Effect of Larval Swimming Duration on Success of Metamorphosis and Size of the Ancestrular Lophophore in Bugula neritina (Bryozoa)

10 Pages·1996·4 MB·English

by  D E Wendt

Reference:Bio/. Bull. 191:224-233.(October, 1996)
Effect of Larval Swimming Duration on Success
of Metamorphosis and Size of the Ancestrular
Lophophore in Bugula neritina (Bryozoa)
DEAN WENDT
E.
Department ofOrganismicandEvolutionaryBiology, Harvard University,
Cambridge, Massachusetts 02138
Abstract. There is a growing realization that events larval swimmingaffectsboth metamorphosisandthede-
during one portion ofan organism's life cycle can have velopment of postlarval structures, which may ulti-
both subtle and dramatic effects on other stages in the mately influencecolony fitness.
life history. Lethal and sublethal effects associated with
theduration oflarval swimming in marine invertebrates
wereexamined forthebryozoan Bugulaneritina. Larvae
Introduction
were kept swimming up to a maximum of28 h at 20C
by exposure to continuous bright fluorescent illumina- Manysedentaryorsessilemarineinvertebratespossess
tion. At 4-h intervals, samples of20-40 larvae were re- a larval stage that on an ecological time scale can func-
moved from bright illummiMnation and were exposed to tion to (1) extend species ranges, (2) connect otherwise
seawater containing 10 excess KC1, an inducer of geographically separated adult populations, (3) alleviate
metamorphosis in this species. Overthe first 12 h oflar- parent-offspring and intraspecific competition, and (4)
val swimming, an averageofabout 90% ofthe larvaeini- facilitate the recolonization of disturbed habitats. The
tiated and completed metamorphosis: at 16 h, the per- longer a larva spends in the plankton, however, the
centage of larvae initiating and completing metamor- greaterthe chance that it will incuracost due to physio-
phosis dropped significantly. By 28 h, about halfofthe logical stress, starvation, predation, and advection away
larvaewere initiatingmetamorphosis, whereasonlyone- from suitablesites(Thorson, 1950; Rumrill, 1990; Mor-
fifth werecompleting metamorphosis. Larval swimming gan, 1995). Thus, theoreticallya trade-offexists between
duration also significantly affected the duration ofmeta- the benefits of dispersal and its attendant costs (see
morphosis. By 30 hoflarvalswimming, individualswere Vance, 1973; Strathmann, 1985, for models examining
taking about 25% longer to complete metamorphosis. life historystrategies).
Compared to ancestrulae that developed from larvae Recent evidence suggests that, in addition to lethal
thatwere inducedto metamorphose shortly aftertheon- effects, there are also sublethal costs associated with du-
set of swimming, those that swam for greater than 8 h rationofthelarvalswimmingstage,especiallyforspecies
had significantly smaller lophophores. For example, by with nonfeeding larvae (reviewed by Pechenik, 1990).
28 h oflarval swimming the ancestrular lophophore de- Sublethal costs influencing juvenile fitness have yet to
creased in height, surface area, and volume by about be incorporated into modelsoflife-historystrategiesand
25%, 40% and 55%, respectively. This marked decrease have not been rigorously characterized empirically. Pre-
in lophophore size may ultimately affect the ability of sumably any sublethal costs associated with remaining
juvenilestosequesterfood,competeforspace,andattain in the plankton are due to effects oflarval senescence or
reproductive maturity. Thus, increasing the duration of depletion ofenergy reservesto a level at whichjuveniles
have reduced fitness.
Feedinglarvaeshould bebuffered againstcostsrelated
Received20March 1996:accepted 12July 1996. to the depletion of energy stores, because they can re-
224
EFFECTS OF LARVAL SWIMMING DURATION 225
plenish their energy reserves continuously (Highsmith This generalization is supported by the few studies that
and Emlet, 1986; Pechenik and Eyster, 1989). However, have addressed the issue explicitly. For example. High-
they are unable to extend their lives indefinitely, and smith and Emlet (1986) found no significantcorrelation
eventually they either senesce and die or undergo spon- between delay time andjuvenile growth rate in the sand
taneous metamorphosis (Pechenik. 1990). Because of dollarEchinorachninsparma, which has planktotrophic
the limited energy supply (barring use of dissolved or- larvae. Also, Pechenik and Eyster ( 1989) found no sig-
ganic material [DOM]), aplanktotrophic larvae, i.e., lar- nificant differences in average survival, feeding, respira-
vaethatdo notrelyon particulate food,1 have morerigid tion, or growth rates between juveniles ofthe plankto-
constraintson the amount oftimethey can spend in the trophicgastropod Crepidulafomicatathatwere induced
plankton. tometamorphoseshortlyafterattainingcompetenceand
A larva is considered to be in an extended swimming thosethatwere kept swimminguntil metamorphosisoc-
period when it is physiologically capable ofresponding curred spontaneously. Results ofthese two studies sug-
to cues that elicit metamorphosis, but instead continues gestthatplanktotrophiclarvaecan haveanextended lar-
swimming in the absence ofthose cues. Marine inverte- val swimming period without incurring substantial cost
bratesdo not possessendogenousclocks thatcontrol the tojuvenile fitness.
