REPRODUCTIVE CYCLES OF DIADEMA

BULLETIN OF MARINE SCIENCE, 67(2): 845–856, 2000

CORAL REEF PAPER

REPRODUCTIVE CYCLES OF DIADEMA SETOSUM AND ECHINOMETRA MATHAEI (ECHINOIDEA: ECHINODERMATA) FROM KUWAIT (NORTHERN ARABIAN GULF) Adel H. Alsaffar and Khalid P. Lone ABSTRACT A study was undertaken on the seasonal variations in the reproductive biology of Diadema setosum and Echinometra mathaei from the coral reefs of Kuwait. Sixteen monthly samples were taken for both species and gonads were processed for histological studies. Both species had peak spawning in summer months when maximum seawater temperature was between 24.2 and 28.8ºC. Peak spawning was seen for Diadema in AprilMay (24–28ºC), while this point for Echinometra was achieved in June (28.8ºC). The spawning peak was much broader for Diadema. The breeding season in both species coincided well with increasing seawater temperature and day-length. The gonad color was not related to sex and there was no difference in drained weight of male and female of both the species. Both spermatogenesis and oogenesis were histologically similar to other echinoid species described by other authorities.

The Indo-Pacific echinoids Diadema setosum and Echinometra mathaei are distributed from Japan to southern Australia and from Mexico to the Gulf of Suez (Khamala, 1971). Throughout their distribution, their ecology, biology and reproduction have been studied (Pearse, 1968, 1969; Kobayashi, 1969; Lessios, 1981; Illiffe and Pearse, 1982; Drummond, 1995). Reproduction in previously studied populations was either continuous or restricted to certain part of the year (Pearse and Cameron, 1991). Reproduction of these species has not been studied on the coral reefs of Kuwait. Despite the extreme difference in seawater temperatures (minimum 10.6ºC in January; maximum 32.8ºC in August with air temperature reaching beyond 50ºC), the populations of both species are well established at the coral reef, with E. mathaei being more prevalent than D. setosum. The population density of D. setosum has been reported to range from 3 to 15 urchins m−2 while that of E. mathaei exceeds 100 urchins m−2 (Downing and El-Zahr, 1987; Downing, 1992; Downing and Roberts, 1993; Carpenter et al., 1997; Harrison et al., 1997). Here we report the reproductive periodicity of these species and compare it with studies on these species elsewhere. MATERIALS AND METHODS Urchins were collected from Kuwait’s Kubbar Island reef (29º 04.25'N, 48º 29.50'E) from the sampling positions shown in Figure 1. Diadema setosum were taken from the reef edge at a depth ranging from 3 to 5 m, at a bearing of 140o magnetic to the light tower on the Island. E. mathaei were taken from the reef flat at a position 70 m from the reef edge along the previous bearing at a depth ranging from 1–2 m. The urchins were collected in early morning in the middle of the lunar month (at full moon), or as soon as possible thereafter. Each month, 20 to 30 individual urchin of each species were collected by divers in mesh bags, transported to the laboratory and immediately laid on a table with the oral opening facing down to allow the excess of water to drain. The sampling was done for 16 mo starting from the month of November 1985 through February 1987. 845

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Figure 1. Map showing the location of Kuwait’s main coral reefs and the sampling sites at the island of Kubbar. The expanded view of the island and the reef shows the island in solid line with its light tower while the reef surrounding the islands is shown in dotted line. The numbers one and two correspond to the sampling sites for Diadema setosum and Echinometra mathaei respectively. The position two was 70 m from the bigger reef edge. The solid arrow represents 140º magnetic from sampling site 1 to the light tower. Each urchin was weighed to the nearest 10 mg and then carefully cut in half and the color, sex and the state of maturity of the gonad were estimated. The gonads were removed and weighed to the nearest mg. The drained weights for Diadema ranged from 27.91–105.13 g (n = 346) while the weights for Echinometra were 23.61–66.32 g (n = 329). After weighing, the gonad was fixed in 10% buffered formalin and embedded in paraffin. Sections were cut at 6–8 μ and stained with haematoxylin-eosin and examined for male and female gametogenic cycle. The gonad index (GI) was computed according to the formula (Lamare and Stewart, 1998; Meidel and Scheibling, 1998; Walker and Lesser, 1998) given below:

