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Abstract
The osteological ontogeny of Pagellus erythrinus (Linnaeus, 1758) and its temperature-induced
plasticity is studied. The ontogeny of the skeleton follows the pattern described in all other Sparidae
studied so far: the onset of the ontogeny of the vertebral column and the caudal fin is at 4.3 mm total
length (TL) and the completion at 17.6 and 15.4 mm TL, respectively. Dorsal and anal fin
development appears at about 5.2 mm TL and completes at 7.5 mm TL. The pelvic are the last fins to
develop (7.5 – 11.5 mm TL). Although the pectorals are the only fins present before first feeding,
their ontogeny is completed only after 12.0 mm TL. Temperature affects the developmental rate of
the skeleton giving as much as 10.9% of differentiation in total length between 16 and 21 jC (caudal
lepidotrichia), 9.2% between 16 and 18 jC (caudal lepidotrichia) and 6.7% between 18 and 21 jC
(pelvic lepidotrichia). The role of temperature in developmental plasticity is enhanced by the
induction of abnormalities mainly in the area of the caudal fin, which reached (in total) 75%
occurrence in the higher temperature regime (23 jC) tested. The results of the skeletal ontogeny are
compared with the pattern of development of the Sparidae, and are discussed in respect to the role of
temperature in the developmental plasticity of fish.
D 2004 Elsevier B.V. All rights reserved.
* Corresponding author. Current address: Laboratory of Zoology, Biology Department, University of Patras,
26110 Patras, Rio, Greece. Tel.: +30-2810-394062; fax: +30-2810-394408.
E-mail addresses: g.koumoundouros@biology.uoc.gr, koumound@upatras.gr (G. Koumoundouros).
0044-8486/$ - see front matter D 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquaculture.2003.08.014
408 D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424
1. Introduction
al. (2001c), appropriately modified (briefly summarized in Fig. 1) to meet the requirements
of P. erythrinus. Initial stocking density was 4 eggs/l.
In order to study the effect of temperature on the rate of development, we used fish
reared with the intensive method at three different water temperatures (16.0 F 0.4,
18.0 F 0.2 and 21.0 F 0.2 jC). The intensive rearing method was selected due to its
precision in adjusting water temperature. It was performed in cylinder-conical tanks of 2.5
m3 volume, in open recirculation system (5– 10% day 1 water exchange rate). Initial
stocking density was 20 eggs/l. The photoperiod was 24-h light up to 8.5 mm TL and 14-
h light to 10-h dark thereafter. Oxygen saturation was over 90%, salinity was 40 ppt and
pH was around 7.8. Ammonia and nitrite never exceeded 0.02 and 0.05 mg l 1,
respectively. The enrichment of the live prey was identical to that of the mesocosm
rearing. The feeding protocol applied is described in Fig. 1.
Although intensive and mesocosm rearing did not use sibling eggs, they came from
wild breeders, caught in the same geographic area (Eastern Mediterranean, Aegean Sea),
therefore belonging to the same stock. In all the cases studied, spontaneous maturation and
spawning were carried out under ambient photoperiod and temperature conditions (35jN).
Breeders were fed on repro-type commercial pellets, enriched twice a week with fresh-
frozen fish and squids.
The comparison among the different temperature conditions was conducted with
reference to the TL at which each different set of meristic characters was completed.
The meristic characters studied were caudal, dorsal, anal, pectoral and pelvic lepidotrichia
and dorsal and anal spines, in respect to the completion of their formation. The preceding
characters were chosen because the precise definition of their full assembly is possible, as
opposed to other skeletal characters where it is not always possible to determine with
accuracy the end of their ontogeny. Pelvic fin formation and the completion of pectoral
rays could not be studied for the 16 jC reared fish due to lack of suitable specimens.
Instead, the developmental time (in mm TL) at which the ontogeny process had reached
Fig. 1. Feeding protocol utilised for the two different rearing methods in relation to total length (TL). Art I and II,
Artemia nauplii and metanauplii, respectively. Crum, commercial crumbles. Phyto, phytoplankton. Rot, rotifers.
