Marine Biology (1999) 135: 521±532 Ó Springer-Verlag 1999

M. D. Herrero-Pe rezrul á H. Reyes Bonilla F. Garcõ a-Domõ nguez á C. E. Cintra-Buenrostro Reproduction and growth of fuscus (Echinodermata: Holothuroidea) in the southern Gulf of California, MeÂxico

Received: 15 July 1998 / Accepted: 19 August 1999

Abstract The reproduction and growth of Isostichopus artisanal ®sheries in several American countries, princi- fuscus (Ludwig, 1875) at Isla Espõ ritu Santo, Baja Cali- pally Me xico, Costa Rica and (Powell and fornia Sur, Me xico from July 1992 to September 1993 Gibbs 1995; Fajardo Leo n and Ve lez Barajas 1996; and from August 1996 to July 1997 were analyzed. The Singh Cabanillas and Ve lez Barajas 1996; Son- reproductive cycle was monitored by using histological nenholzner 1997). In all these countries, it has been analysis. Five gonadal stages were described according suggested that the populations of I. fuscus and other to cell types present in the gonad; undetermined, ga- holothurian species have been overexploited (Camhi metogenesis, maturity, spawning and post-spawning. 1995; Fajardo Leo n and Ve lez Barajas 1996). In Me xico, This holothurian reproduces annually during summer I. fuscus is considered an endangered species (Norma (July to September), when sea surface temperature O®cial Mexicana 1994), though no studies were made to reaches 27 °C. The gonad index is related to the gonadal support this. In general, studies of the biology and stages. The ®rst sexual maturity for I. fuscus was cal- population dynamics of this holothurian are scarce. In culated at 367 g (4 to 5 years old) according to the von Me xico, most of the early papers dealt only with tax- Bertalan€y equation, and nearly all the specimens at Isla onomy and ecology (Caso 1967), but more recently Espõ ritu Santo were 5 to 7 years old (including some studies about the reproductive biology and brief ana- individuals over 35 years old). Data of the length±weight lyses of the ®shery of this holothurian along the south- relationship showed that I. fuscus grows allometrically at ern coasts of the Gulf of California have been made the studied site (b = 1.83). The mortality rate was rel- (Sing Cabanillas and Velez Barajas 1996; Fajardo Leo n atively high (M = 0.51), indicating that in a typical et al. 1995). cohort, 40% of the recruits does not survive the ®rst Most of the studies on reproductive biology of ho- year, and less than 20% reaches maturity. lothurians have focused on tropical and commercial species (Bakus 1973; Conand 1990), which commonly belong to the Families (Cameron and Fankboner 1986; Conand 1988, 1993a, b) and Ho- Introduction lothuriidae (Engstrom 1980; Harriot 1985; Ong Che and Go mez 1985). The objective of the present paper was to The holothurian is a common species describe the main patterns of the reproductive cycle of that inhabits shallow waters (0 to 40 m, mostly on coral Isostichopus fuscus and some aspects of its population and rocky bottoms) from the northern Gulf of Califor- biology. The study was done at Isla Espõ ritu Santo, in nia, Me xico to Ecuador (Maluf 1988). This holothurian the southern Gulf of California, Me xico. represents an important economic resource and supports

