-
The Associates of Four Species of Marine Spongesof Oregon and
Washington
EDWARD R. LONGl
ABSTRACT : Four species of sponge from the coasts of Oregon and
W ashingtonwere studied and dissected for inhabitants and
associates. The four species differedin texture, composition, and
habitat, and likewise, the populations of associates ofeach
differed, even when samples of two of these species were found
adjacent to oneanother. Generally, the relationships of the
associates to the host sponges were offour sorts: (1 ) inquilinism
or lodging, either accidental or intentional; ( 2) preda-tion or
grazing; (3) competition for space resulting in "co-habitation" of
an area(i. e., a plant or animal growing up through a sponge) ; and
(4) mutualism. Fish eggsin the hollow chambers of H omaxinella sp.
represented fish-in-sponge inquilinism,which is the first such
instance reported in the Pacific Ocean and in this sponge.The
sponge Halichondria panicea, with an intracellular algal symbiont ,
was foundto emit an attractant into the water, which Archidoris
montereyensis followed, inbehavior experiments, in preference to
other sponges simultaneously offered. Atotal of 6,098 organisms,
representing 68 species, were found associated with thesamples of
Halicbondria panicea with densit ies of up to 19 organisms per cm3
ofsponge tissue. There were 9,581 plants and animals found with Mic
rociona prolif era,and 150 with Suberites lata.
SPONGES FREQUENTLY SERVE as hosts for manyplant and animal
associates. The relationshipsof such organisms vary from loose
lodging orinquil inism to mutualism, a close type of sym-biosis.
The first account of sponge symbiosiswas that of Radcliffe (19 17)
in which he re-ported the goby Garmannia spongicola livingwithin
unidentified sponges off N orth Carolina.Other early reports
include those of Vosmaer(191 1) who found invertebrates in the
canalsof tropical sponges, and Ridley and Dendy(1887) who found a
very abundant oscillator-ian alga in H alicbondria panicea.
Perhaps the most significant reports concern-ing sponge
symbioses were those of Pearse( 1935, 1949) who described the
inhabitantsof various Caribbean sponges, Gudger (19 35)who found
many fish living in Atlantic sponges,and Forbes (1964, 1966) who
described themutualistic relationship between the spongeStellate gm
bii and the oyster Ostrea permollis
1 Department of Zoology, Oregon State Un iversity.Present
address: U.S. N aval Oceanographi c Office,W ashington, D .C.
20390. Manuscript received Jul y18 , 1967.
from the Gulf of Mexico. Caullery (1952) ,Dales (19 57) , Nicol
(1 964 ) , and Henry( 1966) have summarized the symbiotic
relation-ships of marine animals and included in theirdescriptions
many previous reports of spongesymbioses. The following is a
description of theassociates of four species of sponge,
threesubtidal and one intertidal in Pacific N orthwestmarine
waters.
METHODS AND MATERIALS
Because the sponges studied occupied variedhabitats, the methods
of collection differed.Mic rociona prolifera and Suberites lata,
whichwere subtidal, were obtained with SCUBA. Theywere pulled or
scraped off their substrate andimmediately placed into zippered
plastic bagswhich were sealed underwater. Halicbondriapanicea,
which occurred intertidally upon un-protected rocks, was scraped
off the rocks by useof the fingernails and placed into plastic
bags.H omaxlnella sp. was collected from 10 to 15fathoms with an
otter trawl. The collected speci-mens were subsequently taken to
the laboratory
347
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348
to recover the associates. The sponges werepulled apart and
examined under a binocularmicroscope (120 X ) . The inhab itants
foundwere preserved in AFA for further examinationand
identification. The results are summarizedin Table 1.
OBSERVATIONS AND EXPERIMENTS
Suberites lata
Snberites lata occurred in Hood Canal, W ash-ington, in a
distinct zone of its own at a depthof 5- 10 meters (MLLW ) on
nearly verticalrocks that were lightly covered with a fine mud.The
water conditi ons in this narrow inlet werequite stable and
calm.
The consistency of the sponge was very toughand impenetrable. It
harb ored very few orga-nisms. The 15 samples studied had 150
associ-ates, representing 25 species and 6 phyla. Thedensities of
the associates varied from 0.001 to0.03 (mea n 0.1) organisms per
ern" of sponge(Table 1) . The sparsity of inhabitants was
mostlikely due to the toughness of the sponge. Thepred ominant
organisms were the small spionidpolychaete Polydora socialis which
was foundin every Hood Canal sample, the gammaridA oiroides
columbine, the ectoproct Crisia sp. ,and unidentified, filamentous
green algae.
P. socialis was the only organism actuallyliving within the
sponge, the remainder weresimply attached to the surface. The
largeranimals, such as the crabs, were usually foundhiding among
the convolutions and contortionsof the sponge.
One clump of S. lata was found in an un-protected rocky coast
situation at Yaquin a Head,
PACIFIC SCIENCE, Vol. XXII, July 1968
Oregon. It harbored only a few more organismsthan the Hood Canal
samples. The organismsfound on the Yaqu ina Head sample were
thoseof the local community .