410 D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424
the development of the first 10 pectoral lepidotrichia for all three temperatures was
utilised.
The ontogeny was studied in respect to TL (mm) as the latter constitutes a better
measure of ontogenetic state than age (Fuiman et al., 1998). At the yolk sac larval stage,
time after hatching expressed relative to the total duration of the stage (RTi) was used in
order to describe development accurately (Koumoundouros et al., 1998).
3. Results
All the elements that comprise the vertebral column and the fins studied, as well as the
basic developmental processes, are described thoroughly in Koumoundouros et al.
(2001c). Fig. 2 demonstrates collectively the developmental sequence of all skeletal
elements against total length.
Fig. 2. Developmental sequence of vertebral column and fin supports and rays in P. erythrinus. Open bar,
.
cartilaginous state; stippled bar, ossification state; solid bar, ossified state; o or , full complement of elements.
composed of HS1 – HS8 and HS13 (4.7 mm TL). The first parapophysis formed is Pp5 and
the ontogeny continues rostrad until the formation of Pp1 (Fig. 3D).
Vertebral centra U2 – U3 form first, followed almost simultaneously by U1 and U4 (5.8
mm TL). The formation of the rest continues caudad, whereas the urostyle forms together
with U12 at 6.8 mm TL (Fig. 3E). The ossification of each centrum proceeds ventrad with
the exception of U22 and U23 where it proceeds dorsad.
Each pair of the ventral and the dorsal ribs forms separately from the others with Pr1
and Drl1 being the first to appear. The rest of the ontogeny continues caudad. The
412 D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424
D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424 413
ossification of Pr’s follow the same pattern, however it was not completed until the end of
the studied developmental stage (17.6 mm TL) (Fig. 3F).
The ossification of all the above cartilaginous elements (first appearance and comple-
tion) follows precisely the pattern of the cartilage formation (Figs. 2 and 3C –F).
Fig. 3. Development of the vertebral column, dorsal and anal fins. (A) 4.3 mm TL; (B) 4.8 mm TL; (C) 5.1 mm
TL; (D) 5.9 mm TL; (E) 8.1 mm TL; (F) 12.0 mm TL. Open area, cartilage (with the exception of the notochord);
stippled area, ossification. The ossification state of the caudal rays is not drawn. The intermediate rays of dorsal
and anal fin are not drawn in (F). Drl, dorsal rib; Ep, epurals; HS, haemal processes; Hy, hypurals; Nc,
notochord; NS, neural processes; Pp, parapophysis; Pr, pleural rib; Prd, predorsal; PrH, parhypural; PrR,
proximal radial; S, hard spine; R, lepidotrichium; Rd, distal radial; U, vertebral centra; Ur, urostyle. Scale bars
are equal to 0.5 mm.
414 D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424
D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424 415
7.5 mm TL (Fig. 5E). The ossification process on the Prx’s begins at 8.1 mm TL (Prx1) and
by 9.2 mm all four of them are under the ossification process (Fig. 5E,F).
The ontogeny of lepidotrichia starts at 6.0 mm TL, almost simultaneously with the
appearance of the propterygium cartilage (Prop) (Fig. 5D), and they reach their final
number (14) at 11.0 mm TL (Fig. 5F). Following the development of R’s, the first
distal radials (Dr’s) appear at 6.2 mm TL (Fig. 5D) and the last at 12.0 mm TL (Fig.
5F).
All membranous bones that participate in the pectoral fins are drawn in Fig. 5 and their
exact ossification onset is been given in Fig. 2.
Fig. 4. Development of the caudal fin. (A) 3.8 mm TL; (B) 4.8 mm TL; (C) 5.1 mm TL; (D) 5.9 mm TL; (E) 9.6 mm
TL; (F) 15.4 mm TL. Open area, cartilage; stippled area, ossification. Ac, accessory cartilages; Ep, epurals; HS,
haemal processes; Hy, hypurals; Nc, notochord; NS, neural processes; PCR, caudal lepidotrichia; PrH, parhypural;
PU, preural centra; SCR, caudal dermatotrichia; Ur, urostyle; UrN, uroneural. Scale bars are equal to 0.5 mm.