duration ofthe larval period, but instead they metamor- In contrast, species with aplanktotrophic larvae can
phose in response to cues associated with a favorable incur sublethal costs as the duration ofthe larval swim-
adult habitat (Scheltema, 1974; Hadfield, 1978; Morse mingperiodincreases. Forexample, in 12 outof14cases
and Morse, 1984;Chia, 1989; Pawlik, 1992). Oncecom- Woollacott et at. (1989) demonstrated that after 10 h of
petenttometamorphose,alarvacan remainintheswim- swimming, larvae ofB. stolonifera developed intojuve-
mingphaseforoneoftworeasons: ( 1 ) it has notencoun- niles that grew significantly slower thanjuveniles devel-
tered a suitable cue to trigger metamorphosis; or (2) it oped from larvaethat hadaswimmingperiodof6 h. For
has encountered the cue, but additional factors prevent the barnacle Balanns amphitrite. prolonging the swim-
the normal metamorphic response. An example of the ming period of cyprids for 3-5 days dramatically de-
lattersituation wasprovidedby YoungandChia(1981). pressed juvenile growth rate compared to controls (Pe-
Theydemonstrated that competent larvae ofBugulapa- chenik et ai, 1993). Conversely, Pechenik and Cerulli
cificadelay metamorphosisin the presence ofextractsof (1991) found that prolonging the swimming period of
a dominant competitor, the compound ascidian Diplo- the aplanktotrophic larvae ofthe marine polychaete Ca-
soma macdonaldi. In eithercase, the benefits associated pilella sp. I for up to 216 h had no effect on postmeta-
with remaining in the plankton seem readily apparent: a morphic growth rate, time to first reproductive activity,
larva is able to synchronize the onset ofmetamorphosis orfecundity. However, increasinglarval swimmingtime
with encountering a favorable site. However, the longer did significantly decrease postsettlement survivorship
a larva is in the plankton the greater its exposure to the from 100% (not prolonged) to 12.5% (prolonged for
potential lethal and sublethal effects ofa planktonic ex- 216h). Although those individuals that survived in-
istence(Rumrill, 1990; Morgan, 1995). curred nosublethal costs, therewasasubstantial postlar-
Because planktotrophic larvae can feed on particulate val mortality.
matterthroughoutthe larvalstage,theyshould not incur Clearly, being able to initiate and to complete meta-
substantial sublethal costs; aplanktotrophic larvae, on morphosis is central to survival. More subtle, however,
the other hand, have finite energy reserves, and thus are the sublethal effects associated with a prolonged pe-
should incurthese costsquickerand with more severity. riod oflarval swimming. Intra-and interspecificcompe-
tition between sessile invertebrates forspace and food is
directly related to size (Buss, 1979; Buss and Jackson,
lec'iItphrotorpoopsheict.hetrtaenrsmlocaaptliaonnkatlo.troorphaidceltpohoipnchlaugdiec.laLrevcaietthhoattroaprheiecitlhaerr- 1981). Inaddition, forBiigulanerilina, reproductivema-
vae acquire nutrients (yolk) during oogenesis; translocational larvae turity is attained only after a minimum number of bi-
havenutrientstransferredtothedevelopingembryoafterfertilization; furcations (Keough, 1987). Therefore, an individual's
and adelphophagic larvae feed on siblings during encapsulation or fitnessmaybecompromisedbybeingsmalleraftermeta-
brooding. These terms refer to the specific processes by which larvae morphosisorbytakinglongerto metamorphose.
