Chemical  Defense  in  Tropical  Marine  Algae
James  N.  Norris
and  William  Fenical
herbivores  (Fraenkel,  1959;  Whittaker  and  Fee-
ABSTRACT ney,  1971).  Since  Janzen  (1973)  put  forth  the
Chemical  and  taxonomic  studies  of  the  benthic working  hypothesis  that  the  primary  role  of  sec-
algae  of  Carrie  Bow  Cay,  Belize,  have  revealed ondary  compounds  in  higher  plant  vegetation
that  species  of  certain  families  of  the  Rhodophyta, and  seeds  is  defense  against  herbivores  and  micro-
Phaeophyta,  and  Chlorophyta  produce  unique  or
unusual  secondary  compounds.  Analysis  of  the organisms,  it  has  been  generally  recognized  that
structural  organic  chemistries  of  these  natural these  natural  products  may  either  serve  as  feeding
products  shows  that  the  substances  produced  con- deterrents  or  attractants  in  terrestrial  plant-ani-
sist  largely  of  halogenated  and  non-halogenated mal  interactions  (see,  for  example,  Harbourne,
terpenoids  including  monoterpenoids  (Cio  com- 1977),  or  function  as  allelopathic  chemicals
pounds),  sesquiterpenoids  (Cis  compounds),  and (Muller,  1970)  or  antibiotics.  The  same  evolution-
diterpenoids  (C2  compounds),  and  larger  com-
pounds  of  mixed  acetate-mevalonate  origin. ary  pressures  responsible  for  the  many  biologi-
These  secondary  compounds,  hypothesized  to  be cally  active  compounds  found  in  terrestrial  vege-
feeding  deterrents  developed  as  defenses  against tation  have  been  predicted  to  have  parallels  in
herbivores,  were  examined  for  antibiotic  activity marine  vegetation  (Whittaker  and  Feeney,  1971;
and  toxicity.  Fish  toxicity  experiments  using  Eu- Kittredge,  1976).  Predaceous  fishes  and  inverte-
pomacentrus  leucostictus  and  these  compounds  re-
vealed  sublethal  to  lethal  effects.  One  compound, brate  animals  have  been  important  forces  acting
elatol,  from  Laurencia  obtusa  was  found  to  inhibit as  agents  of  natural  selection  in  the  evolution  of
sea  urchin  egg  development  totally.  Field  obser- protective  mechanisms  (Bakus,  1964;  1966;  1969).
vations  indicate  that  marine  algae  having  these The  world-wide  distribution  of  herbivorous
secondary  metabolites  are  not  eaten  by  many marine  fishes  shows  a  concentration,  both  in  spe-
herbivores,  and  biological  activity  testing  suggests cies  diversity  and  biomass,  on  tropical  reefs  (Hiatt
that  certain  of  these  compounds  may  be  respon-
sible.  In  some  cases,  specialized  grazers  have  ap- and  Strasburg,  1960).  Herbivorous  fishes  gener-
parently  co-evolved  to  tolerate  these  potential ally  dominate  fish  communities  on  tropical  reefs
chemical  “deterrents,”  and  may  in  turn  use  them (Bardach,  1959;  Hiatt  and  Strasburg,  1960);  and
in  their  own  defense  against  predation. the  number  and  biomass  of  both  vertebrate  and
invertebrate  herbivores  are  two  of  the  striking
Introduction features  of  Caribbean  coral  reefs  (Ogden,  1976).
Marine  algae  have  developed  several  defenses
Land  plants  have  evolved  elaborate  morpho- in  response  to  herbivory  (see  for  example,  Paine
logical  and  chemical  defense  mechanisms  against and  Vadas,  1969;  Vadas,  1977;  1979).  Algal Spc-
cies  may  deter  herbivores  in  one  or  more  ae  ae
Jame sN N. orris D, epartmen ot Bf otany N, ationa Ml useum o Nf atural following  ways:  (1)  by  having  a  resistant  or  un-
Flistory S, mithsonian Institution W, ashington D, .C .20560 ;and
William Fenica lI,nstitut eo Mf arin eResources S,cripp sInstitution palatable  physical  structure  (for  example,  the
o fOceanography ,La Jolla ,Calif 92093. calcareous  nature  of  some  Rhodophyta,  Chloro-
417
418  SMITHSONIAN  CONTRIBUTIONS  TO  THE  MARINE  SCIENCES
phyta,  and  Phaeophyta,  or  the  tough  texture  of ics  in  marine  algal-algal  and  algal-animal  inter-
certain  Phaeophyta),  or  a  morphology  that  makes actions.  Unfortunately,  there  have  been  few
it  difficult  for  the  herbivore  to  attach  to  feed  (see quantitative  studies  on  the  diets  of  marine  her-
Hay,  1981);  (2)  by  residing  in  habitats  that  are bivores,  and  our  knowledge  of  feeding  behavior
cryptic  or  unfavorable  for  herbivore  feeding  (Og- and  food  preferences  of  tropical  herbivores  is  still
den  et  al.,  1973;  Adey  and  Vassar,  1975),  such  as too  inadequate  to  be  conclusive.  What  is  known
in  crevices  where  they  are  inaccessible,  in  areas  of on  tropical  fish  diets  can  be  found  in  Randall
high  surf  or  strong  surge  where  herbivores  cannot (1967),  while  sea  urchin  diets  have.  been  summa-
attach  themselves  for  feeding,  or  in  areas  where rized  by  Lawrence  (1975).
herbivores  are  subject  to  increased  predation;  (3) In  this  paper  we  provide  an  overview  of  inter-
by  having  heteromorphic  life  histories,  with  a  fast actions  between  tropical  reef  algae  and  herbivores
growing  stage  and  a  resistant  stage  (Lubchenco in  the  Caribbean,  with  reference  to  our  identifi-
and  Cubit,  1980);  (4)  by  living  in  association  with cation  of  specific  compounds  from  Belize  reef
toxic  or  unpalatable  algae  (see  plant  defense algae.  On  the  basis  of  the  antimicrobial  activity
guilds  of  Atsatt  and  O’Dowd,  1976);  (5)  by  being and  fish  toxicity  of  these  compounds  we  present
unpredictable  in  occurrence  in  time  or  space  (for hypotheses  of  their  ecological  role  in  reef  algal-
example,  ephemeral  species,  or  species  having animal  interactions.
rare  or  patchy  distribution)  (Littler  and  Littler, Over  the  past  four  years  at  Carrie  Bow  Cay,
1980);  and/or  (6)  by  producing  secondary  metab- off  the  coast  of  Belize,  we  have  investigated  the
olites  (Fenical,  1975),  ranging  from  unpalatable systematics  of  the  benthic  algae  as  well  as  the
to  toxic,  as  chemical  defense  against  herbivores. chemical  nature  of  their  secondary  compounds.
Since  the  pioneering  work  of  Pratt  et  al.  (1951) Some  of  the  Chlorophyta,  Phaeophyta,  and  Rho-
reporting  antibacterial  activity  of  various  sea- dophyta  synthesized  unusual  secondary  products
weed  extracts,  several  investigators  have  demon- which  in  the  laboratory  showed  biological  activity
strated  the  antibiotic  activity  of  extracts  from against  selected  micro-organisms  and  a  reef  fish.
some  tropical  algae  (for  example,  Burkholder  et Many  of  the  relatively  abundant  algae  that  were
al.,  1960;  Olesen  et  al.,  1964;  Sieburth,  1964; accessible  to  potential  herbivores  were  found  to
Burkholder,  1973;  Bhakuni  and  Silva,  1974;  Nu- contain  these  biologically  active  substances.  We
nez  and  Serpa  Sanabria,  1975).  Studies  of  Boyd hypothesize  that  these  compounds  have  been  se-
et  al.  (1966)  on  the  effects  of  selected  tropical lected  for  by  the  intense  grazing  pressure  on
algae  on  human  erythrocytes  found  that  the  ex- tropical  marine  algae  and  that  they  function  to
tracts  from  six  brown  algae  agglutinated  blood minimize  population  losses  by  inhibiting  or  re-
groups  O  and  A.  More  recently,  Targett  and pelling  herbivores.  Our  present  analysis  indicates
Mitsui  (1979)  studied  the  effects  of  aqueous  ex- that  tropical  reef  algae  are  chemically  defended
tracts  from  tropical  algae  on  fish  erythrocyte from  many  generalist  herbivores,  while  some  spe-
hemolysis  and  fish  mortality,  and  Targett  (1979) cialist  herbivores  have  evolved  a  physiological
developed  a  behavioral  bioassay  (gastropod  ten- tolerance  to  these  natural  products.
tacle  withdrawal)  to  test  extracts  from  marine ACKNOWLEDGMENTS.—  We  thank  our  colleagues
algae  for  biological  activity.  In  another  study, who  have  discussed  aspects  of  this  research  with
both  seasonal  variability  and  locality  differences us.  Particularly  helpful  were  the  reviews  of  I.
of  the  tropical  algal  extract’s  antibiotic  activity Abbott,  W.  Adey,  S.  Brawley,  K.  Bucher,  D.
against  selected  pathogenic  bacteria  was  observed Cheney,  J.  Cubit,  M.  Hay,  R.  Houbrick,  M.
