Coexistence of Hydroid Eating Nudibranchs: Do Feeding Biology and Habitat Use Matter?

13 Pages·1991·5.1 MB·English

by  W J Lambert

Reference: Bin/ Bull 181: 248-260. (October, 1991)
Coexistence of Hydroid Eating Nudibranchs:
Do Feeding Biology and Habitat Use Matter?
WALTER LAMBERT
J.
Department ofZoology, University ofNewHampshire. Durham, New Hampshire 03824
Abstract. The feedingbiologiesand habitatsoffournu- amples of pre-emptive or overgrowth competition of
dibranchs in colonies of the hydroid Obelia geniculala clonal invertebrates(Schoener, 1983). Theco-occurrence
wereinvestigated todetermine whetherthese factorscon- ofmotile invertebratesinepifaunal andalgal communities
tributetothecoexistenceofthenudibranchs. Theradulae iswell documented (Edgar, 1983; Coyer, 1984; Virnstein
and feedingbehaviorsshowed species-specifictraits. Den- and Howard, 1987; Hall and Bell, 1988), but the mech-
dronotusfrondosushasa multi-seriate radula; when small anisms allowing theircoexistence aregenerally unknown
(<5 mm), individualsaresuctorial feeders, whereaslarger (Seed, 1986). Although variability in diet (Nybakken and
nudibranchs (>5 mm), bite whole polyps. Doto coronata Eastman, 1977; Shonman and Nybakken, 1978; Fernan-
uses a flat, uniseriate radula to penetrate stolons. EH- dez et al.. 1988), radular structure (Bloom, 1976; Blinn
branchusexiguuspenetrates hydrothecae with atriseriate et til.. 1989), feeding behavior (Hawkins et al.. 1989),
radula. Tergipes tergipes has a curved, uniseriate radula habitat preference (Bloom, 1981) and temporal appear-
and rakes naked tissue. ance on the food resource (Yoshioka, 1986) provides ex-
Each species of nudibranch occupied a distinct area planations for the coexistence of epifaunal gastropod
withinthe hydroid colony, suggestingthatthe micro-hab- predators, little is known ofthe relationship ofco-occur-
itatsaredictated by feedingbiology. D.frondosusoccupies ring nudibranchs in hydroid colonies (Todd, 1981).
hydrocauli towards the center ofthe colony, D. coronata The majorityofnudibranchs intheGulfofMaine prey
occurs along the edge ofthe colony on the kelp surface, on hydroids (Meyer, 1971; Clark, 1975; Lambert, 1985).
E. exiguus is found on hydrocauli at the edge ofthe col- Often nudibranchs demonstrate considerable overlap in
ony, and T. tergipes sitsatoptall hydrocauli in the center their distribution with many nudibranch species feeding
ofthe colony. in the same hydroid colony (Kuzirian, 1979). Coexistence
Separation in the hydroid food resource exists among in these hydroid colonies maybe mediated bydifferences
these nudibranchs and equilibria! coexistencecould have in habitat or food, but the underlying mechanisms are
operated, but equilibria! conditions necessary for exclu- unknown.
sion are unlikely to occur or persist significantly long. The hydroid Obeliageniculata grows epiphytically on
Thus, this assemblage ofnudibranchs appears structured laminarian kelps, often coveringthe entire blade surface.
by non-equilibrial processes perhaps similar to popula- Fourspeciesofnudibranchs(Dendronotusfrondosus, Doto
tions ofphytophagous insects. coronata, Eitbranchusexiguus. and Tergipestergipes) in-
habit these colonies sympatrically. Their spatial distri-
Introduction bution within the colony suggests a separation in their
use ofthe hydroid as food and micro-habitat. This study
Inaquaticenvironments, thecoexistenceofsessilespe- focuses on the feeding biology and micro-habitat use of
cieshasreceived muchattention (Osman, 1978;Jackson,
those nudibranchs inhabiting colonies of O. geniculata.