Communicated by O. Kinne, Oldendorf/Luhe Materials and methods M.D. Herrero-Pe rezrul (&) á F. Garcõ a-Domõ nguez Centro Interdisciplinario de Ciencias Marinas, Specimens of Isostichopus fuscus (Ludwig, 1875) were collected at Calle Madero 1865-2, Centro, Isla Espõ ritu Santo, Gulf of California (24°30¢N; 110°15¢W), par- C.P. 23000 La Paz, Baja California Sur, Me xico ticularly in San Gabriel Bay, which is characterized by shallow waters (maximum depth 6 m) and two large coral patch reefs H. Reyes Bonilla á C.E. Cintra-Buenrostro composed of Pocillopora spp. with occasional appearances of Universidad Auto noma de Baja California Sur, massive colonies (Porites spp. and Pavona spp.: Reyes Bonilla Depto. de Biologia Marina, Carretera al Sur km 5.5, 1993), which are exposed during extreme low tides in summer. At C.P. 23080 La Paz, Baja California Sur, Me xico the shore there is a mangrove forest composed of Rhizophora 522 mangle. Sea surface-water temperature ranges from 20 to 30 °C in The constants, Linf and K, and mean sea surface temperature in the bay. the studied area (averaged from monthly measurements in 1992 to 1993, and data from 1960 to 1990 included in the CD-ROM CO- ADS, produced by the NOAA) were used to estimate the natural Reproduction analysis mortality rate (M) of the population with Pauly's empirical model (Sparre and Venema 1995). In turn, this rate was used in the general For the reproduction analysis, sampling was done monthly from equation for determination of population size in a non-exploited July 1992 to September 1993. A total of 259 specimens (20 ()M*t) )1 stock: (Nt = N0 à e ), where t is the number of years (Ricker ind mo ) were collected by hand and ®xed in 10% seawater-for- 1975) to calculate yearly percentage of survival in a ``typical'' cohort. malin. Each individual was kept inside a separate plastic bag to Finally, to more precisely determine the von Bertalan€y model keep the gonads from mixing in case of evisceration. Once the constants and mortality rates, the con®dence intervals of Linf, Winf gonads were dissected, measured, weighed and stored in 70% al- (asymptotic weight), K and M were calculated with the jacknife cohol, they were histologically processed and embedded in paran. method, in which each parameter was recomputed 11 times, ig- Sections (7 lm thick) were stained with haematoxylin-eosin and noring one observation in turn each time (Sokal and Rohlf 1995). examined under a microscope (10 and 20´). The reproductive cycle of Isostichopus fuscus was monitored by using histological exami- nation of the gonadal stages and by changes in the gonad index (GI), calculated with the equation: GI = (gonad weight/drained weight) ´ 100 (Giese and Pearse 1974). To compare the monthly Results variations of the GI in both sexes, a one-way ANOVA test was used (a = 0.05). As GI is a percentage, the arcsin transformation Isostichopus fuscus is a dioecious species. There is no (Sokal and Rohlf 1995) was used to attain normality and homo- evidence of external sexual dimorphism, and the gonads scedasticity of data. The Tukey a posteriori test (Day and Quinn 1989) was used to determine the origin of the statistical di€erences, can only be sexed by microscopic examination. When when appropriate. Lastly, to test the hypothesis that the sex ratio ripe, the gonads consist of a single tuft of numerous was not signi®cantly di€erent from 1:1, a v2 goodness-of-®t analysis unbranched tubules that lie on the anterior end of the was carried out (Sokal and Rohlf 1995). coelom. After spawning, the gonad decreases in size by The size to attain ®rst sexual maturity in this species was cal- culated plotting the cumulative percentage of individuals which >90%. Of the 259 specimens dissected for reproduction were in gametogenesis, maturity or spawning stage, against length. analysis, only 173 (66.7%) had visible gonads: 64 were The point of the curve where 50% of the individuals were in those males, 78 females, 29 undetermined and 2 hermaphro- stages was considered the weight at ®rst maturity (Conand 1990). dites. The annual sex ratio was not signi®cantly di€erent We considered drained weight (DW) a more reliable measure for from 1:1 (v2 = 20.27, df = 12, P > 0.05). the analysis, because length is highly variable in holothurians. Dry weight is a still better choice to estimate ®rst sexual maturity On the basis of morphological and histological ob- (Conand 1982, 1988, 1990), but the use of this parameter implies servations, ®ve gonadal stages were described for Iso- the loss of the gonad, an unacceptable condition for this study. fuscus: undetermined, gametogenesis (oogenesis and spermatogenesis), mature, spawning and Growth analysis post-spawning. These stages showed an annual period- icity and were related to the GI variations. For growth determination, length measurements of a monthly mean of 120 individuals were obtained in six locations around Isla Espõ ritu Santo, from August 1996 to July 1997 (total = 1446 in- dividuals). Specimens were measured underwater from mouth to Undetermined (Fig. 1a) anus with ¯exible tapes (‹0.5 cm precision) trying to avoid body contraction. They were then put into individual plastic bags and In this stage, no gametes could be distinguished. All taken to a boat, where the weight of each was determined with undetermined gonads were similar. We found no evi- spring scales. The search for specimens was haphazard, looking at open sites on the sandy bottom and near rocky and coral reef areas, dence of gametes. The presence of abundant connective as well as under large coral heads (Pocillopora spp.), boulders and tissue was observed in the lumen and between the folli- coral rubble. Once length and weight were measured, all sampled cles, which were collapsed. It was common to observe holothurians were returned to the bottom in areas delimited by small phagocytes (about 3 lm diameter). The gonad natural markings, with the purpose of collecting in approximately wall was thick. The GI values were <2% at this stage the same locations every month and thus measuring as many of the same organisms as possible each time. As in the case of gonad (see Fig. 4). Undetermined gonads were seen from Oc- index, di€erences of weight and length among months were de- tober to January. A total of 86 specimens found during termined with ANOVA (a = 0.05) and Tukey tests. this period had no gonads, but it is possible that they Size-frequency data (grouped in 2-cm intervals) and its monthly were undetermined gonads. modal composition were analyzed to calculate the parameters of the von Bertalan€y growth model (Ricker 1975) using the com- puter package FiSAT, programmed by the FAO and ICLARM (Gayanillo et al. 1996). The following routines were used: Powell± Developmental stages of the male Wetherall (for calculation of mean asymptotic length, Linf), Shep- herd (to estimate K, individual growth coecient), and Pauly's Spermatogenesis (Fig. 1b) empirical equation (to obtain t0, the hypothetical age when growth is zero). Further details of all the analytical techniques used and their respective assumptions were presented by Pauly and Morgan In the gonad wall, longitudinal folds were observed, (1987), Sparre and Venema (1995) and Gayanillo et al. (1996). The extending towards the lumen. At the periphery of the ®nal model for growth in length was arranged to also estimate follicles, rounded spermatocytes proliferated. Sperm- growth in weight, on the basis of von Bertalan€y's length±weight equation calculated by a non-linear regression of all data (Ricker atocytes were ovate (<1 lm diameter) and strongly 1975; Sparre and Venema 1995). stained with haematoxylin. Some mature spermatozoa 523