(Almodovar,  1964).  Hornsey  and  Hide  (1974) Littler,  and  R.  Vadas,  and  the  editoral  comments
found  similar  seasonal  variation  in  their  screening of  V.  Macintyre.  We  especially  thank  R.  Jacobs
experiments  for  antimicrobial  activity  of  British (University  of  California,  Santa  Barbara)  for  pro-
marine  algae.  Sieburth  (1968)  offered  some  eco- viding  the  data  from  his  experiment  for  Figure
logical  interpretation  of  the  role  of  algal  antibiot- 182.
NUMBER 12 419
Materials  and  Methods Fenical,  1979),  and  the  crude  extract.  In  each
treatment  (three  replicates),  either  the  extract  or
Field  trips  were  made  to  Carrie  Bow  Cay  on the  pure  compound  was  added  directly  to  the
the  barrier  reef  of  Belize  (16°48’N;  88°05’W), seawater  with  the  aid  of  an  ethanol  dispersant;
during  the  spring  (March-May)  of  1976,  1977, controls  were  untreated  seawater  and  seawater
and  1978  (for  a  review  of  the  biological  and containing  only  the  ethanol.  Fish  mortality
geological  features  of  Carrie  Bow  Cay,  see  Rutzler within  one  hour  was  considered  to  indicate  a
and  Macintyre,  herein:  9).  During  each  expedi- toxic  compound,  and  sublethal  effects,  such  as
tion,  benthic  macro-algae  were  collected  for  sub- loss  of  equilibrium  and  respiratory  stress  were
sequent  studies  on  their  systematics  and  chemis- noted  as  “strong”  or  “mild.”  Results  of  the  anti-
try.  Homogeneous  collections  were  identified  and microbial  and  ichthyotoxic  experiments  are  sum-
separated  into  specimens  for  chemical  analysis marized  in  Table  32.
and  vouchers  for  taxonomic  verfication;  the  for-
mer  were  preserved  in  isopropanol,  the  latter  in Results  and  Discussion
4%  Formalin-seawater.
Voucher  specimens  have  been  deposited  in  the CHLoropHyta.—Of  the  benthic  algae  in  the
U.S.  National  Herbarium,  Smithsonian  Institu- vicinity  of  Carrie  Bow  Cay  (Norris  and  Bucher,
tion.  The  following  algal  species  were  chemically herein:  167),  the  green  algae  are  perhaps  the  most
investigated  in  this  study.  Chlorophyta:  Caulerpa abundant  in  biomass,  having  representatives
cupressoides  (Vahl)  C.  Agardh,  C.  mexicana  (Sonder) throughout  the  diverse  intertidal  and  subtidal
Kutzing,  C.  racemosa  (Forsskal)  J.  Agardh,  C.  ser- habitats.  Three  families  predominate,  the  Codi-
rulata  (Forsskal)  J.  Agardh  emend  Bgrgesen,  C. aceae  with  species  of  Avrainvillea  and  Codium,
sertularioides  (Gmelin)  Howe,  C.  verticillata  J. Udoteaceae  with  Halimeda,  Penicillus,  Rhipoce-
Agardh,  Rhipocephalus  phoenix  (Ellis  and  Solander) phalus,  and  Udotea,  and  the  Caulerpaceae  with
Kutzing,  and  Udotea  flabellum  (Ellis  and  Solander) species  of  its  monotypic  genus,  Caulerpa.
Howe.  Phaeophyta:  Dictyota  bartayrest:1  Lamour- The  species  we  investigated  from  these  families
oux,  Stypopodium  zonale  (Lamouroux)  Papenfuss, produced  unusual  secondary  metabolites.  Of  six
Sargassum  polyceratim  var.  ovatum  (Collins)  Taylor, species  of  Caulerpa  from  Carrie  Bow  Cay,  C.  cu-
and  Turbinaria  turbinata  (Linnaeus)  Kuntze.  Rho- pressoides,  C.  mexicana,  C.  racemosa,  C.  serrulata,  C.
dophyta:  Liagora  farinosa  Lamouroux,  Asparagopsis sertularioides,  and  C.  verticillata,  all  but  C.  mexicana
taxiformis  (Delile)  Trevisan;  Ochtodes  secundiramea contained  the  known  compound  caulerpin  (Fig-
(Montagne)  Howe,  Laurencia  caraibica  Silva,  and ure  18la,  compound  I).  This  substance  was  orig-
L.  obtusa  (Hudson)  Lamouroux. inally  isolated  from  C.  racemosa,  C.  serrulata,  and
The  biological  activity  of  the  secondary  com- C.  sertularioides  by  Aguilar-Santos  and  Doty
pounds  produced  by  the  marine  algae  was  inves- (1968).  In  recent  studies  of  C.  taxifolia  (Vahl)  C.
tigated  by  nutrient  agar  plate  disc  assay  methods Agardh,  Maiti  and  Thomson  (1977)  re-examined
in  the  laboratory  of  W.  Fenical,  and  by  fish the  structure  of  caulerpin  (Aguilar-Santos,  1970)
toxicity  experiments.  Antibacterial  activity  was and  found  it  to  be  a  derivatized  indole  dimer.
examined  on  the  basis  of  inhibition  of  Staphylococ- We  found  that  species  of  Caulerpa,  Halimeda,
cus  aureus  Rosenbach,  Bacillus  subtilis  (Ehrenberg) Penicillus,  Rhipocephalus,  and  Udotea  also  produce
Cohn,  and  Escherichia  coli  (Migula)  Castellani  and terpenoids  of  rather  complex  structure.  Although
Chalmers,  and  antifungal  activity  was  assessed it  is  difficult  to  analyze  many  of  these  compounds
against  the  human  pathogen  Candida  albicans  (Ro- thoroughly  because  of  their  instability,  we  have
bin)  Berkhout.  Toxicity  to  fish  was  tested  using isolated  from  Rhipocephalus  phoenix  two  sesquiter-
Eupomacentrus  leucostictus  (Muller  and  Troschel) penoids,  rhipocephenal  and  rhipocephalin,  des-
with  serial  dilutions  of  the  alga’s  natural  com- ignated  as  compounds  II  and  III  respectively
pounds  in  seawater  (as  outlined  by  Sun  and (Figure  1815).  These  compounds  typify  the  struc-
420  SMITHSONIAN  CONTRIBUTIONS  TO  THE  MARINE  SCIENCES
TasLe 32.—Compounds identified from tropical benthic algae of Carrie Bow Cay, and results
of biological activity tests (compound designations identified in Figures 181, 182; 0 = no
response, + = positive response, NT = not tested)
Shresies  Antimicrobial  Toxicity
Compound  activity  to  fish
CHLOROPHYTA
Caulerpa  cupressoides  I  0  NT
C.  racemosa  I  0  +!
C.  serrulata  I  0  ING
C.  sertularioides  I  0  NT
C.  verticillata  I  0  NT
Rhipocephalus  phoenix  II  =F  +?
R.  phoenix  Iil  ste  ate
PHAEOPHYTA
Sargassum  polyceratinum  var.  ovatum  IV  +°  NT
Turbinaria  turbinata  IV  SF  Nt
Dictyota  bartayresi  Vv  ts  0
Stypopodium  zonale  VI  aF  +
RHODOPHYTA
Asparagopsis  taxiformis  vil  a  NT
Ochtodes  secundiramea  Vill  at  NT
O.  secundiramea  IX  <r  INE
Liagora  farinosa  xX  oF  =
Laurencia  caraibica  XI  +4  ING
L.  obtusa  XII  aF  NT
‘Lewin, 1970 * Sun and Fenical, 1979 °*Glombitza, 1977 * Izac, 1979
tural  types  we  have  detected  in  the  Caulerpaceae the  urchin  Echinometra  lucunter  (Linnaeus)  near  St.
and  in  some  species  of  the  Codiaceae  and  Udo- Croix,  Virgin  Islands,  does  not  eat  Caulerpa  and
taceae.  Compounds  II  and  III  were  ichthyotoxic Halimeda,  even  though  they  are  available  in  small
at  the  2  and  10  ug/ml  levels,  respectively,  against amounts  on  substrate  (Juliana  and  Ambrosetti,
Eupomacentrus  leucostictus;  when  these  compounds 1974;  Ogden,  1976)  and  as  drift  (D.  Abbott  et  al.,
were  placed  in  food  offered  to  this  fish  it  was  not 1974).  Rates  of  feeding  by  Lytechinus  vaniegatus
eaten  (Sun  and  Fenical,  1979).  We  are  continuing (Lamarck)  varied  in  laboratory  experiments,  with  —
studies  with  Halimeda  species,  Udotea  flabellum,  U. Caulerpa  being  eaten  least  rapidly  when  offered
conglutinata  (Ellis  and  Solander)  Lamouroux,  Pen- alone  and  most  rapidly  when  offered  with  five
icillus  capitatus  Lamark,  and  Avrainvillea  longicaults other  marine  plants;  Halimeda  was  consistently  ©
(Kutzing)  Murray  and  Boodle,  each  of  which the  least  preferred  alga  (Lawrence,  1975).  Lowe
appears  to  contain  unique  and  biologically  active and  Lawrence  (1976)  suggest  that  L.  variegatus  in
secondary  metabolites. Florida  may  be  feeding  preferentially  on  detrital
Our  field  observations  indicate  that  the  tropi- seagrasses.  Similarly,  Vadas  et  al.  (in  press)
cal  algae  of  these  three  families  are  avoided  by showed  the  preferred  diet  of  field  populations  of
most  herbivores,  at  least  by  the  “generalists” L.  variegatus  was  detrital  Thalassia,  while  siphon-
(sensu  Emlen,  1973).  Few  quantitative  studies aceous  greens  were  largely  not  eaten  (except  by
have  been  done  on  food  preferences  of  tropical one  population  in  which  approximately  30%  of
fish  and  invertebrates.  Those  dealing  with  the their  diet  consisted  of  these  algae).  Lowe  and
herbivores  and  green  algae  we  studied  (see  Law- Lawrence  (1976)  suggested  a  mixed  diet  might  be
rence,  1975;  Ogden  and  Lobel,  1978)  noted  that superior  in  nutrients  for  L.  variegatus.