1984; Keough, 1984; McGuinnessand Underwood, 1986; Foreach nudibranch speciesthe followingparametersare
Ojeda and Dearborn, 1989) where most studies are ex-
described: morphology of the radula, feeding behavior,
and location within the hydroid colony. Skeletal mor-
Received 29October 1990;accepted 13 May 1991. phology ofthe hydroid prey isalsodescribed. Differences
248
COEXISTENCE OF NUD1BRANCHS 249
in trophic morphology and feeding mechanisms among A.
predators may reflect the diets ofthese predators within
hydroidcolonies. Thepossibilitythatdifferencesin feeding
biology and habitat use help facilitate coexistence among
these nudibranchs is considered.
Materials and Methods
Collection ofanimals
Nudibranchs and colonies of Obelia geniculata were
collected from ashallow(4-10m), kelpbedatCape Ned-
dick, York, Maine, (43 10' N, 70 36' W) from Septem-
ber, 1988, to September, 1989. Kelp blades (Laminaria
saccharina and L. digitata) were examined underwater
for nudibranchs, individually placed in plastic bags, and
brought tothe lab. Inthe lab, fourspeciesofnudibranchs
(Dendronotusfrondosus, Doto coronata, Eubranchus ex-
igitus, and Tergipes lergipes) were imsomlated from the hy-
droid colonies, sized to the nearest with a dissecting
microscope, andseparated fordifferentpartsofthestudy.
Analysis ofradulae
distance EF
Radulae from four individuals each of D. frondosus, ndex = distance CD
D. coronata, and E. exiguus and seven individuals of T. (Bloom. 1976)
tergipeswere examined. Entire animalsw^redissolved in RakeAngle-
10% NaOH for 10-12 h. The radulae were then teased
freeand placed into 70% ethanol until theywere mounted Figure 1. Drawings ofa radula tooth from a (A.) dorsal and (B.I
wfwoaertreesrcmaaonnundinntageldleoloewncettdrootngolamasiisrc-rcdoorvyse.crosTplhyiepsy(SiwEneMar)e.drsCoplpuetaotnefrdricasodtiaultlleaeded lLraartde=urlalalrepnesgrttsrhpuecocttfuirrveae..c(hSiWcdRhiae=nmawttoiiodcttshh,sohdfor=wadtduhelneat,imceWlaessr.u=)rewimdetnhtsofmraadcehitdoiaqnuatnotoitthy,
with a 200-300 A coating ofAu/Pd and viewed with an
AMR
1000 Scanning Electron Microscope at 20 kV.
Six parameters from three tooth rows from the center differences in radular structure existed among the nudi-
ofeach radula were quantified for each species; the aim branchs (Harris, 1985). Data were In (x + 1) and square
was to characterize the morphology of the radula from root (x + 0.5) transformed to correct for non-normality
each nudibranch species. From a dorsal perspective, the and heteroscedastic variances (Zar, 1984).
width (nm) ofthe radula and the length (/jm) and width
(^m) ofthe rachidian tooth were measured and the den- Feeding behavior andfeeding damage
ticles on one side of the rachidian tooth were counted
(Fig. 1A). Therakeangleandcurvatureoftheradulawere Feeding mechanisms were identified for each species
measured from a lateral view (Fig. IB). The rake angle ofnudibranch. Nudibranchs were starved overnight and
(defined as the angle ofthe radula to the feeding surface werethenplaced in 10cm (diameter)stackingdishescon-
when protruded from the mouth) was measured as the taining kelp blades covered with O. geniculata. The feed-
angle made from thetipofthe rachidian tooth tothebase ing behaviors ofeach nudibranch were observed with a
ofthe tooth row. Curvature is the degree ofhook or the stereo microscope during a minimum ofsix feeding ses-
amountofconcavityalongtheinnermargin oftheradula sions. A feeding session consisted of approach, attack,
(Bloom, 1976). Curvature was measured as the ratio be- manipulation, andconsumption ofthe hydroid prey, and
tween the height ofthe concavity alongthe inner margin a session was considered complete when the nudibranch
of the rachidian tooth and the length of the rachidian retreated from the polyp or stolon it had been eating.
tooth. All length measurementsand angleswereobtained Portions ofhydroids that had been manipulated were
from the SEM photos with a digitizing tablet. collectedfromthecolonyasthenudibranchswerefeeding.
