Release of allelochemicals by three tropical sponges (Demospongiae) and their toxic effect on coral substrate competitors

7 Pages·1999·2.5 MB·

by  G K Nishiyama

RELEASE Ob ALLLLoaiLMICALS BY KREE TROPICAL SPONGES
MOSPONOIAE) AND THEIR TOXIC EFFiECTS ON CORAL SUBSTRATE
s I >\ COMPETITORS
GREGORY K. NISHIYAMA AND GERALD h &AKI !S
Nishiyama. G.K. & Bakus, G.J. 1999 06 30: Release ofallelochemicals by three tropical
sponges(Dernospongiae) and their toxic ei'fecison coral sub rate coropetltotv 1/
riw Queensland Museum 44: 411-417. Brisbane- ISSN 0079^8835.
three sponge species (Xcytospottgia. Accnwlutlina, Plakortis spp.) from Maclan L
Philippines, were shown U,- release allelochemicals directly into the water. These
;! 4i!tep!oopacrhte*m*icFdolisiwHco-proeraJ,,iPmonitesi.;is,p.p'..),anI d.fcfOoJCr*on\e0oofntheIstptrtOifnlgeSsCtleesrtaecdt,intioanonceorhalvdsmpzecoiaens
coral [Millepora sp.j. The five coral species tested (including Montiporo) were both
numerically EUld Spatiall) dominant i . the Stud} site. Toxicity teats involved
exposing carats brought into the laboratory to water that had been conditioned by the
sponges. Responses o\' each coral species to each spi biochemical varied. The
allclOf Ilerpical froitl 4tierVbckdIinU was fouiMl to be highly toxic {51-75% tissue death) to
both Pocillopwa and icwporfe and had only a moderate efteel (26-50°.. tissue death) Ofl
Paeites. Allelochemicals ofXostospoi rtis were moderately and weakly toxic
( 1 1-25% tissuedeath) to Millepors, respectively. Neilhei spongewastexictowardsflieo
ll SpeOieS. IfOfittpOr*^ Was not affected by allelochemicals liom anyojthesponges, Dead
eora] wasnotedinmanyposition:;around the sportges in the Held, but mainls inthedirection
i 11!rent Thisanuhi support,althoughnotconlinn,ana)lelopathieeffect.Theinfluence
ofallelochemicals on the ma)l scale and large scalfi Spfl I coral reel
discussed. Ll Porlfera, coral:.. pllelocJiewjtXil cofal
PMitippities,Xe&to&pongfu Icervoehatina, >' bom
".,. '
GrqgpiyK Vis ...;.' .,.',, I nld£ Bakux, Departmentoj
Biological Science diversity ofSouthern Ccdffartii lo CA, 9006
i s
1 \:%February T9Q9,
Release ofallelochemicals into the surround- necrosis was observed in all eontact pairs. Only
ing water, as a defense against benthic spatial one speciesofsoftcoral producedtissuenecrosis
competitors, fouling organisms, or micro- when placed near, but not in contact with, the
organisms, has been demonstrated in several other two species ofsoli coral. They suggested
groups of marine organisms (see Bakus et al, that avoidance behavior, such as those causedby
1986), These organisms include sponges allelopathy, may contribute to the dispersion
(Thompson. 1985; WalkeretaL, 19*5; Porter & patternsofplantsandanimals inspace-inanother
TargetL 1988; Tardea, 1988;Bingham & Youne, study on soft corals, Sammarco et al (1985)
1991), soft corals (Coll & Sammarco, 1983; found that seleractmian corals varied in their
Sammarco et al.. 1983, 1985: La Barre et al.., susceptibility when exposed to soft corals in both
1986; Maida et al., 1995), an anemone (Bak & contact and non-contact conditions.