Fig. 1 Isostichopus fuscus. Photomicrographs of gonadal stages of the males at Isla EspõÂritu Santo (July 1992 to September 1993). a Undetermined, b spermatogenesis, c maturity, d spawning, e post- spawning (c connective tissue; f follicles; g gonad wall; ph phagocytes; sp spermatocytes; s mature spermatozoa). Scale bars 100 lm were found in the lumen. The connective tissue was Maturity (Fig. 1c) thinner and the follicles increased their size because of accumulation of sperm. Spermatogenesis was seen from All the follicles were completely ®lled with dense layers February to June (Fig. 3a). of mature spermatozoa, which had rounded heads 524 (about 1 lm diameter). The gonad wall was thin and Spawning (Fig. 2c) distended, and at the periphery, a thin layer of sperm- atocytes was present. In this stage, some spherule cells There was a noticeable decrease in the abundance of were observed. Male gonads appeared in July to August oocytes inside the tubules. Almost all were ripe, though (Fig. 3a). This stage showed the highest GI values 8 to a few developing oocytes were still present near the go- 12% (Fig. 4). nad wall. Large, empty spaces were observed in the lu- men because of the absence of gametes. A few phagocytes were observed. Spawning occurred during Spawning (Fig. 1d) summer (July to September). The GI values decreased by one-half in this stage (Fig. 4). Spawned gonads showed empty spaces inside the folli- cles because spermatozoa had already been released. Some developing spermatocytes were still observed at the periphery. On the gonad wall, the presence of a layer Post-spawning (Fig. 2d) of connective tissue was seen. Spawning occurred during summer, and the GI values decreased by almost one-half The few oocytes that were observed in this stage had in this stage (Figs. 3a, 4). decreased in volume. The presence of many phagocytes inside and outside the tubules was detected, and their activity was related to a signi®cant decrease in the size of Post-spawning (Fig. 1e) the gonads. The phagocytes had a granular appearance. Large amounts of connective tissue were seen in the The post-spawning gonads were reabsorbed by phago- gonad walls. Post-spawning female gonads were ob- cytes. In the gonad wall of the follicles, abundant con- served in October and November, with very low GI nective tissue was observed. Some follicles still presented values (Figs. 3b, 4). mature spermatozoa. Numerous groups of phagocytes were observed inside and outside the follicles. Post- spawning gonads were observed in November, with low GI values (Figs. 3a, 4). Reproductive cycle The reproductive cycle of Isostichopus fuscus showed a Developmental stages of the female clear annual pattern for both sexes. Spawning occurred from July to September in 1992 and in 1993. Post- Oogenesis (Fig. 2a) spawning gonads were found in October of both years. Undetermined gonads were found from October to The oogonia were embedded in the germinal epithelium, January, but because their frequency of occurrence was and this made them dicult to identify. The oogonial low, we did not include this stage in the graph (Fig. 3a, cells began to proliferate towards the lumen. Developing b). Gametogenesis was observed from January to June oocytes were arranged in a single layer. Numerous pre- 1993, and females started gametogenesis a month earlier vitellogenic oocytes (20 lm average diameter) were than males (Fig. 3a, b). observed in this stage, each having a large nucleus, with The female and male GI evolution had a signi®cant two or three peripheric nucleoli, and being surrounded relation with sea surface temperature variations and by small follicular cells. The presence of spherule cells with the gonadal stages. There was no signi®cant was seen during this stage. Gametogenesis was observed di€erence between GI values of males and females from January to June (Fig. 3b). The GI values for this (ANOVA: F2,142 = 2.036, P > 0.05). The highest GI stage were low, 2 to 4% (Fig. 4). values coincided with mature gonads which were found during summer, the warmest months of the year. The GI values for this stage were <12%. During spawning, the Maturity (Fig. 2b) GI values diminished when sea surface temperature was up to 27 °C (Fig. 4). The lowest GI values corresponded Mature oocytes reached their maximum size (104 lm to post-spawning, undetermined and early gametogenic diameter) and occupied the entire lumen of all tubules. gonads, which were found during the winter months The oocyte membranes were separated from the cyto- (October to January). plasm because of tissue contraction caused by the ®xa- Monthly di€erences in the GI values were detected tion process. At the periphery, there were some (ANOVA: F12,171 = 53.01, P < 0.05). A Tukey test developing oocytes. The nucleus and nucleoli are well recorded three groups; the ®rst included the colder de®ned in the cells. In this stage, it was common to ob- months, from October 1992 to January 1993, which serve groups of phagocytes forming spherule cells inside showed GI values <1% (undetermined and post- the tubules. Male gonads appeared from June to August spawning stages). The second group had the highest GI and in females from July to August (Fig. 3b). The GI values, corresponding to July and August of both years, values for this stage were high, 8 to 12% (Fig. 4). when gonads were ripe. The third group was represented 525