obtaintheirenergyreserves.Theinappropriatesynonymyoftheterms
lecithotrophyand nonfeedingiscommonly encountered in the litera- The effects ofthe duration oflarval swimming were
ture. Clearly all nonfeeding larvae are not lecithotrophic. The term assessed forthecheilostomebryozoan B. nerilina. which
aplanktotrophicisa moreappropriategeneral classification forlarvae has an aplanktotrophic larva that acquires its nutrient
thatderivetheirenergy reservesfromsourcesotherthantheplankton, reservestranslocationallythroughaplacenta-likesystem
afeneddiintgemopnhapsliaznketsontihec upanrdteircluylianteg smiamtitlearr)i.tyFrofomtheasneelnaerrvgaeeti(ci.es.,tannodt- (WoolacottandZimmer, 1975). Specifically, I examined
point,aplanktotrophiclarvaeareindependentofparticulatefoodinthe (1) duration of metamorphosis; (2) ability of larvae to
plankton. initiate metamorphosis;(3)abilityofindividualstocom-
226 D. E. WENDT
plete metamorphosis; and (4) size ofand tentacles in the intervals for 28 h. They were then pipetted into glass
ancestrularlophophore. BecauselarvaeofB. neritina&K Stendor dishes containing 20 ml of0.2-Mm-filtered sea-
aplanktotrophic and therefore limited energetically, I waterwith an excessof 10 mAfK.C1, an inducerofbryo-
predicted ( 1 ) a positive correlation between larval swim- zoan metamorphosis (Wendt and Woollacott, 1995).
mingduration and time required to complete metamor- The swimming times reported are minimum estimates
phosis (a result of the utilization of less labile energy in thatlarvaedid not initiate metamorphosisinstantane-
sourcesto complete metamorphosis); (2) an inverse cor- ously. However, preliminary experiments showed that
relation between larval swimming duration and ability > 70% ofthe larvae initiated metamorphosis within the
to initiate and complete metamorphosis; and (3) a nega- first hour after transfer. Initiation and completion of
tive correlation between size ofthe lophophore and du- metamorphosisweredetermined foreach samplecondi-
ration ofthe larval swimming stage. These factors influ- tion after72 h (see below on how initiation and comple-
encetheabilitytosequesterfood, competeforspace,and tion aredefined).
attain reproductive maturity, which undoubtedly affects Each time condition was sampled and metamor-
an individual's fitness. phosed individuals were "relaxed" in 7.5% MgCN. Ten-
tacle length, lophophore crown diameter, and lopho-
Materialsand Methods phore base diameterwere measured for each ancestrula
(Fig. 1). These parameterswere used tocalculate height,
Gravid colonies of Bitguki ncritina were collected volume, and surface area ofthe lophophore on the basis
fromthe undersidesoffloatingdocksneartheSmithson- ofthe followingequations(Beyer. 1987),
ian Marine Station in Fort Pierce, Florida, from Febru- = r - -
ary through April 1995 and in February 1996. Colonies Height V ('/,) (a b)~ (1)
were shipped to Cambridge. Massachusetts, and were Volume = w/i[a2 + ab + b2]/l2 (2)
20C
imnaidnatrakinnesesdwiintthhecolnatbionruaotuosryaeirnatpiloasnt.icNoaqufaoroidawaats pro- Surfacearea = Ttc(a + b)/2 (3)
vided forthecolonies. where a is diameter ofthe lophophore at its crown, /> is
Larvae were obtained from pools ofcolonies to foster
genetically heterogeneous populations for the experi-
ments. Colonies were removed from the dark, placed in
glass bowls with 1.5 1 ofseawater, and exposed to fluo-
rescent light. Within 30 min ofillumination, larvae ap-
peared; by 2 h, release was complete. B. ncritina larvae
are positively phototactic on release, and this behavior
facilitatedtheircollection becausetheyaggregatedonthe
illuminatedsideofdishes. Larvaewerecollectedanddis-
pensed to experimental vessels with pipettes. Experi-
ments were started within 1.5 h after the appearance of
larvae; therefore, at most, larvae would differ in age by
90 min. Larvae used in experiments were obtained only
from parent colonies kept in the laboratory less than
6 days,andparentcolonieswerere-used forreleasesover
this 5-day period in the laboratory.
Larvae ofB. neritina did not initiate metamorphosis
when exposed tobright fluorescent illumination;thusby
removing larvae from the illumination at regular in-
tervals, itwaspossible tocreatepopulationsthatdiffered
inthelengthofswimmingtime. Followingrelease, larvae
weretransferredto aglass fingerbowl containing250 ml
of0.2-^m-filtered seawater. The finger bowl was illumi-
nated from below using three 50-watt fluorescent Vita
Lites. Illumination levels ranged from 130 to 145//E
m 2s '. Due totheirsmall size, the larvae in each condi- Figure I. Schematic ofan ancestrula ofBugula neritina showing
tion could only be counted accurately after the experi- the measured parameters, crown diameter(a), basediameter(h). and
ment was over. Approximately 20-40 larvae were re- tentaclelength(c),andthecalculatedparameter,height(h).Theheight
moved from the bright fluorescent illumination at 4-h wascalculatedusingequation I in Materialsand Methods.
