Larval Morphometrics and Influence of Adults on Settlement in the Gregarious Ophiuroid Ophiothrix fragilis (Echinodermata)

2005·3.2 MB·English

by  Raphael Morgan

Reference: Biol. Bull. 208: 92-99. (April 2005)
2005 Marine Biological Laboratory
Larval Morphometrics and Influence of Adults on
Settlement in the Gregarious Ophiuroid
Ophiothrix fragilis (Echinodermata)
RAPHAEL MORGAN1'* AND MICHEL JANGOUX'-2
1 Universite Libre tie Bruxelles. Laboratoire tie Biologic Marine (CP 160/15), 50 Av Franklin Roosevelt,
BI050 Brussels, Belgium; and : Universite de Mons-Hnimiut, Laboratoire de Biologie Marine,
20 Place dii Pan; B7000 Mons, Belgium
Abstract. The development of Ophiothrix fragilis was the rudiment ofthejuvenile is constructed in preparation for
documented using light microscopy, and the allometry of settlement. As a consequence, functional requirements and
larval growth was quantified. Larval development to the ontogenic changes can impose demands on larval design
suspendedjuvenile stage took 21 days underconditions that (McEdward, 1984. 1986: McEdward and Herrera. 1999).
were probably optimal compared to those in the plankton. Therefore, the analysisofthe developmentoffeeding larvae
Larval shape changed through development as the larval requires an understanding of the requirements and capabil-
body and arms grew. Growth of the posterolateral larval ities of particular stages as well as an understanding of the
arms was continuous throughout development, even during patterns of larval growth that define the developmental
metamorphosis when the larva became endotrophic. During trajectory (McEdward and Herrera, 1999).
thisperiod, theselarval armsfunction as locomotory organs, Planktotrophic plutei of ophiuroids can develop via two
and theircontinuous growth is probably essential to support pathways depending on their metamorphosis, which occurs
the juvenile as it increases in density through development in the plankton and precedes settlement (Mladenov, 1985a).
of its calcareous plates. In induction assays using adult In type I developers, metamorphosis is characterized by the
conspecifics, initiation of metamorphosis was spontaneous. regression of all larval arms except for the posterolateral
Release of the posterolateral arms was induced by the pair and the differentiation of a juvenile between these. In
presence of adults. This response is likely to enhance a type II developers, all larval arms regress and a vitellaria
juvenile's chance of recruiting to a suitable habitat in the that differentiates into a juvenile is formed. The larval
Ophiothrixfragilis beds of the North Sea. development of type I developers has been described in
detail for four species (MacBride. 1907; Narasimhamurti.
Introduction 1933; Olsen, 1942; Tominaga et al., 2004).
The brittle star Ophiothrix fragilis (Abildgaard, 1789)
Planktotrophic larvae of marine benthic invertebrates occurs in high densities throughout the English Channel-
face two sets ofchallenges during development (McEdward North Sea region where the major populations are known
and Herrera, 1999). Firstly, they must function as feeding and have been studied throughout the late 19th and 20th
planktonic organisms which must acquire food, swim, con- centuries (Allen. 1899; Warner. 1970; Holme. 1984;
trol their position in the water column, and select a micro- Davoult et al., 1990). These populations are considered
habitat. Secondly, they must undergo ontogenetic transfor- stable through time and space. O.fragilis is a type I plank-
mationsthat result in continuouschanges in body form. This totrophic developer whose development was described by
is especially true in the later stages of development when MacBride (1907). The fact that in the English Channel-
North Sea regionjuveniles are preferentially found on adult
Received 26 May 2004; accepted 4 February 2005. conspecifics has led many to believe that settlement occurs
*To whom correspondence should be addressed. E-mail: rmorgan preferentially on adults (Warner. 1971; Davoult etal., 1990;
'"ulb.ac.be Morgan and Jangoux, 2004). Morgan and Jangoux (2004)
92
OPHIOTHRIX FRAGILIS LARVAL DEVELOPMENT 93
have also shown the close relationship between juveniles (body length) and the length of the longest posterolateral
and adults in this species; this relationship is particularly rod (Fig. 1).
