Hendler 1975

AMER. ZOOL., 15:691-715 (1975).
Adaptational Significance of the Patterns of Ophiuroid Development
GORDON HENDLER
Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543
. and
Biological Sciences Group, University of Connecticut, Storrs, Connecticut 06268
SYNOPSIS. There is only limited information on ophiuroid developmental patterns, larvae

being known for only 4% of the 2000 living ophiuroids. Three modes of development are
distinguished (planktotrophic, direct, abbreviated) on the basis of egg size and number, larval
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form and life span, and post-larval size. This generalization is applied to an analysis of the
larval form(s) of deep-sea ophiuroids and the ancestral ophiuroid larva. Quantitative infor-
mation on rate of development and reproductive period, which has been lacking for
viviparous ophiuroids, is presented for Axiognathus ( = Amphipholis) squamatus on the basis of
original size-frequency data. Reproduction is seasonal in the population studied and de-
velopment to metamorphosis takes no longer than for planktotrophic species though the
brooding period ranges from 3 to 7 months. Additional data indicate post-larvae of
planktotrophic species have fewer arm segments than newly-hatched viviparous young,
supporting the hypothesis that large size of juveniles is characteristic and selectively advan-
tageous for viviparous ophiuroids.
INTRODUCTION grand style a groundwork for future re-

search (1898-1938). Major contributions on
Johannes Miiller (1846, 1848) initiated ophiuroid development have prompted
the study of ophiuroid larvae with his re- successive revisions of evolutionary theory.
port "Uber Pluteus paradoxus, die Larve Such are the works of MacBride (1907),
einer Ophiura und ihre Metamorphose," Mortensen (1921), Grave (1903, 1916),and
and Theodor Mortensen provided with Fell (1945, 1946, 1967).
Recent contributions such as those of
Fenaux (1963, 1968, 1969), Patent (1970),
Contribution No. 3438 of the Woods Hole and Hendler (1973) have not yet been
Oceanographic Institution, and Contribution No. 95 coordinated with the classical literature,
of the Marine Research Laboratory, University of and this is, in part, the objective of the pre-
Connecticut, Noank, Connecticut.
I would like to thank Fu-Shiang Chia, David R. Franz, sent paper. This re-examination is made
Gilbert Rowe, Rudolf S. Scheltema, and Amy from an ecological rather than the custom-
Schoener for reading and criticizing this manuscript; ary phylogenetic point of view, ecological
A. Ament, D. Ashton, D. Leibowitz, J. Pechenik, C. groups of larvae being defined on the basis
Schaefer, and N. Scott for examining early drafts; and of egg size and number, larval form, larval
librarians of the Marine Biology Laboratory, Woods
Hole, and the University of Connecticut, Storrs for life span, and juvenile size.
their assistance. Three types of development in
Preparation of this paper and original research de- ophiuroids are designated: Planktotrophic
scribed were aided by an NDEA Title IV Fellowship, a developers with large, slow-growing larvae
University of Connecticut Summer Fellowship, NSF
Travel Grants GB-8258 and GB-27162, and a and relatively small post-larvae produced
W.H.O.I. Postdoctoral Fellowship. Portions of this in prodigious quantities; Direct developers
paper are from a dissertation submitted to the Univer- including viviparous (and possibly brood-
sity of Connecticut in partial fulfillment of the re- ing) forms with small numbers of slow-
quirements for a Ph.D.
The present address of the author is: Smithsonian
growing embryos and post-larvae which
Tropical Research Institute, P.O. Box 2072, Balboa, hatch at an advanced stage; and Ab-
Canal Zone 8. breviated development with extremely rapid
691
692 GORDON HENDLER
development and small post-larvae pro- nathus (= Amphipholis) squamatus (Morten-

duced from moderate numbers of yolky sen, 1898; Fell, 1946). In this species and in
eggs. Abbreviated development is found in 0. hexactis cleavage appears to be total and
lecithotrophic and demersal forms and equal, while in Amphiura stimpsoni cleavage
predicted for some reduced plutei with un- is meroblastic. A. squamatus and O. hexactis
certain development. are known to produce coeloblastulae and
Amphipholis torelli has a stereoblastula. Am-
PATTERNS OF OPHIUROID DEVELOPMENT: QUAL- phiura belgicae has a telolecithal egg and ap-
ITATIVE parently a discoblastula while A. stimpsoni
may have either a discoblastula or periblas-
At present, ophioplutei or viviparous de- tula as judged from the incomplete descrip-
velopment has been described for about 4% tions of their development. The process of
of the known ophiuroids and there are coelcm formation in viviparous ophiuroids

enough unassigned larvae to account for seems undiversified compared with cleav-
another 3%. Of the approximately 2000 age and blastulation, but only three species
species of recent ophiuroids, about 55 are have been studied in this regard. Axiog-
reported as viviparous, 23 have ophioplutei nathus japonicus, A. squamatus, and
and at least 48 ophiopluteus species without Ophiomyxa brevirima apparently undergo
putative adults have been named. The schizocoely within a mesodermal mesen-
adult stages are known for 11 of the 17 chyme cell mass or within the general
reported abbreviated larval forms. For mesoderm.
about 50 other species of ophiuroids, some Embryos as such have been described for
information exists regarding the diameter few viviparous species. In Axiognathus
or number of eggs. The larval form of these japonicus and A. squamatus they are attached
species could be deduced if there were a to an "umbilicus" produced by the bursa
reliable correlation between gamete size or and in other species they have been de-
number and the mode of development. scribed "within thin extensions of the bur-
Concurrent appearance of young in the sa" though it is not clear whether or how the
genital bursae (brood sacs) and large yolky bursal wall is modified. The embryo of
eggs have been adopted as the criteria of Stegophiura sculpta has a variable number of
viviparity. Thus, many species have been "provisional spicules" which are resorbed
characterized as viviparous while the actual early in morphogenesis, while A. japonicus,
process of development in most viviparous A. squamatus, and 0. hexactis have irregular
ophiuroids is not known. Even the site of but paired larval skeletons. Of the latter two
brooding in viviparous forms is open to species, A. squamatus lacks embryonic cilia-
doubt. Seven species reported by Morten- tion but O. hexactis possesses a thick perioral
sen to have intraovarian development were band. It is also known that A. squamatus,
never convincingly illustrated. Intraova- Ophiacantha vivipara, and S. sculpta lack any
rian development would seem a necessity embryonic anus and mouth while 0. hexactis
for Amphiufa monorima, which lacks bursae, has both (Thomson, 1876; Mortensen,
but the process of intraovarian develop- 1898, 1921, 1933d, 1936; Fell, 1941a, 1946;
ment is detailed for only one species Murakami, 1940, 1941).
Ophionotus hexactis (Mortensen, 1920a, Aside from viviparous development,
1921, 1936). Likewise, adequate informa- where juveniles are maintained in the bur-
tion on reproduction is unavailable for sae, two possible cases of brooding have been
species which, according to Mortensen, reported in the ophiuroids. Ophiophycis
have one or another form of hermaphro- gracilis holds its embryos beneath the disc,
ditism. while the embryos of Astrotoma waitei may
The sole viviparous species whose com- develop on the oral surface of the arms
plete development has been described (Mortensen, 19336; Fell, 1952). Interest-
(cleavage, germ-layer formation, or- ingly, Ophiophycis is among the smallest of
ganogenesis, and metamorphosis) is the ophiuroids and its 10 eggs, each 0.15 to
tiny cosmopolitan hermaphrodite Axiog- 0.20 mm in diameter could conceivably be
PATTERNS OF OPHIUROID DEVELOPMENT 693
too large for bursal brooding, hence exter- mechanisms for ontogenesis of coelomic
nal brooding. sacs, and larval arms and skeleton. Arms
"Kirk's ophiuroid," studied by Fell and their skeletal supports are resorbed in
(19416), shows a clear case of direct develop- different numbers, order, and extent in dif-
ment. Development of this unknown ferent species as reviewed by Mortensen
species occurs within egg capsules of un- (1931). For example, it is typical of the
known origin and structure. The egg is ophiothricids to discard the postero-lateral
about 0.5 mm in diameter and gives rise to a arms and body skeleton during metamor-
juvenile presumably of the same size. The phosis. Other characters of possible sys-
embryo, superficially bilateral on account tematic and evolutionary importance in-
of two "epibolic crests" formed during gas- clude vibratile lobes of ophiocomids, simple
trulation, ultimately assumes a penta- versus compound skeletons, and transverse
radiate shape. A juvenile emerges from the or median rods, as well as changes in cilia-