M icrociona prolifera
M icl'ociona prolij er« was found attached tosubtidal rocks in
Willapa Bay, W ashington. Thissponge was erect, branching, and
bushy, some-times forming a mass of branches 1 foot or morein
diameter and 6 or 7 inches high .
M . pl'olifera provided a place to live for manyanimals and
plants; the population densityvaried from 0.27 to 3.64 (mean 0.80)
orga-nisms per cm3 of sponge. The organisms mostcommonly found were
the gammarid Coropb iumacberusicnm, various caprellids, the
polynoidH arm otboe imbricate, the sabell id Sabellamedia, and the
anemone Diadumene lncine. The15 samples of sponge dissected
harbored 9,581organisms of at least 52 species from 9 phyla.The
most common and abundant of this arraywere the amphipods Coropb ium
acherusicnmand various caprell ids.
The majority of the inhabitants were foundattached to the
surface of the sponge and rela-tively few were found within the
sponge tissue.Some of the amphipods, sabellids , nereids,
andnematodes occurred within the sponge. It wasapparently difficult
for the associates to pene-trate into the tough and fibrous M .
prolifera.
Due to the branching and bushy morphologyof the sponge, mud
often collected on it andthis mud harbored many of the
associatesthat were found . Therefore, there is a questionwhether
the associates were attracted to the
TABLE 1
A VERAGE THICKN ESS, V OL U ME, T OTAL A SSOCI ATES, AN D D
ENSITY OF P OP ULATION F OR
SAMP LES OF Suberites lata, Microcion« prolijera, AND
Halicbondria panicea
AVERAGE AVERAGE AVERAGE
SPECI ES N O. OF T H ICK NESS VOLU M E TOTAL AVERAGE
OF SPON GE SAM PLES (CM) (CM3) ASSOC IATES DENSITY
Suberiteslata 14 4.5(3 -7 ) 503( 195-820 ) 10(1-59)
0.2(0.001-0.8 )
Min'ocionaprolij ern 15 5(2-13 ) 594 ( 24-2,340 ) 640 ( 21-
1,885) 1.2 (0 .27- 3.64 )
Halicbondriapanicea 33 1(0.5-3) 104 ( 20- 540 ) 188(1 8-670) 1.8
(0.126- 19.14 )
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Associates of Marin e Sponges-LONG
sponge itself or to the mud collected thereupon.The fact that
relatively clean samples of thesponge also harbored many associates
indicatedthat there was a definite attraction to it. Otherspecies
of sponge occurring near or upon M .prolij era were completely
devoid of associates,suggesting that the associates preferred
M.prolifera .
H alicbondria panicea
GENERAL OBSERVATIONS : H alicbondria pani-cea occurred as an
encrusting sheet 1-5 cm thickupon unp rotected rocky coast areas in
violentsurf. It was green in its upper layers and yellowbelow, the
coloration being due to an intra-cellular single -cell alga.
H. panicea harb ored many associates of agreat variety. A total
of 6,098 organisms of 68species were found in 32 samples with
densitiesof population of from 0.26 to 19.0 (mean 1.15)organisms
per em", The most common associ-ates were amphipods (Jassa falcata
and caprel-lids); the barnacles Balanus gland,tia and B.nubilis;
the isopods D ynamen e sbeareri and D.dilata; and the coralline
alga Coralline gracilis.
The relationships of these associates to thesponges varied
considerably. The associates canbe grouped in four general headings
: ( 1) thosethat were caught in the sponge as larvae
andsubsequently matured; (2) those that were onthe sponge
accidentally at the time of collection;(3) those that grew
simultaneously with thesponge on the same substrate ; and (4)
thosethat clung to the sponge because it was abundantand provided
purchase.
Such organisms as algae, hydroids, ectoprocts,some crabs,
barnacles, mussels, and some mol-luscs and annelids probably were
caught amongthe sponge spicules as planktonic larvae and,having
survived digestion, developed into adultsthereupon and therein .
Many of the nereids,large crabs, caprellids , gammarids, and
fishwere found by chance upon the particular spongecollected when
they were feeding or using itfor temporary shelter . It is most
likely thatsome of the algae (e .g., M icrocladia borealis)grew
simultaneously with the sponge.
Several animals were grazing on the sponge.Acmaea asmi, M opalia
lignosa, Oedognatbnsinetm is, Pachycheles rndis, Cancer
productns,and , particularly Arcbidoris montereyensis were
349
found to have H . panicea spicules in theirstomachs.
The only possible examples of truly mutual-istic associations
were those concerning theintracellular algae of H. panicea and the
clean-ing action of the crustacea associated with H.panicea, as
well as with Snb erites lata andM icrociona prolifera. The algae
may have pro-vided needed oxygen or other nutrients to thesponge .
The sponge without algae could sur-vive, but it usually appeared as
thin , rubberysheets. The numerous crustacea fed on thematerial wh
ich collected upon the sponge .
Generally, the samples of H . panicea fromdifferent areas
harbored the same species, andthe various members of the community
wereusually found in the same proportions fromsample to sample. H
owever, the exact composi-tion of the sponge communities varied
enoughamong the samples to suggest that a g iven in-dividual
community was related to the fauna ofthe immediate area.
