e d t o v a r y the scaling factors (for  m o d i f y i n g the c o l u m n s o f the predation mortality matrix, see section 3.3.4) w i t h i n the range o f 0.25 t o 1.75. I f a w i d e r range w a s used, the resulting predation mortality matrix c o u l d subsequently not be used f o r re-calibration o f the original E c o p a t h m o d e l w i t h o u t seriously v i o l a t i n g the concept o f mass-balance. T h e m o d e l is parameterized f r o m the t o p - d o w n so that the biomass f l o w s at the l o w e r trophic levels are estimated t o m a t c h the f o o d demand o f the upper levels. A s a consequence, the predation mortalities generated b y miscellaneous p i s c i v o r o u s fish (ultimate t o p predator) o n their prey w a s restricted t o either stay the same o r decrease (scaling factor < 1). 64  m  1-1  o > rt  CD  in  § .2 G  W  ^  T3  rt  ^  °  U-i  •  O  >r>  <+H  H — <^  "H E 2 o p. o  CD  1  o  *I cf  Vt  o § £  T3  OI  "o  OH  3  fl  O  I  o  CD  03 JD  o CD  o  : ::*""*::  ;::;;;;:o:: H  .as  toO C  ft* o  S  CD  CN <D  3  T3 23  O  3fl  bO O o  E  ab  S  4.2.3  R e - c a l i b r a t i n g the E c o p a t h m o d e l .  T a b l e 4 . 2 summarizes the changes to the predation mortality matrix required f o r m i n i m i z i n g the residuals (see section 3.3.4) and re-calibrating the E c o p a t h m o d e l b y m o d i f y i n g the input biomasses.  T h e modifications w e r e justifiable as the biomasses w e r e associated w i t h h i g h  uncertainties, most o f t h e m derived f r o m the study b y O d u m a n d O d u m (1955) (see section 1.4, 3.2.2, and 3.2.3) and based o n visual censuses (the fish groups, see section 3.2.3.1 and 5.1.2.1) o r generated b y the E c o p a t h p r o g r a m (zooplankton). T h e re-calibrated E c o p a t h m o d e l w a s very close t o balancing. H o w e v e r , it w a s necessary t o m o d i f y the scaling factors f o r miscellaneous p i s c i v o r o u s fish, snappers / groupers, and small c a r n i v o r o u s fish f r o m 1 t o 0.5, 0.25 to 0.5, and 0.67 t o 0.8 respectively (see Table 4.2). A s a consequence the s u m o f squared deviations ( S S Q ) between the observed and predicted levels o f beta radioactivity (see section 3.3.4) increased f r o m 1.02-10 to 1.14-10 . A slightly better 2  2  fit (reducing S S Q t o 1.13 1 0 ) w a s obtained w h e n S o l v e r w a s a l l o w e d t o also m o d i f y the 2  'detritus m o r t a l i t y ' (the part o f the mortality o f a g r o u p caused b y n o n - p r e d a t i o n losses such as diseases, starvation, etc. See section 5.3.3), increasing it f o r all g r o u p s b y a c o m m o n factor o f 1.18. T h i s , however, w a s not used for the re-calibration o f the m o d e l (see section 5.3.3).  1E+13  (b)  ' J 1E+11 &  & 1E+09 o ca o i l 1E-KJ7  o  ca  100000  100000 0.1  0.1  1 10 100 1000 Days after nuclear detonation  1 10 100 1000 Days after nuclear detonation  Figure 4-4. Result o f modifying either the columns or the rows o f the predation mortality matrix, respectively, in the minimization process, here illustrated for surgeonfish. The dots are the observed levels o f beta radioactivity, thin lines the simulated trends using the predation mortality matrix from the original model, and thick lines the simulated trends obtained by modifying only the columns (a) or the rows (b) of the original predation mortality matrix. 68  Table 4.2. Scaling factors generated by Solver for modifying the predation mortalities, i.e., columns of the predation mortality matrix (and re-calibrating the original Ecopath model), resulting in the best fit between the observed and predicted levels of beta radioactivity. Scaling factor  Functional group  1.00 0.25 1.75 1.75 0.67 0.25 1.75 0.55 1.75 1.75 1.75 1.75 0.91  Miscellaneous piscivorous fish Snappers / groupers Parrotfish Large carnivorous fish Small carnivorous fish Herring Gastropods Butterflyfish Small omnivorous fish Corals Holothurians Zooplankton Giant clams  a  a  a  a. Later modified to 0.5 for miscellaneous piscivorous fish and snappers / groupers, and 0.8 for small carnivorous fish. Finally, the biomass o f p h y t o p l a n k t o n , w h i c h was a m o d e l estimate (section 3.2.1.3), increased  by  a factor  of  1.3  to  accommodate  z o o p l a n k t o n . T h e adjusted biomass w a s  an  increased  predation  pressure  still w i t h i n the range o f p h y t o p l a n k t o n  was from  biomass  estimates i n other models o f similar reef ecosystems ( A r i a s - G o n z a l e s 1993, O p i t z 1996). T h e basic estimates o f the re-calibrated m o d e l are s h o w n i n T a b l e 4.1 together w i t h the estimates o f the o r i g i n a l m o d e l . T h e ' a d d i t i o n a l m o r t a l i t y ' (IVT) (added to the s u m m e d predation mortality o f a groups,  see  section 3.3.4), set by S o l v e r i n the course o f m i n i m i z a t i o n and s h o w n i n T a b l e 4.3, cannot readily be related to the E c o p a t h outputs, a point to w h i c h I return i n the D i s c u s s i o n (section 5.3.3).  69  Table 4.3. 'Additional mortalities' ( M ) added to the summed predation mortality of the groups. +  'Additional mortality' ( M )  Group Phytoplankton Benthic primary producers Sessile invertebrates Bivalves Giant clams Zooplankton Foraminiferans Echinoderms Miscellaneous crustaceans Surgeonfish Shrimps Holothurians Polychaetes Stomatopods Corals Small omnivorous fish Butterflyfish Large omnivorous fish Gastropods Herring Small carnivorous fish Cephalopods Large carnivorous fish Parrotfish Snappers / groupers Miscellaneous piscivorous fish 4.2.4  +  0.000 0.003 0.047 0.053 0.023 0.000 0.038 0.066 0.052 0.394 0.046 0.015 0.027 0.026 0.153 0.602 0.267 0.010 0.003 0.078 0.285 0.125 0.064 0.603 0.082 0.049  B e t a radioactivity and t r o p h i c levels.  T h e result o f the simulation (Figure 4.3) indicates that g r o u p s at higher t r o p h i c levels are delayed i n reaching their m a x i m u m level o f measured beta r a d i o a c t i v i t y c o m p a r e d w i t h groups at l o w e r t r o p h i c levels. T h e relationship is s h o w n explicitly i n F i g u r e 4.5, w h i c h is a regression o f the t r o p h i c level o f the functional g r o u p s as a function o f the number o f days required for t h e m to reach their m a x i m u m level o f radioactivity. T h e result o f the simulation (Figure 4.3) also indicates that the m a x i m u m level o f beta radioactivity i n the v a r i o u s g r o u p s diminishes w i t h higher t r o p h i c levels. T h i s is illustrated i n F i g u r e 4.6, w h i c h is a regression o f the m a x i m u m level o f radioactivity i n the functional g r o u p s as a f u n c t i o n o f their t r o p h i c level.  70  6  r  4  V  Parrotfish 60 CD >  m O  y = 2.564 + 0.121x R = 0.506  > 2  2  y = 6.304 - 1.017x 1^ = 0.545  o  > CO  o '-3  Giant clams  Pi  12  1  Time (days)  2  3  4  Trophic level  Figure 4-5. Regression o f the trophic level of the 14 functional groups as a function o f days required for them to reach their maximum level o f beta radioactivity. Note that parrotfish and giant clams are outliers (see text).  Figure 4-6. Regression o f the maximum level o f beta radioactivity (Bq-g'ww) in the functional groups as a function o f their trophic level.  4.3 Parameter estimation and network analysis. 4.3.1  S u m m a r y statistics.  T a b l e 4.4 lists selected summary statistics o f the original a n d re-calibrated m o d e l , respectively, c o m p u t e d b y E c o p a t h a n d useful f o r c o m p a r i n g the m o d e l s w i t h each other and w i t h other reef o r n o n - r e e f ecosystems. Several o f the parameters are quantifications o f O d u m s (1969) 24 ecosystem attributes f o r assessing ecosystem development and maturity.  4.3.2 Transfer efficiencies. A t r o p h i c aggregation routine i n E c o p a t h reverses the c a l c u l a t i o n o f fractional t r o p h i c levels and quantifies the t r o p h i c flows o n discrete t r o p h i c levels sensu L i n d e m a n ( 1 9 4 2 ) (Christensen and P a u l y 1992a). It hereby becomes possible t o estimate the transfer efficiency  between  successive t r o p h i c levels and the result o f the analysis f o r the re-calibrated m o d e l is s h o w n i n T a b l e 4.5. T h e transfer efficiencies m a y be further split into f l o w s o r i g i n a t i n g f r o m primary producers and f r o m detritus.  71  Table 4.4. Summary statistics computed by Ecopath and useful for comparison o f the original and the re-calibrated model. Dashes indicate that the corresponding parameter has no dimension.  Parameter  3  Sum of all consumption Sum of all exports Sum of all respiratory flows Sum of all flows to detritus Total system throughput Total biomass (excluding detritus) Total net primary production Net system production 'Total primary production/total respiration Total primary production/total biomass Total biomass/total throughput System omnivory index Fraction of total flow originating from detritus Finn's cycling index (% of total throughput) Finn's mean path length Nutrient conservation 2  3  5 5  15  16  21  Symbol  Unit  -  t-km" -year" t-km" -year" t-km" -year" t-km" -year"  EXP R -  T B Pp P Pp/R Pp/B B/T SOI Dom.Det. FCI PL Oex  2  1  2  1  2  1  2  1  Original model 10187 3681 5938 11228 31035 3718 9430 3492 1.59 2.54 0.12 0.24 0.66 12.47 3.23 0.12  -  t-km" t-km" -year t-km" -year" 2  2  _1  2  1  -  year" year  1  -  -  Re-calibrated model 15468 1082 9008 12837 38394 3949 9793 785 1.09 2.48 0.10 0.25 0.71 18.97 3.81 0.18  a. Numbers to the left of the parameters refer to the corresponding ecosystem attribute i n Table 1 in Odum (1969).  Table 4.5. The transfer efficiency (%) by trophic level. Source \ T L  I  From producers From detritus A l l flows  4.3.3  II  III  IV  V  VI  VII  10.3 13.2 12.9  9.5 10.9 10.8  14.1 14.5 14.4  6.3 6.2 6.2  4.7 4.6 4.6  3.0 3.0 3.0  M i x e d t r o p h i c impact.  F i g u r e 4.7 shows the direct and indirect impact, i n relative terms, that the groups i n the r o w s have o n the g r o u p s i n the columns. A positive impact is indicated b y a solid bar p o i n t i n g u p w a r d s , w h i l e a negative impact is indicated b y a gray bar p o i n t i n g d o w n w a r d s . T h e figure is f r o m the re-calibrated m o d e l .  72  IMPACTED GROUP T3  o  ^ •« -s -s o W  CO  l3  C+H  CO  ca  CO  c+_,  >>£:£: 6o 6 g 9 2 >• c _ CL ~  IS  op  fc « on  eg  *H  ca  g •J oo  c/3  T3  CD  o -o C .2 o >*3 o u -g  3  ca  CQ 00 CL,  b 3  O CM  q  O CL  5  o  ~  ca  CQ O  55  II  | M |  o  ca  6 -a  co  I  W  cn ^ca  CL  O  O  S PH  S C CL  CO  O CL  o  O O  Misc. pisciv. fish Herring Small carniv. fish Large carniv. fish Small omniv. fish Large omniv. fish Snappers / groupers... Butterflyfish Surgeonfish Parrotfish Polychaetes Echinoderms Holothurians Sessile invertebrates... Shrimps Misc. crustaceans Gastropods Bivalves Giant clams Stomatopods Zooplankton  •'  II  II  I  I  I  I  I  Foraminiferans Corals Phytoplankton Benthic primary prod. Cephalopods Detritus  Figure 4-7. M i x e d trophic impact diagram from the re-calibrated Ecopath model. Solid bars pointing upwards indicate the relative positive impact and gray bars pointing downwards the relative negative impact that the groups in the rows have on groups in the columns.  