egg capsule after 15 days, its enteron de- tion during development (Grave, 1903;
velops with the mouth at or near the site of Mortensen, 1921). Functional explanations
the blastopore, the coelom develops by for modifications of "typical" ophiopluteus
splitting of the mesoderm cell mass and the morphology have not been put forward.
skeleton finally materializes after two arm Ophiuroids with abbreviated development
segments have differentiated. This process have free-living larvae but do not constitute
of development is unique. Lacking con- an embryologically or systematically
trary evidence, Fell's deduction that this is a homogeneous group. Several abbreviated
modification of a form with viviparous de- forms are pluteus-like but very rarely sam-
velopment may be reasonable, but the pled in the plankton. For example, Ophio-
"missing link," a truly viviparous species pluteus claparedi has only vestigial larval
with a similar type of development, is un- arms but possesses a larval skeleton, dense
known. ciliation, a complete gut, and coelomic
Ophiopluteus larvae show more uniform- pouches including a well-developed hydro-
ity than the embryos of viviparous species. coel. The morphology of Ophiopluteus
In the former, holoblastic cleavage re- metschnikoffi and the "braune Pluteus" of
sults in a coeloblastula and gastrulation is Muller are poorly known. They have larval
by ingression of mesenchyme with embolic skeletons and a pluteus-like form, but their
invagination. Metamorphosis invariably rudimentary arms must limit their mobility,
produces an ophiuroid rudiment with its explaining their absence from the plank-
mouth at the site of the larval mouth. Most ton. Coincidentally, their feeding ability
known ophioplutei are 8-armed, but Am- may be reduced due to the abbreviation of
phiura chiajei and Amphiura filiformis have the ciliary band and it is possible they are
two and three pairs of larval arms, respec- lecithotrophic.
tively, while the larva Ophiopluteus opulentus I have recently studied the development
species A, of an unknown ophiuroid, was of Amphioplus abditus, a burrowing shallow-
reported to have twelve larval arms (Mor- water amphiurid of the eastern United
tensen, 1921; Fenaux, 1963). The ophio- States coast (Hendler, 1973). This species
pluteus arms are supported by extensions of bypasses planktonic development and
a symmetrical larval skeleton and bordered undergoes metamorphosis within an
externally by a band of cilia. Ophiopluteus adhesive, demersal fertilization membrane.
costatus was illustrated by Mortensen (1921) The embryo is a ciliated pluteus-like form
with an extra skeletal piece, a preoral rod with a reduced, paired, larval skeleton. The
resembling an echinopluteus dorsal arch. embryonic and adult mouths form at the
The development of several ophioplutei same site and the blastopore is transient.
has been studied in detail (Muller, 1851; Development, which takes place on the sur-
MacBride, 1907; Narasimhamurti, 1933; face of the sediment, is completed within 4
Olsen, 1942). These classical embryological days, and the slow-growing post-larva,
works and brief observations scattered in about 0.3 mm in disc diameter, is active and
the literature reveal a variety of capable of burrowing and feeding.
694 GORDON HENDLER
The young of. A. abditus and possibly mentioned, Patent (1970) has described a
Ophiophragmus wurdemani as well as the unique larva for Gorgonocephalus caryi. This
"Jugendformen von Ophiuren" found in a species shows an irregular bilateral sym-
deep plankton haul off Antarctica by Mor- metry, lacks a larval skeleton and cilia, is
tensen (19136) develop within a fertiliza- schizocoelous, and apparently develops
tion membrane (Hendler, 1973). Although demersally. The significance of this exotic
A. abditus and possibly 0. wurdemani have form will be discussed later.
pluteus-like embryos, the early stages of the
Jugendformed are unknown (Nachtrieb,
1885; Mortensen, 19136). Development PATTERNS OF OPHIUROID DEVELOPMENT: QUAN-
within the fertilization membrane may be TITATIVE
an important ecological adaptation, and I
have discussed the value of demersal de- The foregoing section has documented
similarities and differences in ophiuroid

velopment within a fertilization membrane
for avoiding environmental stress on the developmental processes. The basic types
basis of salinity and temperature tolerance were: direct development involving either vi-
experiments with A. abditus embryos (Hen- viparous development with free or attach-
dler, 1973). There are so few species known ed embryos in the ovaries or bursae, brood-
with this pattern of development that it is ing beneath the disc or arms, or direct de-
impossible to evaluate its systematic sig- velopment in permanently attached egg
nificance but the embryonic skeleton and capsules (as exemplified by Kirk's
ciliation reflect the affinity of the embryo of ophiuroid), and planktotrophic development
A. abditus to that of viviparous species and of relatively long-lived ophioplutei. In ad-
the ophioplutei. dition, the conglomerate of abbreviated
forms may develop as: free-living reduced
Another abbreviated form is the lecitho- ophioplutei, embryos within a demersal
trophic vitellaria as described for fertilization membrane, lecithotrophic
Ophioderma brevispinum (Grave, 1900, 1916),vitellaria, or in the manner of Gorgonoceph-
Ophioderma longicaudum (Fenaux, 1969), alus caryi. The group with abbreviated de-
Ophioderma sp. (?) (Mortensen, 1921), velopment seems especially inconsistent
Ophiolepis cincta (Mortensen, 1938), with regard to the developmental process.
Ophiolepis elegans (Stancyk, 1973), The following discussion, however, indi-
Ophionereis squamulosa (Mortensen, 1921),cates that members of this "unnatural"
Ophiopluteus elongatus (Krohn, 1857) and grouping are ecological analogues, and the
possibly Muller's (1851) dubious "Larve von major groups of direct, planktotrophic,
Nizza." Their rapid development and al- and abbreviated developers, though de-
leged tendency to remain near the bottom, velopmentally and systematically "fuzzy,"
especially during later stages of develop- are ecologically and energetically distinct.
ment, make these larvae rare in plankton This section is devoted to characters that
collections. One species, however, O. brevis- have been used to distinguish these groups
pinum, has floating eggs and begins its de- and suggests new characters including egg,
velopment near the surface. Among forms larval, and post-larval size; rate of de-
with vitellaria larvae the process of mor- velopment; and fecundity in terms of num-
phogenesis is known in detail only for 0. bers and total volume of eggs.
brevispinum. All these larvae are barrel-
shaped and ringed by 4 ciliary bands, but
only two, O. cincta and O. elongatus, are re-Egg and larval size, number and total volume of
ported to have rudiments of the larval eggs
skeleton. The very existence of these In general, viviparous forms have rela-
skeletal rudiments however, needs tively large yolky eggs (Thorson, 1950). In
confirmation. It is questionable that they the ophiuroids viviparous development has
indicate an affinity with the pluteus larva as been thought to occur in species with egg
suggested by Mortensen (1921). diameters greater than 0.3 and less than
In addition to other abbreviated forms 0.65 mm (Fell, 1945). Schoener (1972) indi-
cated the actual range is broader, and data magnitude in the numbers of eggs per indi-
for 22 species (Table 1) show values from vidual. Ophionereis vivipara, on the other
0.1- to 0.9-mm egg diameter. hand, has broods of juveniles at mixed
The possibility that viviparous forms stages of development. Its eggs are 0.23
with small eggs contribute to the nutrition mm in diameter while another tropical vi-
of their young by secretions from their bur- viparous form, Amphiura vivipara, has
sae is suggested (but not proven) for Axiog- 0.5-mm eggs.
nathus squamatus (Fell, 1940; Fontaine and The number of eggs and the total volume
Chia, 1968) and is likely in Ophionotus hexac- of eggs per individual show a gradation
tis which reportedly has intraovarian rather among viviparous species as does egg
than bursal brooding (Mortensen, 1920a, diameter (see Figs. 1, 2). But a striking
1921). The fact that the diameter of the margin of at least an order of magnitude
viviparous embryo may be two or three separates values for egg number and total