evident in the wayjuveniles respond to adults at a distance. To establish the chronology ofdevelopment and morpho-
In this study, the development and growth of the larval logical change, the larvae were observed every 1-2 days
body and skeleton of O.fragilis was followed to document under a microscope with or without polarized light (obser-
the larval morphometric changes. Considering the well- vation of the skeleton). The timing of development or re-
known aggregative behavior of O. fragilis, the role that gression of various features (e.g.. larval arms, juvenile
conspecific adults may play in induction of settlement was mouth) was determined and used as a quantifiable character
investigated. when at least 50% of the observed larvae had acquired the
new feature.
=
Late larvae from a culture (n 1) were used to test for
Materials and Methods induction of metamorphosis and settlement. They were
placed in a small aquaria filled with 500 ml of filtered
In 1999, specimens of Ophiothrixfragilis were collected autoclaved seawater with (experimental) or without (con-
by scuba diving (20-25 m) from Wemeldinge (Zeeland, trol) an adult conspecific. In total, 90 larvae divided into
Netherlands). Individuals were taken during the period of three trials were used for each experimental and control
sexual maturity between the monthsofMay and Augustand assay. The larvae were separated from the adult by a 90-^im
brought back to the Marine Biology Laboratory in Brussels. mesh. In the case of metamorphosis induction assays, the
They were kept in aclosed-circuit aquarium underthe same larvae were observed for 48 h to check whether adult
abiotic conditions oftemperature and salinity asthose found conspecifics could initiate or accelerate metamorphosis. In
in the field (16-18 C. 329ff). the case of settlement induction assays, the number of
Fertilizations assays were made using ripe individuals. settled individuals was counted after 12 h in experimental
Individuals were considered ripe when their gonads (white and control batches.
testes; orange ovaries) could be seen through the extended
wall of the bursae. Water used for fertilizations and subse-
quent larval cultures came from the sampling site. Water
was allowed to settle for 48 h, then filtered ( 15 jam) before
use.
In each fertilization assay, one male and one female were
placed in a small aquarium with 500 ml of filtered and
aerated seawater(16 C. 32</rr). The male was agitated for5
severy minute until it startedtoliberate itsgametes. Release
of sperm induced the female to spawn, and the male was
removed (Morgan and Jangoux, 2002). Embryos at the
gastrulastage were transferred to 30-1 larval rearing tanks at
a density of 500 embryos/liter.
Larvae from a single spawning event were reared under a
12:12 dark/light photoperiod at 16 C and 32%c salinity.
Seawater was constantly aerated, and half the volume of
water from each tank was siphoned off every 5 days and
replaced with filtered seawater. At the onset of larval exo-
trophy (3rd day after fertilization) the larvae were fed the
diatom Chaetoceros calcitrans at a concentration of30.000
cells larva"1 day"1
.
The larvae from this culture were followed from fertili-
zation to completion of development (settled juveniles). bup
Every 1-2 days, a subsample of 30 to 50 larvae was brp
photographed, using a digital camera mounted on a dissect-
ing microscope. Measurements were then made using an
image analysis program (UTHSCSA image tool developed Figure 1. Ophiothrixfragilis. Drawingofa5-day-old larva(A) and a
at the University of Texas Health Science Center at San 21-day-old suspendedjuvenile (B). showing the measurements taken (not
Antonio. Texas, and available from the Internet through toscale),b.l.: bodylength:pi. 1.: posterolateralrodlength; al: anterolateral
http://ddsdx.uthscsa.edu/dig/itdesc.html). Two measure- aporsmtse:rolbartpe:rablraachrima:lppoo:dipao;stbourpa:l baurcmcsa;ltap:odtiear;mijnma:l jaurvteicnliel;ettm:outtehr;minpail:
ments were taken on each individual: the height ofthe body tentacle.