416 D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424
Fig. 5. Development of the pectoral fins. (A) 3.1 mm TL, 100% R.T.i; (B) 3.4 mm TL; (C) 4.3 mm TL; (D) 6.3 mm
TL; (E) 8.9 mm TL; (F) 12.0 mm TL. Open area, cartilage; stippled area, ossification. Bp, Basipterygium; Cl,
cleithrum; Co, coracoid; Fp, fin plate; PocLo, metacleithrum lower; PocUp, metacleithrum upper; Pot,
posttemporal; Prop, propterygium; Prx, proximal pterygiophore; R, lepidotrichium; Rd, distal radial; Sca, scapula;
ScF, scapular foramen; Suc, hypercleithrum; SutLo, extrascapula lower; SutUp, extrascapula upper. Scale bars are
equal to 0.5 mm.
Rd’s follow closely the developmental pattern of PrR’s. They are first observed at 5.9
mm TL (Rd4 – Rd7) and, by 6.8 mm TL, they are all formed (Fig. 3E). Their ossification
begins at 11.0 mm TL (Rd1) and by the end of the studied developmental period only Rd1
was completely ossified.
The ontogeny of lepidotrichia starts at 6.0 mm TL and lasts until 6.8 mm (9 in total
meristic count) TL whereas the hard spines follow them and are formed by 7.5 mm TL.
D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424 417
The stay cartilage forms at 6.5 mm TL and begins to fuse with the last PrR at 9.2 mm
TL (Fig. 3E,F).
The pattern of the osteological development was the same at the three temperatures
tested and did not differ from the standard one (fish reared with the semi-intensive method)
that was described above.
In all cases, as temperature rises the ontogeny in respect to TL accelerates (Fig. 7).
Comparing fish reared at 16 jC and fish reared at 21 jC, the biggest difference is observed
in the caudal lepidotrichia (10.9% in total length) and the smallest in the anal spines (5.1%
in total length). Fish reared at 16 and 18 jC exhibit the highest differentiation in the caudal
lepidotrichia again (9.2% in total length) and the smallest in the anal spines (1.9% in total
length), whereas those reared at 18 and 21 jC present the highest differentiation in the
Fig. 6. Development of the pelvic fins. (A) 8.1 mm TL; (B) 9.7 mm TL; (C) 14.0 mm TL. Open area, cartilage;
stippled area, ossification. The ossification state of the rays is not drawn. Bp, basipterygium; Mep,
metapterygium; R, lepidotrichium; S, hard spine. Scale bars are equal to 0.5 mm.
418 D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424
Fig. 7. Schematic representation of the completion of caudal lepidotrichia, of dorsal and anal spines and
lepidotrichia, of pectoral and pelvic lepidotrichia and of the first 10 pectoral lepidotrichia at the three different
temperatures. n, completion of the above meristic characters was present in all specimen examined.
pelvic lepidotrichia (6.7% in total length) and the smallest in the caudal lepidotrichia
(1.5% in total length).
In all examined lots, skeletal abnormalities affected only the caudal fin, and especially
the neural and haemal processes of the two preural vertebrae. The incidence of abnormal
fish gradually increased as temperature increased, from 33% at 16 jC to 57%, 73% and
75% at 18, 21 and 23 jC, respectively. Additionally, temperature was directly correlated
with the severity of the deformities, mainly expressed as incidence of fish with more
caudal elements affected simultaneously (Fig. 8), with the exception of mesocosm rearing
at 23 jC. The abnormalities of the preural processes consisted of duplication of the arches
and/or shape deformations (Fig. 8). The remaining abnormalities consisted of (a) extra or
deformed epural elements, (b) extra, deformed or fused preural centra, and (c) deformed or
fused hypural elements (Fig. 8). In the mesocosm lot, observed deformities were of very
low intensity and mainly in the form of a light fusion between only two neighbouring
elements.
