Table Of ContentReference: Bwl. Bull 187: 304-308. (December, 1994)
Temperature and the Larval Ecology of the Crown-of-
Thorns Acanthaster
Starfish, planci
LELAND G. JOHNSON1 AND RUSSELL C. BABCOCK2*
^Department ofBiology, Augustana College, Sioux Falls, South Dakota 57197, andAustralian
Institute ofMarineScience. Townsville, Queensland 4810. Australia
The recently reported dramatic population increases TwoseriesofoutbreaksofAcanthasterplancihavebeen
(outbreaks) ofthe coral-eating crown-of-thorns starfish. recorded on Australia's Great Barrier Reef(GBR) since
Acanthaster planci, which have damaged many reefs in the early 1960s, affecting reefs over approximately the
theIndo-Paciftc. areending(1), butquestionsremainabout central third of that system (12). Kenchington (13) hy-
thefactors that affect Acanthaster distribution and den- pothesized that outbreaks (termed primary) began some-
sities. Forexample, thenarrowtemperaturetolerance(26 where to the north ofGreen Island (Fig. 1), and in turn
or 27 to 30 or 3IC) reportedfor Acanthaster's larval initiated a cascade of additional outbreaks (termed sec-
development (2) isproblematicbecauseAcanthasteroccurs ondary)thatspread southwardasaresultoftheadvection
where temperatures do not rise into this range (3, 4). HV of larvae by southward-flowing currents during the
havefurtherexaminedsometemperature relationships in spawningseason. Recent data from broadscalepopulation
Acanthaster's early development. Cleavage proceeded surveys(1), geneticstudies(14), and hydrodynamic mod-
normallyovera rangeofabout 10 C, butspecificlimiting els (15, 16) support Kenchington's hypothesis, though
temperatures dependedupon thegeographicsourceofthe questions have been raised regarding some hydrodynamic
parents or their recent history oftemperature exposure. models (17).
Hatched, swimming gastrulae continued normal devel- Population outbreaks ofAcanthasteron theGBR have
opment to bipinnaria throughout a temperature range of occurredoversome 1000 kmofreef(6 degreesoflatitude).
13C. Theseresultsindicatethatthenarrowdevelopmental The main wave of outbreaks declined at around 20 S
temperaturetolerancesreportedearlierforAcanthasterdo (18), which lies to the south ofDavies Reef(Fig. 1); only
not apply toall earlydevelopmentalstages, andtheyadd a fewsmalleroutbreaks are now being recorded atthe far
tothelistoflarvaladaptationsthatcanfacilitatedispersal southern end of the system in the Swain complex (1).
ofAcanthaster larvae andpropagation ofoutbreaks. Lucas (2) has hypothesized that southern limits ofAcan-
Acanthasterplanci is one ofseveral Indo-Pacific aster- thaster's distribution may be dictated by larval tempera-
oids that prey on coral polyps (5). Unlike other tropical ture requirements. However, Acanthasteroccursin cooler
starfish, however,Acanthasterundergoesoccasional pop- waters near the limits ofhard coral distribution (3, 4, 7).
ulation outbreaks that have severely reduced coral cover Temporally variable aggregations ofAcanthasteral some
on many reefs overthe last 30 years. The causes ofthese Japanese sites appear to be derived entirely from settle-
outbreaks remain obscure despite much recent research ment of larvae carried by currents from warmer water
(6-8). The outbreaks may be natural phenomena with a areas(19),butatothercoolerwatersitestherearerelatively
long history ofoccurrence (9), or they may be relatively stable Acanthaster populations. For example, there is ev-
recent in origin, brought about as a result ofhuman ac- idence ofincreasing Acanthaster numbers at Lord Howe
tivities (10). A combination ofboth explanations is also Island (Fig. 1) (20). although the mean surfacewatertem-
possible (11). perature there duringJanuary, the warmest month ofthe
year, is about 24C, which is below the reported range
of developmental temperature tolerance. Population
Received 3 January 1994;accepted 3October 1994.