A multivariate analysis of variance (MANOVA) was Where possible, thepiecesofstolon werecut0.5 cm from
used to test the null hypothesis that no morphological a site of feeding and lifted from the kelp surface. Ifthe
250 W. J. LAMBERT
stolon could notbeeasily removed, the kelpitselfwascut Results
so that the feedingarea could be obtained. Uprightswere
Structure of the radulae
also removed from thecolony afterhavingbeen fed upon
bynudibranchs. Hydroidskeletal piecesthathadbeen fed Theradulaeofthe fournudibranchspeciesdifferedsta-
upon were taken from each nudibranch speciesexcept T. tistically in the six parameters measured (Table I). Only
tergipes, which feeds on naked tissue. All hydroid pieces the radula ofTergipestergipeswascurved; theothershad
were preserved in 2.5% phosphate buttered glutaraldehyde nohook. Theradulaisan importanttaxonomiccharacter
for 1-2 h and then stored in 70% ethanol. For SEM, the for opisthobranchs (Thompson and Brown, 1984) and
tissues were dehydrated through a graded ethanol series varied little among the individuals ofa species.
and placed in hexamethyldisilizane (HMDS) for final Dendronotusfrondosus had a wide (X SE = 157.70
drying(Nation, 1983). Skeletonswere mounted on stain- 4.51 /urn), multiseriate radula with 5-9 lateral teeth
less steel stubs with double-stick tape and coated as de- flankingthe rachidian tooth (Fig. 2a). The rachidian tooth
scribed for the radulae. The dimensions ofthe holes pro- (width = 39.36 1.01 ^m, length = 29.93 1.33 urn)
ducedbythe nudibranchsweremeasuredonSEM photos was triangular with 9-1 1 small, lateral denticles. Each
with a digitizing tablet. lateraltooth hadasinglecuspand3-5 denticles. Therake
angle was wide (58.2 2.8) (Fig. 2b).
Nudibranch habitats The uniseriate radula of Doto coronata was narrow
seaHwyadtreoriadnsdwietxhatmhienirednuwdiitbhriann2c4hsh.weTrheeplloaccaetdioinnfolfoewaicnhg (a1n7d.8s0tub0b.y25(wjiidmt)h(Fi=g.127c.).73Ther0a.c2h6idMia,n tloeontghthwa=ss7h.o7r8t
nudibranch within its colony was determined and quan- 0.36 fim) with 3-4 large lateral denticles on each side.
tified by four habitat parameters: (a) height ofthe nudi- Thecentral denticle ofthe rachidian toothwasdepressed,
branch above the kelp surface (mm), (b) density of hy- makingthedorsal surfaceoftheradulaconcave. Therake
drocauli around the nudibranch (number/2.25 cm2), (c) angle was narrow (21.6 1.0) (Fig. 2d).
cmneranarheeaigahrto(unmdm)thoefnhuyddirborcaanuclhi,(nan=d 5()d)witthheindiast2a.n2c5e triEseurbiartaencrahduuslaex(iFiggu.us3ah).adAaswinigdlee (la1t0e3r.a7l0toot3h.8f7lajnukme)d,
(cm) between the nudibranch and the closest edge ofits tthhienr(awcihditdhian= t2o8o.t6h2. Th2e.8r0acfhiimd,ialnentgothoth= w2a2s.71long0a.n6d0
colony.