94 R. MORGAN AND M. JANGOUX
Results
Lamil development
Table 1 gives the chronology of development of
Ophiothrixfragilis from fertilization through appearance
of settledjuveniles. Under our rearing conditions, devel-
opment was completed in about 21 days. A well-formed
oval larva with a vacuolated crest appeared 12 h after
fertilization (Fig. 2A). The first pair ofarms, the postero-
lateral ones, appeared after 24 h (Fig. 2B), and on the 3rd
day the openings of the mouth and anus marked the start
of the exotrophic larval period. The following days were
essentially characterized by the acquisition of additional
arms : the anterolateral. postoral and postdorsal pair (Fig.
2D-G). From the 13th day, the left hydrocoele, visible by
transparency, started to differentiate five lobes whose
development was completed 2 days later, marking the
onset of metamorphosis (Fig. 2H). Metamorphosis was
initiated when the complete tive-lobed hydrocoele began
to encircle the esophagus and the so-called ophiurid
rudiment began to appear. The larval arms, except the
posterolaterals and their respective skeletal rods, started
to regress (Fig. 21, J). Rod regression occurred parallel to
Table 1
Ophiothrix fragilis: Chronology ofmajordevelopmentalstages and
events
Time after fertilization (days
Developmental stages and
events
OPH1OTHRIX FRAG1L1S LARVAL DEVELOPMENT 95
Figure 2. Ophiothrixfragilis. Larval development: (A) 12-hour-old larva (inset shows developing larval
skeleton); (B) 24-hour-old larva (2-arm endotrophic pluteus); (C) 2-day-oldlarva (2-arm endotrophic pluteus);
(D) 3-day-old larva (6-arm exotrophic pluteus); (E) 5-day-old larva (6-arm exotrophic pluteus); (F) 7-day-old
larva (8-arm exotrophic pluteus); (G) 11-day-old larva (inset shows a general view of the 8-arm exotrophic
pluteus); (H) 15-day-old larva; (I) 16-day-old larva (metamorphic larva); (J) 19-day-old individual (suspended
prejuvenile) (inset shows the regression of the larval skeleton [except for the posterolateral rods] and the
developingjuvenileskeletalplates); (K)21-day-oldindividual atthesettlementstage (insetshowsthecomplete
juvenile skeleton and the remaining posterolateral rods), al: anterolateral arms: h: hydrocoele;j: juvenile; pd:
postdorsal arms; pi: posterolateral arms; po: postoral arms; rla: regressing larval arms (also rl in part J); vc:
vacuolated crest. Scale bars: 50 ;um (A); 100 /urn (B. C. F, G, H, I); 200 /am (D. J, K).
96 R. MORGAN AND M. JANGOUX
30 30 Induction ofmetamorphosis and settlement
1600-
1400- 30 30 I I
"? 1200-
II
1000 50
O)
g 800- 50
TJ 600- 50 50 I
2 50
50
-r 400- 50 I
d. 50.5
200-
012345678
9101112131415161718192021
Days
B 300-,
250-
200-
150-
100J
Jl
50-
012345678
9101112131415161718192021
Days
OPH1OTHRIX FRAG1L1S LARVAL DEVELOPMENT 97
and metabolism, which also increase during development, lowed the appearance of the five-lobed hydrocoele. Delay
especially during rudiment formation. While this could be could therefore have occurred, not due to the absence ofan
what happens in echinoplutei, which do not lose theirability induceras inechinoids since in ophiuroids metamorphosis
to feed during rudiment differentiation, in ophioplutei the begins spontaneously but due to some other factor, such
futurejuvenile (orrudiment) is formed from the larval body as a shortage of food resources. In type II developers,
and the larva passes through a second endotrophic period delayed metamorphosis is also known to occur at this stage
during which the juvenile digestive tract differentiates. (Mladenov, 1985b). Furthermore, Turon et al. (2000, p.