* PresentAddress:UniversityofAuckland,LeighMarineLaboratory, maintenancethereconceivablycoulddepend solely upon
P. O. Box 349, Warkworth, NewZealand. recruitment oflarvae carried by currents from the GBR,
304
TEMPERATURE AND ACANTHASTER LARVAE 305
Goise PeninsuIa a combination ofthe two (22-24). We conducted a lab-
oratory acclimation experiment to investigate a possible
parental acclimatization effect inAcanthaster. Agroupof
adults from Davies Reefwas separated into two samples.
One sample was held for 18 days at 31 C and the other
\ BA^IETR at25 C for21 days. We observed differencesbetween the
* offspring of25-acclimated animals and 31"-acclimated
animals in tolerance to lower temperatures (Table I) and
inearlycleavage rates(Fig. 2), which inotherechinoderms
Suiain Reefs are proportional to overall developmental rates at least
to the gastrula stage (25). The tolerance difference indi-
cates an acclimatory translation oftolerance range, but
more data at several temperatures would be needed to
determine if the observed rate difference resulted from
rotation ofthe rate: temperature curve.
We also examined possible parental effects due to sea-
sonal changein watertemperature inanimalsstudied im-
mediatelyaftercollectionatDaviesReefinOctober(tem-
perature at collection site: 25.5C) and in November
(temperature: 27C). Offspringofthe twogroupsdiffered
in their tolerance to high temperature. In October-col-
lected animals, development to early bipinnaria larvae
proceeded normally between 21 and 27C, but not at
32C. However, offspring ofNovember-collected animals
developed into normal bipinnaria at 32. This seasonal
change resembles those reported for other echinoderms
Figure 1. Mapshowingcollectionsitesandotherlocationsmentioned
(26, 27).
in thetext.
Thus early developmental temperature tolerances in
Acanthaster vary with recent parental temperature ex-
posure as well asgeographic source. However, our results
but the Lord Howe Island population is genetically di- do not distinguish the relative contributions made by
vergent from GBR populations (21), and gene flow into
GBR
it from the appears to be very limited, indicating a
relatively isolated, locally reproducing population. Such Table I
evidence of successful reproduction under diverse envi-
ronmental temperature regimes and genetic evidence for Development otembryosfrom each ofjourgroupsatlowexperimental
temperatures
long-distance larval transport (14) suggest complexity in
Acanthaster's developmental temperature relationships.
Zygote to Bipinn.
We have investigated both thedevelopmental temperature
tolerances ofoffspring ofgeographically widely separated
groups ofAcanthaster and the effects ofexperimentally
altering temperature exposures ofadult, embryonic, and
larval starfish.
Offspring ofanimals collected offthe Gove Peninsula
near Nhulunbuy and at Davies Reefin the GBR (Fig. 1)
completed development to bipinnaria larvae equally well
at 31, 27, and 24C. At 22.3 and 21C, Davies Reef
embryos produced normal bipinnariae (Table I). At the
sametemperatures, someGoveembryoshatched, butthey
ceased development as abnormal early gastrulae.
Such geographic differences in developmental temper-
ature tolerance may be due to genetic differentiation of
separated populations, physiological acclimatization ef-
fects reflecting recent parental temperature exposure, or
306 L. G. JOHNSON AND R. C. BABCOCK
Table II
Resultsofgastrulatransferexperiments with Gaveembryos
Percent Bipinn.