&
Borsboom, 1984). possibly an alga (Littler &
Littler, 1997) and hard corals (Fearon, 1997; Porter Targett (1988) demonstraled that the
Koh, 1997). Although only few studies have yet spongePlakortishulkhondroideswascapable11f
been undertaken, allelochemicals are believed lo damaging ordestroying tissue inall coralspecies
play a role in structuring particular marine examined, with almost half the corals growing
habitats (Jackson & Buss, 1975; Davis ct al.. na'tirally in contact with, or near to, these
1989; Turon et aL 1996; Thacker ct al.. 1998). sponges experiencing bleaching or tissue
whereas the magnitude of this role is still necrosis. It was suggested that by creating dead
uncertain, zones on the corals P. hciluho/iclruuk:s was
subsequently able io overgrow them. In a more
La Banc ct al. (1986} demonstrated thai when recent study, Turon ct al (1996) suggested that
threespeciesofsoftcoralswererelocatedinpairs Crambcc/runbecould havean impacton adjacent
under contact and non-contact conditions, tissue organisms by possibly releasing allelochemicals
1
412 MEMOIRS OF THE QUEENSLAND MUSEUM
into the surrounding water. The allelochemical in the vicinity ofthe study site ranged from 5m,
effect ofthis sponge was at the small scale level where a seagrass bed began, to 15m, which
(centimeters)(Turonetal., 1996),wherepatterns borderedthestartofasteepslope.However,most
suchasanincreaseintheamountofdeadcoral or ofthe experiments conducted in this study were
m
tolerantspecies foundadjacenttotheproducerof located between 8-1 1 depth. The study was
allelochemicals became evident. Turon et al. conductedinMayandJune, 1996. (Foradetailed
(1996) suggestedthatatdifferentscales different description and map of the site see Bakus &
patterns might be recognised. On previous trips Nishiyama, 1999, this volume). Species of
to the Philippines we observed similar bleached sponges included: Xestospongia sp.
areas or dead zones up to 1cm in width in areas (Haplosclerida: Petrosiidae), Acervochalina sp.
where some ofthe species of sponges came in (Haplosclerida: Chalinidae), and Plakortis sp.
contact, or close contact, with coral species. (Homosclerophorida: Plakinidae), and the
The purpose of the present study was to: 1) corals:Acroporasp.(Scleractinia:Acroporidae),
Determineifthreetropicalspongeswerereleasing Millepora sp. (Milleporina: Milleporidae),
allelochemicals potentially toxic to five hard Montipora sp. (Scleractinia: Acroporidae),
corals on a coral reef; 2) Identify patterns due to Pocilloporasp. (Scleractinia: Pocilloporidae) and
allelochemical effects, such as the presence or Porites sp. (Scleractinia: Poritidae).
absenceofdeadspaceadjacenttosponges(given
ALLELOCHEMICAL DETECTION AND
that sponges releasing toxic allelochemicals
would have a preponderance for dead coral, or ISOLATION. To determine if sponges were
tolerantspeciesadjacenttothem,andthesemight releasing chemicals into the water, an allelo-
be predominantly located in the direction where chemical collecting apparatus was constructed
theallelochemicalsweremostconcentrated),and fromabatteryoperatedbilgepumpandSEPpaks
3) Determineifthe allelochemicals weretoxicto (Fig. 1).Thisapparatuswasamodifiedversionof
common substrate competitors. one used by Coll et al. (1982), and later by
Schulte et al. (1991). The battery operated bilge
MATERIALS AND METHODS pump was fitted at its outflow hose with a step-
down tubing connector (2cm to 0.7cm), which
Our study site was located on a limestone reef allowedtwoplastic screwvalvestobeconnected
approximately0.25km offtheTambuli Resorton (diameter 0.7cm). C18 SEP paks were initially
MactanI.,Philippines.Thestudysitewaschosen conditionedbypassing 10mlofEtohfollowedby
onthebasisofitshighmarinediversityandclose 10ml ofdeionised water through each SEP pak
proximity to the Maribago Marine Station, using a plastic pipette. Conditioning SEP paks
operatedbytheUniversityofSanCarlos. Depths before use was critical, otherwise flowwouldbe
Plastic Container
Outflow Hose
— SEP pak
\ S
\ 1
r^
Pump
Bilge
Sponge
FIG. 1. Allelochemical isolatingapparatus used to isolate allelochemicals from sponges.