73  5. Discussion T h e f o l l o w i n g discussion is structured into three parts. F i r s t some  o f the m o d e l input  parameters are discussed, i n c l u d i n g the time span c o v e r e d b y the m o d e l and the fish biomass estimates. A l s o discussed here is the role o f herbivorous and p l a n k t i v o r o u s fish o n the reef. T h e second part deals w i t h m o d e l outputs, i n particular the role o f detritus r e c y c l i n g and ecosystem maturity. F i n a l l y , the re-calibration process and the u s e o f radioactivity data are discussed, as w e l l as the result o f the simulation and some potentials o f the approach.  5.1 Model input parameters. 5.1.1  T h e time span c o v e r e d by the m o d e l .  T h e E c o p a t h m o d e l w a s constructed w i t h data f r o m a variety o f sources, representing w o r k spanning several decades. W i t h i n the same p e r i o d , the atoll w a s u s e d f o r nuclear testing and w h o l e islands disappeared, others were burned t o the g r o u n d , and yet others w e r e completely restructured t o a c c o m m o d a t e military facilities ( A n o n . 1991, D e v a n e y et al. 1987). U n d e r these circumstances it seems appropriate t o ask whether it w a s legitimate t o use the data collected w i t h i n this p e r i o d for the synthesized o f a steady-state / mass-balance m o d e l . F e w signs o f destruction, however, were observed i n the marine environment. I n atmospheric tests (41 o f the 43 test at E n e w e t a k , T a b l e 2.3), the marine organisms w e r e partly protected by the water. W h i l e the explosions at l o w tide k i l l e d exposed organisms, e.g., those l i v i n g i n the intertidal zone, organisms l i v i n g b e y o n d the algal ridge o r h i d i n g under r o c k s and corals w e r e hardly damaged at all (Bablet and Perrault 1987a). D e a d fish w e r e observed repeatedly i n the v i c i n i t y o f the detonation sites immediately after a nuclear test (Bablet and Perrault 1987a), but were not observed f o r extended periods o f time, as might have been expected  f r o m the elevated  levels o f r a d i o a c t i v i t y ( S e y m o r e  1960).  W e a k e n e d fish w o u l d q u i c k l y have been r e m o v e d b y predators, and therefore, w o u l d not have been observed. H o w e v e r , it w a s still believed that the increase i n radioactivity w a s not enough to k i l l the fish directly ( S e y m o r e  1960). I n addition, o f the thousands o f fish that  were  examined, none s h o w e d apparent signs o f internal damages, the only exception being the thyroids where damages ranged f r o m zero t o a hundred percent ( G o r b m a n and James 1963). 74  Superficially, the damaged fish appeared n o r m a l ( S e y m o r e  1960). G e n e t i c effects,  which  should s h o w u p i n the progeny, are not easily studied in situ, b u t requires that the natural variability o f the populations is perfectly k n o w n (Bablet and P e r r a u l t 1987b). R e g a r d i n g l o w e r t r o p h i c level organisms, K n u t s o n and B u d d e m e i r (1973) f o u n d that "results to date indicate that the m a c r o s c o p i c g r o w t h rates a n d patterns o f [massive] corals are relatively unaffected b y uptake o f the observed amounts o f r a d i o a c t i v i t y . . . " M o r e o v e r , the absorbed lethal radiation dose has been s h o w n t o be inversely related t o the evolutionary level o f the organism, i m p l y i n g that less derived species are less sensitive t o r a d i a t i o n (Bablet and Perrault 1987b). B a s e d o n these observations I therefore conclude that it w a s legitimate t o use a w i d e range o f data f o r the c o n s t r u c t i o n o f the m o d e l , a n d thus assuming that the reef ecosystem d i d not change w i t h i n the m o d e l e d p e r i o d . It is v e r y l i k e l y that the reef ecosystem has been m o r e harmfully affected b y physical damages than b y radioactivity. A constant leakage o f silt f r o m the craters w o u l d c l o g u p the coral p o l y p s and reduce water visibility, r e d u c i n g photosynthesis. H o w e v e r , this p r o b l e m has t o m y k n o w l e d g e not been reported for the part o f the reef m o d e l e d here.  5.1.2  F i s h biomass and abundance estimates.  5.1.2.1 Visual census and rotenone sampling. T h e fish biomass estimates (Table 3.17) w e r e either estimated b y the p r o g r a m o r derived f r o m the O d u m s ' study (1955). T h e latter used rotenone sampling a n d v i s u a l census based o n a m e t h o d b y B r o c k (1954) (see section 3.2.3.1 a n d A p p e n d i x 5). A c c o r d i n g t o R a n d a l l (1963) and S m i t h (1973 a), v i s u a l census, however, is o f limited value f o r quantitative studies o n c o r a l reefs. H u m a n s errors are i n v o l v e d i n estimating the numbers a n d sizes o f fish a n d secretive, h o l e - d w e l l i n g , a n d n o c t u r n a l species are not observed. L a t e r , i n a r e v i e w o f the m e t h o d himself, B r o c k (1982) f o u n d that it "underestimates b o t h the most c r y p t i c as w e l l as the most abundant fish species... [and that] only diurnally exposed fish species are censused w i t h any accuracy u s i n g the v i s u a l census technique." H e then c o m p a r e d the results obtained w i t h visual  census  w i t h results  obtained  using  rotenone,  75  and found  the f o l l o w i n g  power-  relationship: Y = 0.74 • X  1  1  5  , where X is the number o f individuals visually assessed and Y is  the number r e m o v e d b y rotenone. Rotenone  sampling, however,  is not w i t h o u t problems  necessary to obtain a reliable p o p u l a t i o n estimate  either, a n d repeated  (Smith  sampling is  1973a). A n idea o f the real  p o p u l a t i o n size c a n be obtained w i t h a L e s l i e plot, as s h o w n by P a u l y (1984) f o r t w o c o r a l reef species (Figure 5.1). H e r e , the catch/effort (where effort is the a p p l i c a t i o n o f poison) has been plotted as a function o f the cumulative catch, and the intercept o f the regression w i t h the abscissa is an estimate o f the real p o p u l a t i o n number ( N ) . T h e regressions indicate that only 0  about one third o f the populations are sampled w i t h the first a p p l i c a t i o n o f p o i s o n .  Catch/uit of effort  8 c  •  Gramma  •  Kaupichthys  loreto hyoproroides  6 <  4 N  2  0  1  0 10  5  0  15  20  25  Cumulative catch Figure 5-1. Leslie plots for reef eels {Kaupichthys hyoproroides) and F a i r y basslet (Gramma loreto) from an isolated Bahamian reef patch, with estimates o f virgin population sizes (redrawn and modified from Figure 6.1 i n Pauly (1984); mis-labeled Thalassoma bifasciatum (Bluehead wrasse) i n Pauly (1984)). The arrows identify the original population sizes ( N ) . a  a  0  5.1.2.2 Fish biomass estimates at Enewetak A toll. It c a n be inferred f r o m the discussion above that O d u m s ' fish biomass estimates o f 6 g d w m "  2  or 2 6 g w w - m " (Table 3.17, A p p e n d i x 5) are highly conservative. T h e real stock size is m o r e 2  likely i n the area o f 80 g w w - m " o r even higher. T h e p r o b l e m w a s r e c o g n i z e d b y the authors 2  who  wrote  that " m o r a y  eels w e r e estimated  f r o m the rotenone  samples  o n the surely  underestimating assumption that all the morays had c l i m b e d out into the channels t o d i e . " B o t h the o r i g i n a l and the re-calibrated E c o p a t h m o d e l , however, o n l y estimated a fish biomass o f 35 g w w - m "  2  (Table 4.1). T h i s l o w estimate c o u l d be the result o f using the O d u m s ' 76  estimates as input, and balancing the m o d e l w i t h E c o r a n g e r a l l o w i n g f o r a variability o f 9 9 % . T h o u g h this might seem as a high variability, it is not e n o u g h to capture the ' r e a l ' stock size. F u r t h e r m o r e , as the m o d e l is parameterized f r o m the t o p - d o w n , the rest o f the system is balanced so that the biomass flows at the l o w e r t r o p h i c levels m a t c h the f o o d demands o f the upper levels. L o w input values i n the top therefore 'scale d o w n ' the w h o l e system. M o r e o v e r , i n the re-calibration process, the biomass estimates w e r e only a l l o w e d to vary w i t h i n 75%o, and for many o f the l o w e r t r o p h i c level groups they w e r e not a l l o w e d to vary at all. T h e overall result, given the constraints, w a s therefore that the ' r e a l ' stock size w a s  never  simulated.  5.1.2.3 Comparing the standing stock of coral reeffish. T a b l e 5.1 lists the standing stock o f fish o n various reefs. A g a i n , these estimates are probably t o o l o w . H o w e v e r , assuming that they are t o o l o w b y the same factor, it is still possible to c o m p a r e a m o n g them. E x c e p t for L o o e K e y , the standing s t o c k varies b y an order  of  magnitude, f r o m 26 to 243 g w w - m " , w i t h E n e w e t a k A t o l l at the l o w e r end o f the scale. 2  S o r o k i n (1993) presents similar results. R a n d a l l (1963) listed four reasons explaining w h y the standing stock might differ between reefs. T h e first o f these w a s that the standing stock is largely determined b y the amount o f c o v e r / shelter afforded by the reef. A l s o , since reefs typically differ substantially i n the degree o f sculpturing, measuring only the h o r i z o n t a l plane introduces considerable error w h e n c o m p a r i n g a m o n g reefs. T h e type o f benthic g r o w t h is a third factor affecting the stock size; finally, the fishing effort w i l l tend to reduce biomasses.  5.1.2.4 The abundance and role of herbivorous fish. T h e shallow w a t e r fish fauna at E n w e t a k A t o l l , as w e l l as o n m a n y other reefs, is dominated b y h e r b i v o r o u s surgeonfish (Acanthuridae) and o m n i v o r o u s parrotfish (Scaridae) that invade the reef flat w i t h the i n c o m i n g tide [present study; O d u m and O d u m 1955, B a k u s 1967, W i e b e et al. 1975, O g d e n and L o b e s 1978, L e w i s 1981, M i l l e r 1982, C h a r t o c k 1983b).  77  Table 5-1. Standing stock of fish on coral reefs in different regions. Standing stock (g w w m " )  Location  Source  2  Windward reef, Enewetak A t o l l , (Ecopath) Windward reef, Enewetak Atoll  35 26  Barrier reef, Moorea (Ecopath) Fringing reef, Moorea (Ecopath) French Frigate Shoals, H a w a i i (Ecopath) ' Keahole Pt., K o n a , H a w a i i H a w a i i , mean of Table 1 in Brock (1954) (not incl. Keahole and Rabbit Island) Fringing Reef, St. John, V i r g i n Islands '  243 146 24 185 20  Present study (Odum and Odum 1955) (Arias-Gonzales 1993) (Arias-Gonzales 1993) (Polovina 1984) (Brock 1954) (Brock 1954)  160 158 104 785 49  (Randall 1963) (Randall 1963) (Opitz 1996) (Venier 1997) (Bardach 1959)  b c  0  0  3 0  Fringing reef, V i r g i n Islands (Ecopath) Looe Key, Florida (Ecopath) Patch reef, Bermuda a. N o t including small pelagics and large apex predators; b. Only including reef fishes; c. Fished.  