Fig. 2 Isostichopus fuscus. Photomicrographs of gonadal stages of 23.25 ‹ 0.26 cm and 385.97 ‹ 7.81 g, with modes of females at Isla EspõÂritu Santo (July 1992 to September 1993). a 24 cm and 350 g (Fig. 6; Table 1). Because ®rst matu- Oogenesis, b maturity, c spawning, d post-spawning (c connective tissue; do developing oocytes; f follicles; fc follicular cells; g gonad rity was attained at 367 g, size-frequencies indicated wall; n nucleus; o ripe oocytes; ph phagocytes; po previtellogenic that most of the sampled specimens were actively in oocytes). Scale bars 100 lm reproduction. The smallest individuals (<5 cm and <50 g) were observed from August to November 1996, and again from May to July 1997. Mean size of the by August and September 1992, when most specimens species di€ered signi®cantly among months (F11, 1434 = had spawned and had post-spawning gonads; in these 8.85, P < 0.001 for length; F11,1434 = 8.87, P < 0.001 months, GI values were 1% to 5% (Fig. 4). for weight); individuals were especially heavier and The weight at ®rst maturity (when 50% of the indi- longer in January, February and April, 1997 (Table 1). viduals in the population showed developing gonads) The length±weight regression was signi®cant was calculated considering only specimens that could be 2 (r = 0.714, F1,1144 = 3607.5, P < 0.001), and showed sexed (n = 142) and that were in gametogenic, mature that I. fuscus grows allometrically at the studied site or spawning stage. The smallest reproductive specimen (Fig. 7). weighed 167 g, but the calculated ®rst-maturity weight The estimated von Bertalan€y growth equations for was 367 g (Fig. 5). length and weight were:

‰0:180 t0:024†Š Lt ˆ 36:118‰1 e †Š; Growth ‰0:180 t0:024†Š 1:832 Wt ˆ 815:485‰1 e †Š ;

The population of Isostichopus fuscus at Isla Espõ ritu where Lt is length in time t (years), Wt is weight in time Santo had an average (‹SE) length and weight of t (years), 36.118 = Linf (asymptotic length in cm; 526

Fig. 5 Isostichopus fuscus. Weight at ®rst sexual maturity (July 1992 to September 1993)

Fig. 3 Isostichopus fuscus. Monthly frequencies of gonadal stages of I. fuscus at Isla EspõÂritu Santo (July 1992 to September 1993). a Males, b females

Fig. 4 Isostichopus fuscus. Mean monthly gonad index (July 1992 to September 1993) and mean sea surface-water temperature at the study Fig. 6 Isostichopus fuscus. Frequency histogram of sizes of I. fuscus at site Isla EspõÂritu Santo (August 1996 to July 1997). a Length, b weight 527

Table 1 Isostichopus fuscus. Length (L, in cm) and weight (W, in g) modal values included individuals 5 to 6 years old, but 7- data of the population from Isla Espõ ritu Santo, Me xico year-old were also very abundant in the area Month n Mean Mode SE Min. Max. (Fig. 9). An age of 5 years also signals the time for ®rst maturity in Isostichopus fuscus. Aug 1996 W 97 362.1 480 11.4 15 525 The estimated natural mortality of the population was L 97 23.3 23 0.4 7 33 0.51 ‹ 0.03. Survival percentage abruptly decreased Sep W 105 383.3 410 12.5 45 660 L 105 24.3 26 0.5 9 35 during the ®rst year (about 40% of original recruits die Oct W 113 348.7 410 11.6 20 650 within that time), and during the following 2 years L 113 23.1 22 0.4 5 33 (Fig. 10). By age ®ve, <10% of the cohort remains. Nov W 103 366.9 320 13.4 20 790 L 103 21.9 24 0.4 5 30 Dec W 99 389.9 340 11.7 105 700 L 99 23.9 26 0.4 16 33 Discussion Jan 1997 W 107 444.9 310 13.7 65 800 L 107 24.6 24 0.5 12 40 Reproduction Feb W 131 470.2 420 13.0 70 810 L 131 25.9 26 0.4 11 36 Mar W 152 391.0 320 10.6 120 690 The holothurian Isostichopus fuscus is a dioecious spe- L 152 23.4 24 0.4 11 34 cies. Specimens exhibit no sexual dimorphism, except Apr W 108 411.3 380 14.9 70 760 when the gonad is ripe. Female gonads are pale orange, L 108 23.3 28 0.4 11 34 whilst male gonads are whitish. The population sex ratio May W 134 381.1 350 15.3 45 830 was approximately 1:1, as is the case for most aspido- L 134 22.5 26 0.4 9 33 Jun W 164 340.1 330 14.9 20 810 chirotes (Cameron and Fankboner 1986; Conand 1993a; L 164 21.4 25 0.5 7 35 Foster and Hodgson 1995). The gonochoric condition is Jul 1997 W 133 353.9 290 13.1 45 760 a common feature of holothurians, although complete L 133 22.1 22 0.4 8 33 or casual hermaphroditism has been reported (Harriot Overall W 1446 385.97 350 3.99 15 830 L 1446 23.25 24 0.13 5 40 con®dence interval: ‹0.244), 815.485 = Winf (asymp- totic weight in g; con®dence interval: ‹5.509), 0.180 = K (individual annual growth rate; con®dence interval: ‹0.044), 0.024 = t0 (estimated age when growth is zero) and 1.832 = b (allometry coecient calculated with the length±weight relation; con®dence interval: ‹0.003). Graphic representations of the models (Fig. 8) showed that in this population, individuals with sizes of <6 cm or 40 g were younger than a year, whereas the largest specimens (>35 cm and 700 g) were very scarce, and were about 15 years old. The population mean and