In addition to the skeletal deformities, reared fish suffered from the presence of urinary
calculi, the incidence of which increased from 8% at 16 jC to 17%, and 54% at 18 and 21 jC,
D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424 419
Fig. 8. Indicative drawing of the caudal fin summarizing all types of observed deformities. (1) Malformed and
fused vertebral centra 22 and 23; (2) malformed ‘‘Na’’ (includes two arches and deformation in shape); (3) extra
epural; (4) malformed Hy3; (5) malformed Hy2; (6) fused Prh, Hy1 and Hy2; (7) malformed HS12. Scale bar is
equal to 0.5 mm.
respectively. However, the incidence of this abnormality decreased to 35% in the mesocosm
lot reared at 23 jC.
4. Discussion
The sequence of appearance of the principal fin structures in each of the fins studied,
caudal, pectoral, dorsal, anal and pelvic, was identical in larvae reared at 16, 18 and 21 jC
and the same as the standard larvae reared in the semi-intensive regime.
The skeletal ontogeny of P. erythrinus is similar to that of other Sparidae (Archosargus
rhomboidalis (L.), Houde and Potthoff, 1976; Pagrus major Temminck and Schlegel;
Matsuoka, 1987; Sparus aurata L., Koumoundouros et al., 1997; Faustino and Power,
1998, 1999; Dentex dentex L., Koumoundouros et al., 1999b, 2001d; Diplodus sargus L.
Koumoundouros et al., 2001c) as far as the pattern of development is concerned; there is
no osteological development at hatching, and the first anatomical regions that bear skeletal
structures are the pectoral fins (cleithrum) followed by the caudal fin, the vertebral
column, the dorsal and anal fins and lastly the pelvic fins. All Sparidae (including P.
erythrinus) also resemble each other in the sequence of development of their fin rays; the
caudal fin is always first to present rays and complete all of its lepidotrichia, in contrast to
its dermatotrichia which are the last rays of the body to be formed. After the caudal
lepidotrichia, the next fins which attain full meristic counts are the pectoral, the dorsal,
420 D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424
anal and finally the pelvic fins (Houde and Potthoff, 1976; Matsuoka, 1987; Faustino and
Power, 1998, 1999; Koumoundouros et al., 1997, 1999b, 2001c,d).
The proximal radials and the distal radials of P. erythrinus originate from different
cartilaginous elements, a common feature of Sparidae that can also be found in some other
fish species (Potthoff and Tellock, 1993). P. erythrinus also presents certain characteristics
typical not only of the Sparidae, but also of all Perciformes. One of these characteristics is
the development of anal and posterior dorsal fins together and before the anterior dorsal
fin, the presence of stay cartilage, and the presence of scapular foramen (Houde and
Potthoff, 1976; Johnson, 1984; Potthoff et al., 1984; Watson, 1987; Watson and Walker,
1992; Faustino and Power, 1999; Koumoundouros et al., 2001c,d). The presence of
metapterygium in the pelvic fins is an extraordinarily rare feature among the Perciformes
(Potthoff and Tellock, 1993; Koumoundouros et al., 2001c).
The only important difference in the procedure of osteological development between
Sparids is the developmental time (in mm TL) at which each species concludes its
ontogeny. P. erythrinus seems to be one of the fastest, presenting almost all the different
ontogenetic stages at significantly smaller TL’s than all the other Sparidae species (Houde
and Potthoff, 1976; Matsuoka, 1987; Faustino and Power, 1998, 1999; Koumoundouros et
al., 1997, 1999b, 2001c,d). Of course, taking into account the effect of temperature on
skeletal ontogeny in the present study, it is clear that the intraspecific variation exhibited
here due to temperature makes such comparisons of dubious use especially when referring
to different species. Moreover, a study of the osteological development (caudal fin area) of
S. aurata, by two different authors (Faustino and Power, 1998; Koumoundouros et al.,
1997) gave such dissimilar results that could account for different species. Therefore, in
order to make the comparison of osteological development rates meaningful, one should
take into account the temperature during development.