TROPICAL SPONGE ALLELOCHEMICALS
41
interrupted.Insitu,oneconditionedSEPpakwas to, or within approximately 5cm from, sponges
inserted into each end ofthe plastic screw valve. were investigated by first taking photographs of
Attheinflow endofthepump,aplasticcollapsible between 29-39 individuals ofeach species and
container (20x30x50cm) was attached which had theiradjacentorganismsinsituwithaNikonos V
a large hole cut at the bottom (diameters camera. A scale bar with a waterproofcompass
20x30cm; Fig. 1). The purpose ofthe container attached to it was laid parallel tothe direction of
wasto assist in concentrating allelochemicals to thecurrentandplacednexttoeachspongebefore
increase probability ofdetection. Once the SEP photographs were taken. Sponges in each photo-
paks were attached, the apparatus was placed graph were divided into four quadrants and the
overthesponge,withthespongeprotrudinginto, presence or absence ofdead coral in each quad-
butnot touching, the plastic container. Although rant was recorded. The widths ofthe dead zones
flow rate was determined both at sea level and oncoralsranged from t-lOmm. Sevencategories
10m depth by allowing the output water to flow were devised to quantify the positions of dead
into an empty container for 30mins, no flow coral: 1) Horizontal: dead coral only on two
meter continuously measured flow rates in this quadrants that faced currents (roughly in the E
W
initial model. Water surrounding eight and positions); 2)Vertical: dead coral in two
unidentified sponges was sampled for 1.5hrs, quadrants perpendicular to the current (roughly
coinciding with the maximum continuous in the N and S directions); 3) Dead coral found
run-time forthepumps. Acontrolapparatus was more in horizontal than vertical positions; 4)
set-up approximately 0.5m upstream from each Half-half: dead coral found equally in horizontal
apparatus covering a sponge. A newer model is and vertical positions; 5) More dead coral in
currently being constructed with a flow meter vertical than horizontal positions; 6) Dead coral
and an added battery included for longer run foundcompletelyaroundthesponge;and7)Only
timesandcontinuousmonitoring. Eightdifferent live organisms completely surrounding the
sponge species were sampled at the study site sponge.
using this apparatus to detect the release ofany
TOXICITY OF ALLELOCHEMICALS ON
allelochemicals. After each run, the SEP paks
and the whole sponge specimens being sampled HARD CORALS. Fifty pieces (approximately
were immediately sealed separately in small 3-4cm long) from each oftwo individuals ofthe
plastic bags, and upon arrival to the laboratory five coral species were obtained at the study site
(not more than 20mins later), were placed in a using a geological pick, and placed in separate
freezer (-5°C). Upon departure from the plastic bags foreach coral species. These plastic
Philippines the SEP paks and sponge specimens bags were then placed into buckets to ensure
were placed in dry ice, and upon arrival in the minima] mechanical stress during transport.
USA the items were placed into a deep freezer Sponges were removed from the substrate by
(-20°C). Chemicals were initially eluted out by chiselling around each sponge and carefully
passing 20ml of dichloromethane, followed by removing them. Sponges were then positioned
20mlofEtohthroughSEPpaks.Extractionswere and left on dead coral for one week to allowr
air evaporated for approximately 24hrs. It was recuperation following their removal. When
subsequently discovered that extraction with ready for use, two whole sponges ofeach ofthe
50ml acetone produced higher extractionyields. three sponge species were placed in separate
Thereafter, only acetone extractions wrere used. plasticbags. Carewastakentominimisedamage
Thin layer chromatographies (TLC) were when removing and transporting corals and
conducted using acetone as the mobile phase sponges. Both were returned to the laboratory
throughout the extraction process to insure that and sponges were immediately placed in a 1L
chemicals were not lost during the evaporation beakerfilledwithfilteredseawaterobtainedfrom
TLCs were visualised using both long and short. the study site (ambient water, gravity filtered
UV light. There was no noticeable changes in with a#1 Whatman filter). Corals wereplaced in
chemical composition ofthe extract within this separate plastic buckets with unfiltered seawater
period. TLCs were run on SEP pak extracts, from the site until ready for use. Sponges were
control SEP paks, and whole sponge extracts allowed to condition the water for 1hrbefore the
(5grnsamplesofeachspongespeciesextractedin water was passed through a Whatman #1 filter
and gravity filtered. This filtration process
acetone).