Fig. 7 Isostichopus fuscus. Length±weight relationship of I. fuscus at Isla EspõÂritu Santo (August 1996 to July 1997). Equation: Weight = 1.142 (Length)1.832; con®dence intervals: a = Fig. 8 Isostichopus fuscus. Individual growth in a length and b weight 1.142 ‹ 1.100; b = 1.832 ‹ 0.003 of I. fuscus at Isla EspõÂritu Santo (August 1996 to July 1997) 528 months (October to January), a time when the popula- tion was characterized by the presence of individuals in post-spawning and undetermined gonadal stages (Fig. 3a, b). The presence of spherule cells in the early stages of development (gametogenesis) in females has also been noted in other holothurians; the phagocyted material is used to nurture other developing gametes (Hyman 1955; Boolotian 1966; Costelloe 1985, 1988; Smiley and Clo- ney 1985; Tyler and Billet 1987; Sewell and Bergquist 1990; Sewell 1992; Hammel et al. 1993). After spawning, the gonads of I. fuscus decreased in size because of phagocytosis, and by January the gonad was practically reabsorbed. Also during gametogenesis, the germinal layer of the gonads of I. fuscus became thinner, and longitudinal folds extended to the lumen. This process is common in the Class Holothuroidea and produces a Fig. 9 Isostichopus fuscus. Age structure of the population from Isla signi®cant increase in the surface area for development EspõÂritu Santo (August 1996 to July 1997) of gametes (Costelloe 1985; Tyler et al. 1985; Cameron and Fankboner 1986). 1982; Tyler et al. 1985; Tyler and Billet 1987; Herrero It was common to observe the presence of gametes in Pe rezrul et al. 1998). both female and male gonads during the post-spawning The histological analysis of the gonad of Isostichopus stage. This may show that partial events of shedding fuscus showed that its characteristics resembled those take place. Mosher (1982) showed that some ho- described previously for other aspidochirotes (Harriot lothurians are capable of spawning more than once 1982, 1985; Ong Che and Go mez 1985; Smiley 1988; during the reproductive period, as a way of maximizing Tuwo and Conand 1992; Fajardo Leo n et al. 1996). In reproductive success. This strategy might be very useful the undetermined stage, there was no evidence of for Isostichopus fuscus, because its oocytes are very small gametogenic activity (Fig. 1a). The gonad was so small (100 lm) and size is a factor that decreases the proba- that it became very dicult to see, a situation that has bility of fertilization (Levitan 1993). Repeated events of been previously reported in studies of other holothurians gamete expulsion, possibly triggered by proximity to (Hyman 1955; Bakus 1973; Conand 1981). Although the conspeci®cs, would help to avoid this problem. absence of gonads due to evisceration processes is The spawning of invertebrates is under the in¯uence mentioned in the literature (Bakus 1973), evidence of of endogenous and exogenous factors. Temperature such a situation was not found in our study; except for seems to be one of the most important variables that the gonads, all organs were present. At Isla Espõ ritu determines the timing of reproduction (Boolotian 1966; Santo, we found 83 specimens of I. fuscus without go- Giese and Pearse 1974). In the tropical eastern Paci®c, nads. Most of these individuals were found in the colder the reproductive seasonality of other coincides with high temperatures and upwellings (Strathmann 1985; Lessios 1990). Isostichopus fuscus showed a clear annual reproductive pattern at Isla Espõ ritu Santo, in which this holothurian spawned dur- ing summer. In this season, sea surface temperature was 27 to 30 °C. Although other aspidochirotes also repro- duce in months with high water temperatures or in summer (Table 2), this does not seem to pervade throughout the family, as reproduction can also occur during cold months (Conand 1993b), twice a year (Krishnaswamy and Krishnan 1967; Ong Che and Go mez 1985), or during the whole year (Hyman 1955). It is probable that temperature only synchronizes the timing of spawning in I. fuscus, as occurs in other eastern Paci®c holothurians (Cameron and Fankboner 1986).