T h e diet o f parrotfish is somewhat controversial ( R a n d a l l 1963, 1974, B a k u s 1967, S m i t h and P a u l s o n 1974). C o n t r a r y to most studies, H i a t t and Strasburg (1960) f o u n d an abundance o f c o r a l p o l y p s i n the stomach o f parrotfish f r o m the M a r s h a l l Islands, and characterized t h e m as g r a z i n g omnivores. In a comment, R a n d a l l (1967) w r o t e : " T h e greater u t i l i z a t i o n o f coral b y scarids i n the M a r s h a l l Islands noted by H i a t t & Strasburg may be related to the h i g h coral c o v e r o f the reefs." A f t e r having d i v e d at E n e w e t a k , R a n d a l l (1974) later w r o t e : " W i t h i n the last t w o years the author has d i v e d at b o t h H e r o n Island o n the G r e a t B a r r i e r R e e f and E n i w e t o k i n the M a r s h a l l Islands and finds it difficult t o explain the apparent difference i n the amount o f c o r a l i n the diet o f scarids at these t w o localities. M o s t o f the scarid species are c o m m o n to b o t h islands, and there appears to be no notable o v e r a l l difference i n the amount o f c o r a l cover.  T h e c o r a l g r o w t h can vary enormously,  o f course,  a m o n g the marine  environments o f the islands. P o s s i b l y H i a t t and Strasburg's specimens w e r e collected mainly f r o m a zone o f heavy c o r a l but little algal g r o w t h " ( R a n d a l l 1974). I n retrospect, the diet c o m p o s i t i o n o f parrotfish used i n the present  study ( 7 0 % corals, 3 0 % benthic primary  producers, based o n H i a t t and Strasburg (1960), see A p p e n d i x 2) is therefore questionable. T h e diet c o m p o s i t i o n is also partly responsible for the h i g h t r o p h i c level o f parrotfish (3.46, see T a b l e 4.1) estimated by E c o p a t h . A n o t h e r reason for this h i g h t r o p h i c level is that, i n the 78  v e r s i o n o f E c o p a t h used here, t r o p h i c levels w e r e c o m p u t e d as: 1 + m e a n t r o p h i c level o f prey. Since autotrophy is not i n c l u d e d i n the calculation, the t r o p h i c level o f partly autotrophic organisms like giant clams and corals is i n fact t o o high, w h i c h i n t u r n affects the t r o p h i c level o f the organisms feeding o n them, e.g., parrotfish. A n o t h e r c o n t r o v e r s y is the dominance o f herbivorous fish o n c o r a l reefs i n general ( O d u m and O d u m 1955, B a r d a c h 1959, R a n d a l l 1963, B a k u s 1966, O g d e n and L o b e s 1978, S o r o k i n 1993). B o u c h o n - N a v a r o and H a r m e l i n - V i v i e n (1981) f o u n d that, i n contrast to O d u m s ' study, most authors have estimated that herbivorous fish constitute b e t w e e n 10 and 1 5 % o f the fish fauna o n c o r a l reefs, b o t h i n terms o f numbers and biomass. L i k e w i s e , B a k u s (1966) f o u n d that c o r a l reef fish generally consist o f r o u g h l y 25%> herbivores and 65%> carnivores. H e based this o n the three studies described b e l o w , w h i c h I have consulted w i t h o u t being able to reach the same c o n c l u s i o n : •  B a r d a c h (1959), w o r k i n g o n a patch reef i n B e r m u d a , f o u n d that the w e i g h t o f carnivores (many feeding o n a close by seagrass bed) w a s almost t w i c e that o f o m n i v o r e s , but o n a large r e e f f o u n d that herbivorous / o m n i v o r o u s fish o u t w e i g h e d the carnivores by about nine to one;  •  R a n d a l l (1963, 1967) f o u n d that Scaridae appear to be the largest family b y weight i n most t r o p i c a l reef areas; and  •  H i a t t and Strasburg (1960) f o u n d that carnivores i n the M a r s h a l l Islands dominated by number, however, b o t h the present study and the study b y O d u m and O d u m (1955) estimated that herbivorous / o m n i v o r o u s fish dominate b y weight.  S u p p o r t i n g the findings at E n e w e t a k , S o r o k i n (1993) reported that h e r b i v o r o u s " r e e f fish f o r m one o f the most important t r o p h i c guilds, w h i c h includes some 10 - 2 0 % o f the total species and 15 - 50%> o f total fish b i o m a s s . . . Sometimes their biomass comprises o v e r 50%> even o f the t o t a l . . . " F i n a l l y , C o l i n (1987a) w r o t e that the "general l a c k o f herbivores as significant as fishes at E n e w e t a k presents an interesting contrast to reefs i n some other areas o f the w o r l d . " T h e r e is little doubt that herbivorous fish are m u c h m o r e abundant o n c o r a l reefs than they are i n temperate waters ( S o r o k i n 1993), and play the important role o f channeling primary p r o d u c t i v i t y up the f o o d w e b ( O g d e n and L o b e s 1978). Surgeonfish are, a c c o r d i n g to H i a t t and Strasburg (1960), the most important g r o u p o n the reef i n c o n v e r t i n g p r i m a r y p r o d u c t i v i t y 79  into animal tissue. T h e m o d e l predicted that o f the benthic p r i m a r y p r o d u c t i o n that is grazed directly, 6 4 % is grazed b y invertebrates and 3 6 % by fish. O f the latter, 6 7 % is grazed b y surgeonfish alone. T h e assimilation efficiency o f surgeonfish, h o w e v e r , is quite l o w ( C h a r t o c k 1983b). M o s t o f the algae they eat are recycled into detritus before they, i n the f o r m o f D O M and P O M (see section 3.2.1.1), are u t i l i z e d b y the various suspension and sediment feeders ( C h a r t o c k 1983b) that are so abundant o n the reef (see T a b l e 4.1). Interestingly, the e c o t r o p h i c efficiency ( E E ) o f the h e r b i v o r o u s / o m n i v o r o u s surgeonfish, parrotfish, and butterflyfish are particularly l o w (0.12 - 0.14), i m p l y i n g that the majority o f their p r o d u c t i o n is recycled to the detritus p o o l . S i m i l a r observations have been made o n other c o r a l reefs ( O p i t z 1996, P a r r i s h et al. 1986 (cited i n O p i t z ) ) , and the explanation is not clear. It c o u l d perhaps have something to do w i t h the behavior o f these fish. H e r b i v o r o u s fish are most active d u r i n g daytime w h e n predators are also m o r e visible and easier to escape. F u r t h e r m o r e , h e r b i v o r o u s fish tend to concentrate i n the shallower parts o f the reef where the primary p r o d u c t i v i t y is highest ( O g d e n and L o b e s 1978), and it c o u l d be that their predators are not w e l l adapted to the physical conditions at these s h a l l o w depths. F o r example, studies o f some c o r a l reefs i n the R e d Sea have s h o w n that 7 1 % o f the h e r b i v o r o u s fish concentrated at 0 to 5 m o f depth, w h i l e the remaining 2 9 % o c c u r r e d between 10 and 4 0 m ( B o u c h o n N a v a r o and H a r m e l i n - V i v i e n 1981).  5.1.2.5 The fish fauna and zooplankton on the fore reef. Aside  from  herbivorous  fish,  coral  reefs  are  characterized  by  a  high  abundance  p l a n k t i v o r o u s fish feeding o n resident and oceanic z o o p l a n k t o n ( H o b s o n and Chess  of  1978,  S o r o k i n 1993). T h e oceanic z o o p l a n k t o n provides an external input o f energy and nutrients to the reef, and the feces o f the fish feeding o n t h e m p r o v i d e s f o o d f o r corals and other benthic filter feeders ( S o r o k i n 1993). A c c o r d i n g to W i l l i a m s (1991), the " t r a d i t i o n a l v i e w o f coral reefs as energetically self-contained ecosystems o c c u r r i n g only i n clear oceanic.waters ( O d u m and O d u m , 1955) suggests little environmental variability and relatively little variation i n the structure o f fish communities a m o n g reefs. T h i s v i e w is grossly i n error. A s far as fishes are concerned, c o r a l reefs are not energetically self-contained. A major p r o p o r t i o n o f the  80  fish  biomass feeds o n z o o p l a n k t o n derived f r o m an external source - the waters surrounding the reef." T h i s w a s clearly s h o w n i n a study by H a m n e r et al. (1988) o n the fore reef o f D a v i e s Reef, central Great B a r r i e r Reef. H e r e they found that oceanic z o o p l a n k t o n w a s c o n s u m e d b y a " w a l l o f m o u t h " f o r m e d by the many p l a n k t i v o r o u s fish o n the fore reef. " M o s t o f the z o o p l a n k t o n i n this water is captured and eaten b y p l a n k t i v o r o u s fish w h i c h i n t u r n defecate onto the reef surface, a process w h i c h enhances the g r o w t h o f corals and benthic algae. B r e a k i n g w a v e s tear benthic algae o f f the reef crest and the floating assemblage o f algal fragments and fecal material w h i c h has not yet settled f l o w s across the r e e f top. It is this admixture o f algae, feces, and even sand w h i c h most previous investigators [e.g., at E n e w e t a k A t o l l ] have treated as i f it w e r e oceanic i n o r i g i n (Johannes and G e r b e r 1 9 7 4 ) " ( H a m n e r et al. 1988). That the situation is probably the same at E n e w e t a k A t o l l is supported b y some observations by H o b s o n and Chess (1978, 1986) (see also section 3.2.1.4). I n places o f strong currents at the l a g o o n w a r d side o f the w i n d w a r d reef they observed that the abundance z o o p l a n k t o n increases dramatically at night, and explained it as a consequence  of  oceanic  o f a general  rise o f z o o p l a n k t o n t o w a r d s the surface waters at night i n the o p e n sea. Inferring f r o m the study by H a m n e r et al. (1988)  it c o u l d , however,  also be the consequence  o f reduced  predation o f z o o p l a n k t o n o n the fore reef at night, as most p l a n k t i v o r e s fish are diurnal ( H a m n e r et al. 1988). I f this is the case, it w o u l d i n t u r n explain the h i g h f o o d c o n s u m p t i o n , estimated b y the p r o g r a m , o f z o o p l a n k t o n b y corals w h i c h m a i n l y takes place at night (see section 3.2.1.5) Generally, the fore reef is physically very difficult to m o n i t o r and no reliable fish biomass estimates are available ( H a r m e l i n - V i v i e n 1977). H o w e v e r , H a r r y ( 1 9 5 3 , cited f r o m Stevenson and M a r s h a l l (1974)), e.g., "offered the general impression that the outer r e e f at R a r o i a A t o l l supported fifty per cent o f the fish p o p u l a t i o n o f the entire a t o l l . . . "  81  5.2 Outputs of the model. 5.2.1  T h e role o f benthic primary producers.  