NUMBER  12  421
COOMe
H
my  m
aes  lI  one  HO  OH
N  ‘ie
gd  H
MeOOC
x |
Br
Ficure 181.—Structures of biologically active metabolites isolated from Carrie Bow Cay marine
algae :a ,caulerpin (compound I) from species of Caulerpa ;b ,sesquiterpenoids ,rhipocephenal
(II) and rhipocephalin (III) ,from Rhipocephalus phoenix ;c ,polypheno l(IV) from Sargassum and
Turbinaria; d, pachydictyol A (V) from Dictyota bartayresi; e, stypotriol (VI) from Stppopodium
|  zonale;  f,  acetylene  containing  lipid  (VII)  from  Lzagora  farinosa;  g,  bromoform  (VIII)  from
Asparagopsis taxiformis ;h ,polhyalogenated monoterpenoids ,ochtodene (IX )and ochtodia l(X),
|  from  Ochtodes  secundiramea;  1,  allolaurinterol  (XI)  from  Laurencia  caraibica.
|  Lewis  (1958)  suggested  that  77ipneustes  ventrico- Halimeda.  Green  algae  not  eaten  by  the  urchin
sus  (Lamarck)  refused  Halimeda  because  of  its Diadema  antillarum  Philippi  included  Penzczllus
calcified  structure,  but  we  suggest  this  rejection (Ogden  et  al.,  1973;  Ogden,  1976)  and  Halimeda
may  also  be  due  to  the  chemical  component  of (Ogden,  1976).  Feeding  preferences  of  sea  urchins
422  SMITHSONIAN  CONTRIBUTIONS  TO  THE  MARINE  SCIENCES
have  been  summarized  by  Lawrence  (1975)  and were  shelled  sacoglossans,  Lobiger  souverbeu
studied  by  Vadas  (1977),  Larson  et  al.  (1980), (Fischer)  and  Oxynoe  species,  and  the  non-shelled
and  Vadas  et  al.  (in  press). sacoglossans,  Elysta  cauzae  (Er.  Marcus),  Elysia
Of  the  Chlorophyta  in  fish-feeding  trials,  Earle species,  and  Volvatella  species  (the  latter  two  and
(1972)  observed  that  Codium  and  Halimeda  were the  Oxynoe  may  represent  undescribed  species,  J.
rapidly  consumed,  only  portions  of  Caulerpa  and R.  Lance,  pers.  comm.).
Udotea  were  eaten,  and  Penicillus  and  Avrainvillea Some  sacoglossans  not  only  ingest  intact  chlo-
were  largely  not  eaten.  Similarly,  Mathieson  et roplasts  from  Caulerpa  and  utilize  their  products
al.  (1975)  found  that  Avrainvillea  nigricans  Des- (see  Taylor,  1966;  Greene;  1974.  aiiemeina9)/5))
caisne  was  mostly  not  eaten,  that  most  fish,  except but  ingest  some  of  the  alga’s  secondary  metabo-
the  parrotfish,  did  not  eat  Halimeda,  that  only  the lites  as  well.  Caulerpicin  and  caulerpin  were  iden-
Grey  Angelfish  consumed  Caulerpa,  and  that  Pen- tified  from  Elysta  panamensis  Pilsbry  and  Olsson
icillus  capitatus  and  Udotea  conglutinata  remained (Doty  and  Aguilar-Santos,  1970)  collected  off
uneaten  at  the  end  of  their  feeding  trials.  Tsuda Baja  California  feeding  on  Caulerpa  sertulanioides.
and  Bryan  (1973)  noted  that  the  siganid  fishes This  sacoglossan  can  secrete  a  milky  mucus  that
readily  consumed  Caulerpa  during  feeding  trials. is  toxic  to  fish  (Lewin,  1970).  The  biological
It  is  difficult  to  generalize  about  tropical  herbi- activity  of  caulerpin  (Figures  181a,  compound  I)
vores  and  their  feeding  habits  and  preferences  on and  caulerpicin  (Doty  and  Aguilar-Santos,  1966)
the  basis  of  such  scant  information.  Of  the  greens was  reported  by  Doty  and  Aguilar-Santos  (1970)
we  studied,  however,  most  are  apparently  not to  be  toxic  to,  and  physiologically  active  in,  mice
eaten  by  many  herbivores  in  habitat. and  rats,  respectively.
A  few  herbivores  apparently  can  physiologi- While  Caulerpa,  Halimeda,  Udotea,  Penicillus,  Rhi-
cally  cope  with,  or  perhaps  even  selectively  eat, pocephalus,  and  Avrainvillea  have  evolved  secondary
algae  having  chemical  defenses.  Sacoglossan  op- compounds  that  deter  a  wide  variety  of  herbi-
isthobranchs  are  a  notable  exception  to  the  gen- vores,  the  sacoglossans  have  evolved  a  physiolog-
eral  avoidance  of  Caulerpa  and  members  of  the ical  mechanism  for  tolerating  the  chemical  deter-
Codiaceae  as  a  food  source.  In  fact,  bivalved rents  produced  by  the  algae,  and  thus  have  be-
sacoglossans  are  restricted  to  Caulerpa,  while  non- come  “specialists”  feeding  on  a  restricted  but
shelled  sacoglossans  have  been  reported  in  asso- exclusive  diet.  It  also  appears  that  these  specialists
ciation  with  a  variety  of  algae  that  include  several deter  predation  upon  themselves  by  concentrat-
species  of  Codiaceae  (MacNae,  1954),  and  a  few ing  these  compounds.  More  than  three  times  the
other  Chlorophyta  and  Vaucheria  (Chrysophyta) amount  of  caulerpicin  and  more  than  twice  the
(see  Kay,  1968). amount  of  caulerpin  were  found  concentrated  in
The  association  between  these  algae  and  saco- the  sacoglossan  Elysta  panamensis  than  were  found
glossans  in  the  Caribbean  has  been  reported  from in  the  algal  host,  Caulerpa  (Doty  and  Aguilar-
Puerto  Rico  (Warmke  and  Almodovar,  1963), Santos,  1970).
and  in  the  Pacific  from  Japan  (Hamatani,  1972) PHAEOPHYTA.—  The  abundant  brown  algae  at
and  Fiji  (Burn,  1966).  The  distribution  of  saco- Carrie  Bow  Cay  belong  to  two  families,  the  Sar-
glossans  appears  dependent  on  the  range  of  their gassaceae  and  the  Dictyotaceae.  Species  of  Sar-
food  source,  Caulerpa  (Burn,  1966),  with  members gassum  and  Turbinaria  (Sargassaceae)  are  appar-
of  the  family  Juliidae  reflecting  the  distribution ently  not  eaten  by  some  herbivores,  at  least  in
of  Caulerpa  throughout  the  Indo—West  Pacific,  the areas  where  these  browns  are  common.
‘Caribbean,  the  Mediterranean  and  Victoria,  Aus- In  the  Caribbean,  Sargassum  and  Turbinarna
tralia  (Kay,  1968). sometimes  grow  in  areas  of  the  reef  where  herbi-
Specialist  herbivores  were  relatively  common vores  may  have  difficulty  reaching  them  or  re-
at  Carrie  Bow  Cay.  Found  on  Caulerpa  racemosa maining  attached  to  feed.  Also,  in  preliminary
NUMBER 12 Aes
subtidal  feeding  trials  and  translocation  experi- removed  Diadema;  a  diet  of  Turbinaria  also  pro-
ments  of  Sargassum  in  Caribbean  Panama  (J. vided  the  best  growth  for  77ipneustes  of  the  algae
Cubit  and  M.  Hay,  pers.  comm.)  and  Islas  San tested  in  St.  Croix  (J.  Ogden,  R.  Vadas,  and  S.