EFFECTS OF LARVAL SWIMMING DURATION 227
diameter of the lophophore at its base, c is tentacle 50-,
length, and // isheight ofthe lophophore.
Anadditionalthreetrialsofthisexperiment(using270
individuals) were carried out to extend the larval swim-
mingperiod by 12 more hoursand to increase the num-
ber ofindividuals at later time points. This experiment
followed an identical protocol, but larvae were sampled 45-
onlyat h, 30 h, and40 h. Duetothedifference in sam-
I
pling times, data from these three trials are presented
separately.
A second experiment was conducted to determine if
c
thetimeto metamorphosischanged asa function oflar- o
val swimming duration. In this experiment larvae were I 40H
Q
sampled at 10-h intervals, and they were transferred to
and kept separate in 2-ml multiwelleddishes. Individual
larvae were followed on an hourly basis to provide an
accuratedetermination ofwhen metamorphosiswasini-
tiated and completed.
35
Attachment (often referred to as settlement in the lit-
10 20 30
erature) ofbryozoan larvae is tightly coupled to meta-
morphosis in that attachment is not reversible and is Larval SwimmingDuration (h)
markedbyeversion ofthemetasomal(internal)sac.This
iisntlhaervfairestomfoBrupghiotglaenseptpi.camndovoetmheerntbroyfozmoeatnasmo(rZpihmomseirs vbaalsFiissgwfuirremomm2i.innigtBiipaietgriuiotonad(.nactIrtnitadicinvhaim.deunDatulrbalytairevovaeneroswifeomrneeotffaotmlholeropmwheeodtsaoisnsomvaaenlrshsuaoscu)lraltryo-
andWoollacott 1977). Thus, attachment in bryozoansis completion (eversion ofthe lophophore) ofmetamorphosis. All time
not exclusively a behavioral change associated with sub- classes are significantly different from each other (bars = 1 standard
stratum exploration. I will hereafter refer to this process error,n = 26-35 foreachcondition).
asthe initiation ofmetamorphosis. Metamorphosiswas
consideredcompleteaftertheancestrulaeverteditsloph-
ophore. 0, 10, 20, and 30 h, respectively(Fig. 2).Cumulativeper-
The number of larvae that initiated and completed cent completion of metamorphosis was sigmoidal, al-
metamorphosisineachtreatmentwasexpressedasaper- thoughthecurvewasright-shiftedforeachsuccessivelar-
centage. Theresultsofeachofthereplicateswereplotted val swimming period (Fig. 3). The amount oftime for
individuallytodeterminebetween-trial similarity. With- 50% ofthe individuals to complete metamorphosis (A' )
outexception, the general trends were similar in each of wasapproximately 37.5, 40.5, 44.0, and 49.0 h for indi-
thereplicates, andthe replicateswerethustreated assin- viduals that developed from larvae swimming0, 10. 20,
gle data sets for statistical analysis and graphing. Data and30 h,respectively(Fig. 3). Durationofmetamorpho-
from within treatments did not differ significantly from sisranged from 36 to62 h.
a normal distribution, so a factorial ANOVA was per-
formed to identify heterogeneity ofvariances within the Initiation andcompletion ofmetamorphosis
data set. Fisher's protected least significant difference
(PLSD), a post hoc test, was used to identify sources of An increased larval swimming period significantly
such variation amongthedata. affectedthepercentageofindividualsinitiatingandcom-
ANOVA
pleting metamorphosis. revealed significant
Results heterogeneityofvariancesforpercent initiation and per-
cent completion ofmetamorphosis over the duration of
Duration ofmetamorphosis theexperiment(TableI). Onaverage,closeto95% ofthe
Time required from initiation to completion ofmeta- larvae initiated metamorphosisthrough 12 h (Fig. 4). At
morphosis increased significantly foreach 10-h increase 16 h, 67 7%(mean standarderror)ofthelarvaewere
in larval swimming period (ANOVA, F = 55.7; P = initiatingmetamorphosis(P= 0.01; FisherPLSD). After
<0.0001: FisherPLSD, vs. 10, P= 0.004, 1 vs. 20and 16 h the percentage of larvae initiating metamorphosis
20 vs. 30,P= <0.0001). Meandurationofmetamorpho- decreasedslightly, although the variabilitybetween trials
siswas39 0.4 h, 42 0.3 h, 46 0.7 h, and49 0.9 h wassuch that nosignificantdeclineoccurredbetween 16
forindividualsthatdevelopedfrom larvaeswimmingfor and 28 h. On average for through 12 h, the percentage