U n l i k e most aquatic ecosystem where the secondary p r o d u c t i o n is t y p i c a l l y p h y t o p l a n k t o n driven, benthic p r i m a r y producers are the c h i e f supporter (directly or indirectly t h r o u g h detritus, see b e l o w ) o f the secondary p r o d u c t i o n o n c o r a l reefs ( L e w i s 1981, P o l u n i n and K l u m p p 1992b, P o l u n i n 1996). Therefore, despite the visible d o m i n a n c e o f corals, benthic primary producers are the most abundant organisms i n terms o f l i v i n g biomass (Table 4.1). T h e p r i m a r y p r o d u c t i o n o n c o r a l reefs is generally v e r y high, and they rank a m o n g the most p r o d u c t i v e ecosystems i n the w o r l d ( O d u m and O d u m 1955, L e w i s 1977, S o r o k i n 1990). A t E n e w e t a k A t o l l , as o n many other reefs, the b u l k o f the benthic p r i m a r y p r o d u c t i o n ( 9 3 % ) is not c o n s u m e d directly, but is recycled to the detritus p o o l . T h e 7 % that is c o n s u m e d / grazed directly is a relatively l o w fraction c o m p a r e d to other c o r a l r e e f systems, e.g., 2 2 to 3 3 % o n T i a h u r a reef, M o o r e a Island, F r e n c h P o l y n e s i a ( A r i a s - G o n z a l e s et al. 1997), 3 6 % at a V i r g i n Island reef ( O p i t z 1996), 3 3 % i n the L o o e K e y ' s ( V e n i e r 1997), and 43 and 6 5 % o n the reef crest o f D a v i e s Reef, central Great B a r r i e r Reef, ( P o l u n i n and K l u m p p 1992a). T h e 7 % f r o m E n e w e t a k , however, is a w e i g h t e d mean o f all the r e e f zones, i n c l u d i n g the sand / shingle z o n e w h i c h comprises 5 7 % o f the total area i n c l u d e d i n the E c o p a t h m o d e l (see Table 3.1). T h e intensity o f g r a z i n g probably varies considerably between the zones, highest o n the outer reef flat ( B a k u s 1967, M i l l e r 1982, C h a r t o c k 1983b, P o l u n i n 1996) and lowest i n the sand / shingle zone.  5.2.2  T h e role o f detritus.  T h e e c o t r o p h i c efficiency  o f most groups  i n the system  is relatively l o w (Table  4.1),  suggesting that m u c h o f their p r o d u c t i o n is recycled directly to the detritus p o o l . In turn, approximately 9 2 % o f the detritus is recycled, and 7 1 % o f all f l o w s i n the system originates f r o m there (Table 4.1  and 4.4). T h e secondary p r o d u c t i o n is thus largely dependent  on  detritus, a characteristic o f c o r a l reefs i n general ( S o r o k i n 1990, A r i a s - G o n z a l e s et al. 1997, O p i t z 1996, V e n i e r 1997). A high degree o f r e c y c l i n g is also a characteristic o f mature ecosystems a c c o r d i n g to O d u m (1969), w h o hypothesized that " f o o d chains b e c o m e c o m p l e x  82  w e b s i n mature stages, w i t h the b u l k o f b i o l o g i c a l energy f l o w f o l l o w i n g detritus p a t h w a y s . . . heterotrophic u t i l i z a t i o n o f p r i m a r y p r o d u c t i o n i n mature ecosystems  i n v o l v e s largely a  delayed c o n s u m p t i o n o f detritus" S o m e o f the detritus, such as benthic algal fragments t o r n l o o s e at the fore reef, is c o n s u m e d directly b y v a r i o u s herbivores and detritivores ( i n c l u d i n g fish) ( W i e b e et al. 1975). T h e bulk, however, is channeled v i a bacteria into a m i c r o b i a l l o o p ( A r i a s - G o n z a l e s et al. 1997, A z a m 1998) w h e r e u p o n it again becomes including  polychaetes,  sessile  accessible to the abundance o f benthic  invertebrates  (e.g.,  sponges),  miscellaneous  filter-feeders crustaceans,  bivalves, z o o p l a n k t o n , foraminiferans, corals, and others, that characterizes the reef. T h e importance o f detritus c a n also be seen i n F i g u r e 4.7 w h i c h s h o w s that detritus has a positive impact o n most groups i n the system. F e w fish consume detritus directly, but many o f their prey d o and detritus therefore still has a positive impact o n fish, t h o u g h indirectly.  5.2.3  C o m p a r i n g w i t h other models.  5.2.3. J Trophic transfer efficiencies. T h e transfer efficiencies between successive t r o p h i c levels w e r e presented i n T a b l e 4.5. T h e p r o g r a m estimated relatively h i g h efficiencies at t r o p h i c levels II, III, and I V , higher for  flows  originating f r o m detritus than f r o m primary producers. T h i s indicates that the energy context o f the organic material is higher and m o r e accessible to the organisms after it has been processed / enriched by bacteria. A t higher t r o p h i c levels ( V , V I , V I I ) , the efficiencies are considerably l o w e r , and overall decreasing. T h e r e is no longer any difference between flows that originated f r o m detritus and f r o m p r i m a r y producers. A s organisms tend to be m o r e m o b i l e at higher t r o p h i c levels, increasingly m o r e energy is lost t h r o u g h respiration at the expense o f b e i n g transferred up the system. O p i t z (1996) reasoned that "the r e e f s 'strategy'  is not t o achieve high transfer  efficiencies between t r o p h i c levels but to b u i l d up biomass t h r o u g h maintenance o f short cycles for an effective r e c y c l i n g o f matter back to its base, the detrital p o o l . . . " In Table 5.2, the transfer efficiencies f r o m E n e w e t a k A t o l l are c o m p a r e d w i t h those o f three other non-fished c o r a l reef ecosystems. There seems to be no clear o v e r a l l trend, except that the efficiencies always are higher at l o w e r t r o p h i c levels. Since the transfer efficiencies depend 83  strongly on the gross food conversion efficiencies, G E (i.e. the fraction o f the consumption of a group that is channeled toward production), and since these are not standardized for similar functional groups in different ecosystem models, the variation among systems tends to be high (Christensen and Pauly 1993). Table 5-2. Trophic transfer efficiencies (%) of four coral reef ecosystem models. Non of the systems are fishes to any extent. System II III IV V 10.8 14.4 6.2 Enewetak 12.9 10.1 4.0 4.1 3.3 FFS, Hawaii 9.9 9.0 13.1 16.6 Virgin Islands 25.7 29.4 14.9 7.6 Looe Key a. Present study; b. French Frigate Shoals (Christensen and Pauly 1993); c. Opitz (1996); d. Florida (Venier 1997). b  0  d  VIII 7.4  VII 3.0 11.0 9.0  VI 4.6 10.9 8.8  3  IX 4.8  5.2.3.2 Biomass by trophic level. The biomass at successive trophic levels, estimated in the present study and by Odum and Odum (1955), are compared in Table 5.3 and graphically in Figure 5.2. Table 5-3. Biomass at discrete trophic levels for the windward reef ecosystem at Enewetak Atoll as estimated by Odum and Odum (1955) and in the present study. Trophic level Odum and Odum (1955) Ecopath (this study)  I 2812 3198  3  II 528 372  III 44 356  IV  V  VI  Total 3384 3950  VII  -  -  -  -  18  6  0.4  0.02  a. Assuming dw = 25% ww. @ 0.5 Wet weight (t/km ) 2  C -11 U H-132 PRODUCERS - 703  Figure 5-2. Biomass pyramids of the marine food web of the windward reef at Enewetak Atoll. The pyramid to the left is redrawn and modified from Odum and Odum (1955), and shows the average biomass (in g dry weight) for the reef where H = herbivores and C = carnivores. The pyramid to the right was created using a routine in Ecopath and is scaled such that the volume of each layer is proportional to the biomass on the corresponding discrete trophic level. 84  T h e total biomass is very similar w h i c h is no surprise, as many o f the input data for the E c o p a t h m o d e l w e r e based o n the O d u m s ' data. T h e biomass i n the present study, however, is distributed over seven t r o p h i c levels as c o m p a r e d to three i n O d u m s ' study. T h e m o r e detailed t r o p h i c structure is the result o f estimating the t r o p h i c levels instead o f assigning them. I n the latter case, the c o m p l e x f o o d web interactions that characterizes most ecosystems (see F i g u r e 4.1) are not taken into account, w h i c h i n t u r n has important i m p l i c a t i o n s for the predictability o f such models (see section  1.1).  5.2.3.3 Ecosystem maturity. Quantitative measures are very useful for assessing and c o m p a r i n g the state and performance o f ecosystems ( D a l s g a a r d ecosystem network  and O f i c i a l 1998).  O d u m (1969) identified 24  maturity, hypothesizing h o w ecosystems develop analysis,  Christensen (1992) quantified several  ( A p p e n d i x 6) and used a selection o f t h e m to ranked 41  attributes  of  o v e r time. O n the basis  of  of Odums  ecosystem  attributes  steady state f o o d w e b  models  c o m p r i s i n g ponds, lakes, rivers, temperate and t r o p i c a l coastal areas, c o r a l reefs, t r o p i c a l shelves and upwellings. O f the 41 systems, c o r a l reefs w e r e f o u n d t o rank intermediate i n maturity w i t h lakes / rivers r a n k i n g lowest and coastal areas highest. A c c o r d i n g to O d u m (1969), the capacity o f an ecosystem to entrap, w i t h h o l d , and cycle nutrients increases w i t h maturity. T h e degree o f r e c y c l i n g can be measured b y F i n n ' s c y c l i n g index ( F C I , see A p p e n d i x 6), w h i c h expresses the fraction o f the total system throughput that is recycled ( F i n n 1976, Christensen and P a u l y 1992a, (1993) ranked the 41  systems,  mentioned above,  1993). W h e n Christensen and P a u l y  after this index, they f o u n d a strong  correlation w i t h the maturity ranking by Christensen (1992). S i m i l a r l y , i n a study o f ecosystem stability, V a s c o n c e l l o s et al. (1997) s h o w e d that r e c y c l i n g plays an important role i n the maintenance o f ecosystem stability as does path length, the average number o f groups that a unit o f f l o w passes t h r o u g h (Christensen and P a u l y 1993, V a s c o n c e l l o s et al. 1997). I n F i g u r e 5.3, E n e w e t a k A t o l l is c o m p a r e d w i t h three other c o r a l reef ecosystems.  T h e figure  shows  that; a) c o r a l reefs w i t h l o w Pp/R (net p r i m a r y production/respiration) ratio display h i g h degree o f r e c y c l i n g ; and b) r e c y c l i n g is positively correlated w i t h path length. B o t h trends are consistent w i t h O d u m s theory o f ecosystem maturity (Christensen and P a u l y 1993,  85  Odum  1969), and it c a n be inferred f r o m the figure that E n e w e t a k A t o l l is m o r e ' m a t u r e ' o r stable ( V a s c o n c e l l o s et al. 1997) than the three other reef systems.  (a)  g  20  (b)  Enewetak Looe Key  15  g  Enewetak^ Looe Key  15  #  X <a  X rr-t  B  10  10 -  M  5  FFS  •  #  i  0 0  1  i 2  Finn's cyclir  Finn's cycling inc  20  Virgin Is. i  3  i 4  5  FFS Virgin Is.^  0 0  Primary productivity /respiration  i  1  2  4  6  Path length  Figure 5-3. a) Finn's cycling index versus primary productivity/respiration ratio and; b) Finn's cycling index versus average path length for four coral reef ecosystems. Based on data i n the present study, Christensen (1992), and Venier (1997). F F S is the French Frigate Shoals i n Hawaii. Looe K e y and the V i r g i n Islands are both in the Caribbean.  