times that of the egg (a difference in volume volume of eggs per individual from corres-
of 8 to 27 times) and that there must be a ponding values for planktotrophic forms.
larger differential for egg versus juvenile, Therefore, if nutrient contributed to the
indicates that energy must be obtained young during brooding is negligible,
from nutrients elaborated by the parent or oviparity would be more expensive in terms
drawn from the outside by bursal ciliary of energy loss than viviparity.
currents. Estimates from illustrations show The eggs of planktotrophic larvae are
thatAxiognathusjaponicus and/4, squamatus invariably less than 0.2 mm diameter, a
with eggs 0.1 to 0.15 mm in diameter have a much smaller range than found in vivipa-
pre-metamorphosed embryo of 0.24 mm rous species (Table 1). In addition, egg
length. Similarly, the size of Ophionotus number is at least two and total volume of
hexactis increases from 0.2 to 0.48 mm and eggs per individual at least three orders of
Stegophiura sculpta from 0.14 to 0.36 mm. magnitude higher than viviparous species.
Another viviparous species, Amphiura For 14 species of ophioplutei for which data
stimpsoni, has a much larger (0.5 mm) egg have been recorded, the length of the larval
and an embryo of no greater size, indicat- body ranges from 0.2 to 0.7 mm with the
ing that this and other large-egged forms longest of the four paired larval arms be-
may have sufficient yolk reserves for de- tween 0.5 and 3.8 mm and the arm/body
velopment. For two species there is evi- ratios ranging from 1 to 16 (Mortensen,
dence for cannibalism of embryos or nurse 1898,1901,1913a, 1921, 1931, 1937, 1938;
cells by mature brooded juveniles (Morten- Fenaux, 1968). In seven planktotrophic
sen, 1936; Murakami, 1941). species for which data are available the
It is possible that egg size as well as other diameter of the post-larval ophiuroid disc is
quantifiable aspects of viviparous de- 0.2 to 0.4 mm and the arms, shorter than
velopment are associated with adaptations the disc diameter, consist of terminal plates
to the physical environment. The majority only or an additional one or two segments
of viviparous ophiuroids have been found (Muller, 1851; Chadwick, 1914; Morten-
in cold, antarctic waters. However, the four sen, 1921, 1938). Original data, which will
species that Mortensen (1933d) described be presented more fully below, indicate
as tropical viviparous forms show diverse that disc diameters of planktonic post-
sizes and numbers of eggs. Cryptopelta larvae may reach 0.9 mm and arm lengths
granulifera and Ophioconis vivipara brood may approach 2 mm. Number of arm seg-
young all at a uniform stage of develop- ments is generally 5 or fewer, but one
ment, though they differ by an order of specimen with 8 segments was found.
TABLE 1. Size of viviparous eggs.

Maximum egg
diameter (mm) 0-0.1 0.1-0.2 0.2-0.3 0.3-0.4 0.4-0.5 0.5-0.6 0.6-0.7 0.9-1.0
Number of vivi-
parous spp. 1 2 3 3 4 5 3 1
696 GORDON HENDLER
Larger sizes might be expected in the cold, Its ophiopluteus, however, is a reduced
dense waters of high latitudes, but the Ant- form with only one pair of larval arms and
arctic form Ophiopluteus irregularis, has metamorphosis has been found to occur
only two arm segments, a terminal plate within 8 days (Fenaux, 1963).
and a fairly large disc diameter of 0.7 mm My contention presented above, that
(Mortensen, 1913*). other reduced plutei (e.g., Ophiopluteus
Newly hatched young of viviparous claparedi) have abbreviated development, is
forms generally have disc diameters of 1.0 strengthened since A. chiajei, with a re-
mm and 10 or more arm segments (e.g., duced pluteus, has several of the quantita-
Ludwig, 1899). The range encompasses tive characteristics of the abbreviated de-
diameters of 0.6 to 5.0 mm and 8 to 40 arm velopers (Table 3). I would also predict that
segments, appreciably different from A. chiajei post-larvae are a small size at set-
planktonic post-larvae (Fig. 9). The major tlement as are other abbreviated forms.

limitation on size for brooded young ap- Figures 1 and 2 show that the fecundity of
pears to be the size of the parent. abbreviated developers in terms of egg
Because there is such variety in develop- number and total egg volume is inter-
mental patterns of the abbreviated forms mediate to the planktotrophic and vivipa-
there is a considerable spread of egg sizes. rous species, though values for total egg vol-
The 0.13- to 0.35-mm egg diameter of ab- ume are closer to those for planktotrophic
breviated developers bridges values for forms. Data tor A. chiajei are not included in
planktotrophic forms and the large-egged these figures but are similar to values for
viviparous forms. The larvae (and em- abbreviated forms.
bryos) of all direct developers are of similar Clearly, the assemblage of abbreviated
length (and probably similar volumes). The developers is not systematically cohesive.
few abbreviated species for which informa- Similarity in size of eggs, larvae, and post-
tion is available have post-larvae of a size larvae as well as the related similarity in the
comparable to small planktotrophic forms number and mass of gametes produced
(Tables 2, 3). Total egg volume per indi- and the rate of development indicate they
vidual can be estimated for only three are ecologically and physiologically con-
species, but these agree closely and it is ex- vergent. Apparently the abbreviated de-
pected that other abbreviated forms will be velopers have been selected from different
similar. stocks and combine some of the advantages
I have recently examined a series of ripe of viviparous and planktotrophic develop-
Amphiura chiajei supplied by Dr. Lucienne ment to suit a specific larval "niche."
Fenaux (Station Zoologique, Villefranche- Figures for egg number and total volume
sur-Mer). Number and size of the ova var- of eggs per individual as presented above
ied directly with size of the specimen. The indicate, more reliably than egg diameters,
smallest individual (disc diameter = 4.6 that planktotrophic, viviparous, and ab-
mm) has 1,695 ova with an average diame- breviated forms have distinct and different
ter of 0.14 mm giving a total volume of eggs energy budgets and survival strategies. The
of 2.69 mm3. The largest specimen (d.d. = disparity of these values between the differ-
6.9 mm) has 5,775 ova with an average ent groups makes a useful predictive tool.
diameter of 0.16 mm and an estimated total In fact, the volume of eggs per individual
volume of eggs of 12.38 mm3. The species and the differential of larval and post-larval
may reach a disc diameter of 10 to 11 mm size have not previously been used to dis-
and by extrapolation maximum egg tinguish the different groups from one
number may be estimated at 30,000 and another, but could help to predict larval
maximum total volume of eggs per indi- form from adult gonads or gametic charac-
vidual at 30 mm3. The observed and esti- ters for unknown larvae (Table 3).
mated values are much closer to those for
abbreviated developers than plankto- Developmental rates
trophic developers (see Figs. 1, 2) even
though A. chiajei has a free-living pluteus. In addition to parameters of gamete size,
TABLE 2. Characteristics of abbreviated developers.

E
gg Total vol. Larval Postlarva Time to
diameter Egg eggs/indiv. length disc diam. metamorph.
Species
Ophiopluteus claparedi
(mm) number (mm3) (mm)
0.3
(mm) (Days) Authority
Mortensen (1901)
3
7>
Ophiopluteus metschnikojfi 0.2* Metschnikoff (1869) zen

Braune Ophiuren-pluteus v. Triest ca. 0.3 Muller (1851) O
Amphioplus abditus 0.13-0.16 5000- 64.3 0.3 0.3 2-3 Hendler (1973) •n
30,000 o 13
Jugendformen von Ophiuren 0.5 Mortensen (1913) X
Gorgonocephalus caryi 0.22 ca. 5 Patent (1970) c
Ophioderma brevispinum 0.30 ca. 5 Grave (1916) 5?
o
Ophioderma longicaudum 0.20-0.35 1000-2000 45.2 0.6 ca. 5 Mortensen (1898), B
Fenaux (1972) O
Ophiolepis cincta 0.30 0.53* ca. 4 Mortensen (1938)
PI
Ophiolepis elegans 0.25 6720- 132.0 0.34* 0.2* 3 Stancyk (1973)
16,500 r
O
Ophionereis squamulosa 0.20 90 +++ 0.39* 0.3 2.5-5 Mortensen (1921)
Ophiopluteus elongatus pi
Less than Krohn (1857), z
0. longicaudum Mortensen (1898) H
* Measurement calculated from illustration
a
ID
698 GORDON HENDLER
TABLE 3. Quantitative characteristics of major developmental patterns.
Direct Abbreviated Planktotrophic

development development development
Maximum range egg diameter (mm) 0.10-1.00 0.13-0.35 0.07-0.90
Larval volume/egg volume 8.0-27.0 5.0-12.0 50 ±
Post-larval disc diameter (mm) 0.6-5.0 0.2-0.5 0.2-0.9