WENDT
228 D. E.
100-
75-
larval swimming
duration
50--
r~
45 50 55 60
Duration ofMetamorphosis (h)
Figure3. BiiKiilanentina Cumulativepercentcompletionofmetamorphosisversuslarvalswimming
cpeorninoedc.tiA'ncgva5l0u%es,cotmhpelteitmieonfotro5t0h%e.ovf-atxhies.iLnidniveisdautal1s0t0o%cocmopmlpelteetimoentaamreorspthaogsgeirse,dwfeorreclaapriptryo,xnim=at2e6d-3b5y
individualsforeachswimmingtime.
of individuals completing metamorphosis was almost
identicaltothenumberoflarvaeinitiatingmetamorpho-
sis (Fig. 4). The percentage of individuals completing
metamorphosis declined significantly at 16 h to 52%
TableI
One-factorANOl'A resultsfortheeffectoflarvalswimmingduration
ondurationofmetamorphosis, oninitiationandcompletionof
metamorphosis,ontheheight,surfacearea,andvolumeofthe
lophophore, andonthemeasuredparametersofthelophophore
Parameter
EFFECTS OF LARVAL SWIMMING DURATION 229
100-,
%
Initiated
%
Completed
80-
60-
s
o
40-
20-
12 16 20 24 28
Larval Swimming Duration (h)
Figure 4. Percent initiation and completion ofmetamorphosis versus larval swimming duration in
Bugiilaneritina. Larvae keptswimmingfor 16 h were lesslikelyto both initiateandcomplete metamor-
phosis.Thelinesarestaggeredslightlyforclanty(bars = 1 standarderror;n= 5).
each of these calculated parameters (Table I), and sig- vidualsthatdeveloped from larvaeinducedtometamor-
nificant declines occurred after 8 h oflarval swimming. phose shortly after the onset oflarval swimming (Table
By28 hoflarval swimmingthepercentdecreasein mean II). Minimum numberoftentacles(16: range 16-20)oc-
lophophore height, surface area, and volume was 25%, curred in ancestrulae that developed from larvae kept
40%, and 55%, respectively, compared to individuals swimming for 24 h prior to the onset ofmetamorphosis
that developed from larvae induced to metamorphose (Table II).
shortly after the onset of larval swimming. Maximum Significant declines were observed for all parameters
number oftentacles (21: range 19-21) occurred in indi- in thesecond experimentalso. After40 hoflarval swim-
TableII
Tentaclelength,topandbasediameterofthelophophore, andrangesoltentaclenumberasafunctionoflarvalswimmingduration
(mean standarderrorofthemean):measurementsweremadeonancestrulaelessthan24hpostmetamorphosis
N
SwimmingDuration(h) TentacleLength(^m)
WENDT
230 D. E.
ming, the mean height, surface area, and volume de-
500H creased by ca. 30%, 50%, and 62%, respectively, when
compared to those of individuals that developed from
larvae induced to metamorphose shortly after the onset
450- of larval swimming (ANOVA; F - >100.00, P =
<0.0001 for each parameter; n = 3; a total of 107, 143,
and 20 individuals were measured for 0. 30, and 40 h,
400- respectively).
T Discussion
350-
Duration ofmetamorphosis
Duration ofmetamorphosison average increased as a
300 y= -4.098x +469.500 r = 0.967 function oflarvalswimmingperiod(Figs. 2and 3). After
30 h oflarval swimming, individualswere takingalmost
8 12 16 20 24 28
10 h longer to complete metamorphosis than those in-
duced shortly after the onset of larval swimming. The
observed increase in duration ofmetamorphosisisprob-
0.6- B
ably due to the utilization ofless labile energy sourcesto
complete metamorphosis. In Bugula spp. certain larval
tissues (e.g., the corona, ciliated epithelia, and vesicular
0.5- collarettes)aretransitory. Attheonsetofmetamorphosis
thesetissuesareinternalized and ultimately undergohis-
tolysis(Woollacott and Zimmer, 1978). Individuals that
0.4- swim longer before initiating metamorphosisdeplete la-
bileenergy storesto agreaterdegreeand, therefore, they
must rely more heavilyon thesetransitorytissues forthe
energy necessarytocomplete metamorphosis. It is likely
0.3- y= -O.OOSx +0.568 r = 0.960 that the biochemical processes needed to histolyze these
i I i i i i tissuesincreasethedurationofmetamorphosis. Whether
4 8 12 16 20 24 28
the increase in duration ofmetamorphosiscompromises
juvenile fitnesshasyetto bedetermined.