5.3 Simulating radioactivity. 5.3.1  T h e re-calibrated E c o p a t h m o d e l .  R e - c a l i b r a t i n g the E c o p a t h m o d e l , using observed data o n beta radioactivity, resulted i n a m o r e ' m a t u r e ' ecosystem as seen b y c o m p a r i n g the summary statistics o f the original and r e calibrated m o d e l presented i n T a b l e 4.4. Several o f the statistics are quantification's o f O d u m s 24 attributes o f ecosystem maturity ( O d u m 1969, Christensen 1992, 1995) (see also section 5.2.3.3 and A p p e n d i x 6 ) , and the general trend supports a m o v e t o w a r d s a m o r e mature ecosystem. F o r example, the degree o f r e c y c l i n g and nutrient c o n s e r v a t i o n is higher, Pp/R moves t o w a r d unity, and the average path length gets longer, all properties that are ascribed t o mature ecosystems such as a coral reef. T h e re-calibrated m o d e l thus represents  a more  'realistic' system than the original, i m p l y i n g that the i n c o r p o r a t i o n o f radioactivity has added valuable i n f o r m a t i o n t o the m o d e l . T h i s is a n important finding that might help i m p r o v e the t r o p h i c f l o w assessments b y E c o p a t h models once the a p p r o a c h is i n c o r p o r a t e d as a general routine i n the p r o g r a m . 86  5.3.2  T r o p h i c transfer o f radioactivity and the ' f o o d w e b time l a g ' .  T r o p h i c transfer o f persistent pollutants, such as radioactivity, w i t h i n aquatic f o o d w e b s should i n theory i m p l y a time lag between the observed m a x i m u m and the t r o p h i c p o s i t i o n o f the functional g r o u p , reflecting the time required for the pollutant to be m o v i n g up the f o o d web. M a x i m u m values should be observed first i n the p r i m a r y producers, then i n herbivores, then i n higher t r o p h i c levels, w i t h top predators reaching their m a x i m u m concentrations last ( E l l i o t t et al. 1992). A clear example has recently been presented for the C e n t r a l B a l t i c Sea, f o l l o w i n g the C h e r n o b y l accident, by D a l s g a a r d et al. (1998). T h e scenario w a s also observed at E n e w e t a k A t o l l ( F i g u r e 4.3), t h o u g h the partly autotrophic giant clams and parrotfish differed f r o m the expected trend (see F i g u r e 4.3 and 4.5). T h e reason for this is that, i n the v e r s i o n o f E c o p a t h used here, autotrophy was not accounted for i n the calculation o f trophic levels (see also section 5.1.2.4). P a r t l y autotrophic organisms are therefore assigned a higher t r o p h i c level than they should, w h i c h unfortunately also has i m p l i c a t i o n for all the predators feeding o n them. A detailed analysis o f the ' f o o d w e b time l a g ' w i l l therefore have to await until autotrophy is explicitly included into E c o p a t h , and thus into the c o m p u t a t i o n o f t r o p h i c levels.  5.3.3  D i l u t i o n effects and the additional mortality ( M ) . +  M o s t laboratory experiments have indicated that direct uptake o f radioisotopes f r o m the water b y the organisms is m o r e important than is f o o d w e b Polikarpov  1966,  transfer ( O p h e l and J u d d  T h o m a n n 1981). L a b o r a t o r y experiments,  however,  can only  1966,  simulate  simple f o o d chain relationships, and typically place the organisms under highly unnatural conditions, such as constant concentrations o f radioisotopes i n the s u r r o u n d i n g media. In their natural settings, reef organisms are part o f c o m p l e x f o o d w e b s ( F i g u r e 4.1) and many o f them are highly m o b i l e , m o v i n g i n and out o f the radiation contaminated area. I n addition, currents, winds,  tides,  and  rain  work  to  dilute the  radioactivity  (Welander  1957)  so  that  its  concentration is anything but u n i f o r m . U n d e r these circumstances, " r a d i o n u c l i d e concentration factors [the ratio o f the concentration o f the isotope i n the o r g a n i s m and i n the water] lose their meaning, and the operative factors b e c o m e the elimination o f radionuclides f r o m the organisms and the assimilation o f radioactive f o o d by predators" ( P o l i k a r p o v 1966).  87  A n necessary assumption i n E c o p a t h is that foraging takes place only w i t h i n the m o d e l e d area (even w h e n ' i m p o r t s ' are included as f o o d items), as defined b y the diet c o m p o s i t i o n o f the functional groups explicitly included i n the m o d e l . V i o l a t i o n s o f this assumption undoubtedly accounts for at least some o f the differences  between the observed and predicted trends  ( F i g u r e 4.3) b o t h before and after re-calibration o f the m o d e l . T h i s p r o b l e m o f ' d i l u t i o n ' / ' m i g r a t i o n ' w a s solved by treating it as an additional mortality ( M ) , o n top o f the total +  mortality ( Z , i.e., P / B ) to w h i c h a functional g r o u p is subjected (section 3.3.4, 4.2.3, and Table 4.3). C o n t r a r y to what might have been expected, k n o w i n g that higher t r o p h i c level organisms tend to be m o r e mobile, no correlation w a s f o u n d between M " and the t r o p h i c level 4  o f the functional groups. T h i s suggests that the physical d i l u t i o n effects discussed above w e r e m o r e important at the w i n d w a r d reef than the effects o f m i g r a t i o n . T h i s is not surprising as the reef is small and swept b y relatively strong currents ( A t k i n s o n et al. 1981, A t k i n s o n 1987). M o r e o v e r , most o f the organisms are either sessile, or have restricted ranges, w i t h fish s h o w i n g strong territorial behavior. A s mentioned i n section 4 . 2 . 3 , increasing slightly the detritus m o r t a l i t y / 'other m o r t a l i t y ' (organisms d y i n g because o f disease, starvation, etc., and entered as E E , i.e., as (1 - other mortality)) o f all groups by a c o m m o n factor, resulted i n a slightly better fit between  the  observed and predicted trends. T h i s result w a s not used for the re-calibration o f the m o d e l , but implies that all E E values should be l o w e r e d , i.e., the n o n - p r e d a t i o n losses o f all groups should be higher. T h e interpretation is not straightforward, but perhaps indicates that the organisms experienced at slightly higher non-predation mortality as a result o f the increased radiation.  5.3.4  B i o - d i m i n u t i o n o f beta radioactivity.  O v e r a l l , the result i n F i g u r e 4.3 shows g o o d agreement between the m o d e l predictions and the observed trends, R  2  ranging between 0.57 - 0.98. T h e regression i n F i g u r e 4.6 further suggests  that beta radioactivity is not accumulated i n the f o o d w e b but diminishes w i t h higher trophic levels. A similar result w a s observed i n a study at E n e w e t a k A t o l l o f radiation damages i n fish thyroids, caused by a c c u m u l a t i o n o f  1 3 1  I o d i n e ( G o r b m a n and James 1963). It w a s found that,  aside f r o m the distance f r o m the e x p l o s i o n site, diet w a s the most important factor paralleling  88  the degree o f t h y r o i d damage. F i s h at l o w e r t r o p h i c levels w e r e m o r e severely affected than fish at higher t r o p h i c levels. A possible explanation, i n b o t h cases, is that the majority o f isotopes p r o d u c e d d u r i n g a nuclear detonation have v e r y short h a l f lives (  1 3 1  I o d i n e has a h a l f  life o f approximately eight days; see also section 2.1.4, and 2.2.1) and, c o m b i n e d w i t h the time lag discussed above, this leads to a reduced amount o f radioactivity being transferred up the food  web.  T h i s , however,  does not  rule out  the  possibility that  certain isotopes  are  b i o a c c u m u l a t e d w i t h higher t r o p h i c levels. A s described i n section 2.2.3, selective uptake o f beta emitting radioisotopes by aquatic organisms is k n o w n to occur. A n o t h e r explanation, related to the former, c o u l d be that b i o a c c u m u l a t i o n is related to the w a y that c o n t a m i n a t i o n takes place, i.e., as a pulse release versus a constant release / equilibrated system. T h e latter w o u l d v e r y likely give a different result ( R o w a n and R a s m u s s e n 1994).  5.3.5  Potentials o f the approach.  B e s i d e s simulating the levels o f beta radioactivity i n the m o n i t o r e d groups, the simulation was extrapolated to also m a k e predictions about the levels o f c o n t a m i n a t i o n i n the n o n - m o n i t o r e d groups ( F i g u r e 4.2 and 4.3). T h i s is an important o u t c o m e as, i n most cases o f marine p o l l u t i o n , there is not e n o u g h time and / or m o n e y to m o n i t o r all g r o u p s i n a system, or there is uncertainty as to w h i c h groups to monitor. F o r example, it w a s recently found that flounders, soles and mussels i n B r i t a i n ' s largest estuary contain levels o f radioactive T r i t i u m hundreds o f times higher than expected ( E d w a r d s 1998). T h e expected levels w e r e based o n the assumption that one k i l o fish w o u l d acquire the same c o n c e n t r a t i o n as one liter o f sea water.  Scientist n o w  suspect  that the organisms  accumulated the radioactivity t h r o u g h  c o n s u m p t i o n ( E d w a r d s 1998). In a case like this it w o u l d be v e r y helpful, p r i o r to initiating a comprehensive field study, i f one c o u l d use the data obtained so far to simulate the fate o f T r i t i u m w i t h i n the w h o l e f o o d w e b , m a k i n g predictions about the level o f c o n t a m i n a t i o n i n the n o n - m o n i t o r e d groups. T h e result c o u l d then be used as a guide as to w h i c h organisms might have accumulated critical levels o f contamination and s h o u l d be sampled f o r further testing. For  this to  be  realized, h o w e v e r ,  the  approach  presented  here  o f mapping  available  measurements onto Ecopath-generated f o o d w e b s must first be generalized to any type o f contaminant, and the m i n i m i z a t i o n routine should be i m p r o v e d . R e g a r d i n g the first point,  89  E q u a t i o n (3.4) c o u l d be modified to include, for example, 'affinity factors' i n cases where one is dealing w i t h fat-soluble contaminants. T h e second point refers to the use o f scaling factors and fixed relationships between the elements o f the predation mortality m a t r i x (Figure 4.4). Ideally, to o p t i m i z e the fit between the observed and predicted levels o f contamination, it should  be  possible  independently  to  modify  all the  parameters  of  the  o f each other, to a v o i d the situation presented  predation  mortality  i n F i g u r e 4.4. A  matrix possible  solution, suggested by D r . C . W a l t e r s and D r . D . P a u l y ( p e r s . c o m ) , is t o add a m i n i m i z a t i o n routine to the E c o r a n g e r m o d u l e o f E c o p a t h . A s described i n section 2.3.2, this m o d u l e already includes a M o n t e - C a r l o resampling routine (Christensen and P a u l y 1995) w h i c h c o u l d be used as an ' i m p o r t a n c e - s a m p l i n g ' routine to combine p r i o r distributions f r o m E c o p a t h ( w h i c h are g i v e n by the uncertainties o f the input data), w i t h a l i k e l i h o o d function g i v e n by the fits o f the observed to the predicted pollutants series. T h i s w o u l d a l l o w generating distributions o f k e y parameters,  thus a l l o w i n g their interpretation i n a B a y e s i a n  (Walters 1996).  