EXPERIMENTS: Sponges of similar consistencyliving immediately
adjacent to Halicbondriapanicea normally had very few associates of
anykind , while the clumps of H . panicea were wellprovided with
associates. Also, when the nudi -branch A rcbidoris montereyensis
was placed intoa laborat ory tank upon a piece of Sub erites
latadownstream from H. panicea, the animal wouldinvariably crawl to
the H . panicea, indi cating achemotaxis toward the H .
panicea.
An apparatus similar to that of Davenport(1 950) was set up to
determine if there was achemical attr action of A. monterevensis to
H .panicea. The apparatus consisted of a series ofwaterways which
gave the nudibranchs a choicebetween water passing over H . panicea
and Sub-erites lata. The majority of the nudibranchs al-ways moved
toward the H . panicea water outlet :9 individuals of 15, 10 of 15,
13 of 15 in thethree experiments went to the H. panicea outlet.N
one ever moved to the S. lata outlet.
H omaxinella sp.
This sponge had much the same shape asM icrociona prolifera, but
it was branched fewertimes, and its branches were thicker and
hollow.H omaxin ella sp. occurred at a depth of 20-30meters off the
Oregon coast.
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350
The hollow branches were found to containclusters of 20- 30 fish
eggs with living embryosinside. The eggs were probably those of a
smallblenn y or goby that normally deposits its eggswithin sponges
. All the eggs found died beforehatching.
Assuming that these eggs are from a sponge-dwelling fish, th is
example of fish-sponge in-quilinism is the first recorded for H
omaxinellasp. and for the Pacific Ocean.
DISCUSSION
The four species of sponge studied showedgreat variation in the
community of associatesf ound. These variations were due to the
differ-ent habitats of the sponges and also to differentpr operties
of the sponges that acted as attrac-tants and inhibitors. Other
species of spongeadjacent to those studied harbored fewer
associ-ates, probably because they lacked factors thatattracted the
associates, or they possessed some-thing that discouraged them.
In comparing H alicbondria panicea, M icro-ciona prolij era, and
Suberites lata, which oc-curred in progressively deeper waters, the
com-munity of associates was pr ogressively morestable, consistent
, and predictable and its com-position fluctuated less from sample
to sample.The intertidal H . panicea showed great varia-tion in
community density and composition, in-dicating that these
parameters were related tothe fauna of the immediate area. When
twospecies of sponge (e.g., S. lata and H . panicea)occurred next
to each other, the tougher, moreimpenetrable species harbored fewer
associates.
The majority of associates did little harm tothe host sponge.
The numerous crustacea mayhave benefited the sponges by cleaning
them .Such a relationship can be considered mutu alist-ic. The
intracellular algae of H . panicea werealso pr obably mutualistic
with the sponge. Themost deleterious associate was Arcbidoris
mon-tereyensis, which, along with other pred ators,fed voraciously
on H . panicea. Some of the tubeworms and amphipods associated with
M.prolifera caused minor structural damage to thesponge. The
sponge-dwelling fish whose eggswere deposited within H omaxinella
sp. obvious-ly benefited from the water currents and shelterof the
sponge, while it did not appear to inhibitthe growth or functi on
of the host.
PACIFIC SCIENCE, Vol. XXII, July 1968
CONCLUSIONS
Four species of sponge from the coasts ofOregon and W ashington
were stud ied forassociates. A large number and great variety
ofassociates were found . The great numbers ofsponge associates
suggests that sponges are im-portant to the ecology of the numer
ous associ-ates. The relationships of these associates fallinto
four general categories: (1 ) inquilinism,or lodging, with in or
upon the sponges; (2) co-existence of two organisms on the same
substrate as a result of simultaneous growth ; (3)predation or
grazing ; (4 ) mutu alism.
The 32 samples of Halicbondrin pnniceaharbored 6,098 organisms,
representing 68species, with a mean density of 1.15 organismsper
em" of sponge. The 15 samples of Micro -ciona prolijer« had 9 ,581
associates with a meandensity of 0.80 organism per ern". The 14
sam-ples of Suberites lata had 150 associates at amean density of
0.1 organism per cm3 ofsponge.
Significant differences in composition anddensity among the
sponge communities wereattributed to the different habitats of the
speciesstudied, and to differences in the exudates andconsistencies
of the species of sponge. The nudi-branch A rcbidoris
montereyensis, which fre-quently occurred on Halicbondria panicea,
ex-hibited a distinct preference for that species inlaboratory
experiments.
The tubular sponge H omaxinella sp. harboredthe eggs of a fish,
which was assumed to be anunidentified, sponge-dwelling
inquiline.
ACKNOWLEDGMENTS
Space and facilities were provided by Prof.Ivan Pratt at his
laboratories in Corvallis and atthe Marine Science Center ,
Newport. The fol-lowing persons provided identifications of manyof
the sponge associates: Dr. Joel Hedgpeth( insects), Dr. J. Laurens
Barnard (amphi pods) ,Mr. Danil Hancock (annelids) .
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