Habitat parameters were analyzed with a MANOVA jim) with 3-7 large denticles on each side; it appeared
(H nudibranch habitats do not differ within colonies of rake-like. The lateral teeth were wide at their base and
Obel:ia geniculata). Habitat data were In (x + 1) and re- tapered sharply to a thin, narrow, single cusp. The rake
cmiepertoctahle(axs+sum1)pttiroannssfoofrmaenadly(sZiasr,of19v8a4r;iaKnrceeb.s, 1989) to angTleergwiapsesmotedregriapteeslhyadwiadena(r3r6o.w5 (34.19.99) (F2i.g2.93^bm).), uni-
seriate radula (Fig. 3c) with a short, wide rachidian tooth
Perisarc analysis (width = 30.84 2.19 M, length = 19.50 1.09 ^m)
that bore a prominent central denticle and 5-10 large,
Five stolons and hydrocauli were isolated from the lateral denticles. The central denticle was approximately
central and peripheral (outer 2 cm) portions offive col- twotimes longer than the lateral denticles and had a nar-
onies ofO. geniculata and fixed overnight in Bouin's so-
lution. Afterbeingwashed in 50%- ethanol, thepieceswere
dehydrated, stained with acid fuchsin, embedded in par- Table I
affin, and sectioned. The perisarcwasstainedwith Lugol's Analyses ofvarianceofparameters<>/radularstructureforthejour
solution (Lillie, 1954) according to procedures adapted spt-cii-sofmidibranchx(Dendronotus frondosus. Dotocoronata,
from Drury and Wallington (1980). Thickness (nm) of EubranchusexiguusandTergipestergipes,!
the perisarc ofstolons, hydrocauli, and theca from each
areaofthecolonyweremeasuredwithan ocularmicrom- Variable df
eter. lnW
A two-way analysis of variance was used to compare R
thethicknessofperisarcsfromthecenterandtheperiphery
ofthe hydroid colony. Data were log transformed to sta-
bilize variances. A Tukey-Kramer HSD multiple com-
parisontestwasusedtotestcomparisonsofinterestamong
structures within and between areas ofthe colony (Zar,
1984; Day and Quinn, 1989).
COEXISTENCE OF NUDIBRANCHS 251
/
i
Figure 2. Scanningelectron micrographsofradulae from Dendronotusfrondosus(size = 4 mm)(a, b)
and Doloconmata (size = 5 mm)(c, d) from adorsal(a, c)and lateral (b. d) view. Scalebars: a = 20 ^m,
b = 15 urn, c, d = 5 turn, (d = denticles, L = lateral teeth. R = rachidian tooth.)
row rake angle (22.5 1.9) (Fig. 3d, e). The radula of Depending upon their size, D. frondosus showed one
T. tergipes was the only one with a hook. The curvature oftwo feeding mechanisms; small individuals were suc-
index forall 21 tooth rowsexaminedwas0.293, butthere torial feeders,whereaslargeindividualswerepolypbiters.
wasconsiderable variation (SE = 0.04). Someofthisvari- Individuals less than 5 mm long (n = 7) penetrated the
ability could have occurred when the radulae were dried perisarcofthecaeandstolonsbyscrapingwiththeradula;
for viewing with the SEM. they then grasped the hydroid with the anterior portion
oftheir foot and sucked the tissue out. The average time
Feeding behavior required to penetrate a theca was 4.2 min (SE = 2.9).
Species specific behaviors for handlingand consuming Onceahole had been made, suctioncreatedbythebuccal
hydroid preywereobserved in feedingnudibranchs; feed- apparatus served to draw out either the hydranth from a
ing behaviors among conspecifics varied little. hydrotheca, or the juvenile medusae from a gonotheca.
252 W. J. LAMBERT
IfTFI
Figure3. Scanningelectron micrographsofradulaefromEuhniiu'lHisi:\iguus(size = 4 mm)(a.b)and
Tergipestergipes(size = 4 mm)(c, d, e)from adorsal (a,c)and lateral (h, d, e)view. Scale bars: a, b, c, d
= 10nm,e = 15 urn. (d = denticles. L = lateral teeth, R = rachidian tooth.)