90  posterior context  References A l i n o , P. M . , L . T . M c M a n u s , J . W . M c M a n u s , C . L . J . N a n o l a , M . D . F o r t e s , G . C J . T r o n o , and G . S. Jacinto. 1993. 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Phytoplankton Zooplankton Corals Foraminiferans Gastropods Giant clams Bivalves Shrimps / lobsters Stomatopods Misc. crustaceans Echinoderms Holothurians Polychaetes Sessile invertebrates Cephalopods  o  -a  o a, o  o  CJ  T3 O ft O  >  o  CD >  g  CD  O  cj  I  o "o  .3 o  -  0.130 0.100 -  0.012 0.070 0.020 - 0.300 0.020 0.400 - 0.020 0.004 - 0.020 0.010 -  0.450  o a, _o 73 X!  CJ  CO  0.740 0.400 0.430 0.450 - 0.750 0.851 0.500 0.777 0.450 0.500 0.700 1.000 0.430 - 0.011 - 0.010 0.450 0.050 0.160 - 1.000 0.250 0.100 0.600 0.010 0.010 -  T3  PH  CJ  o -  -  0.050  0.005 0.001 - 0.010  0.010  0.022 0.035 0.099 0.020 0.007 - 0.010 0.005 - 0.010 0.054 0.375 0.006 0.020 0.018 - 0.088 0.020 0.010  0.420  0.460 0.060  a. Diet composition based on Gerber and Marshall (1982). Cannibalism was reduced to 10% by scaling the predation pressure exerted on the other groups, b. From Heron Island, Australia (Sorokin 1993); c. Diet composition based on Sorokin (1993). 3 0 % o f the diet is assumed to be covered by symbiotic zooxanthellae; d. Diet composition based on K o h n (1987); e. From Arias-Gonzales (1993); f. A weighted mean between a diet composition for spiny lobster from K o h n (1987): gastropods 3 0 % , bivalves 7%, crustaceans 3 2 % , polychaetes 12%, echinoderms 10%, corals 4 % , algae 5 % , and a diet composition for shrimps from Arias-Gonzales (1993): polychaetes 1%, corals 1%, algae 1%, sessile invertebrates 2 % , meiobenthos 5 % , and detritus 9 0 % ; g. h. i. j. k.  Diet composition based on Chartock (1983b); Diet composition based on Bakus (1968, 1973); Diet composition based on Sorokin (1993); Diet composition based on Reiswig (1971); Diet composition based on Helsinga and Fitt (1987). 7 5 % o f the diet is assumed to be contributed by symbiotic zooxanthellae; 1. Dashes indicate that there is no interactions between the two groups.  104  irsguos^jns irsgAoJannB  sjsdnojS / sjaddEus  ijsg snoJOAiuuio neuis  o  o  o  o  o  qsy snojOAtLUG3 3§JBT  UBTJ snojOAruiBD rpuis  d©  SSJOAlDSld 3STJV  ^luauiSag irst J  ei m o n n o  o o  ©  ©  ©  ©  S3]Rjq3U3AUT 3ffSS3S  SajaEipAJOd  suii3pounio3 — spodonsEo  —  o  o o © ©  S3ATBAIR vo s£> d d  pdurmig — — ©  SUB33B18TU3 OSIW  o  ©  © Csl f l © © ©  ©  ©  o o o <ri —; <N  odd  r  g o o © d d d d  ©  o  spodoiBiuois  spodoieqdao  O  —  (^Xuois / yos) sfoioo  uoi^uEidoo^  3B§rv  M  ^  O  vi  d d d d  VO VO T © *T <*"> — —  d d d d vr> o o\ © r—' o o do do  © © vo © d o d o  o  irsiiuoGSjns  iisgXTjjgrms  siadnorS / sjaddEus  fN  ITSTJ snOJOATUUIO [fBUIS  O  d d  •qsg snojoAnireo 3§JBT|  qsy snojoATUJE3 TTEUIS  sgjoApsrd osnA]  o o  o o o  ssiaiqaysAui arissas  1 * 1o o oo  d d  o o o — VO  d d >n <N o o r- vo W « « -T " 1 o o d d d d d d d  spodoiisEO  ^S3ArBAig  o g  ^duruiis  — o d d  d d  VO O  o o  o o o  d d  spodoiBuiojs,  spodoiEudao  o v ro o d d  ^umajnraiiBJOj  O O O  ^Xuow / y o s ) S J B J C O  uoi^uEidocrz  o  o  o vo d d  o vo d d < M O VO  -a  a  <u CL  a  <  ©  O <N  o d d  TlSTJUOaSjTlS  iisijXiiJaiing  usy snojOAnnuo news  iisy snojOAruiE3 32IBI  qsy snojoAjuiBO [TBUIS  S3JOApSld  © o o o o d d ©  ^uaurSaij IJSTJ  S3]Ejq3y3AUT 3[ISS3S  O  pi  — — as  d  d  o d d  o © © ©  ^suuapounpg  spodoxisBO  S3ATBAIQ  o o o ^duruiis © «1 "1 o d d © © — o o o  o o o  spodo"fBuiois  spodoTBLjdao  JAUOIS i y o s ) sraioo  -  O  CN  © © o o o ©  O  O  W  ^uopruBidooz  M M n  M  t- <0 O  O  O  t- O—O —© ©  O  —  o  K3 a <u CL CL  I i  8 -S  Hi  K o o o o o o S  o o © o  •S .2  I i I  CN  o  a 11 3 ..  3 3  3 -S is  CN © rn ©  o d d © © ©  11  i o-  % •  n -a  3 3  1I  11 ll  S.  s. ^  i i i i i ""  ° ^ *o *° 3=1 m u O O c a O o - o c j U f J U D - Q ,  P OD oil o W 60 (  22 ,  PH  'fl  irsiiuoaSjns  HsyXijJswng  sjadnojS / siaddeus  1[SIJ SnOJOATUUIO HEUIS  o — d d  qsy snojOArujBO aftreq  usu snojOApjjBa rreiug  sajOAiosid *OSIJ\  3 9 o o o d  ^JUSIUSEJI USI-J  CM 00 O CM  d d  8 8  sajRiqayaAui anssag  — O  CO O  d d sujjapounpg  spodoijsEfj  saATEAig  00 O  ^duiinrs  ^ P d o d o  (N  SUE33EJSIU0 'OSI|^  spodoiBiuois  spodoreiids^  |UEJ3jnnurcjcr}  8 8 d d  (Auois i yos) srejoQ  uoj^uEidoo2|  o o  o o o  m \o r- o S 5 8 8 8 d o o o d d — do  T3  C  cu  o. D-  o d d  CN o do-^  iisyuoaSjns  ijsy^uj3)]ne|  sjadnarS / siaddEus  usy snoJOAnruio  neuis  trsy snojOAiuiBO a S i B i  qsy snojoAiuiBD TIBIUS  i  sajoApsid osn>v  ^puaurSBij u s i ^  satEjqauaAui snsssg  ON  pduruirs  o  EUB33B1STU3 '3SnAJ  spodotEuiois  spodoisqdao  o o © d  J A U O J S / U O S ) SpjJOQ  uoi^iiEidoo^l  o © ©© © © —o ©© — —  s R R O  ! I-1 » a s S .a '6  H  a •  of X  I 1 1 11  '-5 c  o. o.  '  i  is sit  B  |  i l i a  CU  <!  8  o  cv) _C> O T3 CD  c+4  00  43 • - i  PH  H  C  O  00 OH  3  >  X  A p p e n d i x 2, Table 2. D i e t matrix o f the ten fish groups i n c l u d e d i n the m o d e l . B a s e d o n A p p e n d i x 2 Table 1.  Prey \ Predator  — J H  « X I  CJ  rv  X  X  trt  ^  'f  g  W  «  •§ P  Stony / soft corals Detritus Zooplankton Benthic prim prod. Foraminiferans Misc. crustaceans Stomatopods Shrimps Cephalopods Bivalves Gastropods Echinoderms Sessile invertebrates Polychaetes Small omniv. fish Small camiv. fish Surgeonfish Herring Parrotfish Groupers / snappers Butterflyfish Large camiv. fish Misc. pisciv. fish  tH  X  '5  'I n  O  O  '3 C  J  i  n  g  o  '§ t  g  O  W  o O m co j DH J x 0.027 0.183 0.040 0.078 0.700 0.042 0.007 0.037 0.018 0.830 0.315 0.173 0.042 0.030 0.057 0.454 0.900 0.007 0.300 0.382 0.256 0.090 0.021 0.030 0.050 0.054 0.193 0.135 0.080 0.287 0.060 0.007 0.004 0.016 0.027 0.131 0.046 0.030 0.096 0.125 0.031 0.005 0.022 0.057 0.101 0.012 0.017 0.054 0.100 0.046 0.027 0.021 0.019 0.030 0.008 0.039 0.020 0.040 0.011 0.021 0.064 0.170 0.053 0.051 0.046 0.154 0.047 0.000 0.099 0.027 0.037 0.046 0.000 0.050 0.199 0.046 0.117 0.005 0.521 0.043 0.021 0.010 0.074 0.005 0.060 0.028 0.007 i-l -  c o c 0.027 0.258 0.010 0.023 0.209 0.009 0.165 0.002 0.008 0.071 0.002 0.003 0.058 0.061 0.073  Ill  A p p e n d i x 3. Scientific and c o m m o n names o f the fish species i n c l u d e d i n the m o d e l Scientific name  Common name  0  Miscellaenous piscivorous fish  Carcharhinus melanopterus Carcharhinus amblyrhynchos Triaenodon obesus Nebrius ferrugineus Sphyraena qenie Selar crumenophthalmus (all juveniles) Trachinotus baillonii Carangoides orthogrammus Caranx melampygus Caranx ignobilis Elagatis bipinnulata Synodus variegatus Saurida gracilis Fistularia petimba Gymnosarda unicolor Euthynnus affmis Katsuwonus pelamis Tylosurus crocodilus crocodilus Aulostomus chinensis  Blacktip reef shark Grey reef shark Whitetip reef shark Tawny nurse shark Blackfin barracuda Bigeye scad Smallspotted dart Island trevally Bluefin trevally Giant trevally Rainbow runner Variegated lizardfish Gracile lizardfish Red cornetfish Dogtooth tuna Kawakawa Skipjack tuna Hound needlefish Chinese trumpetfish  Herring  Spratelloides delicatulus  Delicate round herring  Small carnivorous fish  Rhabdamia gracilis Apogon novaeguineae Apogon fuscus Apogon novemfasciatus Apogon kallopterus Apogon nigrofasciatus Apogon erythrinus Cheilodipterus quinquelineatus Pseudocheilinus hexataenia Labroides dimidiatus Novaculichthys taeniourus Stethojulis balteata Stethojulis sp. Halichoeres trimaculatus Halichoeres margaritaceus Macropharyngodon meleagris Thalassoma lucasanum Thalassoma hardwickii Cheilinus oxycephalus Pempheris oualensis Paracirrhites arcatus  Luminous cardinalfish Samoan cardinalfish Sevenstriped cardinalfish Iridescent cardinalfish Blackstripe cardinalfish Fivelined cardinalfish Pyjama Bluestreak cleaner wrasse Rockmover wrasse Belted wrasse wrasse d  Threespot wrasse Pink-belly wrasse Blakspotted wrasse Cortez rainbow wrasse Sixbar wrasse Snooty wrasse Silver sweeper Arc-eye hawkfish  112  3  Appendix 3  (continued).  Scientific name  Common name  Cirrhitus pinnulatus Scorpaenopsis gibbosa Pterois radiata  Stocky hawkfish Humpbacked scorpionfish Radial firefish Y e l l o w pigmy brotula Blueband goby Network pipefish Samoan silverside Crimsontip longfin Whitespotted longfin Stonefish  Dinematichthys iluocoeteoides Valenciennea strigata Corythoichthys jlavofasciatus Hypoatherina temminckii Plesiops melas Plesiops nigricans Synanceia verrucosa Caracanthus unipinnus (unipinna ?) Thysanophrys sp. Parapercis cephalopunctata Myripristis pralinia Myripristis murdjan Myripristis violacea Neoniphon sammara Sargocentron microstoma Holocentrus laeris ? Sargocentron diadema Gymnothorax margaritophorus Oxymonacanthus longirostris Gomphosus varius Halichoeres melanurus Halichoeres marginatus Halichoeres hortulanus Thalassoma quinquevittata Thalassoma lutescens L a r g e carnivorous fish Thalassoma purpureum Epibulus insidiator Cheilinus chlorourus Cheilinus trilobatus Coris aygula Coris gaimard gaimard Hemigymnus melapterus Mulloidichthys flavolineatus Parupeneus trifasciatus Parupeneus barberinus Parupeneus cyclostomus Upeneus arge Balistoides viridescens Pseudobalistes flavimarginatus Melichthys vidua Monotaxis grandoculis  0  Pygmy coral croucher ? flathead" Scarlet soldierfish Pinecone soldierfish Lattice soldierfish Sammara squirrelfish Smallmouth squirrelfish Crown squirrelfish Blotched-neck moray Longnose fielfish B i r d wrasse Tail-spot wrasse Splendid rainbow wrasse Checkerboard wrasse Fivestripe wrasse Sunset wrasse  Surge wrasse Sling-jaw wrasse Floral wrasse Tripletail wrasse C l o w n wrasse Yellowtail coris Blackeye thicklip Yellowtail goatfish Dash-and-dog goatfish Gold-saddle goatfish Band-tail goatfish Titan triggerfish Yellowmargin triggerfish Pinktail triggerfish Humpnose big-eye bream  113  Appendix 3  (continued).  