Blas  (J.  Cubit,  pers.  comm.),  these  algae  were Miller,  pers.  comm.).
readily  consumed,  particularly  by  kyphosid The  common  browns  at  Carrie  Bow  Cay  be-
fishes.  These  observations  suggest  that  herbivory long  to  the  Dictyotaceae;  members  of  Dictyota,
may  limit  the  lower  level  of  distribution  of  certain Dictyopteris, Lobophora, Padina, and Stypopodium are
Sargassum  species.  It  is  also  possible  that  increased represented.  Although  Padina  and  Lobophora  spe-
predation  or  other  factors  may  keep  these  fish cies  are  not  noticeably  grazed  in  the  vicinity  of
from  the  reef  where  Sargassum  grows;  we  also Carrie  Bow  Cay,  we  have  not  found  in  them  the
suggest  that  members  of  this  family  may  not  be unusual  organic  compounds  that  are  present  in
eaten  owing  to  their  inherent  high  concentrations other  tropical  members  of  the  family;  therefore,
of  polyphenolic  substances  based  upon  the  poly- structure  or  some  other  factor  may  be  important,
merization  of  phloroglucinol  (Figure  181c,  com- such  as  increased  predation  upon  potential  her-
pound  IV).  Types  of  biological  activity  shown  by bivores,  or  possibly  water  soluble  compounds  or
polyphenols  include  antibacterial  (Conover  and secondary  compounds  below  our  level  of  detec-
Sieburth,  1964)  and  antilarval  (Conover  and  Sie- tion  may  be  present.  Interestingly,  a  Pacific  spe-
burth,  1966).  These  polyphenols  may  also  be cies  of  Lobophora  from  Palau  was  found  to  contain
ecologically  important  in  plant-plant  interac- unusual  compounds  (Fenical,  in  progress).
tions;  growth  of  certain  phytoplankton  and  mac- Of  the  several  species  of  Dictyota  occurring  in
roalgae  may  be  inhibited  (McLachlan  and  Crai- the  vicinity  of  Carrie  Bow  Cay  (Norris  and
gie,  1964)  or  enhanced  (Ragan  et  al.,  1980)  by Bucher,  herein:  167),  we  investigated  the  most
polyphenols. predominant  one,  D.  bartayrest1,  which  grows
The  presence  and  absence  of  these  compounds among  corals  in  the  spur  and  groove  area  of  the
in  the  Sargassaceae  have  been  reviewed  by  Glom- barrier  reef.  Recognized  in  the  field  by  its  marked
bitza  (1977).  Pfeffer  (1963)  suggested  that  the iridescence,  D.  bartayresit  in  our  chemical  studies
inability  of  fish  to  digest  Sargassum  was  due  to  its was  shown  to  contain  a  series  of  toxic  bicyclic
tannins  (Ogino,  1963).  From  stomach  analysis  of diterpenoids,  the  major  component  being  the
tropical  reef  fish,  Randall  (1967)  concluded  Sar- compound  pachydictyol  A  (Figure  181d,  com-
gassum  was  eaten  only  by  a  few  larger  herbivorous pound  V),  previously  described  by  Hirschfeld  et
and  omniverous  fishes—Kyphosus  incisor  (Cuvier al.  (1973)  from  another  Dictyotaceae  genus,  Pach-
and  Valenciennes),  K.  sectatrix  (Linnaeus),  Poma- ydictyon  (for  review  of  Dictyotaceae  diterpenoid
canthus  arcuatus  (Linnaeus),  P.  para  (Bloch),  and synthesis  see  McEnroe  et  al.,  1977).  Although
Melichthys  niger  (Bloch)—and  that  these  kyphosids some  sea  urchins  have  been  noted  to  feed  on  some
and  M.  niger  feed  on  drifting  algae.  Earle  (1972) species  of  Dictyota  (Atkinson  et  al.,  1973;  Abbott
suggested  it  may  be  eaten  by  certain  fishes,  and etvalk,  (974.  Lawrence,  1975)<-as  yet  none  are
W.  H.  Adey  (pers.  comm.)  reports  that  the  buck- known  to  feed  specifically  on  D.  bartayresi.  This
tooth  parrotfish,  Sparisoma  radians  (Cuvier  and alga  has  been  recorded  in  stomach  contents  of
Valenciennes),  readily  consumes  Sargassum.  At- three  species  of  fish  (Randall,  1967;  Earle,  1972).
kinson  et  al.  (1973)  found  that  Sargassum,  though It  is  also  possible  that  pachydictyol  A  may  not
available,  was  not  present  in  the  guts  of  Diadema function  to  deter  urchin  or  fish  predators,  but
antillarum  (see  also  Lawrence,  1975),  while  another might  be  an  example  of  a  compound  that  acts
sea  urchin,  Paracentrotus  lividus  (Lamarck)  has  been against  certain  micro-organisms.  This  metabo-
recorded  as  feeding  on  Sargassum  (Lawrence, lite’s  toxicity  to  certain  fungi  suggests  it  could  be
1975).  Sammarco  et  al.  (1974)  observed  lush defense  against  microbial  pathogens  (Fenical,  un-
growth  of  Jubinaria  on  a  patch  reef  after  they published  data).
494  SMITHSONIAN  CONTRIBUTIONS  TO  THE  MARINE  SCIENCES
Another  predominant  brown  alga  at  Carrie added  to  the  expanding  list  of  families  known  to
Bow  Cay  is  Stypopodium  zonale,  which  grows  pri- produce  secondary  compounds.
marily  in  open,  shallow  areas  (4-10  m  depths) The  moderately  calcified  red,  Lzagora  farinosa
where  it  is  accessible  to  grazers.  Frequently  to  20 (Helminthocladiaceae),  was  seasonally  abundant
cm  in  length  and  conspicuous  in  its  environment, in  the  spur  and  groove  habitats  of  the  barrier  reef
S.  zonale  is  apparently  not  eaten  by  most  herbi- at  Carrie  Bow  Cay.  We  noted  unusual  com-
vores.  When  freshly  collected  S.  zonale  is  placed  in pounds  present  on  TLC  plates,  and  recently  Paul
cool  seawater  for  10  hours,  the  water  becomes and  Fenical  (1980)  described  the  major  metabo-
dark  brown,  apparently  from  release  of  pigments lite,  an  unusual  acetylene  containing  lipid  (Figure
and  secondary  compounds.  These  substances 181f,  compound  VII),  which  occurs  along  with
were  toxic  to  the  herbivorous  damsel  fish,  Eupo- several  minor,  related  compounds  in  this  species.
macentrus  leucostictus,  found  at  Carrie  Bow  Cay, These  compounds  were  observed  to  be  toxic
and  exhibited  antimicrobial  activity  in  prelimi- against  Eupomacentrus  leucostictus  at  the  5-8  ug/ml
nary  testing.  Ethanol  extracts  of  S.  zonale  were range  in  seawater.  We  did  not  observe  any  grazers
equally  toxic  to  damsel  fish  at  levels  of  approxi- on L. farinosa.
mately  3  ug/ml.  The  toxic  components  have  been Despite  its  fine,  delicate  structure,  Asparagopsis
found  to  consist  of  a  mixture  of  several  related taxiformis  (Bonnemaisoniaceae)  does  not  seem  to
C27  compounds  derived  from  a  mixed  biosynthesis be  utilized  as  a  food  source.  Asparagopsis  species
of  diterpenoid  and  acetate  precursors.  One  of produce  unique  toxins,  the  major  metabolite
these  compounds,  the  triol  stypotriol  (Figure  18  Le, being  the  noxious  compound  bromoform  (Figure
compound  V\]),  has  been  isolated  and  structurally 181g,  compound  VIII)  (McConnell  and  Fenical,
defined  (Gerwick  and  Fenical,  1980).  We  are  not 1976).  Several  halogenated  acetones  are  also  pro-
aware  of  published  records  of  S.  zonale  as  a  food duced  by  A.  taxzformis  (compounds  of  this  type
source  for  fishes  or  urchins.  As  in  the  green  alga- have  been  produced  synthetically  and  used  as
sacoglossan  relationship,  certain  mollusks  may tear  gas).  |
have  co-evolved  as  specialist  predators  of  S.  zonale. Asparagopsis  was not  eaten by the fish Acanthurus
Recent  collections  of  this  alga  from  the  Florida trostegus  (Linnaeus)  (Randall,  1961),  nor  has  it
Keys  contained  large  numbers  of  the  sea  hare been  reported  as  being  grazed  by  sea  urchins
Petalifera  petalifera  Ranger  (Fenical,  unpublished (Lawrence,  1975).  We  suggest  it  is  not  eaten  by
data),  but  it  was  not  observed  on  any  other  algae most  herbivores  because  of  its  toxic  metabolites.
and  may  represent  another  specialist  with  a  pre- These  compounds  inhibited  the  growth  of  all
ferred  or  exclusive  food  source. micro-organisms  tested,  and  they  were  severe  lac-
RuopopuytaA.—Although  they  have  the  largest rymators.  Interestingly,  though  toxic  or  unpalat-
number  of  species  in  the  environs  of  Carrie  Bow able  to  most  grazers,  it  is  consumed  by  man,  for
Cay,  the  red  algae  are  generally  smaller  in  size Asparagopsis  taxiformis  is  the  favorite  seaweed  food
and  individual  species  are  less  abundant  than of  the  Hawauans  (Abbott  and  Williamson,  1974).