requiredlessthan30mins.Twospongeindividuals
SMALL SCALE PATTERNS AROUND from each species were allowed to condition
SPONGES.Patternsoforganismsfoundadjacent waterseparately to test for individual variability
414 MEMOIRS OF THE QUEENSLAND MUSEUM
situ and after the corals were returned to the
laboratory. These photographs were enlarged
(approximately 200%), and the area oF the
exposedsurface ofeachpieceofcoral, aswell as
the area ofdead tissue, traced onto acetate. The
jtospongiasp.
percentage ofdead tissue was determined after
estimating the total area ofeach coral fragment
and the area of dead tissue, using an image
CO analysisprogram(SigmaScan[SPSSlnc], 1998).
CD
oc> f-1 1 DetailednotesandsketchesofeachpieceoFcoral
oQ. in situ were made earlier and were compared to
CO the calculated dead tissue areas. In all instances
PUikartissp.
*o both estimates were comparable. Coral tissue
d
was consideredto be dead ordying iFtherewere
J
signs of cell death or, as in most cases, actual
detachmentoftissue from the skeletalbase. Loss
j^ ofcolorationwasalsoobservedinalldeadtissue.
1 One-wayANOVAandposthocTukeytestswere
conducted onthepercentagetissuedeathofeach
Aiwvochal'musp coral species,withtheallelochemicalandcontrol
treatments being the main factor.
1 RESULTS
_u
>-r Ofthe eight unidentiFied sponges sampled for
allelochemical release at our study site, three
Dead Space Positions were shown to be releasing allelochemicals.
These species were subsequently identified as
Acervochalina, Plakortis,andXestospongiaspp.
TLC comparisons between water immediately
surrounding these three sponges, control water
FIG.2. Positionsofdeadspace foundaround sponges
from Mactan Island, Philippines. (See text for samples, and whole sponge extracts conFirmed
detaileddescriptions ofcategories). that allelochemicals were Found within the
respective sponges but not in the water column
towards allelochemical toxicity. While this upstream from the sponges.
Filtration process was carried out, corals were The presence and position oF dead space
placed in glass Fingerbowls alongwith 100ml of adjacent to the the species oFsponges occurred
ambient water. When sponge-conditioned water predominantly in the direction Facing (either
wasready,waterinFingerbowlswasdecantedoff partially orcompletely)the currentflow(Fig. 2).
and replaced with an equal volume of Since the direction ofwater flow was reversed
sponge-conditionedwater.Acontroltreatmentof periodically, depending on whether the tide was
1Eofnon-conditioned.Filteredseawaterwasalso rising or falling, dead space occurred on both
initially setaside For Ihr. TheconditionoFcorals sides of the sponge facing these currents. In
and water temperature were noted. Corals were Xestospongia dead space occurred in horizontal
exposed to conditioned and control water positions (i.e. facing currents) and positions
experiments For 24hrs. A change in temperature mostly facingcurrentflowsin71%ofspecimens
from 25°C to 22°C was recorded forthe waterin (Fig. 2). Deadspacewaslocatedinthesepositions
the bowls. The ambient watertemperature at the in 73% ofPlakortis, and 66% ofAcervochalina.
study siteduringthe experimentwas27°C. After In no instance for any of the three species of
this 24hr period, corals were returned to their spongeswasdeadspacefoundonlyinthevertical
original site of collection and placed under a position (i.e. not facing current flow).