Therefore, the posterolateral arms would essentially be used 204, fig. 1 ) illustrated a suspended juvenile of O. fragilis
as locomotory organs and not as feeding-locomotory organs bearing two extra articles on each arm. Our results have
as in echinoids (McEdward, 1984, 1986). As the juvenile shown that suspendedjuveniles can settle at a much earlier
differentiates sodoits skeletal plates, which would probably stage, indicating a probable delay of settlement in Turon's
increase its weight and make it sink. Although active move- specimen. Delayed settlement has been observed in other
ment downward probably also occurs, the increase in species, and some authors consider the suspended juvenile
growth rate ofthe posterolateralrodscould helpcompensate to be an exploratory stage, as the vittelaria is considered to
for the reduction of the other larval arms during metamor- be in type II developers (Stancyk, 1973; Strathmann, 1978;
phosis, thus allowing the developing juvenile to remain in Mladenov, 1979, 1985b). This interpretation would indicate
the plankton. a probable selection of settlement site.
Metamorphosis in type I developers has been studied in The larvae of many species settle and metamorphose
the past by MacBride (1907) on Ophiothrix fragilis, selectively on substrata with specific physical or biological
Narasimhamurti (1933) on Ophiocoma nigra, Olsen (1942) characteristics (Scheltema, 1974; Crisp, 1976; Burke,
on Ophiopholis aculeate, and Tominaga et al. (2004) on 1986). Juveniles of O. fragilis in the North Sea-English
Ophiodaphneformata. As numerous authors have already Channel region have been exclusively found on conspecific
established (Burke, 1989; Hendler, 1991; Byrne and Sel- adults (Warner. 1971; Davoult et al.. 1990; Morgan and
vakuramaswamy, 2002), metamorphosis begins spontane- Jangoux, 2004), whereas juveniles of their Mediterranean
ously in the water column when the five-lobed hydrocoele counterparts are found gregariously on sponges before mov-
starts to encircle the esophagus and the larval arms begin ing to the adult habitat where, once growth has taken place,
to regress, and ends with the loss of the two remaining they live solitarily (Turon et al.. 2000). This has led many
posterolateral arms. Therefore, ending of metamorphosis in authors to think that the feeding capabilities ofjuveniles in
ophiuroids coincides with the settlement of the fully func- the first stages ofbenthic life would need to be enhanced by
tional juvenile. Accordingly, a perimetamorphic period, as the suspension-feeding activities of other organisms
defined by Gosselin and Jangoux (1998) for echinoids, can (Warner, 1971; Turon et al.. 2000, Morgan and Jangoux,
be determined. In echinoids the perimetamorphic period 2004). Survival ofthe juveniles therefore depends on find-
starts at larval competence, includes metamorphosis and the ing a suitable settlement site.
endotrophic postlarval development, and stops at the acqui- In ophiuroids, metamorphosis begins spontaneously in
sition ofjuvenile exotrophy. In ophiuroids the perimetamor- the plankton. However, loss of the two posterolateral rods
phic period starts with the initiation of metamorphosis and and settlement, although it can also happen spontaneously,
ends with the settlement of an exotrophic juvenile. So is clearly enhanced in O. fragilis by the presence of adult
metamorphosis in echinoids is rapid, but the benthic post- conspecifics. This is the first case in which an actual induc-
larvastill needs to develop tobecome exotrophic; metamor- tion of settlement has been revealed in ophiuroids. Contact
phosis in ophiuroids is gradual, but it ends with a benthic between the settlement stage and the adult is not necessary
exotrophic juvenile (juvenile mouth open; see Morgan and to induce the breakage of the posterolateral rods. Loss of
We
Jangoux, 2004). see that, although the pathways to the their posterolateral rods in proximity to an Ophiothrixfra-
exotrophic juvenile are different, both rely on a rapid es- gilis bed would ensure that thejuveniles settle on a suitable
tablishment in the benthos. site. Furthermore, the hooked spines onjuveniles that have
Although delay ofmetamorphosis or settlement is known lost their posterolateral rods would help them cling to the
to occur in a number of marine invertebrates (Highsmith adults (Morgan and Jangoux, 2004). While our experimen-
and Emlet, 1986; Pechenik, 1990; Vaitilingon et al., 2001), tal setup has shown that the proximity of an adult conspe-
it is not known ifit takes place in ophiuroids and, ifit does, cific can induce settlement, we still do not know whether
upon which developmental stage it operates. Although juveniles at the settlement stage need to be close to a
McBride (1907) described a five-lobed hydrocoele appear- conspecific adult or can detect them from farther away.