ALSAFFAR AND LONE: REPRODUCTION OF DIADEMA SETOSUM AND ECHINOMETRA MATHAEI

GI =

847

Weight of the gonad (g) × 100 Drained weight of the urchin (g)

The GI data were evaluated using a single-factor (fixed effect of time) ANOVA at a significance level of 5%. Where significant effects were found, the Student-Newman-Keuls (SNK) multiple comparison test was applied to identify differences among sampling times (Sokal and Rohlf, 1981). The relationship between the drained body weight, gonad weight (GW) and GI was also analyzed using linear regression.

RESULTS AND DISCUSSION Minimum water temperature was observed in January (range 10.6º–17.6ºC mean minimum = 16.0ºC) while the maximum was in August (range 28.3º–32.8ºC; mean maximum = 30.3ºC). The day-length ranged from 10 h 20 min in December to 14 h in June; Fig. 2). Salinity ranged from 42–44 ‰ while the pH of the seawater was 8.2–8.4. There was a slight increase in the gonad weight with the increase in the drained body weight in both species, but this relationship was not significant statistically. Similarly, the relationship between drained body weight and GI was also not significant. The regression equations for the two species are given below: Diadema GW = −0.8126 + 0.0462 × drained body weight (r2 = 0.2857; n = 346) GI = 1.6436 + 0.0251 × drained body weight (r2 = 0.0297; n = 346) Echinometra GW = −0.4475 + 0.0378 × drained body weight (r2 = 0.2178; n = 329) GI = 1.6928 + 0.0231 × drained body weight (r2 = 0.0205; n = 329) The relationship between the gonad weight, gonad index and test diameter was recently studied in green urchin (Strongylocentrotus droebachiensis) and a diadematoid urchin (Centrostephanus rodgersii). Both studies found that there was no significant relationship between the gonad output, gonad index and the test diameter (Byrne et al., 1998; Meidel and Scheibling, 1998). This relationship indicates a decreasing investment in reproduction beyond a given size. A decrease in reproductive effort beyond a given maximal size is common in many echinoderms particularly, the echinoids (Lawrence and Lane, 1982; Guillou and Lumingas, 1999). This can also be due to a decrease in feeding activity and metabolism with age. The GI of E. mathaei was low and remained more or less constant during the months of November (2.64 ± 0.16; mean ± S.E.) through April (2.49 ± 0.24) when water temperature averaged less than 25ºC (Fig. 2). The gonads start maturing rapidly from April and peaked in the month of June. The maximum GI (6.62 ± 0.52) was also encountered in June. The spawning activity of this species peaks during June and July, as in July the GI dropped to values comparable to May values. This spawning occurred between the June full moon and the new moon of July. GI values gradually decreased until the minimum was reached in January. The GI at this time was 1.22 ± 0.16 (Fig. 2). The ANOVA (F15, 314 = 20.99, P = 0.000) showed significant differences among the GI values of different months

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Figure 2. Minimum and maximum water temperature, day-length and mean gonad index (percentage of drained body weight, ± SE) of Echinometra mathaei and Diadema setosum between November 1985 and February 1987. Means are based on, at least, 20 sea urchins each every month.

(Fig. 2). Post-hoc comparisons showed that May, June and July GI values were significantly (P < 0.05) higher than those were for the other months (Table 1). January 1987 values were also lower than the November 1985 and April, August 1986 GI values (P < 0.05). The GI for D. setosum was unlike that for E. mathaei, and started increasing slowly from November (2.18 ± 0.27) and reaching an initial maximum in January (3.78 ± 0.32). There was a slight decrease in the GI in February (3.13 ± 0.38), but after this time the values continued increasing until the peak values were observed in April (5.52 ± 0.34). The values remained constant in May (5.53 ± 0.25) and then declined. Diadema, starts spawning from mid April when seawater temperature was 22–28ºC. The spawning activity of Diadema was more prolonged than that of Echinometra and continued until the end