metal cage (5x30x100cm; mesh size approx. Water conditioned individually by each ofthe
Icm). The condition of coral fragments was threespeciesofspongeswastoxictooneormore
monitored For 4 days thereafter. Following this oftheFivecoralspeciestested(Fig.3).Responses
period,close-upphotographsweretaken, both in oF each coral species towards each sponge
c
TROPICA SPONGE ALLELOCHEMICALS 415
I
DISCUSSII
Results show that filtered
water conditioned by all three
species of sponges. Xestospongia,
PlakotUS and AccrvQchalinu. were
&ft
- toxic to at least one species ofhard
coral {Piuiics, Poclllnp<
Wamipoiimp Acroporaand Mitlepom),Responses
of corals towards sponge-condit-
ioned water varied, as expected.
l\>\-ltit>}'fTUIf), ^ Suscept^ibility of corals in contact
r^ with, in proximity to sponges
suggests the possibility that sponge
^ a11elochemicals may influenc
^' patterns of distributions of organ-
isms adjacent to sponges. In other
MiJlrpunit/l words, certain tolerant: species of
corals may grow adjacent to
I sponges, whereas others may never
X iu& or rarely be found in close
proximity
hiaparallelstudy weconductedat
^
our study site, whole sponges were
H transplanted and placed into direct
contact with corals. We determined
that several species of corals were
highly susceptible to (i.e. damaged
FIG 3. Average percentagetissuedeath offive coral speciesex] by) several .species of sponges.
towaterconditionedb>threespongespecies(Key: 1=-Xsstospongia\ Under natural conditions, these
2=Plakorti$\ 3= [cervochaima\ C - control treatments, representing .orals were rarely found growing in
corals exposed to filtered scawaier). (Bar represents I S.F.t. direct contact with these Sponges
(Nishiyama & Bakus, unpublished
allelochemieal varied. Control corals exper- information). In rare cases where they did grow
ienced minimal tissue death, but not always less naturally adjacent to these sponges, a zone of
dealhthanall theOthertreatments(Fig. 3). Forall dead orbleached tissuewasoftennotedatthe site
coral species, except Mtmtipora, significant ofcontact. Furthermore, ifa species of sponge
differences existed among the treatments (one- was not found to be deleterious to a species of
way A.NOVA). Results of the Tukey tests and coral, incidences of growth with direct contaei
average percentage coral tissue death show that between the two species were more often noted.
whencomparedtocontrols, theallelochemical of TPhoritserco&rreTsaprognetd!s (to19f8i8e)ldwohbesrerevaatlimoonsstmhaadlfetbhye
Acen'ochalina was highly toxic (51-75% tissue COrals growingnext toPlakortiShalichondruulcs
death) to Pocillopora (P<0.05) and Acropora experienced bleaching or tissue necrosis. Both
(P<0.05), and had a moderate effect (26-50% these studies support our hypothesis that water
tissuedeath)towardsPoritcs P<0.0S)Thesponge borne allclochenneak may deter particular
I
was not toxie towards MiI!cj>ora. XestQSpongia substrate competitors from growing in direct
and PlakortLs were moderately (26-50% tissue contact with sponges. It should be cautioned,
death; PO.05) and weakly toxic [-25% tissue however, that laboratory bioassays using sponge-
death) iP-0.05) to MUleporq^( Irespectively, conditioned water were conducted on corals in
still water, whereas in nature currents probably
Neuhei sponge wastoxic towardsthe othercoral have a major influence in dissipating
species. Montipora was not affected by allelochemicals, and thus, their physiological
allelochcmieals from any of the sponges impact may notbe asextensive as those observed
(PXl.05). in the laboratory
416 MEMOIRS OF THE QUEENSLAND MUSEUM
Although particular sponges may have an beingreleasedbysponges. They determined thai
impact on adult corals, these toxic effects may Crambecrcunhehadtoxiceffects upto 1cm from
also have a greater impact in preventing coral particular coral substrate competitors, corresp-
larvae settling adjacent to sponges. The occur- onding to the effective distance of
renceofdeadcoralspacearoundsponges,mainly allelochemicals suggested in the present study.