Scientific name  Common name  Hyporhamphus dussumieri Bothus mancus Polydactylies sexfilis Heteropriacanthus cruentatus Pterois volitans Crenimugil crenilabis Echeneis naucrates Leiuranus semicinctus Branchysomophis sauropsis ? Echidna polyzona Siderea picta  Dussumier's halfbeak Tropical flounder Sixfinger threadfin Glasseye Lionfish Fringelip mullet Live sharksucker Saddled snake-eel  Gymnothorax flavimarginatus Gymnothorax buroensis Gymnothorax undulatus Gymnothorax rueppelliae Gymnothorax fimbriatus Conger noordzieki ? Moringua macrochir (microchir ?) Sargocentron spiniferum Arothron meleagris Arothron nigropunctatus Arothron sp. Small omnivorous fish lstiblennius chrysospilos Blenniella periophthalmus Cirripectes variolosus Gnatholepis anjerensis Gobis ornatus ? Bathygobius fuscus fuscus Gobiodon rivulatus Paragobiodon echinocephalus Chromis agilis Chromis caerulea Chromis lepidolepis Chromis margaritifer Chromis atripectoralis Pomacentrus coelestus (coelestis ?) Pomacentrus vaiuli Pomacentrus pavo Stegastes nigricans Stegastes fasciolatus Dascyllus reticulatus Dascyllus aruanus Amblyglyphidodon curacao Abudefduf sordidus  0  Barred moray Peppered moray Yellow-edged moray Vagrant moray Undulated moray Banded moray Fimbriated moray  Sabre squirrelfish Guineafowl puffer Blackspotted puffer puffer d  Redspotted blenny Blue-dashed rockskipper Red-speckled blenny  Dusky frill-goby Rippled coralgoby Redhead goby Agile chromis Green chromis Scaly chromis Bicolor chromis Black-axil chromis (Neon damselfish ?) Ocellate damselfish Sapphire damselfish Dusky farmerfish Pacific gregory Reticulate dascyllus Whitetail dascyllus Staghorn damselfish Blackspot sergeant  114  A p p e n d i x 3 (continued). Scientific name  Common name  Abudefduf septemfasciatus Abudefduf leucopomus (Chrysiptera leucopoma ?) Abudefduf amabilis ? Abudefduf glaucus (Chrysiptera galuca ?) Plectroglyphidodon lacrymatus Abudefduf biocelatus (Chrysiptera leucopoma ?) Centropyge flavissimus Canthigaster solandri Amanses carolae ?  Banded sergeant Surge damselfish ?  0  Grey demoiselle ? Whitespotted devil Surge damselfish ? Lemonpeel angelfish Spotted sharpnose filefish ? d  L a r g e omnivorous fish  Ostracion cubicus Arothron hispidus Siganus argenteus Kyphosus cinerascens Rhinecanthus rectangulus Rhinecanthus aculeatus Balistapus undulatus  Y e l l o w boxfish White-spotted puffer Streamlined spinefoot Blue sea chub Wedge-tail triggerfish White-banded triggerfish Orange-lined triggerfish  Snappers / groupers  Epinephelus merra Epinephelus fuscoguttatus Epinephelus cyanopodus Epinephelus macrospilos Epinephelus howlandi Variola louti Cephalopholis urodeta Cephalopholis miniata Cephalopholis argus Anyperodon leucogrammicus Plectropomus areolatus Pseudanthias pascalus Lutjanus monostigma Lutjanus vitta Lutjanus gibbus Gymnocranius griseus Lethrinus microdon Aprion virescens Gnathodentex aureolineatus Pterocaesio tile  Honeycomb grouper Brown-marbled grouper Speckled blue grouper Snubnose grouper Blacksaddle grouper Yellow-edged lyretail Darkfin hind Coral hind Peacock hind Slender grouper Squaretail coralgrouper Amethyst anthias One-spotted snapper Brownstripe red snapper Humpback snapper Grey large-eye bream Smalltooth emperor Green jobfish Striped large-eye bream Dark-banned fusilier  Butterflyfish  Chaetodon lunula Chaetodon citrinellus Chaetodon ephippium  Raccoon butterflyfish Speckled butterflyfish Saddle butterflyfish  115  Appendix 3  (continued).  Scientific name Chaetodon reticulatus Chaetodon trifascialis Chaetodon auriga b  Surgeonfish Acanthurus mata Acanthurus xanthopterus Acanthurus gahhm Acanthurus olivaceus Acanthurus triostegus Acanthurus achilles Acanthurus nigricans Acanthurus nigroris Acanthurus guttatus Acanthurus lineatus Ctenochaetus striatus Naso lituratus Naso unicornis Zebrasoma veliferum Parrotfish Cetoscarus bicolor Scarus sordidus  Common name  0  Mailed butterflyfish Chevron butterflyfish Threadfin butterflyfish Blue-lined surgeonfish Yellowfin surgeonfish  Orangespot surgeonfish Convict surgeonfish Achilles tang Whitecheek surgeonfish Bluelined surgeonfish Whitespotted surgeonfish Lined surgeonfish Striated surgeonfish Orangespine unicornfish Bluespine unicornfish Sailfin tang Bicolour parrotfish Daisy parrotfish  a. Hiatt and Strasburg (1960) examined the food and feeding habits and ecological relationship o f 223 fish species o f the Marshall Islands. B y comparing this work with that o f Schultz and collaborators (1953, 1960, 1966) and Randall and Randall (1987), 190 o f Hiatt and Strasburgs 223 species were found to occur at Enewetak Atoll. The 190 species were grouped into the ten functional groups: miscellaneous piscivorous fish, snappers / groupers, herring, large carnivorous fish, small carnivorous fish, large omnivorous fish, small omnivorous fish, parrotfish, surgeonfish, and butterflyfish. Dashes indicate that FishBase (1998) does not have a common name for the species; Question marks either indicate that the species name was not found in FishBase, or indicate an inconsistency i n spelling in which case the closest 'match' / synonym i n FishBase (1998) is given in brackets; b. The scientific names were cross-checked with FishBase 98 (1998); c. FishBase (1998) common name; d. Family.  116  A p p e n d i x 4. D e r i v i n g the Q / B values o f the t e n fish groups.  T h e Q / B values f o r the fish species i n c l u d e d i n the m o d e l w e r e estimated u s i n g the e m p i r i c a l regression b y P a u l y et al. (Christensen and P a u l y 1992b, P a u l y et al. 1990): Q / B = 10 where; W mean  6 3 7  • 0.0313^ •  W ^ "  0  1  6  8  • 1.38 • 1.89 pf  Hd  is the asymptotic o r m a x i m u m w e i g h t o f the fish i n g r a m w e t weight; T  r o  annual habitat temperature  expressed  as 1000/(T°C  + 273.1)  k  ( a n annual  is the mean  temperature o f 2 7 . 5 w a s used i n a l l cases, based o n A t k i n s o n (1987)); P f is o n e f o r apex predators, pelagic predators, a n d z o o p l a n k t o n feeders, a n d z e r o f o r a l l other feeding types; and H  d  characterizes the f o o d type and is set t o one f o r herbivores and z e r o f o r carnivores.  Estimates o f W many cases  W  m  m  a  a  x  w e r e obtained f r o m F i s h B a s e (1998) f o r as many species as possible. I n  x  w a s g i v e n directly, but i n some cases it had t o be estimated u s i n g the weight-  length relationship:  W  m  a  x  - a-L  b  ; w h e r e a a n d b are t w o constants a n d L is the t o t a l length  ( T L ) (see T a b l e 1). W  m  a  x  was converted to W  B  assuming that  Woo =  W  m a x  / 0 . 9 5 (see T a b l e 2).  A p p e n d i x 4, T a b l e 1. D e r i v i n g the m a x i m u m weight o f fish species i n the m o d e l . B a s e d o n F i s h B a s e (1998). Species  LnjJ (TL, SL.orFL)  &  t/  300 TL? 100 TL 165 TL 150 TL? 36/32 TIVSL 200 TL? 120 TL  0.003 0.024 0.028 0.014 0.005 0.000 0.009  3.649 2.980 2.940 2.920 3.150 3.160 3.050  Australia Philippines Philippines Philippines New Caledonia New Caledonia New Caledonia  3610185 22253 91267 30515 367 3735 19319  40 TL 40 TL  0.003 0.003  3.300 3.310  New Caledonia New Caledonia  523 502 512  3  Place of origin of a and b  W  J (g) w  M s c . piscivorous fish Carcharhinus melanopterus Caranx melampygus Caranx ignobilis Elagatis bipinnulata Saurida gracilis Fistularia petimba Carcharhinus amblyrhynchos Synodus variegatus "  Average S. variegatus:  117  A p p e n d i x 4, T a b l e 1 (continued). Species Gymnosarda unicolor "  a  Lmax  (TL, SL, or FL) 224/206 Tl/FL 224 TL  a  b  a  Place of origin  0.011 0.041  3.070 2.800  of a and b N. Marianas Vanuatu  0.002  3.290  New Caledonia  1  Average G. unicolor: Herring Spratelloides delicatulus  7 TL?  a Wmax  (g) 172366 155746 164056  Small carnivorous fish Apogon fuscus Apogon kallopterus Cheilodipterus quinquelineatus Labroides dimidiatus Halichoeres trimaculatus Myripristis pralinia Myripristis violacea Neoniphon sammara Sargocentron microstoma Sargocentron diadema Thalassoma lutescens  10/7.7 TL/SL 15/12.2 TL/SL 12 TL 11.5 TL 26/22 TL/SL 21/17 TL/SL 20 TL? 30 19/16 TL/SL 23 TL? 22/19 TL/SL  0.012 0.009 0.014 0.004 0.048 0.021 0.051 0.049 0.002 0.037 0.010  2.600 3.180 3.040 3.180 2.740 3.070 2.900 2.820 3.850 2.890 3.080  New Caledonia New Caledonia New Caledonia New Caledonia New Caledonia New Caledonia New Caledonia New Caledonia Micronesia New Caledonia New Caledonia  5 48 26 10 362 235 305 710 151 321 140  Small omnivorous fish Chromis caerulea Pomacentrus vaiuli Pomacentrus pavo Stegastes nigricans Dascyllus aruanus Amblyglyphidodon curacao  8/6.5 TL/SL 11/10 TL/FL 11/8.5 TL/SL 14/11.5 TL/SL 8/6.5 TL/SL 12/9 TL/SL  0.030 0.037 0.068. 0.081 0.014 0.054  2.410 2.890 2.750 2.350 2.690 2.890  New Caledonia New Caledonia New Caledonia New Caledonia New Caledonia New Caledonia  4 38 49 40 4 71  35/30 TL/SL 120 TL? 122 TL 51 TL 40 TL 55 TL 40 TL 50 TL 96/80 TL/SL 30 TL  0.026 0.016 0.012 0.015 0.066 0.016 0.010 0.021 0.005 0.009  2.890 3.000 3.050 3.000 2.760 3.020 3.090 3.000 3.260 3.290  New Caledonia Philippines New Caledonia New Caledonia New Caledonia New Caledonia Australia New Caledonia N. Marianas Micronisia  745 27648 28630 1963 1730 2794 892 2625 15073 652  81 TL 81 TL  0.018 0.013  2.970 3.040  N. Marianas New Caledonia  8524 8490 8507  12.5 TL 23 TL  0.034 0.023  2.950 3.040  New Caledonia New Caledonia  59 317  50 TL 70 TL 35 TL 21 TL  0.040 0.009 0.007 0.067  2.950 2.770 3.400 2.670  New Caledonia New Caledonia Micronesia Micronesia  4071 1110 1244 227  Groupers / snappers Epinephelus merra Epinephelus fuscoguttatus Epinephelus cyanopodus Epinephelus macrospilos Cephalopholis miniata Cephalopholis argus Lutjanus vitta Lutjanus gibbus Aprion virescens Gnathodentex aureolineatus Variola louti II  Average V. louti: Butterflyfish Chaetodon citrinellus Chaetodon auriga Surgeonfish Acanthurus mata Acanthurus xanthopterus Acanthurus olivaceus Acanthurus nigricans  118  A p p e n d i x 4, T a b l e 1 {continued). Species Acanthurus lineatus Naso lituratus Zebrasoma veliferum Acanthurus lineatus Naso lituratus Zebrasoma veliferum Acanthurus triostegus  Lmax (TL, SL,orFL) 38 TL 45 TL 40 TL 38 TL 45 TL 40 TL 27 TL 27 TL  a a  b  a  Place of origin  0.019 0.050 0.047 0.019 0.050 0.047 0.016 0.052  3.070 2.840 2.860 3.070 2.840 2.860 3.140 2.390  26 TL 26 TL  0.021 0.028  3.040 3.000  Micronesia New Caledonia  420 489 455  70 TL 70 TL  0.023 0.022  2.920 2.990  Micronesia New Caledonia  5567 7298 6432  43/36 TL/SL 62/50 TIVSL 35 TL 34 TL 110 TL? 45 TL  0.009 0.012 0.006 0.019 0.005 0.017  3.150 3.080 3.550 3.000 3.300 3.060  New Caledonia New Caledonia Micronesia USA New Caledonia New Caledonia  1258 4078 1757 739 25627 1947  60 TL 60 TL  0.036 0.026  2.850 2.990  Micronesia New Caledonia  4208 5370 4789  40 TL  0.013  3.140  Micronesia  1362  45 TL 54/45 TL/SL 25 TL 25 TL  0.026 0.009 0.036 0.018  2.590 2.800 2.880 3.100  New Caledonia New Caledonia Micronesia Micronesia  501 638 377 386  40 TL 40 TL  0.025 0.011  2.880 3.100  Micrenesia New Caledonia  1028 981 1004  Average A. triostegus: Ctenochaetus striatus "  Average C. striatus: Naso unicornis Average N. unicornis'. Large carnivorous fish Cheilinus chlorourus Parupeneus barberinus Melichthys vidua Heteropriacanthus cruentatus Echeneis naucrates Sargocentron spiniferum Monotaxis grandoculis II  Average M. grandoculis: Parrotfish Scarus sordidus Large omnivorous fish Ostracion cubicus Arothron hispidus Rhinecanthus rectangulus Rhinecanthus aculeatus Siganus argenteus it