When feeding on gonangia, the nudihranchs plucked in- manner along a hydrocaulus following the alternating
dividual, juvenile medusae from the bottom ofthe gon- pattern ofpolypbranching, feedingatarateof1-2polyps
otheca. On stolons, tissue was extracted by a few, quick per minute over a 5-min observation period (n = 6).
pulses ofthe buccal apparatus. Doto coronata was a suctorial feeder preying predom-
mm
Dendronotusfrondosus individuals greater than 5 inantly on the stolons of Obelia geniculata. The nudi-
were polyp biters or grabbers. The nudibranchs would branch clutched a stolon with the anterior portion ofthe
crawl up a hydrocaulus and lightly contact the tentacles foot to bring the mouth against the stolon. The anterior
ofan exposed hydranth with the anterior portion ofthe portion of the foot flattened against the stolon during
footand mouth. Both suctorial andgraspingmechanisms buccal activity, suggesting that the nudibranch was ex-
were used to consume polyps. Although the radula was erting additional pressure to assist in penetration. When
everted from the mouth, it did not contact a polyp (n a hole was produced through the perisarc, coenosarc was
= 14). Asbuccal activity created a suction that pulled the drawn into the animal's mouth. Tissue moved unidirec-
polyp towards the nudibranch's mouth, the jaws were tionally toward the mouth of the nudibranch in pulses
protruded,andthepolypwasclippedoffatitsbaseleaving thatcoincidedwithpulsesofthebuccalapparatus. Perisarc
only the annuli. A nudibranch would continue in this was penetrated by rasping with the radula. Drill holes
COEXISTENCE OF NUDIBRANCHS 253
produced by D. coronata of4-5 mm were round, with a the foot, thus bringing their mouths against the perisarc.
diameter of 35.7 ^m (SE = 4.8) (Fig. 4). The holes had The radula scraped the thecal surface creating a hole in
beveled sides with groovescorresponding to thedenticles 15-30 s. and the entire hydranth was drawn out through
ofthe rachidian tooth. A raised lip around the perimeter thebase. Thenudibranch leftwhenalltissuewasremoved.
ofthe holes was distinct from the perisarc and is either Penetration and consumption ofthe first polyp took 1-2
coenosarc ofthe hydroid or mucous produced by glands min (SE = 10.6 s), but each successive polyp eaten took
in the foot ofthe nudibranch. Incomplete holes (Fig. 4c, longer to consume.
d) had ajagged or deteriorated perisarc at their center. The penetration hole produced by E. exiguus was el-
The time to penetrate a stolon by D. coronata was dif- liptical (Fig. 5). The sides of the holes were jagged and
ficulttodetermine. Aholewasconsideredcompletewhen the perisarcappeared ripped, ratherthanwornorscraped
the coenosarc was drawn toward the nudibranch. It was as in holes in stolons produced by D. coronata (Fig. 4).
common for an individual nudibranch to position itself The width ofthe hole at its center and widest point (X
atopa portion ofstolon for4-6 h. Duringany single hour, SE = 8.00 1.07 urn) was similar to the width ofthe
several periods ofbuccal activity alternated with longer top three denticles on the rachidian tooth (6.46 0.48
periods ofapparent inactivity. The periods ofbuccal ac- ^m). The lateral teeth on radulae ofE. exiguus were not
tivity were short, usually 1-3 min with up to 15 min be- observedcontactingthethecal perisarcduringthefeeding
tween setsofbuccal pulses. Penetration took a minimum process.
of 1 h, but averaged 3.3 h (SE = 1.2, n = 6). Tergipes tergipes did not penetrate the perisarc, but
Eubranchusexiguuswasalsoasuctorial feeder, but fed attacked naked tissue. Small individuals(<4 mm) placed
only through the perisarc of hydrothecae. Nudibranchs theirmouthsatopa polypand rasped tissuedirectly from
grasped the base ofa theca with the anterior portion of the area around the hypostome. Ifthe hydranth was re-
Figure4. Scanningelectron micrographs ofstolonsofOheliageniculalashowingdrill holes produced
byDotocoronataduringfeeding. Scalebars: a,c = 50nm, b,d = 20^m.