Growth

Fig. 10 Isostichopus fuscus. Survival percentage of a model cohort Mean length and weight of the Isostichopus fuscus (August 1996 to July 1997) population from Isla EspõÂ ritu Santo (23.3 cm and 529

Table 2 Reproductive characters of holothurian species of the Family Stichopodidae (± no data)

Species Location Reproductive Temperature for GI (%) Sex ratio Oocyte Reference season reproduction diameter (lm)

Parastichopus Southern May±Jun ± ± ± ± Kastendiek and parvimensis California Muscat (1982) Stichopus Washington ± ± ± ± 200 Smiley and californicusa Cloney (1985) P. californicus 49°21¢N Jul±Aug 16±18 32 1:1 180 Cameron and Fankboner (1986) S. mollis 36°19¢S Nov±Jan ± ± ± 180 Sewell (1992) S. variegatus 20°S Dec±Apr 24±26 5 1:1 180 Conand (1993a) S. variegatus 20°S Dec±Apr 24±26 2.8 (males) 1:1 180 Conand (1993b) 2.7 (females) Neostichopus 33°58¢S Oct±Jan 22±23 6.9 1:1 350 Foster and grammatus Hodgson (1995) P. parvimensis 31°40¢N Apr±May ± 3.9 1:1 ± Pe rez Plascencia (1995) Isostichopus 24°35¢N Jul±Sep 28±31 11.2 1:1 104 Present study fuscus a Stichopus californicus is synonymous with Parastichopus californicus