either  the  green  or  brown  algal  species.  Red  algae Falkenburgia  hillebrandii  (Ardissone)  Falkenberg,
that  are  apparently  avoided  by  herbivores  at the  alternate  sporophytic  stage  in  the  life  history
Carrie  Bow  Cay  belong  to  four  families:  Hel- of  Asparagopsis  taxiformis  (Chihara,  1961),  has  also
minthocladiaceae,  Bonnemaisoniaceae,  Rhizo- been  collected  at  Carrie  Bow  Cay.  This  morpho-
phyllidaceae,  and  Rhodomelaceae.  Members  of logically  different  stage  also  appears  to  be  avoided
the  latter  three  families  are  known  to  produce by  grazers.  In  other  studies,  McConnell  and  Fen-
elaborate  halogenated,  often  toxic,  metabolites ical  (unpublished  data)  have  found  Falkenburgia
(Fenical,  1975).  With  the  recent  discovery  of from  the  North  Atlantic  also  to  contain  bromo-
unique  compounds  in  Liagora  farinosa  (Paul  and form.  We  suspect  that  the  Carrie  Bow  Cay  Fal-
Fenical, 19 8th0e),  Helminthocladiaceae  was kenburgia,  which  is  generally  not  eaten  by  herbi-
NUMBER 12 425
vores,  also  produces  this  compound.  Fish  have with  L.  obtusa  in  areas  of  intense  water  motion,
not  been  observed  to  feed  on  this  stage  of  Aspar- generally  along  the  outer  reef  crest.  This  alga
agopsis  (Earle,  1972),  but  it  was  found  in  1%  of produces  quantities  of  the  antibiotic  cuparane
Diadema  antillarum  guts  by  Atkinson  et  al.  (1973). derivative  allolaurinterol  (Figure  1812,  compound
Since  that  was  such  a  small  sample,  it  may  have XI),  a  compound  which  has  also  been  isolated  as
indirectly  been  consumed  while  feeding  primarily a  minor  component  of  L.  subopposita  (J.  Agardh)
on  other  turf-forming  algae.  This  possibility,  how- Setchell  from  California  (Wratten  and  Faulkner,
ever,  will  have  to  be  further  investigated. 1977)  and  L.  filiformis  (GC.  Agardh)  Montagne
Another  red  alga  containing  toxic  secondary from  the  east  coast  of  Australia  (Kazlauskas  et
compounds  is  Ochtodes  secundiramea  of  the  Rhizo- al.,  1976).  Izac  and  Sims  (1979)  discovered  a
phyllidaceae.  Ochtodes  secundiramea  grows  in  shal- unique  iodinated  sesquiterpene  in  L.  caraibica,  the
low  water  inside  the  reef  crest  at  South  Water first  report  of  such  a  compound  and  of  iodine
Cay,  in  areas  of  strong  wave  agitation  and  surge. being  found  in  the  genus.  We  found  the  same
This  alga  contains  one  major  and  one  minor major  metabolite  in  this  species,  and  did  not
polyhalogenated  monoterpenoid,  octodene  and observe  this  alga  being  eaten  by  fish  or  urchins.
ochtodial  (Figure  181h,  compounds  [X  and  X) Laurenica  obtusa  was  found  in  large  quantities
(McConnell  and  Fenical,  1978).  Compound  IX, along  the  Carrie  Bow  Cay  reef  crest  (at  least
the  major  metabolite,  is  strongly  antibiotic  and during  April  and  May).  We  found  this  alga  to
made  up  over  50%  of  the  total  organic  extract  of contain  more  than  3%  (dry  weight)  of  the  cyto-
the  alga.  During  our  field  studies  on  freshly  col- toxic  chamigrene  derivative  elatol  (Figure  182,
lected  specimens,  we  observed  iridescence  from compound  XII),  a  compound  originally  isolated
the  large  “glandular  cells”  or  ‘“Drusenzellen” from  the  Australian  species  L.  elata  (C.  Agardh)
(Kylin,  1956)  present  in  the  cortex  of  O.  secundi- Hooker  and  Harvey  (Sims  et  al.,  1974).  Elatol  has
ramea  (Joly  and  Ugadim,  1966).  Whether  these subsequently  been  found  to  be  moderately  anti-
refractive  bodies  are  the  site  of  halogenation  in biotic,  but  more  interestingly  this  compound
O.  secundiramea  is  uncertain,  although  we  observed shows  exceptional  toxicity  against  fertilized  sea
these  bodies  were  no  longer  iridescent  after  the urchin  eggs,  and  totally  inhibits  cell  division  (Fig-
methanol  extraction  and  they  appeared  to  be
“empty  on  examination  with  a  Wild  M5  ster- H oelatol
eomicroscope.  We  are  not  aware  of  any  published
accounts  of  Ochtodes  as  a  food  source;  we  did  not —  Cl  oO  __O  —___—  :
find  it  being  grazed  during  our  daytime  obser- s¢  100  a  2  ge  are  2!
vations  in  Belize. &  “f°
20  XII  A a
Three  species  of  the  cosmopolitan  genus  Lau- 3  @
rencia  (Rhodomelaceae)  from  Carrie  Bow  Cay O  60  a®
contained  interesting  secondary  metabolites.  This op  fe)  ©LJ  rs
genus  is  known  to  produce  a  complex  variety  of ©  a@©  oO
halogen-containing  compounds  (Fenical  and (=S  5
Norris,  1975;  Fenical,  1975).  We  conducted  chem- 2  20  z
ical  studies  on  the  two  abundant  species,  Laurencia £
caraibica  and  L.  obtusa  (identified  following  Taylor, |  2  4  8  I6 ONWm
1960:626),  at  Carrie  Bow  Cay.  The  third  species, Ba Cthoncentrati o(ung/ml)
L.  intricata  Lamouroux,  was  not  abundant  enough Ficure 182.—Dose-response curve o felato l(compound NII
for  further  study,  even  though  an  initial  TLC from Laurencia obtusa ,agains tfertilized egg so fthe sea urchin,
indicated  the  presence  of  secondary  compounds. Stronglyocentrotu psurpuratu (sth seeve mn arke rrsepresen int di-
Laurencia  caraibica  Silva  grows  sympatrically vidu eaxlperiments).
426  SMITHSONIAN  CONTRIBUTIONS  TO  THE  MARINE  SCIENCES
ure  182).  The  dose-response  curve  of  elatol  with dall,  1967).  Opisthobranch  gastropods  used  in
fertilized  eggs  from  Stronglylocentrotus  purpuratus feeding-acceptability  tests  with  selected  fish  by
(Stimpson),  a  California  urchin,  shown  in  Figure Thompson  (1960)  were  almost  invariably  refused.
182,  has  been  provided  by  R.  Jacobs.  The  LDso Recently,  it  was  suggested  that  juveniles  of  the
of  elatol  is  estimated  at  about  7  pg/ml  bath tropical  bridled  burrfish,  Chzlomycterus  antennatus
concentration.  Laurenica  obtusa  1s  not  grazed  by (Cuvier),  in  Caribbean  Panama,  are  Batesian
Diadema  (Ogden,  1976),  and  is  avoided  by  most mimics  of  Aplysia  dactylomela  and  perhaps  avoid
herbivores:  It  is  interesting  to  speculate  on  the predation  by  mimicking  the  shape  and  coloration
ecological  role  of  compounds  such  as  elatol,  which of  the  “unpalatable  sea  hare”  (Heck  and  Wein-
are  now  known  to  inhibit,  or,  at  certain  levels,  to stein,  1978).  We  suggest  that  the  avoidance  could
kill  developing  sea  urchin  eggs.  We  hypothesize be  due  to  the  concentration  of  elatol  by  A.  dacty-
that  if  such  compounds  are  released  or  secreted lomela from Laurencia obtusa.
in  the  vicinity  of  Laurencia  stands,  they  could
inhibit  sea  urchin  egg  development  in  situ,  and Summary  and  Conclusions
thus  give  the  alga  a  selective  advantage  against
the  settlement  and  development  of  potential  pre- Our  studies  of  Belize  macro-algae,  indicate  that
dators  in  their  vicinity. members  of  specific  algal  families—the  Cauler-
In  view  of  the  biologically  active  constituents paceae,  Codiaceae,  Udoteaceae,  Dictyotaceae,
from  Laurencia,  it  is  not  surprising  that  the  alga Sargassaceae,  Helminthocladiaceae,  Bonnemai-
has  few  predators.  The  sea  hares  (Anaspidea), soniaceae,  Rhizophyllidaceae,  and  Rhodomela-
particularly  some  species  of  Aplysia,  have  specific ceae—produce  unusual  secondary  compounds.