254 W. J. LAMBERT
Figure5. ScanningelectronmicrographsofhydrothecaeofObeliageniculatashowingpenetrationholes
produced by Eubrancluis exignusduring feeding. In aand c the arrow points to the area ofdamage; b, d
are magnificationsoftheseareas. Scalebars: a, c = 50fjm.b, d = 10/im.
traded intothe theca, the nudibranch curled itsbodyover (n = 5) of T. tergipes required up to 2 h to consume an
the thecal rim to reach the polyp tissue. Very small in- entire polyp (75 45 min).
dividuals(<1 mm) crawled into hydrothecae to feed upon Largerindividuals(>3 mm)ofT. tergipes(n = 8)either
polyps. While direct observations clarified the use ofthe ripped the entire polyp from a hydrotheca or cropped
radula in raking tissue from the polyp, it was not deter- tentacles. Each process was very rapid compared to the
minedwhetherthejawswerealso used. Small individuals slow rasping of smaller T. tergipes. The approach to a
COEXISTENCE OF NUDIBRANCHS 255
Table II
Analysisofvariancetabletestingtherelationshipbetween habitat
parametersofnudibranchs incolonies<>/Obeliageniculalaandspecies
ofnudibranch (MANOl'A:Filial Truce = 0.510. P< 0.001)
Variable
256 W. J. LAMBERT
colony as D.frondosus (Table III). D. coronata was 2.62
cm(SE = 0.2)from theedgeofthecolonywhileE. exiguus
was 2.28 cm (SE = 0.3) from the edge ofthe colony.
Perisarc analysis
c
ro
ThethicknessoftheperisarcofcoloniesofO.geniculata
differed among structures (stolons, hydrocauli, thecae)
within an area of the hydroid colony (F = 186.73, P
< 0.001)(Fig. 6). Alongtheedge ofthecolony, the thick-
ness of perisarcs ofeach structure differed, while in the Stolons Uprights Theca Stolons Uprights Theca
centerofthecolonytheperisarcssurroundingstolonsand Edge Center
hydrocauliweresimilar, butbothweresignificantlythicker
than the perisarc coveringthe hydrothecae. Between areas Figure6. Meanthickness( SE)ofthepensarcofObcliageniculata
ofthe hydroid colony, the perisarcs surrounding stolons from stolons, hydrocauli. andthecae from central and peripheral areas
and hydrocauli werethicker in thecenterthanattheedge (ofPt<he0.h0y0d1r)oifdorcsotlrouncyt.ureHsorwiiztohnitnalanlianreesaionfditchaetehysdirgnoiifdiccaonltondiyf.ferences
ofthecolony(P< 0.001), whiletheywerenot significantly
different on hydrocauli.
Nybakken and McDonald (1981). The jaws may assist
Discussion penetration ofa hydrothecabypinchingthethin perisarc.
Radular structures, feeding mechanisms and micro- The lateral teeth are very thin, delicate structures that
habitats vary in nudibranchs co-occurring within colonies may have little functional utility and may be vestigial.
ofObeliageniculata. Each nudibranch species used adis- The Eubranchidae are one of only two families within
tinct method to ingest hydroid tissue; little overlapexisted thesuperfamily Acleioproctathat haveretained atriseriate
between species. Individualswithin aspeciesshowed some radula (Schmekel and Portmann, 1982) and Schmekel
variation with respect to the hydroid structure they fed (1985) suggested that a reduction from broad radulae to
upon, but small nudibranchs (<6 mm) appeared to be narrow radulae has occurred in the evolution of opis-
restricted mostly by the structure oftheir radula (Hinde, thobranch radulae. Two mechanisms forremovingtissue
1958;Nybakken, 1970; Mills. 1977). Nudibranchsoccupy afterpenetrating the hydrotheca are feasible: (1) the rach-
areas of O. geniculata colonies in which they can feed, idian tooth pulls the polyp out from the bottom of the
suggesting that feeding biology dictates habitat use forthis cup or (2) the buccal apparatus assists by creating a vac-
suite ofnudibranchs. uum for suction (Kohn, 1983). The second mechanism
is more probable because polyps are rapidly extracted
through the base ofathecaratherthan incremently drawn
Feeding biology
out as would occur ifrasped.