Transfergroup Days development
31 to 31 (Control) 2 93
31 to 21 5 88
31 to 18 17 81
Onlyswimming, newlyhatched,earlygastrulaeweretransferred.The
numbersofdaysfromtransfertofinalobservationaregiven.Comparable
resultswereobtained followingtransfersofembryosthatdeveloped from
fertilization to hatchingat 27C.
o
development (Fig. 4), indicating that Acanthaster's dis-
tribution and abundance need not be as limited by de-
velopmental temperature as previously thought. Clearly,
temperature relationships in later larval stages should be
100
Figure 2. Cleavage ratecomparisonsat27C. Foreachgroup,four
replicateculturesin 20-ml scintillation vials(mean no. ofembryos per
vial=99)werefixedafter 146 min.Embryosineachculturewerecounted
andscored forcleavagescompleted. Barsrepresent meansofindividual
culture means, with standard errors. Because ANOVA indicated a sig-
nificanttreatmenteffect, theTukey test wasapplied. The mean forthe
31- acclimated group differs significantly from the other means (
= 0.05). whichdo notdifferfrom oneanother.
population genetic differentiation and physiological ac-
climatization to the observed geographic variations.
Because ofitsimportance fordispersal, thetemperature
tolerance of newly hatched swimming embryos was ex-
amined. Early gastrulae from cultures ofGove embryos
8C
weretransferredto 21 and 1 (temperatures at which
Goveembryoscannot cleave normally). Transferred em-
bryos continued to swim, completed gastrulation, and
producedbipinnariaeatbothtemperatures(TableII). This
unexpectedly broad temperature tolerance in gastrula-
stageembryosprompted additional transferexperiments.
Newly hatched Davies Reefgastrulaetransferred from 27
tmoal18(F.ig5.C3)d.evEevleonpegdastirnutloabeitpriannnsafreirareedthfartomap2p7earteod1n5orC- dtruarFniisngfgeurrseDew3ec.reembGaasesrdtersu1c9lr9ai2b.terdaEnaisnrfleTyrabedlxeepveeIIrl.ioBmpaemrnestnsrtewpiprterhsoecnDetaevdmieeedasnaRtpeee2rf7ceCann,tiamgaaenlsd,s
and held there for 6 days continued to swim actively, with standard errors, ofbipinnaria development for 12 cultures (40 to
slowly continued archenteron extension, and then quickly 100embryosineach)fromtwoexperiments."27-27"representscontrols;
ctoom2p7leCt.eHdobwiepvienrn,artihaesmeolraprhvoageecnoenstiasinaefdtecrlturmapnssfoerfebxatcrka a"12n57dC-.1"82B.7i5-p"1i5nr-ne2apr7ri"easeerneitpnsrettshreiasnntslsfategtraersatngrrduloacueopnrwteietnruuerinnnegodrdmteaovle2li7onpCsmheaanpfttee,rabt6utId8amy.as5nCay;t
mesenchyme-like cells. contained clumps ofextra mesenchyme-like cells. Embryos that were
In summary, data presented here support a modified notreturnedfrom 15 to27Cshowedsomearchenteronextension,but
concept oftemperaturetoleranceduringearlyAcanthaster eventually regressed anddied.
TEMPERATURE AND ACANTHASTER LARVAE 307
dispersal of larvae and the propagation ofAcanthaster
outbreaks.
o 29
"
Acknowledgments
1
2 25 Thisworkwasfunded bytheGreat Barrier ReefMarine
|
5E 23 Park Authority through the Crown-of-Thorns Starfish
21 Research Committee. We thank C. Cartwright, K. Hall,
19 and D. Whitehead fortechnical assistance, P. Moran and
C. Mundy for discussion and advice, J. Quam for map
preparation, and C. Christie forcollectingAcanthasterat
Nhulunbuy.
i
1
Literature Cited
1. Moran, P. J., G. De'ath, V. J. Baker, D. K. Bass, C. A. Christie,
I. R. Miller, B. A. Miller-Smith, and A. A. Thompson.
31 1992. Patternofoutbreaksofcrown-of-thornsstarfishlAcanthasier
O 29 plunci L.) along the Great Barrier reef. Pp. 555-568 in Crown-of-
a 27 ThornsStarfishontheGreatBarrierReef:Reproduction, Recruitment
3 andHydrodynamics, C.Johnson,ed.Aust.J.Mar.FreshwaterRes
5 25
43(3).
23 2. Lucas,J.S. 1973. ReproductiveandlarvalbiologyofAcanthaster
a
K planciingreat Barrier Reefwaters. Micronesica9: 197-203.