Post-larval arm segments 8-40 0-1 0-8
Fertilization to metamorphosis 5 3-5 3-40 ( + ?)
(days)
Total number of eggs/individual 10 to 2000 4,000-30,000 24,000-27,000
Total volume of eggs/individual (mm3) 0.1-2.3 45.2-132.0 140.5-230.4
Hermaphroditism possible never never

number, and gonadal mass, the direct, (Mortensen, 1913; Murakami, 1937; Olsen,
planktotrophic, and abbreviated forms 1942; Thorson, 1961; Geiger, 1963;
have markedly different rates of develop- Mileikovsky, 19686). Although ophioplutei
ment, and differences in frequency and are concentrated in nearshore waters they
rate of larval dispersal would be expected as may be found in mid-ocean (Mortensen,
a consequence. Better information is avail- 1898; Gardiner, 1904; Mileikovsky, 1968a).
able on developmental rates of the Unfortunately, little is known about the
planktotrophic ophioplutei than those of ability of ophiuroid larvae to delay
viviparous embryos (Table 4). Although metamorphosis or select substrates during
larval food is rarely defined and tempera- metamorphosis, although substrate dis-
ture information is imprecise, there is a crimination for Amphiura filiformis larvae
conspicuous similarity in chronologies for has been suggested from field observations
temperate and tropical species as Thorson and the post-larvae of Ophiothrixfragilis may
(1946) noted in reviewing Mortensen's be attracted to adults (Thorson, 1966;
data. In comparison with teleplanic larvae Warner, 1971).
with planktonic lives of several months, A series of plankton samples provided by
ophioplutei have a fairly short period of Dr. Rudolf Scheltema (Woods Hole
development, and it is unlikely that they are Oceanographic Institution) has allowed me
able to survive long-distance transport in to obtain information on the size and dis-
oceanic currents. As Thorson noted, how- tribution of planktonic post-larvae. The
ever, metamorphosis of ophiuroids often samples, taken as oblique plankton tows
occurs in mid-water. Consequently, post- from 150 m to the surface, provide a survey
larval ophiuroids are commonly sampled in of much of the North Atlantic (Scheltema,
the water column at greater depths and 1971).
farther from shore than early larval stages Planktonic post-larval ophiuroids were
FIG. 1. Egg numbers for species with discs of known Ophiolebella biscutifera, 20-Ophiomitrella clavigera, 21-
diameters. The three major developmental groups are Ophiomitrella ingrata, 23-Ophiomyxa vivipara, 24-
circled. Except for deep-sea forms, species with un- Ophionereis vivipara, 25-Ophionotus hexactis, 28-
known patterns of development are not presented. Ophioscolex nutrix, 29-Ophiotjalfa vivipara, 30-
Closed circles, viviparous. Open circles, viviparous Ophiozonella falklandica, 32-Ophiura meridionalis, 33-
(number of brooded juveniles—data for egg number Ophiura rouchi, 34-Ophiurolepis gelida, 35-Ophiurolepis
unavailable). Closed squares, abbreviated develop- martensi, 36-Stegophiura vivipara, 37-Axiognathus
ment. Open diamonds, planktotrophic development. squamatus. BROODING: 27-Ophiophycis gracilis. AB-
Crosses, deep-sea forms with unknown pattern of de- BREVIATED: 3-Amphioplus abditus, 18-Ophioderma
velopment. VIVIPAROUS: 4-Amphiura annulifera, longicaudum, 38-Ophiolepis elegans. PLANKTOTRO-
5-Amphiura capensis, 6-Amphiura magellanica, PHIC: 16-Ophiocoma echinata, 17-Ophiocoma erinaceus,
7-Amphiura microplax, 8-Amphiura monorima, 26-Ophiopholis aculeata. DEEP-SEA: l-Amphilepis ingol-
9-Amphiophiura rowetti, \0-Asterochlamys bruneus, 11- fiana, 2-Amphiophiurabullata, \2-Homalophiura tesselata,
Cryptopelta granulifera, \3-Ophiacantha densispina, 14-22-Ophiomusium lymani, 3l-Ophiura Ijungmani.
Ophiacantha vivipara, \b-Ophioceres incipiens, 19-
TOTAL NUMBER OF EGGS PER INDIVIDUAL
o
o o
o b "o

o o o o
o o i O
_l L _l I I I I I I I i I i i I i i i i i
>
O1-
o
n O
CJT •o
C
0
m 5
O
pi
pi
en"
3
3
5
"0
PI
Z
OJ.
01
J
to
to
o
o

TOTAL VOLUME OF EGGS PER INDIVIDUAL (mm3) o
_ O
o o
O o
o i ' ' ' I
o
i i i I i i i 11 i i i I i i 11 i
o-
o
(ft O o
o
SB
> o" X
PI
o
pi
so
01
O'
limited to coastal waters. The number of (Grave, 1900; Hendler, personal observa-
arm segments of post-larvae from different tion). If egg buoyancy is an adaptation to
stations is shown in Figure 3. No clear-cut enhance dispersal it may be expected in
correlation between arm segment number other lecithotrophic forms, but it might be
(which is directly related to size and age) only an adaptation to avoid unfavorable
and location emerges from this chart, but benthic conditions where Ophioderma oc-
since it was not possible to determine the curs.
origin of any of the post-larvae, long dis- I have collected post-larvae still bearing
tance transport before metamorphosis functional ciliary bands of vitellaria larvae
cannot be ruled out. One exceptional mid- in the surface waters of the Gulf Stream (1
oceanic specimen, collected between South April 1974: 37°49.9'N, 67°56.0' Wand37°
America and Africa had the hooked arm- 48.2'N, 67° 49.1'W). This suggests that
spines characteristic of an ophiothricid. lecithotrophic ophiuroid larvae may be

This indicates that the ophioplutei of the transported over long distances by oceanic
widespread genus Ophiothrix or possibly currents despite their short period of dis-
Ophiomaza (both of which genera have un- persal. Indeed, the extensive ranges of
usually long larval arms) are capable of genera and species with abbreviated de-
trans-oceanic dispersal. velopment attest to the ultimate effective-
While planktotrophic larvae live about 1 ness of abbreviated development for dis-
month (though a 7 to 10 month period has persal.
been suggested for Ophiocten sericeum by
Pearse, 1965) the abbreviated developers Periodicity and rate of development of viviparous
metamorphose within a week (Table 2). ophiuroids
Their rapidity of development would limit
transport, keeping young relatively near The time estimated for development of
successful adult populations, but they could viviparous species has been based on in-
be dispersed short distances by bottom cur- complete information or speculation.
rents. Naturally, the brief dispersal phase Ophioplocus esmarki, the only viviparous
of abbreviated forms and their modest species for which data are available, ap-
number of eggs would be expected to re- pears to brood a "litter" for 6 months be-
tard the rate of population expansion. fore hatching (Ricketts and Calvin, 1948;
Strathmann (1974) has suggested that this Hyman, 1955). Unfortunately, Ophioplocus
handicap could be mitigated by adaptations was not adequately sampled during the
such as multiple spawnings which could supposed 6-month hiatus between oviposi-
harness changes in current direction and tion and hatching. It is possible that vivip-
velocity to magnify passive dispersal. The arous forms could have a higher fecun-
interesting occurrence of floating eggs of dity than indicated by the number of eggs
Ophioderma brevispinum which produces vitel- per individual if they have extended breed-
laria larvae has been noticed in several loca- ing periods. Indeed, it has been supposed
tions in North Carolina and Massachusetts that viviparous species do have extended
FIG. 2. Total volume of eggs per individual for Stegophiura vivipara, 25-Axiognathus squamatus. AB-
species with discs of a known diameter. Only the three BREVIATED: 3-Amphioplus abditus, 13Ophioderma
major developmental groups are circled. All species longicaudum, 26-Ophiolepis elegans. PLANKTOTRO-
for which values could be calculated are shown. Cir- PHIC: W-Ophiocoma echinata, 12-Ophiocotna erinaceus,
cles, viviparous. Squares, abbreviated development. 23-Ophiopholis aculeata. DEEP-SEA: l-Amphilepis ingol-
Diamond, planktotrophic development. Crosses, fiana, 2-Amphiophiura ingolfiana, 9-Homolophiura lesse-
deep-sea forms with unknown pattern of develop- lata, 14-Ophiomusium lymani, 21 -Ophiura ljungmani.
ment. Stars, shallow-water forms with unknown pat- SHALLOW-WATER: 4-Amphioplus macilentus, b-Am-
tern of development. VIVIPAROUS: 6-Amphiophiura phioplus sp., 8-Gorgonocephalus caput-medusae, \9-Ophio-
rowetti, 7-Amphiura stimpsoni, \Q-Ophiacantha vivipara, pus arcticus, 20-Ophioscolex marionis, 23-Ophiurolepis
15-Ophionereis vivipara, \b-Ophionotus hexactis, 18- partita.
Ophiophycis gracilis, 22-Ophiura meridionalis, 24-
TABLE 4. Chronology of ophiopluteus development.
Metamorphosis