feeding  preferences  for  Laurencia.  In  our  field  stud- The  species  we  studied  are  not  eaten  by  many
ies  in  the  Gulf  of  California,  California,  the  Gal- herbivorous  fishes  or  sea  urchins.  These  herbi-
apagos  Islands  and  now  in  Belize,  we  have  ob- vores  and  the  coral  reef  algae  on  which  they  feed
served  this  grazer-alga  relationship  between  Lau- appear  to  represent  a  co-evolved  system  of  defense
rencia  and  Aplysia.  During  our  spring  studies  at and  counterdefense.  Chemical  defense  appears
Carrie  Bow  Cay,  we  typically  found  A.  dactylomela successfully  to  deter  the  majority  of  herbivores;
(Ranger)  grazing  on  L.  obtusa  on  the  fore-reef however,  some  specialist  grazers  have  co-evolved
crest.  It  appears  that  some  Aplysza  species  may  be physiological  mechanisms  that  enable  them  to
dependent  on  Laurencia,  at  least  during  certain tolerate  or  possibly  even  select  for  some  of  these
stages  of  their  life  cycle,  as  larvae  and  juveniles. same  algae.  In  some  specific  animal-plant  inter-
Culture  studies  on  A.  californica  Cooper  (Krieg- actions,  for  example,  saccoglossan-Caulerpa  and
stein  et  al.,  1974)  indicate  that  settling  and  meta- Aplysia-Laurencia,  the  mollusks  not  only  exclu-
morphosis  of  the  free-swimming  larval  stage  are sively  select  certain  algal  species  for  food  and
enhanced  by  the  presence  of  Laurencia  pacifica. show  preference  for  others  but  they  also  concen-
Stallard  and  Faulkner  (1974)  showed  that  Aply- trate  the  alga’s  secondary  compounds  as  defense
sia  californica  concentrated  the  metabolites  of  Lau- against  being  preyed  upon.  Thus,  it  appears  the  ©
rencia  pacifica  in  their  digestive  glands.  We  have chemical  deterrent  against  most  herbivores  may
found  quantities  of  elatol,  identified  from  L.  obtusa have  become  a  chemical  attractant  to  these  spe-
in  our  study,  in  the  digestive  glands  of  A.  dactylo- cialist  species.  Published  evidence  and  our  own
mela.  It  has  been  proposed  that  the  concentration observations,  though  scant,  indicate  most  herbiv-
of  the  algal  metabolites  by  the  sea  hare  provide orous  reef  fishes  are  highly  selective  in  the  algae
a  selective  advantage  against  potential  predators they  consume.  In  tropical  reef  algal-animal  rela-
(Stallard  and  Faulkner,  1974;  Kittredge  et  al., tionships,  there  is  strong  evolutionary  interaction
1974).  Although  the  defense  role  of  this  concen- between  herbivores  and  algae,  based  on  the  alga’s
tration  needs  to  be  tested,  known  predators  of defenses—structure  (Lubchenco,  1978),  produc-
Aplysia  are  few,  and  opisthobranchs  in  general  are tivity  and  growth  form  (Littler,  1980),  life  history
avoided  as  a  food  source  by  Caribbean  fish  (Ran- strategy  (Lubchenco  and  Cubit,  1980),  habitat,
NUMBER 12 427
and  chemistry—and  the  herbivore’s  feeding defense  (see  for  example  feeding  preference  stud-
habits  (preference  for,  or  not  eating  of,  algae  and ies  of  Vadas,  1977;  Larson  et  al.,  1980;  for  addi-
the  peculiarities  of  their  digestive  physiology). tional  interpretation  of  “evolutionary  arms  race”
Ehrlich  and  Raven  (1965)  first  attributed  to theory,  see  Atsatt  and  O‘Dowd,  1976).
secondary  compounds  of  plants  a  key  role  in The  subject  of  tropical  reef  algal-animal  inter-
determining  the  pattern  of  insect-plant  co-evolu- actions  presents  a  myriad  of  problems  to  be  in-
tion.  As  suggested  by  Feeny  (1975),  we  may  be
vestigated  and  questions  to  be  answered.  Recog-
witnessing  an  “evolutionary  arms  race”  in  which
the  algae  must  deploy  part  of  their  metabolic nizing  the  speculative  nature  of  this  study  we
budget  on  defense  against  herbivory,  and  the concur  with  Janzen  (1977)  that  there  is  “quite
herbivores  must  devote  a  portion  of  their  assim1- enough  hypothetical  biology  on  the  books”  and
lated  energy  on  ways  to  locate  their  algal  food, we  now  need  quantitative  ecological  and  behav-
know  which  species  to  avoid,  and  on  developing ioral  studies  “on  the  pragmatics”  of  tropical
counter  measures  to  tolerate  the  alga’s  chemical plant-animal  interactions.
Literature  Cited
Abbott, D. P., I. A. Abbott, G. Juliana, J. Amborsetti, J. C. Atkinson, C., S. Hopley, L. Mendelsohn, and S. Yacowitz
Ogden, and K. Warner 1973. Food Studies on Diadema antillarum on a Patch
1974. Drifting Macroscopic Plants as Sources of Food Reefs  St.  Croix,  US:  Viremt  Islands:  f  Je  CG:
for the Sea Urchin Echinometra lucunter at Boiler Ogden, D. P. Abbott, and I. A. Abbott, editors,
Bay, St. Croix. Jn D. P. Abbott, J. C. Ogden, and Studies on the Activity and Food of the Echinoid
I. A. Abbott, editors, Studies on the Activity Pat- Diadema antillarum Philipp ion a Wes tIndian Patch
tern, Behavior, and Food of the Echinoid Echino- Reef .Wes tIndie sLaboratory S, pecia lPublication 9, :
metra lucunter (Linnaeus )on Beachrock and Algal 65-80. St. Croix, U.S. Virgin Islands.
Reefs at St Croix, U.S. Virgin Islands. West Indies Atsatt, P. R., and D. J. O Dowd
Laboratory ,Specia lPublication ,4:78-86 .St .Croix, 1976 .Plan tDefense Guilds .Science ,193:24—29.
U.S .Virgin Islands. Bakus ,G. J.
Abbott, I. A., and E. H. Williamson 1964. The Effects of Fish Grazing on Invertebrate Evo-
1974 L. imu A: n Ethnobotanica Sl tud yo fSom eEdibl eHawaiian lution in Shallow Tropical Waters. Allan Hancock
Seaweeds .21 pages .Lawai ,Kauai ,Hawaii: Pacific Foundatio Pnublication Os,ccasion Paal pe 2r7, :1—29.
Tropica lBotanica lGarden. 1966. Some Relationships of Fishes to Benthic Orga-
Adey, W. H., and J. M. Vassar nism son Cora Rl eefs .Nature 2, 10(5033):280—284.
1975. Colonization, Succession and Growth Rates of 1969. Energetics and Feeding in Shallow Marine Wa-
Tropical Crustose Coralline Algae (Rhodophyta, ter sI.nternationa Rleview o Gf enera aln dExperimental
Cryptonemiales P).hycologi a1,4(2):55-69. Zoology, 4:275-369, New York: Academic Press,Inc.
Aguilar-Santo sG,.
1970. Caulerpin, a Red Pigment from Green Algae of Bardach, J. E.
th eGenu sCaulerpa J.ourna ol tfh eAmerican Chemical 1959. ‘The Summer Standing Crop of Fish on a Shallow
Society s, ection c 9, 2:842. Bermud aReef L. imnolog yand Oceanography 4, (1):77-85.
Aguilar-Santos, G., and M. S. Doty Bhakuni, D. S., and M. Silva
1968. Chemical Studies on Three Species of the Marine 1974 .Biodynamic Substances from Marine Flora .Botan-
Alga lGenus Caulerpa .In H .D .Freudenthal ,editor, wc Ma arin a1,7:40-51.
Proceeding so tfh eThir dConferenc eo nFoo dan dDrugs Boyd, W. C., L. R. Almodovar, and L. G. Boyd
from the Sea, pages 173-176. Marine Technology 1966. Agglutinins in Marine Algae for Human Eryth-
Society. rocyte Ts.ransfusio n6,(1):82-83.
Almodovar, L. R. Burkholder ,P .R.
1964. Ecological Aspects of Some Antibiotic Algae in 1973.  The  Ecology  of  Marine  Antibiotics  and  Coral
Puert oRico B. otanic aMarina 6, :143—146. Reefs. In O. A. Jones, and R. Endean, editors,
a
428  SMITHSONIAN  CONTRIBUTIONS  TO  THE  MARINE  SCIENCES
Biology and Geology o fCora lReefs ,pages 117-282. Fraenkel ,G .S.
New York :Academic Press. 1959. The Raison d’Etre of Secondary Plant Substances.
Burkholder, P. R., L. M. Burkholder, and L. R. Almodovar Scienc e1,2 91:466-1470.
1960.  Antibiotic  Activity  of  Some  Marine  Algae  of Gerwick, W. H., and W. Fenical
Puerto Rico .Botanica Marina ,2:149-156. 1980.  Ichthyotoxic  and  Cytotoxic  Metabolites  of  the
Burn ,R. Tropica lBrown Alga ,Stypopodium zonale .Journa lof
1966. The Opisthobranchs of a Caulerpin Microfauna Organ Cichemist r4y6,:22—27.
from Fiji .Proceedings o fthe Malacologica lSociety of Glombitza, K. W.
Londo 3n7,:45-65. 1977. Highly Hydroxylated Phenols of the Phaeophy-
Chihara ,M. ceae. Jn D. J. Faulkner and W. H. Fenical, editors,
1961. Life Cycle of the Bonnemaisoniaceous Algae in Marine Natura Pl roduct sChemistry p, age s191-204.
Japan 1, S. czence Report so fthe Tokyo Kyotku Daigaku, New York :Plenum Press.
section B, 10(153):121-154, plates 1-6. Greene ,R. W.