21 3. Yamaguchi, M. 1973. Early life histories ofcoral reefasteroids,
19 with special reference to Acanthasterplanci (L.). Pp. 369-387 in
Bmlogy and Geology ofCoral Reefs, \'ol 2. O. A. Jones and R.
Endean,eds. Academic Press, New York.
4. Mcknight, D. G. 1978. Acanthosierplanci (Linnaeus)(Asteroidea:
Echinodermata)attheKermedecIslands.N.Z.Oceanogr.lust Rei:
4: 17-19.
5. Birkeland, C. 1989. The influence ofechinoderms on coral-reef
communities. Pp. 1-79in EchinodermStudies. I'ol. 3, M.Jangoux
Figure 4. Conceptual models ofcrown-of-thorns starfish develop- andJ. M. Lawrence,eds. A. A. Balkema, Rotterdam.
mental temperature tolerances. The upper model is one inferred from 6. Zann, L. P.,and P.J.Moran. 1988.Acoordinatedresearchprogram
dataofLucas(2)whotransferred embryosat hatchingand maintained on theAcanlhastcr phenomenon. Pp. 177-182 in Proc. Sixth Int.
culturesuntil settlingand metamorphosis. Thelowermodel retainsthe CoralReefSymp. \'ol. 2.
limitedtemperaturetolerances(dottedlines)reportedby Lucasforlater Birkeland, C. and J. S. Lucas. 1990. Acanthasterplanci: Major
larva] stages, but incorporates the broader tolerances (dashed lines) of ManagementProblemofCoralReefs. CRCPress, BocaRaton. FL.
earlierdevelopmental stagesindicatedbyourdata.Ourdataalsoindicate Johnson,C.,ed. 1992. Crown-of-ThornsStarfishontheGreatBar-
that actual limitingtemperatures, but not necessarily size, oftolerance rierReef:Reproduction, Recruitment andHydrodynamics. Aust. J.
ranges vary with recent parental temperature exposure as well as geo- Mar. FreshwaterRes. 43(3).
graphicsource. Walbran, P. D., R. A. Henderson, A. J. T. Jull, and M. J. Head.
1989. Evidence from sediments oflong-term Acanthasterplanci
predationoncoralsoftheGreatBarrierreef.Science245:847-850.
10 Cameron,A.M.,R.Endean,andL.M.DeVantier. 1991. Predation
reexamined, especially forpopulations at theextremes of on massive corals: Are devastating population outbreaks of.Acan-
Acanthaster's distribution. Further, the temperature tol- thasterplancinovel events?Mar. Ecol. Prog Ser. 75: 251-258.
erance ofAcanthastergastrulae addsto a list oftraitsthat I I sMtoarrfainsh,cPo.ntJr.o,vearnsdy.RS.eaIIr.chBr2a0d:b3u-r6y.. 1989. The crown-of-thorns
make Acanthaster larvae particularly well adapted for Reichelt, R. F,., R. H. Bradbury, and P. J. Moran.
long-distancedispersal. Even larvaeswept intocoolerwa- 1990. Distribution ofAcanthasterplancioutbreakson the Great
tercould very slowly continue normal development dur- BarrierReefbetween 1966and 1989. CoralReefs9: 97-103.
tihneg ltroawnspphoyrtt.opTlhainsk,toanlocnogncweintthratthieoanbsilcitoymtmoodnevienlotrpopa-t 13 pk1le1u8nn.cchiin(gL.t)ono,nRt.heA.Gr1e9a77t.BarGrrieorwtRehefa.ndBirole.crCuointsmeernvtaotfiAocnan11t:ha1s0t3e-r
ical waters(28. 29)and the negativelygeotropicswimming 14 Benzie, J. A. H., and J. A. Stoddart. 1992. Genetic structure of
behaviorcharacteristic ofAcanthastergastrula (3), would outbreaking and non-outbreaking crown-of-thorns starfish (Acan-
allow transport to distant reef sites with conditions ap- thasterplanci) populations on the Great Barrier Reef. Mar. Biol.
