Effect of Steroids on Gonadal Growth and Gametogenesis in the Juvenile Red Sea Urchin Pseudocentrotus depressus

6 Pages·1999·2.6 MB·English

by  T Unuma

Reference: Biul. Hull. 196: 149-204. (April
Effect of Steroids on Gonadal Growth and
Gametogenesis in the Juvenile Red Sea Urchin
Pseudocentrotus
depressus
TATSUYA UNUMA1-*, TAKESHI YAMAMOTO2, AND TOSHIO AKIYAMA3
1 National Research Institute ofAquaculture, Nansei, Mie 516-0193. Japan;
2 Inland Station, National Research Institute ofAquaculture, Tamaki, Mie 519-0423, Japan: and
' National Research Institute ofFisheries Science, Fukuura, Kanazawa, Yokohama 236-8648, Japan
Abstract. Red sea urchins, 10 monthsold, were fed for30 previous reports suggest that steroids are involved in the
days on a casein-based diet containing progesterone, andro- reproduction of starfish.
stenedione. testosterone, estrone, or estradiol-17/B. The The importance of steroids in sea urchin reproduction is
mean gonad indicesofmale animals in the androstenedione- less well known. Estradiol-17/3 induced the synthesis of a
and the estrone-treated groups were significantly higher novel protein in the coelomocytes of Dendraster excentri-
than those in the control group, suggesting that these ste- cus and Strongylocentrotuspurpuratus in vitro (Harrington
roids promote gonadal growth in male animals. Histological and Ozaki, 1986). Levels ofestradiol-17/3 and progesterone
observations indicated that spermatogenesis in the estrone- were determined in the testes and ovaries of Eucidaris
treated group was also promoted compared to that in the tribuloides every 3 months during the annual reproductive
control group. In contrast, female urchins were not obvi- cycle (Hines et al., 1992c). Oral administration of estrone
ously affected by the steroid-treated diets, probably because increased the body weight of Pseudocentrotus depressus,
yearling female P. depressus are not otherwise ready to the red sea urchin (Unuma et al., 1996a). However, we are
carry out gametogenesis. We conclude that androstenedi- just beginning to understand the relationship between ste-
one, estrone. and possibly their derivatives, are involved in roids and the reproduction of sea urchins.
the reproduction of male P. depressus. In P. depressus, gonadal growth occurs from spring to
late autumn, preceding and alsoduring gametogenesis. This
growth is mainly due to the accumulation ofnutrients by the
Introduction
nutritive phagocytesthat occupy the luminaofthe gonadsof
Sex-related steroids, which have regulatory functions in both sexes. Gametogenesis normally begins in Septemberor
vertebrate reproduction, are also found in echinoderms. The October, and gonads are filled with mature gametes in
roles and actions of steroids in starfish have been investi- November or December (unpubl. data). To investigate the
gated often: e.g., biosynthesis and metabolism (Schoenmak- effect ofsteroids on gonadal growth and gametogenesis, we
ers. 1979;Schoenmakersand Voogt, 1980, 1981; Voogtand fed sex-related steroids to P. depressus. Casein-based diets
Van Rheenen. 1986; Voogt et a!., 1986, 1990. 199la. b; containing progesterone, androstenedione, testosterone, es-
Mines et nl., 1992a); seasonal variations in steroid levels trone, orestradiol-17/3 were prepared and fedtojuvenile red
(Schoenmakers and Dieleman. 1981; Voogt and Dieleman, sea urchins for 30 days beginning in early September.
1984; Xu and Barker, 1990; Xu. 1991; Mines et al., 1992b);
and the effects of steroid injections (Schoenmakers el al., Materials and Methods
1981; Takahashi, 1982a. b: Barker and Xu, 1993). These
Animals
Individuals of P. depressus were hatched and reared at
R*eAcuetihvoerd 2t1oOwcthoobmer c1o99r7r;esapcocnedpetnecde25shJoaunludarybe199a9d.dressed. E-mail: the Fukuoka Prefectural Fish Farming Center and were
[email protected] transferred to the Nansei Station of the National Research
199
200 T. UNUMA ET AL
Table I
Composition of the experimental diets
Casein
EFFECT OF STEROIDS ON SEA URCHIN 201
Results
Gonad index
No mortality occurred during these experiments. More-
over, sex could be determined by histological observations
in all but three animals. One specimen in each of the
progesterone-, androstenedione-, and testosterone-treatment
( groups was neuter, and these three cases were omitted when
average GIs were calculated for each sex.
Figure 2 shows the mean Gl values for each sex after the
30-day feeding trial. In male animals, the mean GI of
the control group was 4.87%. The androstenedione- and
estrone-treated groups showed significantly higher values
than the control group, 6.22% (P < 0.05) and 6.94% (P <
0.001), respectively. The values in the progesterone-, the
testosterone-, and the estradiol-17/3-treated groups were not
significantly different from the control group.
E Unlike the male animals, the female animals had similar
mean GI values from all groups; in particular, no significant
difference was foundbetweenthe steroid-treatedgroupsand