Temp. Blastula Gastrula 2-Arm 4-Arm 6-Arm 8-Arm
Species °C (hours) (days) stage stage stage stage incipient complete Authority
Amphiura chiajei 18-20 1 2 M i l l Fenaux (1963)
M i l l
Amphiura filiformis 3 7 Mortensen (19206)
Ophiactis balli 18 1 2 3 Mortensen (1913a)
Ophiactis savignyi 2 3 Mortensen (1931)
Ophiocoma echinata <1 2.5 6-11.5 Grave (1898),
Mortensen (1931-1)
Ophiocoma erinaceus 25-30 — 1 3-6 — 11 1 mo. Mortensen (1937),
Thorson (1946)
Ophiocoma pica 25-30 <24 — 2 6 — 18 — 1 mo. Mortensen (1937),
Thorson (1946)
Ophiocoma pumila 13 Devaney (1970)
Ophiocoma scolopendrina 25-30 — — — — 42 Mortensen (1937),
Thorson (1946)
Ophiocomina nigra — 24-30 1.5-2 — 4 9 — — 35-40 Mortensen (1913),
Narasimhamurti (1933)
Ophiomaza cacaotica 25-30 6 — — — — 5-6 — 12-14 Mortensen (1937),
Thorson (1946)
Ophiopholis aculeata 8 24-36 1.5-2 3 — 10.5 17 30 Fewk.es (1886),
Olsen (1942)
Ophiothrix angulata <1 1 2 4.5 Mortensen (1921)
Ophiothrix fragilis 24 1.5 3 4 10 23 26 MacBride (1907)
Ophiothrix quinque-
maculata 24 1.5 3 6-7 16-20 — Guille (1964)
Ophiothrix savignyi 30 0.5 1 14 21 Mortensen (1938),
Thorson (1946)
Ophiothrix triloba 0.5 >40 Mortensen (1937),
Thorson (1946)

FIG. 3. Geographical distribution of planktonic number of arm segments for post-larvae at each sta-
ophiuroid post-larvae. Squares indicate stations where tion. T, Terminal plate but no arm segments. L,
post-larvae were found. Numbers indicate range in Ophiuroid rudiment attached to larva.
breeding periods (Hyman, 1955). Stegophi- sumed solely because adults with embryos
ura sculpta has been reported to breed from of different stages of development are
January to July. It was apparently examin- found year-round (Fell, 1946).
ed for brooded young from May to March, To show whether reproduction in A.
the only viviparous species to date to have squamatus is continuous or cyclical, it would
been effectively studied on a regular basis be most satisfactory periodically to monitor
(Murakami, 1941). gametogenesis and hatching of a discrete
Axiognathus (= Amphiura = Amphipholis) population in the field and ideally to follow
squamatus (Delle Chiaje, 1829) is a small the reproductive histories of individual
ophiuroid remarkable for its "cosmopoli- specimens. An indirect analysis of the re-
tan" distribution, simultaneous hermaph- productive periodicity of A. squamatus is
roditism, and viviparity. It has been as- presented below. It is based on size fre-
serted that widely separated populations of quency distributions of Axiognathus sam-
A. squamatus breed throughout the year al- pled monthly from September 1971 to Au-
though neither the production of gametes gust 1972. Collections were made from a
nor embryos, nor the hatching of juveniles bed of Mytilus edulis at Ram Island, Noank,
has been studied at regular intervals Connecticut (northeast Long Island
(Fewkes, 1887; MacBride, 1892; Lo Bianco, Sound), an area with little salinity variation
1899; Fell, 1946; Russel, 1957; Boffi, 1972). (29 to 31 ppt) but marked annual tempera-
Continuous gametogenesis has been as- ture fluctuation (2 to 25°C). It is assumed
704 GORDON HENDLER
that monthly collections were representa- B C v

A
B
tive quantitative samples of the ophiuroid CD -
population on mussels.
o 60
O
Periodicity and Rate of Development of Axiog- O
nathus squamatus 1
III
11
40
I-
The percentages of brooding animals in jj
the population are plotted to show fluctua- £20

tions in the intensity of reproduction (Fig.
4). The brooding fraction of the population
is greatest from November to March. The
ii
a.
111
S O N D J F M A M J
III
J A
ratio of brooders to non-brooders falls to 55 ISS 70 90 46 II 102 102 101 103 165 121
unity from April to June, continues to de- FIG. 4. Percent of Axiognathus squamatus brooding es-
cline through October, but rises suddenly timated from monthly samples. A, B, and C respec-

tively indicate periods when brooders are equal, less,
by November. and greater in abundance than non-brooders. Num-
This slump in the percentage of brood- bers of adults analyzed are indicated below the letters
ing individuals (and rise in non-brooding) for months.
between April and October results from an
influx of sexually immature juveniles into sharp drop in the mean number of embryos
the population. This influx is reflected in an brooded per individual during the sum-
increase in the area of the size frequency mer. The low point in the number of em-
polygon for non-brooders and is evident in bryos brooded per individual follows an
Figure 5 by comparing the unshaded por- influx ofjuveniles into the population and a
tions of the polygons for April to October concomitant decrease in the fraction of the
with those for November to March. An an- population bearing embryos. It follows that
nual cyclical fluctuation in the numbers of the pulsed production of young is not sim-
reproductive individuals and juveniles ply due to fluctuation in the numbers of
clearly indicates that breeding is pulsed continuously breeding adults, but implies
rather than continuous. that a finite supply of brooded embryos is
Pulsed spawning is corroborated by the reduced by the end of the summer. It
fact that individuals of a given size brood a should be noted that this periodicity in the
greater number of embryos in winter than release of juveniles does not imply a strictly
in summer. This is shown in Figure 6 by a synchronous gametogenic cycle. In fact,
PERCENT
10 20 10 10 10 10 10 10 10 10 10 10 10
525-
E-
0.25-
OCT NOV DEC MAR APR MAY JUNE JULY AU6
155 70 70 102 102 101 103 168 121
FIG. 5. Size-frequency polygons showing percentage the population brooding embryos. Dotted lines indi-
of adults of different sizes collected each month. cate the trend of growth of age classes that arise early
Shaded portions of polygons indicate the fraction of (E) and late (L) in the spawning period.
testes and ovaries with full-sized oocytes

were present throughout the year.
Further complexities of spawning
periodicity are evident from a plot of fre-
quency distributions of embryo size from
adults collected each month (Fig. 7). It
might be expected that if many embryos
were produced over a short period the re-
sulting size distribution would be skewed
toward smaller sizes, but as growth con-
tinues the percentage of larger sizes would
rise resulting in "level" size frequency
configurations. Thus, the skewed distribu-
tions (October to April) may represent a