in the direction facing currents, may reflect the Turon et a!. (1996) also suggested that these
directions that highest alielochemical concen- small scale effects might only be detected by
trations occur given that toxins are carried away sampling at a small scale (centimeters), whereas
from sponges. Although only suggestive, this sampling at 3cm intervals produced a different
supports the notion that toxic allelochemicals outcome. Where allelochemicals have effective
were being released by sponges. Maida et al. distancesatascaleoflessthan 1cm,observations
(1995) provided evidence to suggest that a soft madeat 1em intervalsmaynotsufficeindetecting
coral could influence the direction from which these chemical interactions. In the present study.
recruitment occurred. An alternative hypothesis extreme care was taken to accurately determine
is thai some hydrodynamic effect prevents dead space and organisms adjacent to sponges,
settlementoflarvaeinareasfacingthecurrent. It and in most cases, measurements were deter-
may also be advantageous for a sponge to mined to the nearest millimeter.
encourageadjacentsettlementandgrowthofcoral The chemical nature of allelochemicals
species which are susceptible to the sponges' released by sponges, as measured by SEP paks,
allelochemicals. This would ensure that the are currently being ascertained, as are the toxic-
spongewouldbeabletogrowandexpandintothe ities ofthese isolated chemicals towardsthe five
adjacent area. species of corals. Although SEP paks retained
Through their release of allelochemicals chemicals released by sponges, this does not
sponges may stop the growth ofadjacent, adult necessarily confirm any toxicity by the sponge.
substrate competitors, such as corais. However, Only isolation of the active chemicals from
this effect may operate only on a local or small spongesandverificationoftheirtoxicitytowards
scale, at least for the three species of sponges corals would confirm that these are allelo-
investigated here, because zones of dead or chemicalsdeleterioustocorals. Datafromanother
bleachedtissueon coralsgrowingadjacenttothe studyconductedbytheauthorsarecurrentlybeing
threespeciesofspongesextendedforonly 1emat analyzed (Nishiyama & Bakus, unpublished
most. Acen'ochalina, however, mayalso possibly data), involving the deterrence ofsettlement of
overgrowcorals,withanobservedhighdensityin substrate competitors by sponges placed next to
comparison to the other two species, generally plates kept in the water at the site for approx-
having the highest toxicity towards corals, and imately one month.
being thinly encrusting with possibly greater After hard corals, sponges were the dominant
lateral growth.Acervochalina was also observed organisms at Mactan I. (Bakus & Nishiyama,
growing on branches ofcorals that were dead at 1999, this volume), also showing relatively high
thebases(wherethe spongesoccupied),yet alive diversity(Bakus&Nishiyama, unpublisheddata).
atthetips(wherethespongehadnotyetextended). Of eight sponges investigated, three released
AllelochemicalsofAcervochalinamay operateto allelochemicals into the water column, suggest-
stop corals from overgrowing it and as a mech- ing that many more sponges, not investigated
anism to kill coral tissue, toopen up space forits here, may release allelochemicals. Thus, sponge
own growth. allelochemicals may play an important role in
In a study conducted by Bakus & Nishiyama structuring the coral reefcommunity at a small
(1999, this volume), data from transects at the scale, local level. Morework isneeded,however,
studysiteshowthatnoapparentsequenceexisted to determine the extent ofthis role.
where a particular substratum type (i.e. live hard
coral, sponges, coral rubble, etc.)was found next ACKNOWLEDGMENTS
to sponges; that is, the succession oforganisms
and substratawere independent ofeach other. In We greatly appreciate the help ofDr Filapina
that study, however, individual species of both B. Sotto, Head of Marine Biology Section,
corals and sponges were not differentiated, and University ofSan Carlos, Cebu City, who made
therefore, specific speciespairs may exist. Using ourstudies possible. We would alsoliketothank
transect line data techniques, Turon et al. (1996) Jason Young, Jonathan Apurado and Ben
investigated the possibility of allelochemicals Pangatunganfortheirhelpthroughouttheproject,
TROPICAL SPONGE ALLELOCHEMICALS 417
both in the laboratory and in the field. We aggressive interactions between alcyonaceans.
appreciatealltheassistancegivenbymany ofthe Marine Ecology Progress Series28: 147-156.
members ofthe Marine Biology Section at the LITTLER, M.M. &L1TTLER, D.S. 1997. Epizoic red
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