ing after 16-20 days of development in O. fragilis. encir- MacBride (1907) noted that when larvae in the plankton
clement ofthe esophagus, and therefore metamorphosis, did were reaching the end of their metamorphosis, they sank
not occur until a few days later. This does not fit our lower in the water. We also observed this in our cultures.
observations, in which the encirclement immediately fol- Juveniles that lose theirposterolateral rods spontaneously
98 R. MORGAN AND M. JANGOUX
will rain down on the available substrata. Ifit is unsuitable, Gosselin, P., and M. Jangoux. 1998. From competent larva to exotro-
heavy mortalities would supposedly occur. However, resus- pohfiPcajruavceenniller:otausmo/rnpihdoufsun(cEtcihoinnaoldesrtmuadtyao.fEtchheinpoeirdiam)e.taZmooormpohripchpoelroigoyd
pension. drifting, and recolonization following settlement 118: 31-43.
has been demonstrated in some ophiuroids (Hendler et til.. Hendler, G. 1991. Echinodermata: Ophiuroidea. Pp. 355-511 in Rcpro-
1999) Juron el til. (2000) have postulated that recoloniza- dnetionnfMarineInvertebrates. Vol. VI. EchinodermsandLophophor-
tion through resuspension could contribute to the mass ates. A. C. Giese. J. J. Pearse. and V. B. Pearse. eds. Boxwood Press.
recruitment of O.fragilisjuveniles on sponges in the Med- HendPlaceirf.icGG.,roCv.e,CC.AB.aldwin, D. G. Smith, and C. E. Thacker. 1999.
iterranean. It could also be that suspended juveniles are Planktonic dispersal ofjuvenile brittle stars (Echinodermata: Ophiu-
induced to settle by some cue released by the sponges, and roidea) on a Caribbean reef. Bull. Mar. Sci. 65: 283-288.
further studies need to be made along that line. Highsmith, R. C., and R. B. Emlet. 1986. Delayed metamorphosis:
Induction of loss of the two posterolateral rods and set- effect on growth and survival ofjuveniles sand dollars (Echinoidea:
tlement implies the recognition of an inducer. In echinoids, HolCmley,peaNs.teAr.oi1d9a)8.4.BullF.luMcatura.tiSoenis. 3o9f:O3p4hi7o-t3h6r1i.xfragilis in the western
the primary podia are used to test the substrata before English Channel. J. Mar. Biol. Assoc. UK64: 351-378.
metamorphosis (Burke, 1980; Gosselin andJangoux. 1998). MacBride, E. W. 1907. The development of Ophiothrix fragilis. Q. J.
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have demonstrated the role that the terminal tentacles of Growth and form of an echinopluteus. J. E.\p. Mar. Biol. Ecol. 82:
settled juveniles of O. fnigilis play in the recognition of McE2d5w9a-r28d7,.L. R. 1986. Comparative morphometrics of echinoderm
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Mladenov, P. V. 1979. Unusual lecithotrophic development ofthe Ca-
Acknowledgments ribbean brittle star Opliiathrix oerstedi. Mar. Biol. 55: 55-62.
We are grateful to two anonymous referees for construc- Mladofentohve,CPa.rVi.bb1e9a8n5a.brittOlebsesrtavratOipohnisootnhrriexprsotdiuecntsioonni a(nEdchdienvoedleorpmmaetna:t
tive comments. Our thanks go to B. Blockmans, Ph. Fernet, Ophiuroidea). Bull. Mar. Sci. 36: 384-388.
and D. Gillan for help during scuba diving missions. R. Mladenov, P. V. I985h. Development and metamorphosis ofthe brittle
Morgan is a recipient of an F.R.I.A. grant and a grant from starOpium,imapninila:evolutionaryandecologicalimplications.Biol.
the David and Alice Van Buuren foundation. This is a Hull. 168: 285-295.
contribution to the CIB1M (Centre Interuniversitaire de Morgan, R.,and M.Jangoux.2002. Reproductivecycle and spawning
induction in the gregarious brittle-star Ophiothrixfragilis (Echinoder-
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