pulse of newly produced young whose
growth is arrested during the winter but
which grow and hatch during the warmer
months of the year (May to September).
This interpretation is supported by the fact
that the influx of newly hatched juveniles
described above (from April to October)
follows a winter period when adults show
no somatic growth as indicated by the
stationary peaks in the winter size-
frequency distributions (Fig. 5). It seems
likely that physical conditions which inhibit
the growth of adults would act similarly on
their embryos.
Early embryos are produced in great
numbers in June and in October and
November. It is not immediately clear why
embryos are produced in two surges, one
during and one following the hatching
period. A re-examination of the dynamics
of the Axiognathus population can clarify
this and the resulting interpretation is dia-
grammed in Figure 8.
The evolution of an "age class" (i.e., a
significant influx of newly hatched
juveniles) is best traced from June when a
group of immature (small, non-breeding)
individuals enters the population (see E in
Fig. 5). During the summer, members of
this age class accumulate and increase in
size as shown by an upward shift in the posi-
FIG. 6. Mean of the number of embryos brooded by

the size range of adults. The greatest number of brood-
ing adults examined were between 2.25 and 3.75 mm
disc diameter. Stippled bars placed at 3 mm range each
month to facilitate following annual trend. Non-
brooding adults were omitted from the average.
0.25 1.25 2.25 3.25 425 Number of embryos brooded varies directly with the
DISC DIAMETER (mm) size of the adult.
706 GORDON HENDLER
AUG tion of the "non-brooding" portion of the

N=250 size-frequency polygons. Between October
and December, members of this age-class
JULY reach sexual maturity, and as they begin to
= 400 brood the modal size of the frequency dis-
tribution for brooders shows a temporary
decrease. It rebounds in December as re-
cruitment of new individuals ceases and
adults slowly grow. Members of the age
class, almost all brooding young, grow little
during the winter, but resume growth from
April to June.
The age class considered above (called
"E" for "early") is out of phase with another

age class designated "L" (late). Individuals
of class L first appear in October (Fig. 2).
Like individuals of class E their growth is
largely restricted to the warmer months.
Consequently, L reaches sexual maturity
MAR by June of the following year but continues
N = 448 to grow until September.
Class E originates in June, begins to ma-
ture in October but releases young only
during the following April to July. Class L
appears in October, matures the following
June and releases young within several
months (August to October). Thus, the
surges in the production of early embryos
(Fig. 7) correspond to peaks in the matura-
tion of each of the age classes. The period
between oviposition and hatching may thus
take 3 to 4 months if initiated in the sum-
mer (as for class L) or around 7 months with
a winter "diapause" (as for class E) (Fig. 8).
Each of the age classes lives for about a
year but they enter the Axiognathus popula-
tion at opposite ends of a hatching period
which lasts from May to October. The E
class must be primarily produced by E class
of the previous year since it appears before
10 most of the L class reach sexual maturity.
The L class of the fall is mostly produced by
summer class animals since they enter the
10- population in October when members of
the E class are either disappearing or just
ESTI 3 5 7 9 II 13
beginning to brood. There is no extensive
discontinuity between the E and L peaks in
SIZE OF BROODED YOUNG
size-frequency polygons since the age class
FIG. 7. Frequency distributions of the different de- phenomenon is a result of low winter water
velopmental stages of embryos in brooding adults
from each monthly sample. Distributions for bilater- advanced embryos with terminal plates (T) or 1 to 14
ally symmetrical embryos (E) and pentaradiate em- arm segments are white. N, Number of embryos per
bryos (S = stars) are blackened and distributions for sample.
temperature which retards the develop-

mental process of both early and advanced
brooded embryos. In addition, the two class-
es are simultaneously sexually mature and
could interbreed. For example, during
April to June when class E animals are
brooding they could interbreed with newly J J A S O N D . J . F M A M J J A S O N D
matured class L individuals (Fig. 8). T I M E
FIG. 8. Generalized diagram of the growth and sex-

The objection to the "age-class" interpre- ual maturation of early (E) and late (L) spawned age
tation for Axiognathus population dynamics classes of Axiognathus squamatus in Connecticut. Black,
hinges on the fact that the events observed Period of sexual immaturity. Stripe, Period of sexual
in September to December (1971) preceded maturity and brooding. White, Period of hatching of
those reported for January to August young. Those animals which hatch at the beginning of
the summer (E) mature by the fall, but their young do
(1972). Thus, the data, arrayed to reflect not hatch until the following year. Those animals (L)

changes during a single year, may not truly which hatch at the end of the summer mature and
indicate an annual sequence of events. An spawn the following year.
alternative explanation might assume that
reproduction in the species is irregular, ment through metamorphosis takes no
with radically different spawning periods longer in this viviparous form than in some
each year. More information is needed be- planktotrophic developers with eggs of
fore a critical evaluation can be made. similar size. It remains to be seen whether
For the population of Axiognathus other viviparous ophiuroids have compara-
ble rates of development.
studied, the intensity of spawning is neither
continuous nor unimodal and synchron- As mentioned above, it had been as-
ous, but it is profoundly seasonal. The sumed that worldwide, populations of A.
complexity of the reproductive cycle shown squamatus had a uniform breeding period. I
for Axiognathus indicates that deductions have shown seasonality in reproduction for
concerning reproductive periodicity are a population subjected to severe fluctua-
suspect even if a large sample of brooding tions in temperature, but a greatly ex-
individuals is examined. The presence of tended breeding period could be expected
embryos at different stages of development at latitudes where seasonal changes exert
in brooding individuals cannot alone indi- less influence on the rate of development.
cate that production of young is continu- Reliable predictions are not possible with-
ous, and does not indicate the length of the
out information on the physiology of
brooding period. In A. squamatus for exam- Axiognathus, but a bit of speculation is possi-
ple, there may be embryos of different ble. Clark (1914) examined a large series of
stages in a brood but the relative abundance
A. squamatus during February and March at
of specific developmental stages varies sea-
Montego Bay, Jamaica. He indicates that
sonally. In cases where a population of vi-each adult was brooding only a few em-
viparous echinoderms are observed to re- bryos, many of which were at advanced
lease young over an extended period it stages of development. In addition, the
cannot be inferred that single adults spawnmeasurements of disc diameters he gives
throughout the breeding period. As shown for the embryos indicate that they were
for/I. squamatus, individuals spawn for only
small compared with Connecticut speci-
a part of a 7-month breeding period. mens of the same stage, and the adults did
Information presented above indicates not reach as large a size as those in Connect-
the period from oviposition to hatching icut. It would seem that the population had
takes about 3 months unless development is been sampled during a hatching period.
interrupted by a decrease in water temper- There would be large numbers of juveniles
ature during the winter. The rapid disap- in the population if this were true, but
pearance of the peak of early embryonic Clark provides no size-frequency informa-
stages during June indicates that develop- tion. An alternate explanation is that the
708 GORDON HENDLER
individuals in this tropical population have ers and the other two groups, it is sig-
a short life-span, each adult producing a nificant that there are distinct discon-
small number of young. The relatively tinuities for direct and planktotrophic
small size of both adults and brooded ophiuroids and some of these gaps are
young supports the latter hypothesis, as filled by abbreviated forms.
does the low maximum numbers of em-
bryos for A. squamatus reported by Bom ADAPTATIONS OF OPHIUROID DEVELOPMENT
(1972) for Sao Paulo, Brazil.
As explained above, it is known that the
LIMITATIONS OF QUANTITATIVE PARAMETERS young of certain viviparous ophiuroids
hatch at a larger size than planktonic post-
The results of the quantitative charac- larvae can possibly attain and most develop
terization of three primary developmental from relatively large eggs as well. Axiog-
patterns are summarized in Table 3. Indi- nathus squamatus, a small viviparous species,