112: 119-130.
cpersospersiatthaetfmoraylatbeerlleasrsvraelsidsetvanetltoopemnevnitroannmdensettatllivnagriaptrioon- 15. Jcaormreesl,atMio.nkw.i,tahndthJe.cPr.oSwcna-nodfo-lt.ho1r9n9s2.starLfiasrhvaolutdbisrpeearkssaldastiambualsaet.ioPnps.:
(2). Early larval hardiness may facilitate both the routine 569-582 in Crown-of-Thorns Starfish on the Great Barrier Reef:
308 L. G. JOHNSON AND R. C. BABCOCK
Reproduction, Recruitment and Hydrodynamics. C. Johnson, ed. 23. Tester, P. A. 1985. Effects ofparental acclimation temperature
Anst. J .Mar. FreshwaterRes 43(3). and egg-incubation temperature on egg-hatching time in Acartia
16. Scandol, J. P., and M. K. James. 1992. Hydrodynamics and lonsii(Copepoda: Calanoida). Alar. Biol 89: 45-53.
larvaldispersal:apopulation modelofAcanthasterplancionthe 24. Johnson, L.G. 1993. Temperaturetolerance, temperature stress,
GreatBarrierReef. Pp. 583-596 in Crown-of-ThornsStarfishon andanimaldevelopment. Pp. 37-40inProceedingsoftheBiostress
the Great Barrier Reef: Reproduction, Recruitment andHydro- Symposia N. H.Granholm,ed. South DakotaStateUniv., Brook-
dynamics.C. Johnson, ed. Anst. J Mar. FreshwaterRes. 43(3).
ings.
17. Wolanski,E.1993. Factsandnumericalartefactsinmodellingthe 25. Fujisawa, H. 1989. Differencesintemperaturedependenceofearly
dispersalofcrown-of-thomsstarfish larvaein theGreat EarnerReef. development ofsea urchins with different growing seasons. Biol.
Ausl. J Mar. FreshwaterRes 44: 427-436. Bull 176:96-102.
18. Moran,P.J. 1986. TheAcanthasterphenomenon. Oceanogr.Mar. 26. O'Connor, C., and J. C. Mulley. 1977. Temperature effects on
19. YBiaomlagAuncmhii.,RMe.v19284:7.379O-c4c8u0r.rencesandpersistencyofAcanthaster periodicity and embryology, with observations on the population
20. paDlleaoVnnacgnittiphesere,PuadcLoi.-fpiMco.pc,uolaaasnttdioofnG.JianpDaernae.cloattn.i.loanla1.9t\o9e0ao.6c:ea2Dn7io7sgt-rr2ai8pb8uh.tiiconcoonfdiAtciaonn-s 27. gAHteeinriesittaicacidsi,ilulnsor,feS1t.2h:e199a97q5-u.1a1c4u.Altunroatle oenchtihneoiedffeHcet/ioofctideamrpiesrattuubreercounlatsae.a
thasterplanciatLord HoweIsland,thesouthern-most Indo-Pacific urchin eggs. E.v/i Alar. Biol Ecol 18: 239-242.
reef. CoralReefs9: 145-148. 28. Olson,R.R. 1987. //;situcultunngasatestofthelarvalstarvation
21. Benzie, J. A. H., and J. A. Stoddart. 1992. Genetic structure of hypothesis for the crown-of-thorns starfish. Acanthaster planci.
crown-of-thornsstarfish(Acanlhasterplanci)in Australia. Mar Biol. Limnol Oceanogr. 32: 895-904.
112:631-639. 29. Ayukai,T. 1994. Ingestionofultraplankton bytheplanktoniclarvae
22. Moore,J.A. 1949. Geographaphicvariationofadaptivecharacters ofthecrown-of-thornsstarfish, Acanthasterplanci. Biol Bull 186:
in RanapipiensSchreher. Evolution3: 1-24. 90-100.