ALSAFFAR AND LONE: REPRODUCTION OF DIADEMA SETOSUM AND ECHINOMETRA MATHAEI

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Table 1. Results of single factor ANOVA on the effects of date (time) on the gonad index of Echinometra mathaei and post-hoc Student-Newman-Keuls (SNK) test according to Sokal and Rohlf (1981). ANOVA Source of variation Between groups Within groups SNK test Month Nov. 85 Dec. 85 Jan. 86 Feb. 86 Mar. 86 Apr. 86 May 86 Jun. 86 Jul. 86 Aug. 86 Sep. 86 Oct. 86 Nov. 86 Dec. 86 Jan. 87 Feb. 87

SS

df

MS

387.25 387.41

15 314

25.82 1.23

May, June, July, Oct. 86, Jan. 87 May, June, July 86, Jan. 87 May, June, July 86, Jan. 87 May, June, July 86, Jan. 87 May, June, July 86, Jan. 87 May, June, July 86, Jan. 87 All months significant All months significant All months significant May, June, July 86, Jan. 87 May, June, July 86, Nov. 85, May, June, July 86 May, June, July 86, May, June, July 86 Nov. 85 to Aug. 86, Dec. 86 May, June, July 86,

P P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05 P < 0.05

F

P

20.99

0.00

All other comparisons, except the ones reported above, were non-significant.

of July, when the GI reached 3.03 ± 0.23 and the water temperature reached 30ºC. There is some overlap between the spawning of the two species. After July, the GI remained more or less constant until October after which time it decreased to its minimum (1.11 ± 0.16) in January. The low GI stage coincides with minimum water temperatures and short day-length. Fujisawa and Shigei (1990) while working with eight species of urchins in Japanese waters described similar temperature optima for the spawning of D. setosum (24–30ºC) and E. mathaei (22–30ºC). When the monthly GI of D. setosum were compared by ANOVA, the month was found to be highly significant (F15, 331 = 28.22, P = 0.000). Detailed post-hoc test (SNK) showed that April, May and June values were significantly different (Table 2) from rest of the months (Fig. 2). The successive phases of gametogenesis in echinoids follow an orderly time course in an individual or within a population (Pearse and Cameron, 1991). At the population level, most species of echinoids undergo discrete annual rhythms of active gametogenesis and spawning and this has been seen for many species and localities (Table 3). Species living near the equator spawn for a longer period of time than the temperate species (Fujisawa and Shigei, 1990; Lessios, 1985; King et al., 1994; Guillou and Michel, 1994; Guillou and Lumingas, 1998, 1999; Byrne et al., 1998; Meidel and Scheibling, 1998). These studies clearly show that environmental conditions have far reaching effects on the reproduction of these echinoderms. Of the environmental factors studied, temperature, photoperiod, food and salinity are more important than are the other factors.

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Table 2. Results of single factor ANOVA on the effects of date (time) on the gonad index of Diadema setosum and post-hoc Student- Newman-Keuls (SNK) test according to Sokal and Rohlf (1981). ANOVA Source of variation Between groups Within groups SNK test Month Nov. 85 Dec. 85 Jan. 86 Feb. 86 Mar. 86 Apr. 86 May 86 Jun. 86 Jul. 86 Aug. 86 Sep. 86 Oct. 86 Nov. 86 Dec. 86 Jan. 87 Feb. 87

SS

df

MS

F

P

588.26

15 459.76

39.22 331

28.22 1.39

0.00

Jan. 86, Apr.−Sep. 86, Jan. 87 Jan. 86, Apr.−Jun. 86, Jan. 87 All months significant except Jun. 86 Jan. 86, Apr.−Jun. 86, Jan. 87 Apr.−June, Dec. 86, Jan.87 All months significant All months significant All months significant Nov. 85, Jan. Apr. Dec. 86, Jan. 87 Nov. 85, Jan. Apr.−Jun. Dec. 86, Jan.87 Nov. 85, Jan. Apr.−Jun. Dec. 86, Jan.87 Jan., Apr.−Jun. 86, Jan. 87 Jan. Apr.−Jun. 86, Jan. 87 Jan. Mar.−Sep. 86, Nov. 85−Nov. 86, Feb. 87 Jan. Apr.−Jun. 86, Jan. 87

P P P P P P P P P

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