cated are some of the ecological and has eggs (0.1-mm diameter) which are
energetical distinctions among the groups. equivalent in size to those of planktotrophic
The accuracy of prediction of developmen- forms. Its young are therefore as small as
tal pattern from one or more characters is might be expected for a viviparous form.
compromised by the fact that the groups Nevertheless, the largest brooded (near-
are not entirely distinct. Values of hatching) young of Axiognathus have sub-
ophiuroid egg size and number which are stantially larger disc-diameter, arm length,
intermediate between values presented in and number of arm segments than any
Table 3 are available for species whose de- North Atlantic planktonic post-larvae
velopmental pattern is unknown. The examined for this study (Fig. 9). As ex-
deep-sea species shown in Figures 1 and 2 pected, most of the planktonic post-larvae
are a case in point. Intraspecific variability had from one to three arm segments. The
also blurs distinctions between the de- generalization that viviparous young
velopmental patterns. For example, in Am- emerge at a size greater than newly settled
phioplus abditus and Amphioplus n. sp. (Hen- planktonic post-larvae is thereby strength-
dler, 1973) both egg diameter and number ened.
of eggs per individual vary directly with the Unfortunately, all measurements for
size of the individual. A. abditus with disc planktonic post-larvae were lumped since
diameter of 5.8 to 11.6 mm have from the specimens (usually decalcified) could
5,000 to 30,000 eggs of 0.13 to 0.16 mm not reliably be separated to species. The
diameter so that total volume of eggs per combined data of planktonic species show a
individual may range from 5.8 to 64.3 mm3 smaller range of arm length or disc diame-
(Hendler, 1973). Obviously, the predictive ter values for individuals with a given
value of such figures is limited without number of arm segments than for the vivip-
knowledge of ranges and maxima. More arous species (A. squamatus) studied indi-
information on the quantitative charac- cating that body size is more uniform for
teristics of abbreviated developers is also planktonic post-larvae than for the gamut
vital, as some values given in Tables 2 and 3 of viviparous species.
are based on only three species. Despite all Some planktonic post-larvae have longer
these handicaps and the fuzziness of some arms and smaller discs than A. squamatus
boundaries between abbreviated develop- with the same number of arm segments,
FIG. 9. Arm length (top) and disc diameter (bottom) examined. Statistics for post-larvae not given because
versus the number of arm segments for planktonic samples were not quantitative and all species were
post-larvae and the viviparous embryos of Axiognathus lumped. "T" indicates forms with only terminal arm
squamatus. Bars indicate the mean and range for 328 plate. Inset figure shows silhouette of planktonic post-
brooded embryos of A. squamatus collected in May larva (white) and A. squamatus (black) with five arm
1972 in Connecticut. Points beside bars indicate size segments.
values for all North Atlantic planktonic post-larvae
DISC DIAMETER (mm) ARM LENGTH (mm)
. . g . . . . 5 . . .P
j—i i '—i—i—•—i—i—i—i m O en
ro
"o
ro-
JO
2*
01- a a a a •
CO
m
m
-oo-
coCO"
710 GORDON HENDLER
and it may be significant that some courages acceptance of the "gene dispersal
planktonic post-larvae with five arm seg- model" offered by Ghiselin (1969) as the
ments have longer arms (almost 2 mm) but selective agent for hermaphroditism.
discs of the same size as five arm segment Nonetheless, as Schoener (1972) mentions,
Axiognathus. Still, they settle with disc hermaphroditism is never found in non-
diameters smaller than hatching Axiog- viviparous species except in aberrant cases.
nathus. A unique planktonic post-larva with There is a considerable latitude in egg
eight arm segments had arms only about 1 size and number of embryos of viviparous
mm long, but this was more than three species (probably correlated with different
times the disc diameter. modes of embryonic nutrition). The major-
In Figure 9 there are hints of several ity of viviparous ophiuroids sacrifice the
options in post-larval adaptations. Com- advantages of a small, superabundant dis-
pared with the viviparous young of Axiog- persal stage, and may also dispense with
nathus, planktonic post-larvae may have rel- common strategies for increased reproduc-

atively high arm-length/disc-diameter tive potential as well, thought, squamatus, a
ratios. After settlement these relatively long small form, has a short generation time and
arms may afford advantages in feeding and the larger viviparous species may be
locomotion. It is possible that long, thin iteroparous. Protection afforded by the parent,
arms may enhance post-larval dispersal, and larger size and greater mobility upon hatch-
but the value of such dispersal following a ing would seem the primary advantage of vi-
planktonic larval stage is not immediately viparity. These factors are evidently more
clear. A number of newly metamorphosed important than independence from fluc-
planktonic post-larvae (those with only a tuating planktonic food and ready availabil-
terminal arm plate) have disc diameters ity of suitable substrate. Otherwise there
greater than the youngest Axiognathus and would be selection for viviparous species
greater than many planktonic post-larvae that could produce young in larger num-
with well-developed arms. A large disc and bers at a smaller size, similar to the juveniles
no arms should insure rapid sinking to the of oviparous forms. It is possible that this
benthos shortly after metamorphosis, de- "small size and large numbers" combina-
creasing exposure in the plankton. A large tion may be adopted by those viviparous
disc would also enable the young to ingest species with exceptionally large broods, but
comparatively large food particles. Still, the dimensions of their juveniles are not
Axiognathus of hatching size have both known. This strategy is evidently the modus
longer arms and larger discs than those of vivendi of abbreviated developers. Their
planktonic post-larvae. lecithotrophic development relieves them
of dependence on planktonic food.
The nature of viviparous development Moreover, the rapidity of their develop-
precludes larval but not post-larval disper- ment, proximity to the substrate, and mod-
sal. The effectiveness of viviparous disper- erately high fecundity are buffers against
sal is manifest in the distribution of vivipa- predation and minimize the disadvantage
rous species, a notable example being the of small post-larval size.
cosmopolitan and hermaphroditic A.
squamatus. It seems possible that the espe- The diminutive size of oviparous post-
cially high occurrence of hermaphroditism larvae may be an adaptation to increase the
in viviparous ophiuroids, documented by period of planktonic transport. Ophioplu-
Mortensen (1920a, 1936), is a function of tei have the advantage of dispersal, large
the relatively inefficient dispersal of these numbers, the propensity to capitalize on
forms and insures the presence of both periodic fluctuations of suitable conditions,
sexes in newly settled areas with low popu- but they are often deposited on unsuitable
lation density. The question of whether the substrates, and they sacrifice the competi-
dispersal mechanisms and distribution of tive advantage and resistance afforded by
dioecious viviparous forms are different large size. It is therefore difficult to see why
remains unanswered. Unreliability of in- they would not attain a larger larval size and
formation on ophiuroid protandry dis- greater juvenile size, but two possibilities
exist. First, the increased time for de- in viviparous or abbreviated development)
velopment could result in excessive preda- and that part of the larval body may be
tion or starvation of the larval forms. This discarded during metamorphosis indicates
idea is untenable considering their toler- the ophiopluteus is an efficient energy-
ance to mass mortalities that result from the harvesting form which should be capable of
transport of ophioplutei in water masses reaching a greater size were it not for limi-
where they were spawned to areas unsuita- tations in the ophiopluteus construction.
ble for settling (Thorson, 1946; Banse,
1956; Muus, 1966; Beyer, 1968; POSSIBLE PATTERNS OF OPHIUROID DEVELOP-
Mileikovsky, 1971). If planktotrophic MENT IN THE DEEP SEA
species can survive high mortality of this
sort, then in more felicitous environments There is no direct information on
they should be able to survive the high pre- ophiuroid larvae of the continental slope or
dation associated with extended larval life. ocean basin. Only one deep-water urchin,