0.06-,
Initiation andcompletion ofmetamorphosis:lethal
effectsandthemechanismsgoverningabilitiesto initiate
0.05 - andcompletemetamorphosis
These data document a substantial lethal cost to B.
> 0.04- neritina in that a significant portion of larvae lose the
K ability overtime to initiate orcomplete metamorphosis.
Woollacott el al. ( 1989) found similar lethal costs in B.
0.03- stolonifera in that 40%. oflarvae lost metamorphic com-
petence after 10 h ofswimming. A loss ofcompetence
was also observed after 24 h oflarval swimming in Cel-
0.02- y = -0.00Ix + 0.052 |- = 0.967 leporella hyalina, another cheilostome bryozoan (Orel-
lana and Cancino, 1991). Pechenik and Cerulli (1991)
i i r i i i i
4 S 12 16 20 24 28 found that delaying metamorphosis of the aplankto-
trophic larvae of the marine polychaete Capitella sp.
Larval Swimming Duration (h) caused an 87% decrease in postsettlement survivorship
Figure5. Bugulaneritina. Height(A),surfacearea(B),andvolume in individuals that developed from larvae that were
(C)oflophophoreasafunctionoflarvalswimmingdurationinBugit/ci swimmingfor216 h,comparedtoindividualsthatdevel-
neritina. Samples oflarvae were taken every 4h, amt Mwhich time they oped from larvae induced to metamorphoseshortlyafter
wereinduced to metamorphose by exposureto 10 excessKC1 in
seawater. Each datum isthe mean of8-32 individualspooled from 5 becomingcompetent.
replicates(bars = 1 standarderror). The mechanismsgoverningtheabilityoflarvaeto ini-
IIIHISOI 1ARVAI SWIMMINCi |)|:K.\||()\ 231
tiatemetamorphosisandtheabilityoflarvaetocomplete although larvaecan successfully respond to cuesand ini-
metamorphosis are unknown. Two hypotheses have tiate metamorphosis, theyare unabletocompleteit(Fig.
been presented to explain loss of metamorphic compe- 4). This observation suggests that factorscontrolling the
tence: (1) an energetic hypothesis statingthat larvae lose ability to initiate metamorphosisare distinct from those
competence as a result ofdepleting energy reserves dur- controlling the ability to complete it. Possibly, as the
ing swimming (Lucas el ai, 1979; Pechenik, 1990; population of larvae continue swimming, a larger por-
Jaeckle, 1994; Pawlik and Mense, 1994); and (2) a sen- tion deplete their energy reserves beyond the amount
sory hypothesisstatingthat larvae are unable to respond needed to complete metamorphosis. This energetic de-
tocuesduetodegradation ofthe receptororotherlimit- pendency is further supported by the observation that
ing elements in the transduction pathway (Pechenik, larvaedieat variousstagesduring metamorphosis.
1980; Pechenik and Fried, 1995). These processes are Thus, for aplanktotrophic bryozoan larvae, ability to
probably not mutually exclusivegiven that the ability of initiate metamorphosis appears independent of energy
larvae to maintain a functional receptoral apparatus is reserves and may depend on degradation of some key
also presumablydependent on energy. element in the receptorpathway responsible forsite rec-
The ability ofB. neritina to successfully initiate meta- ognition. Incontrast, abilitytocomplete metamorphosis
morphosis may not depend directly on depletion ofen- may depend on larval energy reservesand, therefore, in-
ergeticreserves. Ifabilityto initiate metamorphosiswere directly on theduration ofthe larval swimmingperiod.