Nybakken and McDonald (1981) predicted that nu- According to Nybakken and McDonald (1981), nudi-
dibranchs with wide, triseriate radulae should feed upon branchs with uniseriate radulae should feed upon stolons
naked hydranths and gonophores. Dendronotusfrondosus that are covered with perisarc. They suggested that a uni-
has a wide, multiseriate radula (Fig. 2a), and Robilliard seriate radula is betteradapted fordrilling holesthan rad-
(1970) described the general feeding behavior ofD.fron- ulae with three teeth perrow, but Dotocoronataand Ter-
dosus as biting whole polyps and sucking coenosarc. My gipes tergipes both have narrow, uniseriate radulae. D.
findings support Robilliard, but I found that the mecha- coronata feedsby raspinga holethrough stolons, whereas
nisms used by D. frondosus changed from piercing and T. tergipes rakes naked tissue ofhydranths.
suckingtobitingwith increaseinsize. Christensen (1977) The radulaofD. coronataisflatwith thecentraldenticle
described a mechanism ofcoordinatingjaws and radula ofthe rachidian toothdepressed belowthe lateral denticles
for feedingby Precuthonapeachion Hydmctinia echinata (Fig. 2c. d). The penetration holes are circular (Fig. 4)
similar to that for D.frondosus. Because P. peachi has a and similarto those produced by muricid snails (Carriker,
uniseriate radula (Thompson and Brown, 1984) in con- 1969), octopods (Nixon and Maconnachie, 1988) and by
trast to D.frondosus, nudibranch size relative to hydroid the dorid nudibranch Okadaia e/egans (Young, 1969).
prey may be a better indicator of feeding mode than is Each ofthese predators preys upon organisms that have
radular structure. a calcareous exoskeleton (mollusks) or live in calcareous
Eubranchiisexiguuswith a triseriate radula penetrated tubes (serpulid polychaetes) and use chemicals to assist
the base of hydrothecae, contrary to the predictions of the penetration process. Muricid and naticid snails use
COEXISTENCE OF NUDIBRANCHS 257
secretions fromanaccessory boringorgan (Carriker, 1969. intermediatediet forjuvenileD.frondosusbecauseadults
1981), octopods use saliva from the posterior salivary feed on largertubularian hydroids. Both D. coronata and
glands(Nixon, 1979a, b; Nixon and Maconnachie, 1988) E. exiguus feed by penetratingthe perisarc, but it is more
andYoung(1969)suggeststhat O. elegansusessecretions likelythatD. coronata isconstrained bypreysizebecause
from glandular cells around the lumen of the mouth, it feeds through the thicker stolon perisarc. Because long
which he considers are part ofthe stomodeal gland. The periods oftime (2-4 h) are required for an adult D. co-
etched pattern along the sides as well as the deteriorated ronata to penetrate a stolon, one could hypothesize that
top ofthe penetration hole produced by D. comnata sug- meiofaunal-sized juveniles are unable to efficiently drill
gest the presence ofa caustic agent (Fig. 4b, d). The be- through stolons. A microalgal diet would allow tiny nu-
havior of D. comnata, which sits atop stolons for long dibranchsto increase size before shiftingtothe adult prey.
periods oftime with short pulses ofthe buccal apparatus T. tergipes feeds on naked polyp tissue and is not con-
alternating with longer periods ofinactivity, is similar to strained by its size; newly settled nudibranchs crawl into
thedrilling-related behaviorofthe snail Urosalpinx(Car- hydrothecae and rasp tissue directly (Lambert, 1990).