The second possible explanation is that Laganum, from a depth of 200 to 300 m was
greater larval size might be restricted by a reared by Mortensen, and the pluteus of
structural instability inherent in the Allocentrotus fragilis, also a slope form, has
ophiopluteus body plan. The size of those been reared by Strathmann (1971). Chia
ophioplutei now described could be the (1966) has described the development of
largest possible and the characteristic small Pteraster tesselatus, an asteroid with a similar
size of planktonic juveniles might be near bathymetric range. Mortensen did succeed
the critical upper size limit beyond which in obtaining fertilization of a deep-water
dispersal would be hampered. Indirect evi- Ophiothrix sp., but the eggs failed to develop
dence of structural instability with large size (Mortensen, 1914).
is the disproportionate growth of the Less than 20 of the ophiuroid species
postero-lateral arm in the largest (e.g., with known larval development are
ophiothricid) ophioplutei. It is possible that eurybathal, with ranges encompassing the
echinoplutei are mechanically more adapt- continental shelf and slope. Populations of
able than ophioplutei and possibly more certain eurybathal species, especially
seaworthy. Comparing the arm and body boreal-arctic forms such as Ophiopholis
lengths of echino- and ophioplutei illus- aculeata, Ophiocten sericeum, and Ophiura
trated in Mortensen's major works (19206, sarsi, are known to produce ophiopluteus
1921, 1931, 1937, 1938) shows that larvae. It is possible that their mode of de-
echinoplutei are not generally larger than velopment may be modified at the deeper
ophioplutei. However, ophioplutei have a limit of their range or that their deep-water
rigid two-part larval skeleton while populations are non-reproductive "pseu-
echinoplutei have a greater number of do-populations," a possibility suggested by
skeletal rods with a musculature that per- Mileikovsky (19686).
mits movement of the larval arms, as well as It has been assumed that deep-sea
stabilizing elements such as the posterior ophiuroids would lack pelagic larvae.
process. Ophioplutei in the littoral water column
Teleplanic molluscan larvae reach a ter- reflect the benthic adult population (Rees,
minal size at the "delay period" preceding 1954), but plutei have not been taken in
settlement, which implies that the limited deep-sea samples (Wolff, 1960; Colman,
size of ophiopluteus larvae and planktonic 1962; Mileikovsky, 19686). On the basis of
post-larvae is inherent in the very structure newly published data for egg size and
of the larval form. It therefore seems sig- number, Mileikovsky (1971) and Schoener
nificant that several holothuroids and as- (1972) raised the possibility of pelagic, "in-
teroids are endowed with gigantic au- termediate" (i.e., abbreviated), or direct
ricularia and bipinnaria but no giant plutei development.
are known. The fact that the ophiopluteus Of the five deep-sea species examined by
larva is roughly 50 times the volume of the Schoener, only Ophiura ljungmani had eggs
egg (certainly a greater larva/egg ratio than of the same diameter as planktotrophic de-
712 GORDON HENDLER
velopers. Based on all available data (and 1903). Evidence and the logic employed
revising Schoener's figures for viviparous have often been specious, especially the ar-
forms which are for number of brooded gument that the most common larval type is
young rather than "egg number" as writ- the most primitive.
ten) the numbers of eggs of the deep-sea Mortensen's (1921) opinions are
species exceed those of most but not all reflected in the current consensus that the
viviparous developers. The total volume of "dipleurula" is ancestral and other larvae,
eggs per individual of the deep-sea including the elegant ophioplutei, are
ophiuroids is distinct from that of plankto- specialized. Selective pressures on the lar-
trophic developers but approximates values vae leading to different forms within and
known for shallow-water species with ab- between taxonomic groups severely limit
breviated development (Figs. 1, 2). This the value of larvae in constructing
suggests that these deep-sea ophiuroids phylogenies.
have abbreviated development rather than A novel attempt has recently been made

"planktonic larvae" as suggested by to deduce the characteristics of an ancestral
Schoener (1968a), and puts in doubt Thor- ophiuroid larva. Fell (1966) has defined two
son's (1946) statement that lecithotrophic types of direct development: (i) forms with
pelagic larvae are absent in high latitudes a secondarily reduced ophiopluteus of re-
and the deep sea. cent (post-phrynophiuroid) ancestry, and
Several other facts support this sugges- (ii) forms lacking a bilaterally symmetrical
tion. For instance, Ophiomusium lymani, one embryo (passing from a gastrula to a radial
of the deep-sea species with a large number stage) and characteristic of primitive
of large eggs, had previously been reported (phrynophiuroid) groups. The first type
to have post-larvae with only one arm seg- (secondarily reduced) may be justified by
ment (Schoener, 1968ft). As explained above Fell's (1945) theory of the "recession of
this can be taken as evidence (but not proof) metamorphosis." Usually illustrated by a
of abbreviated development as all vivipa- series of ophioplutei such as Ophiura albida,
rous juveniles and most planktotrophic Amphiura filiformis, Amphiura chiajei, and
post-larvae have several arm segments at Ophiopluteus claparedi with progressively
settlement (Table 3). Likewise, abbreviated fewer arms, the theory suggests that plutei
or planktonic development is suggested for with fewer arms have "shifted backward the
other deep-sea forms which are shown by time at which radial form is assumed." The
Schoener (1969) to have one arm segment root of this concept is the obvious similarity
(or less) at settlement such as Ophiomisidium of viviparous embryos having ciliary bands
speciosum and Ophiomusium armigerum. Theand embryonic skeletons (and even vitel-
five deep-sea species reported by Schoener laria with larval skeletons) to free-living
(1972) with egg diameters slightly greater plutei. Since "secondarily reduced" plutei
than those of shallow-water abbreviated are assumed postfacto to be modifications of
developers may either indicate that their a "typical" pluteus, the complex pluteus
pattern of development will differ from rather than a simple pluteus is regarded as
known modes or that due to low tempera- ancestral. This grouping is insufficient be-
ture or high pressure, energy reserves are cause: (i) there is no conclusive evidence
necessary for a more demanding period of that primitive families do or do not have
development. Alternately it is possible that ophioplutei, and (ii) there is no evidence
the greater egg size might be a function of that primitive plutei had 8 rather than 2, 4,
the relatively large size of the adult deep- or 6 arms. In fact, it is quite likely that larval
sea specimens. arms are caenogenetic features. In other
words, viviparous pluteus-like embryos are
not necessarily descended from species
NATURE OF THE ANCESTRAL OPHIUROID LARVA with eight-armed plutei.
The archetypical ophiuroid larva has al- Fell's second grouping indicates a re-
ternatively been considered a pluteus (Hy- duced non-bilateral larva for the primitive
man, 1955) or a vitellaria form (Grave, Phrynophiuroida (a group including the
Euryalids and Ophiomyxa). Unfortunately, tions. The accumulated evidence certainly

Fell's only evidence was his study of does not prove the pluteus is the primitive
Ophiomyxa vivipara for which only the later ophiuroid larval form.
developmental stages are known (Fell,
1941a), since other phrynophiurids with REFERENCES
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AMER. ZOOL., 15:691-715 (1975).

Adaptational Significance of the Patterns of Ophiuroid Development

Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543

Biological Sciences Group, University of Connecticut, Storrs, Connecticut 06268

SYNOPSIS. There is only limited information on ophiuroid developmental patterns, larvae

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INTRODUCTION grand style a groundwork for future re-

development and small post-larvae pro- nathus (= Amphipholis) squamatus (Morten-

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TABLE 1. Size of viviparous eggs.

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Ophiopluteus metschnikojfi 0.2* Metschnikoff (1869) zen

TABLE 3. Quantitative characteristics of major developmental patterns.

Direct Abbreviated Planktotrophic

Post-larval disc diameter (mm) 0.6-5.0 0.2-0.5 0.2-0.9

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Downloaded from http://icb.oxfordjournals.org/ at Ohio State University on June 9, 2014

Downloaded from http://icb.oxfordjournals.org/ at Ohio State University on June 9, 2014

Downloaded from http://icb.oxfordjournals.org/ at Ohio State University on June 9, 2014

Downloaded from http://icb.oxfordjournals.org/ at Ohio State University on June 9, 2014

Amphiura chiajei 18-20 1 2 M i l l Fenaux (1963)

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that monthly collections were representa- B C v

the population are plotted to show fluctua- £20

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testes and ovaries with full-sized oocytes

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FIG. 6. Mean of the number of embryos brooded by

AUG tion of the "non-brooding" portion of the

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temperature which retards the develop-

matured class L individuals (Fig. 8). T I M E

FIG. 8. Generalized diagram of the growth and sex-

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Downloaded from http://icb.oxfordjournals.org/ at Ohio State University on June 9, 2014

Downloaded from http://icb.oxfordjournals.org/ at Ohio State University on June 9, 2014

Downloaded from http://icb.oxfordjournals.org/ at Ohio State University on June 9, 2014

Downloaded from http://icb.oxfordjournals.org/ at Ohio State University on June 9, 2014

Euryalids and Ophiomyxa). Unfortunately, tions. The accumulated evidence certainly

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Downloaded from http://icb.oxfordjournals.org/ at Ohio State University on June 9, 2014

Downloaded from http://icb.oxfordjournals.org/ at Ohio State University on June 9, 2014

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