Conover, J. T., and J. McN. Sieburth 1974. Sacoglossans and Their Chloroplast Endosym-
1964. Effects of Sargassum Distribution on Its Epibiota bionts. In W. B. Vernberg, editor, Symbiosis in the
and Antibacteria lActivity .Botanica Marina ,6:147- Sea, pages 21-27. Columbia, South Carolina: Uni-
aye versity of South Carolina Press.
1966. Effect of Tannins Excreted from Phaeophyta on Hamatan iI,.
Planktonic Animal Survival in Tide Pools. Jn E. 1972. A New Species of Volvatella Pesae 1860 Found in
G .Young and J .L .McLachlan ,editors ,Proceedings the Caulperin Microfauna in the Province of Kail,
o fth eFifth Internationa Sl eaweed Symposium p, ages Middle Japan .Publication so fthe Seto Marine Biolog-
99-100 .Oxford :Pergamon Press. ic aLlaborator y2,1(1):13-20.
Doty, M. S., and G. Aguilar-Santos Harbourne ,J. B.
1966. Caulerpicin, a Toxic Constituent of Caulerpa. Na- 1977. Introduction to Ecological Biochemistry. xiv + 243
tu r2e1,1(5052):990. pages .London :Academic Press.
1970.  Transfer  of  Toxic  Algal  Substances  in  Marine
Food Chains .Pacific Science ,24(3):351-355. Hay, M. E.1981.  The  Functional  Morphology  of  Turf-forming
Earle, S. A. Seaweeds: Persistence in Stressful Marine Habi-
1972. ‘The Influence of Herbivores on the Marine Plants tats.  Ecology,  62(3):739-750.  |
of Great Lameshur Bay, with an Annotated List
of Plants. /n B. B. Collette and S. A. Earle, editors, Heck, K. L., and M. P. Weinstein
Results of the Tektite Program: Ecology of Coral 1978.  Mimetic  Relationship  between  Tropical  Burr-
Reef Fishes .Natura lHistory Museum ,Los Angeles fishe asn dOpisthobranch sB.rotropic a1,0(1):78—79.
Count yS,cienc eBulletin 1,4:17-44. Hiatt, R. W., and D. W. Strasburg
Ehrlich, P. R., and P. H. Raven 1960.  Ecological  Relationships  of  the  Fish  Fauna  on
1965. Butterflies and Plants: A Study in Coevolution. Coral Reefs of the Marshall Islands. Ecological
Evolutio 1n8,:586-608. Monograp 3h0s(,1):65-127.
Emlen, J. M. Hirschfeld, D. R., W. Fenical, G.H.Y. Lin, R. M. Wing, and
1973 .Ecology ,an Evolutionary Approach .493 pages .Read- P. C. Radlick
ing ,Mass. :Addison-Wesley Publishing Company, 1973. Pachydictyol A, a Unique Diterpene Alcohol from
Inc. th eBrow nSeawee dPachydictyo ncortaceum J.ournal
Feen yP, . o tfh eAmerica nChemica Slociety 9, 5:4049.
1975.  Biochemical  Coevolution  between  Plants  and Hornsey, I. S., and D. Hide
Their Insect Herbivores. Jn L. E. Gilbert, and P. 1974. The Production of Antibiotic Compounds by Brit-
H R. aven e, ditors C, o-evolution o fAnimal sand Plants, ish Marine Algae, I: Antibiotic Producing Marine
pages 3-19. Austin: University of Texas Press. Algae .British Journa lo fPhycology ,9:353-361.
Fenica lW, . Zac ReIRe
1975. Halogenation in the Rhodophyta: A Review. Jour- 1979. Secondary Metabolites from the Red Alga Lauren-
na ol Pf hycology 1, 1:245-259. cia. Ph.D. dissertation. University of California,
‘Fenical, W., and J. N. Norris Riverside.
1975. Chemotaxonomy in Marine Algae: Chemical Sep- Izac )RoR? ands |p as Simas
aration of Some Laurenica Species (Rhodophyta) 1979. Marine Natural Products, 18: Iodinated Sesqui-
from the Gul fo fCalifornia .Journa lo fPhycology ,\1: terpenes from the Red Alga lGenus Laurencia .Jour-
104-108. na o ltfh eAmerica nChemica Slociet y1,01:6136—-6137.
NUMBER 12 429
Janzen, D. L. Lawrence, J. M.
1973. Community Structure of Secondary Compounds. 1975. On the Relationships between Marine Plants and
In T .Swain ,editor ,Chemistry in Evolution and Sys- Sea Urchins ./n H .Barnes ,editor ,Oceanography and
tematics p, age s529-538 L. ondon B: utterworths. Marine Biology ,Annua lReview ,1975 ,13:213-286.
1977. Promising Directions of Study in Tropical Animal- London: George Allen and Unwin, Ltd.
Plan tInteractions .Annals o fthe Missour :Botanical Lewin, R. A.
Garden,  64:706-736.  | 1970. ‘Toxic Secretion and Tail Autonomy by Irritated
Joly, A. B., and Y. Ugadim Oxyno peanamens iPs.acif Siccrenc e2,4:356-359.
1966 .The Reproduction o fOchtodes secundiramea (Mon- Lewis, J. B.
tagne) Howe (Gigartinales, Rhizophyllidaceae). 1958 .‘The Biology of the Tropica lSea Urchin ,Trzpneustes
Boletm d oInstitut oOceanografico U, niversida d eSao esculentus Leske in Barbados ,British Wes tIndies.
Paul o15, (1):55-64. Canadia nJourna ol Zfoology 3,6:607-621.
Juliana, G., and J. Ambrosetti Littler, M. M.
1974. Feeding and Diet in Echinometra lucunter. In D. P. 1980. Morphological Form and Photosynthetic Perfor-
Abbott, J. GC. Ogden, and I. A. Abbott, editors, mances of Marine Macroalgae: Tests of a Func-
Studies on the Activity Pattern, Behavior, and tiona lForm Hypothesis .Botanica Marina ,22:161-
Food of the Echinoid Echinometra lucunter (Lin- 165.
naeus) on Beachrock and Algal Reefs at St. Croix, Littler, M. M., and D. S. Littler
U.S .Virgin Islands .Wes tIndies Laboratory ,Special 1980.  The  Evolution  of  Thallus  Form  and  Survival
Publication ,4:65-77. St. Croix ,U.S. Virgin Islands. Strategies in Benthic Marine Macroalgae: Field
Kay, E. A. and  Laboratory  Tests  of  a  Functional  Form
1968. A Review of the Bivalved Gastropods and a Dis- Mode lT.h eAmerica nNaturalis t1,16(1):25—44.
cussion of Evolution within the Sacoglossa. Jn V. Lowe, E. F., and J. M. Lawrence
Fretter, editor, Studies in the Structure, Physiol- 1976 .Absorption Efficiencies o fLytechinus variegatus (La-
ogy and Ecology of Molluscs .Symposia of the Zoo- marck )(Echinodermata :Echinoidea )fo rSelected
logica Slociet yo Lfondo nan dth eMalacologica Slociet yof Marin ePlants J.ourna ol Efxperimenta Ml arin eBiology
London, 22:109-134. New York: Academic Press, an dEcolog y2,1:223-234.
Inc. Lubchenco J,.
Kazlauskas, R., P. T. Murphy, R. J. Quinn, and R. J. Wells 1978.  Plant  Species  Diversity  in  a  Marine  Intertidal
1976 .New Laurene Derivatives from Laurencia filiformis. Community :Importance of Herbivore Food Pref-
Australia nJourna o lCfhemistr y2,9:2533. erence and Alga lCompetitive Abilities .The Amer-
Kittredge ,J. S. ica nNaturalis t1,12:23-39.Lubchenco, J. L., and J. E. Cubit
1976.  Behavioral  Bioassays  and  Biologically  Active
Compounds. Jn H. H. Webber:and G. D. Ruggieri, 1980. Effects of Herbivores on Heteromorphology in
editors P, roceeding so tfh eFourt hConferenc eo nFood Som eMarin eAlgae E. cology 6, 1(3):676—687.
and Drugs from the Sea, pages 467-475. Marine McConnell, O. J., and W. Fenical
Technolog Syociety. 1976. Halogen Chemistry of the Red Alga Asparagopsis.
Kittredge, J. S., F. T. Takahashi, J. Lindsey, and R. Lasker Phytochem i1s6tr:y3,67.
1974. Chemical Signals in the Sea: Marine Allelochem- 1978. Ochtodene and Ochtodiol: Novel Polyhalogen-
ics and Evolution .Fishery Bulletin ,72(1):1-11. ated Cyclic Monoterpenes from the Red Seaweed,
Kriegstein, A. R., V. Castellucci, and E. R. Kandel Ochtode ssecundirame aJo. urn ao Olfrgan iCchemistry,
1974. Chemical Signals in the Sea: Marine Allelochem- 43:4238-4341.
ics and Evolution .Fishery Bulletin ,72(1):1-11. McEnroe, F. J., R. J. Robertson, and W. Fenical
Kriegstein, A. R., V. Castellucci, and E. R. Kandel 1977. Diterpenoid Synthesis in Brown Seaweeds of the
1974 .Metamorphosis o fAplysia californica in Laboratory Family  Dictyotaceae.  Jn  W.  Fenical  and  D.  J.