Average S. argenteus:  Wmax (g) 1359 2463 1799 1359 2463 1799 512 137 325  of a and b Micronesia Micronesia New Caledonia Micronesia Micronesia New Caledonia Micronesia New Caledonia  a. W is the maximum reported weight o f the fish. The values were obtained either directly from FishBase (1998) or estimated using the weight-length relationship: W = a - L where; L is the maximum length reported; and a and b are two constants (all values from FishBase (1998)); b. The maximum reported length o f the fish. A l l values are from FishBase (1998). T L = total length, S L = standard length, F L = fork length; W is estimated using T L , and S L s and F L s were therefore converted to T L by measuring, on a picture o f the species, the ratio between the two lengths. Question marks indicate that the length is not specified i n FishBase (1998), in which case it is assumed to be the total length ( T L ) . m a x  b  m a x  119  A p p e n d i x 4, T a b l e 2. Q / B values o f the fish g r o u p s included i n the m o d e l . a Species HdC Pf w00b W ax  d  Q/B  6  m  (g)  Msc. piscivorous fish  3610185 22253 91267 30515 512 367 3735 164056 18250 6800 900 4300 13600 34500  Carcharhinus melanopterus Caranx melampygus Caranx ignobilis Elagatis bipinnulata Synodus variegatus Saurida gracilis Fistularia petimba Gymnosarda unicolor Triaenodon obesus Sphyraena qenie Trachinotus baillonii Carangoides orthogrammus Euthynnus affinis Katsuwonus pelamis  3800194 23424 96070 32122 539 387 3932 172691 19211 7158 947 4526 14316 36316  0 0 0 0 0 0 0 0 0 0 0 0 0 0  1 1 1 1 0 0 1 1 1 1 1 1 1 1  2.51 5.90 4.66 5.60 8.06 8.52 7.96 4.22 6.10 7.20 10.12 7.78 6.41 5.48  6.47  Average Herring Spratelloides delicatulus  1  1  0  1  30.48  5 48 26 10 362 235 305 710 151 321  5 50 27 11 381 247 321 747 159 338  0 0 0 0 0 0 0 0 0 0 0 -  1 0 0 1 0 1 1 0 0 0 0 -  24.25 12.00 13.30 21.49 8.54 12.68 12.13 7.63 9.90 8.71 17.28 16.90 16.90 10.01 15.73 14.16 10.97  Small carnivorous fish Apogon juscus Apogon kallopterus Cheilodipterus quinquelineatus Labroides dimidiatus Halichoeres trimaculatus Myripristis pralinia Myripristis violacea Neoniphon sammara Sargocentron microstoma Sargocentron diadema Thalassoma hardwickii Pempheris oualensis Paracirrhites arcatus Thalassoma lutescens Gomphosus varius Halichoeres marginatus Halichoeres hortulanus  140  148 -  f g  h f f f  13.68  Average Small omnivorous fish Chromis caerulea Pomacentrus vaiuli Pomacentrus pavo Stegastes nigricans Dascyllus aruanus Amblyglyphidodon curacao Gnatholepis anjerensis  4 38 49 40 4 71 -  5 40 52 42 4 74 -  120  0 1 1 1 0 0 -  1 0 0 0 1 1 -  24.65 23.56 22.56 23.39 25.51 15.51 39.10 i  A p p e n d i x 4, T a b l e 2 (continued). a  Species  W  Bathygobius fiiscus fuscus Centropyge flavissimus Canthigaster solandri  w  b  Hd  C  Pf  d  Q/B  e  m a x  (g)  -  -  -  -  Average  9.50 j 38.08 f 15.00 k  23.69  Groupers / snappers 745 27648 28630 1963 8507 1730 2794 892 2625 15073 652  Epinephelus merra Epinephelus fuscoguttatus Epinephelus cyanopodus Epinephelus macrospilos Variola louti Cephalopholis miniata Cephalopholis argus Lutjanus vitta Lutjanus gibbus Aprion virescens Gnathodentex aureolineatus  784 29103 30137 2067 8955 1821 2941 939 2763 15867 686  0 0 0 0 0 0 0 0 0 0 0  0 0 0 0 0 0 0 0 0 0 0  7.57 4.12 4.10 6.43 5.03 6.57 6.06 7.34 6.12 4.57 7.74  5.97  Average Butterflyfish Chaetodon Chaetodon Chaetodon Chaetodon Chaetodon  citrinellus lunula auriga ephippium reticulatus  59 -  62 -  317 -  334 -  0 0 -  0 0 -  11.59 12.23 f 8.73 23.32 f 14.25 f  14.02  Average Surgeonfish Acanthurus mata Acanthurus xanthopterus Acanthurus olivaceus Acanthurus triostegus Acanthurus nigricans Acanthurus lineatus Ctenochaetus striatus Naso lituratus Naso unicornis Zebrasoma veliferum  4071 1110 1244 325 227 1359 455 2463 6432 1799  4285 1169 1310 342 239 1431 478 2593 6771 1893  1 1 1 1 1 1 1 1 1 1  0 0 0 0 0 0 0 0 0 0  10.75 13.37 13.12 16.44 17.46 12.93 15.54 11.70 9.96 12.33  13.36  Average Large carnivorous fish Cheilinus chlorourus Parupeneus barberinus Melichthys vidua Monotaxis grandoculis Heteropriacanthus cruentatus Echeneis naucrates  1258 4078 1757 4789 739 25627  121  1324 4293 1850 5041 778 26976  0 0 0 0 0 0  0 0 0 0 0 0  6.93 5.69 6.55 5.54 7.58 4.18  A p p e n d i x 4, T a b l e 2 (continued). a  Species  W  (g)  Sargocentron spiniferum Epibulus insidiator Cheilinus trilobatus Bothus mancus Echidna polyzona Gymnothorax jlavimarginatus Gymnothorax buroensis Gymnothorax undulatus Gymnothorax rueppelliae Gymnothorax fimbriatus  wj  5  Hd  C  Pf  d  Q/B  6  m a x  1947  2049  -  -  -  -  -  -  -  0 -  -  0 -  -  -  -  -  -  -  -  -  6.44 12.53 9.10 4.90 5.40 4.50 4.50 4.50 4.50 4.50  f f 1  m n  n n n n  6.08  Average Parrotfish Scants sordidus  1362  1547  1  0  12.76  501 638 1004 377 386  528 672 1057 397 406  0 0 1 0 0  0 0 0 0 0  8.09 7.77 13.60 8.48 8.45  Large omnivorous fish Ostracion cubicus Arothron hispidus Siganus argenteus Rhinecanthus rectangulus Rhinecanthus aculeatus  9.28  Average  a. W is the maximum reported weight of the fish. The values were obtained either directly from FishBase (1998), or from Appendix 4, Table 1; m a x  b. Estimated assuming that W» = W / 0 . 9 5 ; c. Characterizes the food type: Value o f one for herbivores (in this study when 3 0 % or more of the diet comes from primary producers) and zero for carnivores; d. Value o f one for apex predators, pelagic predators, and zooplankton feeders, and zero for all other feeding types; e. Unless otherwise noted, Q/B was estimated using the empirical regression derived from Pauly et al. (1990): Q/B = 1 0 - 0 . 0 3 1 3 - W " - 1 . 3 8 - 1 . 8 9 where; W„c is the asymptotic or maximum weight o f the fish in gram wet weight; T is the mean annual habitat temperature expressed as 1000/(T°C + 273.1) (an annual mean temperature of 27.5 was used in all cases based on Atkinson (1987)); P is one for apex predators, pelagic predators, and zooplankton feeders, and zero for all other feeding types; and H characterizes the food type and is set to one for herbivores and zero for carnivores. max  637  Tk  co  0168  pf  Hd  k  f  d  f. g. h. i. j. k. 1. m. n.  Obtained from Arias-Gonzales (1993) for same species; From Opitz (1996), Pempheris poeyi (a small carnivorous reef fish); From Opitz (1996), Amblycirrhitus pinos (a small carnivorous reef fish); From Opitz (1996), Gnatholepis thompsoni (a small omnivorous reef fish); From Opitz (1996), Bathygobius soporator (a small carnivorous reef fish); From Opitz (1996), Canthigaster rostrata (a small omnivorous reef fish); From Opitz (1996), Bothus lunatus (intermediate carnivorous reef fish); From Opitz (1996), Echidna catenata (intermediate carnivorous reef fish); From Opitz (1996). Average value for three Gymnothorax species (G funebris, miliaris). 122  G. vicinus, G.  A p p e n d i x 5. F i s h biomass estimates i n O d u m and O d u m (1955). A p p e n d i x 5, T a b l e 1. D r y w e i g h t estimates o f fish f o r each o f the zones i n c l u d e d i n O d u m and O d u m (1955).  Zone Algal ridge  Fish category Parrotfish  Biomass (g dwm" )  Quantity measured and basis for calculation  2  Visual count: 0.4 fish-28 m" ; 9.3 g loss on ignition-individual"  0.10  Visual count: 0.4 fish-28 m" ; 9.3 g loss on ignition-individual"  0.10  2  a  1  Reef flat  Parrotfish  2  1  Small heads  Small herbivores  Visual count: 25 fish-36 m" ; 2.42 g dwfish" and 61% herbivores based on rotenone sampling  1.00  Large herbivores  Visual count: 52 fish-692 m" of horizontal visibility in all directions. 120 g dwfish" ; 90% herbivorous; large fishes absent from area 1/3 of time during maximum currents  5.00  Small carnivores  39% of fish counted (see herbivorous fish above)  0.65  Large carnivores  10% of fish counted (see herbivorous fish above)  0.70  1 stone fish-36m" (100 g dw)  2.80  2  1  2  1  2  Large heads  4.80  Small herbivores  Visual count: 71 fish-36 m" ; 2.42 g dwfish"  Large herbivores  Visual count: 30 fish-600 m" horizontally visible area; estimated V* herbivorous; 120 g dwfish"  4.50  Small carnivores  5.3fish-36m" ; 2.42 g dwfish"  0.34  Large carnivores  'A of fishes counted in visible horizontal area (see herbivorous above)  1.50  Small herbivores  Visual count: 23 fish-36 m" ; 2.42 g dwfish"  1.50  sardine/herring  Count of schools: 1.2-600 m" horizontal visible area; About 100 fish-school" ; 1 g dwfish"  0.20  Visual count: 16 fish-600 m" horizontal visible area; 240 g dwfish"  6.40  Large fish not including sharks  Visual count: 3.2 fish-600 m" horizontal visible area; 240 g dwfish"  1.30  Sharks  Counts per 20 min observation: 1.6 sharks-600 m" visible area; 90 degrees visibility at one time; each individual in sight about 30 sec; Weight per shark about 4540 g dw (20% of wet) (Vinogradov 1953).  2  1  2  1  Sand / shingle  2  1  2  1  2  1  Large herbivores  1  2  1  2  1  2  1.20  a. The dry weights (dw) were converted to wet weights (ww) assuming that, except for sharks, dw = 26% w w (Odum and Odum 1955, Sambilay 1993). For sharks, dw = 20% w w (Vinogradov 1953).  123  A p p e n d i x 5, T a b l e 2. W e i g h t e d mean fish biomass estimate across the w i n d w a r d reef as derived f r o m O d u m and O d u m (1955) (see also A p p e n d i x 5, T a b l e 1). Reef area \ fish group  Herbivores (g dwm" )  Carnivores (g dwm" )  Total (g dwm" )  Total (g ww-m" )  3.88 4.68  1.50 1.74  5.37 6.42  20.66 24.69  2  Not including sand / shingle zone Including sand / shingle zone  2  a. Assuming that dw = 2 6 % w w (Sambilay 1993).  124  2  3  2  A p p e n d i x 6. L i s t o f the ecosystem maturity attributes defined b y O d u m (1969) that are quantified i n E c o p a t h (Christensen 1992, 1995). Odums ecosystem attribute  Corresponding Ecopath output  Developmental stage  Mature stage  1. Gross production / community respiration (P/R ratio)  Deviation of Pp/R (Teta)  Greater or less than 1  Approaches 1  2. Gross production / standing crop biomass (P/B ratio)  Production / biomass (Pp/B)  High  Low  3. Biomass supported / unit energy flow (B/E ratio)  Biomass supported (B/T)  Low  High  5. Food chains  Connectance (C)  3  System omnivory index (SOI) Dominance of detritus (Dom.Det.)  Linear, predom. grazing  Web-like, predom. detritus  II  M  It  II  8. Species diversity - variety component  Flow diversity (H)  Low  High  9. Species diversity - equitability component  Flow diversity (H)  Low  High  13. Size of organism  Average organism size (B/P)  Small  Large  15. Mineral cycles  Finn's cycling index (FCI)  Open  Closed  16. Nutrient exchange rate, betw. organisms and environment  Path length (PL)  Rapid  Slow  18. Growth form  Residence time (B/(R+EXP))  Rapid growth ("rselection")  Feedback control ("K-selection")  21. Nutrient conservation  Nutrient conservation (Oex)  Poor  Good  23. Entropy  Schrddinger ratio (R/B)  High  Low  24. Information  Information content of flows (I)  Low  High  a. The numbers in the left column correspond to the numbers in Table 1 in Odum (1969).  125  

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