Fuiman et al. (1998) concluded that higher temperatures accelerate the rate of
development more than the rate of growth, thus resulting in different larval sizes at
specific developmental stages. Koumoundouros et al. (2001b) studied the effect of
temperature on the developmental and growth rate in Dicentrarchus labrax and concluded
that at the highest temperature used (20 jC), the TL of the larvae during first feeding,
notochord flexion, and fin differentiation was much smaller than larvae at the lower
temperature regimes. Studies in other fish species show as well that as temperature rises,
the TL at which various ontogenetic events such as hatching (Batty et al., 1993),
appearance of fins (Fuiman et al., 1998) and metamorphosis (Seikai et al., 1986) take
place, becomes smaller.
Temperature-induced plasticity could be explained as a mechanism responsible for the
larval survival in nature. It is well established that morphological ontogeny and function
are closely related and that all fish species in order to overcome all those environmental
changes threatening their lives have developed similar patterns of ontogeny (Osse and van
den Boogaart, 1995, 1999). So, most marine fish are unable to feed at hatching and their
locomotion abilities also are still very limited (Kentouri, 1985; Koumoundouros et al.,
1998, 2001b). The only means for their movement is the primordial marginal finfold
D.G. Sfakianakis et al. / Aquaculture 232 (2004) 407–424 421
which does not allow delicate manoeuvres or fast swimming, thus restricting the larvae
from prey hunting and predator avoidance. As ontogeny proceeds, the formation of the
caudal and the rest of the fins make the fish able for faster and more complicated
locomotion (Matsuoka, 1987; Koumoundouros et al., 2001b).
Since temperature affects the developmental rate of fish larvae (Fuiman et al., 1998;
Koumoundouros et al., 2001b), it could also play a significant role in their survival and
recruitment in nature. It is therefore easy to presume that the temperature-induced
plasticity of the ontogenetic scaling is a mechanism crucial for the survival of the P.
erythrinus larvae in nature as well. The fact that in the present study the biggest plasticity
is exhibited by the pectoral and pelvic fins could mean that those characters are more
variable than the others studied. This is probably due to their significant role in refined
movements and consequently to life preservation in different conditions.
The plasticity exhibited by sea bass (Koumoundouros et al., 2001b) in the different
temperatures is much higher than the observed here. Moreover, Polo et al. (1991) observed
that in newly hatched and first-feeding S. aurata (L. 1758) smaller TL’s belonged to fish
coming from both extreme temperatures (high and low) and not only from the high ones.
There is also the case of Platichthys stellatus (Policansky, 1982) which as temperature
rises, its size at metamorphosis enlarges as well. All the above lead us to the conclusion
either that this is a certain individuality exhibited by P. erythrinus or that the temperature
range tested was not adequately broad. The 5j range is narrow, in order to totally study the
thermal dependence of ontogenetic processes. Therefore, lower and higher temperature
regimes are required so that one can be certain about the ‘‘behaviour’’ of this species’
development in different temperatures.
the margin of the temperature limits. Under this consideration, it is suggested that the
negative effects of temperature could be remedied by improving certain rearing conditions
(nutrition, fish density, water quality, environmental stratification, etc.) (Koumoundouros
et al., 1997, 2001e; Divanach and Kentouri, 2000).
The deformities of the caudal fin maybe are the most frequent ones present in reared
fish (Marino et al., 1993; Boglione et al., 2001b; Koumoundouros et al., 2001a). This
general trend could be attributed to the fact that in many fish species the caudal fin is the
first fin that starts developing, during the most critical—under rearing conditions—early
developmental stages (Koumoundouros et al., 1999b, 2001d). Taking this into consider-
ation, the deformities of the caudal fin could be proposed as an index of the appropri-
ateness of the rearing conditions, even in cases of low severity, thus providing a valuable
tool for their establishment. Given that different temperature conditions are proposed to be
required for the different developmental stages of each species (Herzig and Winkler, 1986;
Klimogianni et al., submitted for publication), the observed effects of temperature on
morpho-anatomical deformities should be examined in different ontogenetic windows in
order to determine in each case the appropriate conditions for normal development.
Acknowledgements
The authors wish to express their thanks to Eric Maingot for the maintenance of
mesocosm population and to the commercial hatchery for the provision of intensively
reared samples. The authors also acknowledge C. Doxa for conducting part of the staining
procedures.
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