under energetic constraints, then as larvae continue to In light of recent studies on the uptake of dissolved
swim, one might expect a larger portion to deplete their organic matter (DOM) in invertebrate larvae (Langdon,
reserves below the level needed for initiating metamor- 1983; Manahan, 1983, 1989, 1990; Jaeckle and Mana-
phosis. One should then observe a continuous decrease han, 1989a, b; Shilling and Manahan, 1990; Welborn
in successful initiation throughout theduration oflarval and Manahan, 1990; Ronnestad el al. 1992; Fenaux el
swimming. Such a pattern, however, was not observed. al, 1994;Hoegh-Guldberg, 1994;Jaeckle, 1994, 1995b),
Specifically, after 16 h oflarval swimming, the ability to discussions oflarval energetics must incorporate the po-
initiate metamorphosis was not negatively correlated tential metabolic contributionsofthisalternativeenergy
with larval swimmingduration (Fig. 4). Furtherdata for source. It should beemphasized, however, that although
DOM
addressing energetic constraints as an explanation for the transport of by larvae is well established, the
lossofmetamorphiccompetence (i.e.. ability to initiate) metabolic use ofthis additional energy pool and its rele-
in B. neritina is provided by Jaeckle (1994) in his respi- vance to larval ecology remain equivocal (Pechenik,
rometrywork with larvae. Ifweassumean averagerespi- 1990; Jaeckle, 1995a). Experiments are needed that
ration rateof0.1 18 mJ larva"1 h"' (calculated from data compare metamorphic competence, maximum swim-
in table 5; Jaeckle, 1994) and an average energy content ming duration, and size after metamorphosis between
DOM
of 15.24mJ larva"' for larvae of B. neritina (Jaeckle, individuals that have access to and those that
1994), by 16 h of swimming, larvae will have depleted do not.
12% oftheirenergy content. Whethera 12% decrease in
larvalenergy reservesissufficienttocausea lossofmeta- Lophophoreparameters:suhlethaleffectsandtheir
morphic competence is unknown, but on average over potentialcoststojuvenilefitness
60% oflarvae retained metamorphic competence at this
time. These data suggest that an alternative mechanism Inadditiontothelethal costs, such asthelossofmeta-
(e.g., receptor degeneration) may be governing the loss morphic competence and the inability oflarvae to com-
ofmetamorphiccompetence in B. neritina. plete metamorphosis, there exist more subtle, sublethal
Although the ability to initiate metamorphosis may costs to juvenile fitness. These results document that
not be under energetic control, the ability to complete mean sizeoftheancestrularlophophoredecreasesaslar-
metamorphosis is likely to be constrained energetically. val swimming period increases (Table II, Figs. 5a, b, c).
Thefactthatcompletionofmetamorphosiscontinuesto After a larval swimming period of28 h, there were sig-
decrease significantly throughout the duration oflarval nificant reductions in all parameters ofthe lophophore.
swimming indicatesthat energetic limitationsexist. The Sublethalcoststojuvenile fitnesshavealsobeen demon-
exact portion ofindividuals that initiate but fail to com- strated forthecongenerB. stolonifera(Woollacott el ai,
plete metamorphosis is represented by the divergence of 1989) and the barnacle Balamtsamphitrite(Pechenik et
the two curves after 16 h (Fig. 4). On average by 28 h of al.. 1993). The observed reduction in lophophore size
larval swimming, only 30% ofthe individuals that initi- may affect the ability ofancestrulae to clear food parti-
ated metamorphosis successfully completed it. The di- cles from their surrounding medium. The surface area
vergence between the ability of larvae to initiate and and volume ofthe lophophore have not been examined
complete metamorphosis after 12 h demonstrates that explicitlyasvariablesinbryozoan feedingrates,although
WENDT
232 D. E.
the height ofthe lophophore has been shown to be posi- Buss. L. VV. 1979. Bryozoan overgrowth interaction the interde-
t1i9v8e6l)y.coTrhreelaotbesdewrivtehdpdaerctircelaesevelioncihteyig(hBtest(Faign.d5Tah)ormpaey, Bussap,enndLd.seWun.scp,eeanonsfdicoJon.m-pfBee.etCdi.etriJoaancbkufsnoordnas.npca1ce9e:81ae.nvdidPfelonoacdne.ktoNofantiinucrsfeio/2no8dd1e:apvl4aei7tl5ia-bo4inl7.i7tJ.y
have a marked effect on competitive ability ofancestru- E.\f>. Mar. Biol. Ecol. 49: 151-161.
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ion (Keough, 1984; Roberts el at.. 1991). Furthermore, vertebrates.Pp.3-12inReproduction,Genetics,andDistributionoj
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ofBugii/aneritina isashighas 70% withinthefirstweek. Kenaux,L.,M.F.Strathmann,andR.R.Strathmann.199-4. Fivetests
He attributed this high mortality rate to microhabitat offood-limitedgrowth oflarvae in coastal waters by comparisons
differences, but furtherevaluation in thecontext ofpost- ofratesofdevelopment and formofechinopleutei. Lininol Ocea-
metamorphic conspecific competition is needed. Also, m>/>.3989-94.