Culture .Proceeding so fthe Nationa lAcadem yo fSci- Faulkne re,ditor sM, arin eNatura Plroduct Cshemistry,
ence sU, SA 7,1(9):3654-3658. pages 179-189 .New York: Plenum Press.
Kylin ,H. McLachlan, J., and J. S. Craigie
1956 .Die Gattungen der Rhodophyceen .Frontispiece + xv 1964. Algal Inhibition by Yellow Ultraviolet-Absorbing
+ 660 pages. Lund: C.W.K. Gleerups. Substance fsrom Fucu vsestculosu sC.anadia nJournal
Larson, B. R., R. L. Vadas, and M. Keser o Bf otan y4,2:287-292.
1981. Feeding and Nutritional Ecology of the Sea Ur- MacNae W, .
ch Sintr,ongylocentro tdursobachiensis, in Maine, 1954. On Four Sacoglossan Molluscs New to South Af-
U.S.A. Marine Biology ,59:49-62. rica .Annale so fthe Nata lMuseum ,13:51-64.
430  SMITHSONIAN  CONTRIBUTIONS  TO  THE  MARINE  SCIENCES
Maiti, B. C., and R. H. Thomson Zn** by Brown Algal Polyphenols. Journal of Ex-
1977.  Caulerpin.  Jn  D.  J.  Faulkner  and  W.  H.  Fenical, periment aMl arin Beiolog ayn dEcolog y4,4:261—267
editors ,Marine Natura lProducts Chemistry ,pages Randall, J. E.
159-164. New York: Plenum Press. 1961.  Overgrazing  of  Algae  by  Herbivorous  Marine
Mathieson, A. C., R. A. Fralick, R. Burns, and W. Flashive Fishe sE.colog y4,2:812.
1975. Phycological Studies during Tektite II, at St. John 1967. Food Habits of Reef Fishes of the West Indies.
US  Vien  Ss)  A]  Earle  sande  Res  Lavenbers: Studie is nTropica Ol ceanograph y5,:655-897.
editors, Results of the Tektite Program: Coral Sammarco, P. W., J. S. Levinton, and J. C. Ogden
Ree fInvertebrates and Plants .Natura lHistory Mu- 1974. Grazing and Control of Coral Reef Community
seum L, o sAngele sCounty S, cienc eBulletin 2, 0:77-103. Structure by Diadema antillarum Philipp i(Echino-
Muller, C. H. dermata :Echinoidea) :A Preliminary Study ./Jour-
1970.  Phytotoxins as Plant Habitat  Variables.  Recent na ol  fMarine Research 3, 2:47-53.
Advance  iPsnhytochemistr y3,:106-121. Sieburth, J. McN.
Nunez, G., and L. M. Serpa Sanabria 1964. Antibacterial Substances Produced by Marine AI-
1975. Effectos producidos por extractos de algas marina gae D. evelopment si nIndustria Ml icrobiology 5, :124-
macroscopicas sobre el crecimiento bacteriano. 134.
Act aBiologi aVenezuela 9,(1):121-134. 1968. The Influence of Algal Antibiosis on the Ecology
Ogden, J. C. of Marine Microorganisms, Jn M. R. Droop, and
1976. Some Aspects of Herbivore-Plant Relationships on E .J .Ferguson Wood ,editors ,Advances in Microbi-
Caribbean Reefs and Seagrass Beds. Aquatic Bo- ology of the Sea ,pages 63-94 .New York: AcademicPress.
tan 2y,:103-116. Sims,  J.  J..  G-H.Y.  Lin,  and R.  M.  Wing
Ogden, J. C., R. A. Brown, and N. Salesky 1974. Elatol, a Halogenated Sesquiterpene Alcohol from
1973. Grazing by the Echinoid Diadema antillarum Phi- the Red Alga Laurencia elata .Tetrahedron Letters,
lippi: Formation of Halos around West Indian |1974:3487-3490.
Patch Reefs S. czence 1, 82:715-717. Stallard, M. O., and D. J. Faulkner |
Ogden, J. C., and P. S. Lobel 1974. Chemical Constituents of the Digestive Gland of
1978. The Role of Herbivorous Fishes and Urchins in the Sea Hare Aplysia californica, 1: Importance of
Cora lRee fCommunities .Environmenta lBiology of Die tC. omparativ eBiochemistr yan dPhysiology 4, 9B:
Fishe s3,(1):49-63. 25-36.
Ogino C, . Sun, H., and W. Fenical
1962.  Tannins  and  Vacuolar  Pigments.  Jn  R.  Lewin, 1979. Rhipocephenal and Rhipocephalin, Novel Linear
editor ,Physiology and Biochemistry o fAlgae ,pages Sesquiterpenoids from the Tropical Green Alga
437-443. New York: Academic Press, Inc. Rhipocephalu pshoeni xT.etrahedro Lnetter s1,979(8):
Olesen, P. E., A. Maretzki, and L. A. Almodovar 685-688.
1964.  An  Investigation  of  Antimicrobial  Substances Targett, N. M.
from Marine Algae .Botanica Marina ,6:224-232. 1979.  Gastropod  Tentacle  Withdrawal:  A  Screening
Paine, R. T., and R. L: Vadas Procedure for Biological Activity in Marine Mac-
1969.  Calorific  Values  of  Benthic  Marine  Algae  and roalgae B. otanic aMarina 2, 2:543-545.
Their Postulated Relationship to Invertebrate Targett, N. M., and A. Mitsui
Food Preference .Marine Biology 4, :79-86. 1979. Toxicity of Subtropical Marine Algae Using Fish
Paul, V., and W. Fenical Mortality  and  Red  Blood  Cell  Hemolysis  for
1980. ‘Toxic Acetylene Containing Lipids from the Red Bioassays J.ourna ol Pf hycology 1, 5:181-185.
Alga Liagora farinosa Lamouroux T. etrahedron Let- Taylor, D. L.
te r1s9,80(21):3327-3330. 1968. Chloroplasts as Symbiotic Organelles in the Diges-
Pfeffe rR, . tive Gland o fElysza viridis (Gastropoda :Opisthob-
1963 .The Digestion of Algae by Acanthurus sandricensis. ranchia) J.ourna ol fth eMarin eBiologica Al ssociation,
47 pages. Masters thesis, University of Hawaii, Unite Kdingdom 4,8:1-15.
Honolulu. Taylor, W. R.
Pratt,  RO  HH?  Mutner;  G;  ME  Gardner  Yo  shaandny: 1960 .Marine Algae o fthe Eastern Tropica land Sub-tropical
|  Dufrenoy Coasts of the Americas. ix + 870 pages. Ann Arbor:
1951. Report on Antibiotic Activity of Seaweed Extracts. University o fMichigan Press.
Journa o ltfh eAmerica nPharmaceutica Al ssociation 4,0: Thompson, T. E.
1960. Defensive Adaptations in Opisthobranchs. Journal
Ragan, M. A., C. M. Ragan, and A. Jensen o tfh eMarin eBiologica Al ssociation U, nite dKingdom,
1980. Natural Chelators in Seawater: Detoxification of 3 91:23-134.
NUMBER 12 431
iirench, R. K. Vadas, R. L., T. Fenchel, and J. C. Ogden
1975. Of “Leaves that Crawl”: Functional Chloroplasts In press. Ecologica lStudies on the Sea Urchin ,Lytechinus
in Animal Cells. Jn D. H. Jennings and D. L. Lee, ~ variegatus ,and the Algal-Seagrass Community of
editors ,Symbiosis ,page s229-265 .Cambridge Uni- the Mosquito Keys ,Nicaragua .Aquatic Botany.
vers iPtyress. Warmke, G. L., and L. R. Almodovar
Sisnda, Ro 1 and’ P. G. Bryan 1963. Some Associations of Marine Mollusks and Algae
1973 .Food Preferences of Juvenile Szganus rostratus and in Puerto Rico .Malacologia ,1(2):163-177.
S s. pinu sin Guam C. opeza 1, 973:604—606. Whittaker, R. H., and P. P. Feeny
Vadas,  R.  L.  . 1971. Allelochemics: Chemical Interactions between
1977. Preferential Feeding: An Optimization Strategy Specie Ss.czenc e1,71:757-770.
in Se aUrchins E. cologica Ml onographs 4, 7:337-371. Wratten, S. J., and D. J. Faulkner
1979. Seaweeds: An Overview—Ecological and _ Eco- 1977 .Metabolites of the Red Alga Laurencia subopposita.
nomi cImportance E. xperienta 3,5(4):429-432. Journa ol Of rgani cChemistry 4,3:3343.
Norris, James N. and Fenical, William. 1982. "Chemical Defense in Tropical
Marine Algae." The Atlantic Barrier Reef Ecosystem at Carrie Bow Cay, Belize 12, 
417–431. 
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