the control group.
Maturational stages ofgonads
Frequencies ofthe maturational stages ofgonads foreach
sex are shown in Figure 3. In males, the percentages of
Stages 1, 2, and 3 in the control group were 32%, 54% and
14%, respectively. In all the steroid-treated groups except
that treated with estrone, the percentage of each stage was
similar to that in the control group. In the estrone-treated
group, however, the percentage of Stage 1 was only 4%
(one-eighth that of the control group) and that of Stage 3
was 31% (more than twice that of the control group). The
distribution of maturational stages in the estrone-treated
Figure 1. Classification of gonadal maturity in Pseudocentrotus tlc- group was significantly different (P < 0.05) from that ofthe
/'irswiv. Onlythestagesobservedinthisstudyareshown.B,D.F.H:male;
C.E,G: female. (A)Stage0:Noobviousgermcellsareobserved,andsex
is unidentifiable. (B,C) Stage 1: Small clustersofspermatogoniaorafew
young oocytes are present at the periphery ofthe gonad. (D. E) Stage 2: Control
The gonadscontain rows ofspermatogonia orofoocytes. (F. G) Stage 3:
In the center of the lumina, nutritive phagocytes are replaced with sper- Progesterone
matozoa or ripe ova. (H) Stage 4: The gonadal lumina are filled with
spermatozoa. Scale bar: 200 jxm. Androstenedione
Testosterone
Estrone
Statistical analysis
Estradiol-17p
The mean values ofGI and daily food consumption were
compared using unpaired Student's t tests between the ste-
roid-treated groups and the control group, after comparison
of the variances using F test. Figure2. GonadindexofmaleandfemalePseudocentrotusdepressus
The Mann-Whitney U test was used to compare the ifnedthdeiegtsracpohntianidniicnagtesttehreoindus.mbVearluoefsirnedpivriedsueanlts.thVeamlueeasnwithSEa.stNeruimseksraalrse
distribution of the maturational stages of gonads between significantlydifferent from thecontrol ofthesame sex (*. P < 0.05; ***,
the steroid-fed groups and the control group. P < 0.001).
202 T. UNUMA ET AL
Male Female
Control-
Progesterone- n Stage 1
Androstenedione- D Stage 2
Testosterone- Stage 3
Estrone- Stage 4
Estradiol-IZp-
25 25 50 75 100
Figure3. Frequenciesofthe maturational stagesofgonadsformaleand femalePseudocentrotusdepressits
fed diets containing steroids. The frequencies for male animals in the estrone-treated group are significantly
different from those in the control group (P < 0.05).
control group. This suggests that spermatogenesis was pro-
moted in the estrone-treated group.
In the females from all groups, most of the gonads were
in Stage 1, with no specific difference observed between the
steroid-treated and control groups.
Dailyfood consumption
The mean daily consumption, based on wet matter, for
duplicate tanks are shown in Table II. The androstenedione-
and the estrone-treated groups showed higher values than
the control group, but this difference was not significant.
Discussion
In this study ofP. depressus, the responses of males and
females to orally administered steroids was markedly dif-
ferent. In males, the mean GIs in the androstenedione- and
the estrone-treated groups were significantly elevated com-
pared to that in the control group, suggesting that andro-
i..i.i. II
Daily consumption by Pseudocentrotus depressus ofdiets containing
steroids
Diet
EFFECT OF STEROIDS ON SEA URCHIN 203
nin synthesis may be controlled by steroids in sea urchins. fied diet for red sea urchin Pseudocentrotus depressus. Fish. Sci. 63:
881-886.
as it is controlled in oviparous vertebrates by estrogens Barker, M. F., and R. A. Xu. 1993. Effects ofestrogens on gameto-
(Wallace, 1985), and in insects by ecdysteroids (Hagedorn, genesis and steroid levels in the ovaries and pyloric caecaofScleras-
1985). In this study, the accumulation of nutrients into the teriasmollis(Echinodermala: Asteroidea). Invertebr. Reprod. De\: 24:
nutritive phagocytes may have been enhanced by the ste- 53-58.
roids through the synthesis of vitellogenin. Fuji,A. 1960. Studiesonthebiologyoftheseaurchin.I. Superficialand
In sea stars of both sexes, estrogens may promote bio- histological gonadal changes in gametogenic process of two sea ur-
synthesis of protein in the pyloric caeca and its subsequent Hchoiknks.aiSdtoroUnngiyvl.oc1e1n:tr1o-t1u4s.nudus and S. iniermedius. Bull. Fac. Fish.
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injections of androstenedione and estrone over a 16-day Halver, J. E. 1957. Nutrition of salmonid fishes III. Water soluble
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stenedione was metabolized to estrone, which then affected Androgen metabolism in somatic and germinal tissues ofthe sea star
tihnefomrombaitliioznatiisonaovfaiplraobtleeinosnintthoethbeioovsayrnitehse.siHsowoefveers,trloigttelne HineAssst,tereGori.idaAsl.e,vvuSel.lgsaAr.iinsW.tahtCetostm.epst.Se.sB,Ai.oovScaohrewimees.r,,PahanyndsdiopCly..loWr1i.0c2WBca:ela5kc2ea1rd-.u5r21i69n.9g2bg.ameSteox-
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