bceoclaounsyerreeapcrhoedsucaticoenrtianinB.mnienriitmiunamocscizuers(coun.ly1abftiefrura- HadfaMineetlaadn,maloMyrs.pihsGoo.sfis1s9t7io8ml.uMluasrMieanntedamrIoenrsvppeorhntosesebi.rsaPtepinL1ma6ar5vr-ai1en7,e5Fm.mo-SlS.leuCtshtcliaeanmealnnatdrvaaMne.d:
cations) and total reproductive output in colonial ma- E. Rice.eds. ElsevierNorth-Holland,NewYork.
rine organisms is a function of overall colony size Highsmith, R. C., and R. B. Kmlet. 1986. Delayed metamorphosis:
(Keough, 1989), individuals with a greater ability to effectongrowthandsurvival ofjuvenilesanddollars(Echinoidea:
gatherfoodwillattainthereproductivethresholdsooner. Clypeasteroida).Bull. Mar. Sci.39:347-361.
My results demonstrate that increasing the duration of Hoegvahl-Gsutlagdebeorfgt,hOe.c1r9o9w4n.-of-UtphtoarknesotfardfiisssholAvceadnotrhgaasniiecrmpaltatnceir.byMalrar.-
larval swimming in the aplanktotrophic larvae ofB. ner- Bin/ 120:55-63.
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may ultimatelycompromisecolony fitness. by lecithotrophic larvae of Bugiila neritina (Bryozoa: Cheilosto-
Thisstudyclearlydemonstratestheeffectsofextended mata). Mar Biol. 119: 517-523.
larval swimming on the metamorphosis and develop- Jaeckle, \V.B. I995a. Variationinthesize,energycontent,andbio-
ment of postlarval structures in marine invertebrates. cohfelmarivcaalldecvoemlpoopsmietnito.nPopf.i4nv9e-r7t8ebirnatEecoelggosg:ycoofrMraelraitnesetIonvtehretemboradtee
The lethal and sublethal effectsaccrued to individualsas Larvae. L. R. McEdward,ed.CRCPress, BocaRaton,FL.
aresultofeventsthatoccurduringthelarval period have Jaeckle,\V. B. I995b. Transportandmetabolismofalanineandpal-
alsobeen shown in fish (McCormick and Molony, 1992) miticacid by field-collected larvaeofTedania ignis(Porifera, De-
and amphibians (Audo el /., 1995). Understanding the mospongiae): estimated consequences oflimited label transloca-
sficsohpaendofatmhpehsiebeifafencstswiilnl rmeaqruiinreesitnuvdeiretseobrfattheespahsyswieollloga-s Jaectmkielotena.,b\oV;l.<i>/sB.mB,ulbalyn.dl1a8Dr9.v:aeI1.o5fM9at-hn1e6a7hm.aarni.ne19w8o9ar.m UArmecihnioscaacindpnup(Etcahkieuraan)d.
ical underpinnings ofthese effects and the costs tojuve- anewspeciesinaxenicculture.Biol. Bull. 176:317-326.
nile fitness. Jaeckle, W. B.,and D.T. Manahan. I989b. Feedingbya"nonfeed-
ing" larva: uptakeofdissolvedaminoacids from seawaterby leci-
thotrophic larvae ofthe gastropod Haliotis nijescens Mar. Biol.
Acknowledgments
103:87-89.
I thank Sherry Reed at the Smithsonian Marine Sta- Keoulagrhv,aeMo.ftJ.he1b9r8y4.ozoaKninB-ur.etcfuolganinetriiotninaa.ndEvtohleutspiaotnia3l8:di1s4t2ri-b1u4t7i.on of
tionatLinkPort, Fort Pierce, Florida, forgenerouslycol- Keough,M.J. 1987. Dispersalandpopulationvariation inthebryo-
lectingalltheanimalsused intheseexperiments. Colleen zoan Bugulaneritina. Ecology68: 199-210.
Cavanaugh, Edward Seling, Michael Temkin, and Rob- Keough, M. J. 1989. Variation in growth rate and reproduction of
ert Woollacott (all of Harvard University) provided thebryozoanBiiiiiilaneniina. Biol. Bull 177:277-286.
thoughtful discussions and comments. Jan Pechenik Langdon.C.J. 1983. Growthstudieswith bacteria-freeoyster(Cras-
(Tufts University) and an anonymous reviewer offered s1o6s4l:r2ea27g-i2ga3s5).larvae fed on semi-definedartificialdiets. Biol Bull
valuablecommentsandcriticismsthatgreatly improved Lucas, M. I., G. Walker, D. L. Holland, and D.J.Crisp. 1979. An
thispaper. energy budget for the free-swimming and metamorphosing larva
ofBalanusbalanoide.t(Crustacea:Cirripedia). Mar. Biol. 55:221-
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