riker, 1969), and suggests D. coronata may usechemicals
to assist in the penetration of chitinous perisarc of O. Habitats andfeeding
geniculata. No reports show that dotoids possess glands
capable of secreting substances for dissolution of prey Distribution within the hydroid colony and on hydro-
skeleton. The salivary glands are unlikely candidates be- cauli demonstratedthat nudibranchssegregatetoareasin
cause they do not produce secretions containing lytic en- which they can feed. D.frondosus isageneralist predator
zymes(Hyman, 1967;WelschandStorch. 1973);however, withincoloniesof0. geniculata. Nudibranchsgreaterthan
mm
histochemicalwork isneededtoelucidatethismechanism. 12 infrequently occupy colonies of O. geniculata
Nybakkenand Eastman(1977)showedthatthecurved (Lambert, 1991) and associate among athecate hydroids,
radulaofTriophacarpenter!isbetterforrippingflesh from particularly Tnbularia spp. (Swennen, 1961; Thompson,
erect bryozoa than the flat radula of Triopha maculata, 1964;Robilliard, 1970;Clark, 1975;Todd, 1981). Because
which is used to scoop polypides from colonies ofAfem- large D. frondosusare veryobvious in colonies ofO. gen-
branipora membranacea, an encrusting bryozoan. The iculata (pers. obs.), shifting to Tuhularia colonies may
feedingmechanism observedfor T. tergipeswithanarrow, provide abetter refuge from fish predation aswell as nec-
hooked radula is similar to the mechanism used by T. essary calories.
carpenteri. Feeding on polyp tentacles by slurping seems Doto coronata occupied the edge of colonies, at the
to be restricted to larger individuals (>3 mm) and may basesofhydrocauli oronthekelpsurfaceandamongfew,
be a function of mouth size and ability to engulfwhole short hydrocauli and fed predominantly on stolons. The
strands oftissue. perisarc ofstolons is thinner along the perimeter ofcol-
onies than at the center and appears to be selected as a
prey that iseasierto handle (Pyke et al.. 1977). The pref-
Size
erence to feed at the growing edge ofcolonies is similar
The nudibranchs inhabiting colonies of Obelia geni- to that in dorid nudibranchs, which feed at the edges of
culata are all very small; nudibranchs greaterthan 5 mm bryozoan colonies(Harvell, 1984;Toddand Havenhand,
are seldom found (Lambert, 1991). The mechanism each 1989). This behavior in dorids has been related to the
species uses to feed may in part be dictated by its size, in lower calcification and strength ofedge zooids (Best and
addition to the structure of its radula. Heavy jaws are Winston, 1984)and todifferences in palatability ofstruc-
usedtobreakthrough relativelythinexoskeletonsencasing turesbetween zooidsin acolony. Harvell (1984) suggested
zooecia ofectoproct colonies by the large dorids Triopha that colonies of Dendrobeania lichenoides have an on-
carpenteri and T. maculata (Nybakken and Eastman, togenetic gradient marked by morphological and physi-
1977). D. frondosus may grow to 100 mm (Thompson ological variation in tissuecontent ofzooids. Thegradient
mm
and Brown, 1984), and animals larger than 5 use affects the grazing patterns ofnudibranchs, which prefer
jawstobite offwhole polyps, a feedingmechanism similar tofeed uponzooidsattheperimeter,thatarefreeofbrown
to Triopha spp. bodies and reproductive structures. In the case ofD. co-
Newly metamorphosedjuveniles may experience con- ronata. the preference for stolons along the perimeter of
straints due to size (Todd, 1991) when feeding upon O. colonies seems to be due to a greater mechanical ease of
geniculata. Because three ofthe four nudibranchs in col- penetration. Composition ofthecoenosarcdiffersbetween
oniesofO. geniculata feedby penetratingperisarcatsome the growing edge and the center ofcolonies of O. geni-
point during post-larval life, do any ofthese require an culata with respect to cellular activity (Crowell, 1957;
intermediate diet? O. geniculata may be considered an Braverman, 1971), but no reports discuss differences in