385.9 g; Table 1) were lower than values reported for vored (Zann et al. 1987; Ebert and Russell 1993). the species in the central and northern Gulf of Cali- These models are based on three assumptions: that the fornia (27° to 29°N; 25.1 to 32.0 cm and 458 to 562 g: species grow isometrically, recruit annually and underlie Fajardo Leo n et al. 1995; Fajardo Leo n and Ve lez a size limit (Ricker 1975; Sparre and Venema 1995). In Barajas 1996), but higher than in Oaxaca, Me xico general, commercial holothurians reproduce and recruit (16°N; 351 g: Fajardo Leo n et al. 1995) and Gala pagos once every year, and seem to reach determinate size (0°N; 20 cm and 271 g: Sonnenholzner 1997), indicat- (Conand 1990; Lawrence 1987), but they show allo- ing a north±south size gradient for this holothurian. It metric growth (Shelley 1985; Conand 1988; Bulteel et al. is doubtful that this tendency is directly caused by such 1992). Populations of Isostichopus fuscus from the Gulf di€erences in environmental conditions as productivity of California are no exception to the general pattern, or mean temperature, since these oceanographic factors and because of this lack of strict adherence to the as- do not follow latitudinal trends in the cited locations of sumptions of the models, traditional ®shing-stock as- the eastern Paci®c (Fiedler 1992). The appearance of sessment methods can only be considered a heuristic large specimens in the north can be considered just alternative for the estimation of age and growth for this another example of a marine invertebrate which in- species, and for holothurians in general. Consequently, creases in size with latitude (Atkinson and Sibly 1997). the results of such studies (and the derived conclusions) Conand (1990) presented mean length and weight data have to be regarded with caution. for some of the most important commercial ho- Several studies on the growth of tropical commercial lothurians of the South Paci®c; values ranged from 22 holothurians have been published (Table 3). As ob- to >40 cm and 270 to >400 g. The size of I. fuscus is served, maximum length and growth rates of Isostich- noticeably smaller than that of most ``®rst rate'' taxa, opus fuscus are similar and even greater than those of however, the American species has been well received several important taxa, an indication of its adequacy as in Asiatic markets, in part because its price is relatively a commercial species. The speci®c values of the von low (Conand 1997). Bertalan€y parameters for each holothurian are deter- In recent decades, several approaches to estimate mined by the life history and local selective pressures of holothurian growth have been tried, e.g. tagging and each species and population, and therefore they are not enclosure of specimens (Conand 1990; Chao et al. 1994; easily comparable. However, considering that smaller Wiedemeyer 1994). Unfortunately, these techniques species like Holothuria scabra or Actynopyga echinites have some methodological constraints that confound are currently under cultivation (Conand 1990; Anony- their use. For example, animals usually expel tags, a mous 1997), it is feasible to suggest aquaculture as an process which can cause physical damage and tissue alternative for ®shermen interested in commercializing necrosis (Ebert 1978; Conand 1990). Keeping specimens I. fuscus. In this way, the strong di€erences in opinion in restricted spaces may a€ect growth-rate determina- between the government and the ®shermen of Me xico, tions, because food can be a limiting factor when indi- Ecuador and other American countries concerning the viduals grow, or food may be more scarce or abundant exploitation of this resource can be worked out. at the experimental sites than in the natural environ- In the Gulf of California and most of Me xico, ment. Because of these limitations, the use of von Isostichopus fuscus was under strong ®shing pressure Bertalan€y±like numerical models to study growth from 1989 to 1994, a situation that depleted populations, of holothurians and other echinoderms has been fa- a€ecting above all animals larger than 20 to 25 cm 530

Table 3 Comparison of published parameters of the von Bertalan€y growth model calculated for holothurians (ND no data)

Species Latitude Linf (cm) K (annual) M (annual) Reference Holothuria atra 11°N 32.4 0.11 1.02 Ebert (1978) Actynopyga echinites 20°S 23.1 0.78 ND Shelley (1985) A. echinites 20°S 23.0±29.5 0.09±0.30 0.64 Conand (1988) A. mauritania 20°S 34.0 0.12 1.45 Conand (1988) Stichopus japonicus 34°N 36.7 0.33 ND Hamano et al. (1989) Thelenota ananas 20°S 66.3 0.20 0.50±0.63 Conand (1990) S. chloronotus 20°S 34.2 0.45 1.79 Conand (1990) H. scabra 5°S 29.0 0.52 ND Pauly et al. (1993) H. pulla 5°S 30.7 0.24 ND Pauly et al. (1993) Opheodesma spectabilis 5°S 32.6 0.18 ND Pauly et al. (1993) Parastichopus parvimensis 31°N 52.5 0.30 ND Pe rez Plascencia (1995) Isostichopus fuscus 24°N 36.1 ‹ 0.2 0.18 ‹ 0.04 0.51 ‹ 0.03 Present study

(Fajardo Leo n and Ve lez Barajas 1996) which, accord- situation that may explain the lack of chemically active ing to the present model, were older than 4 years agents for defense in I. fuscus (Encarnacio n-Dimayuga (Fig. 9). In 1996 and 1997, the most abundant cohorts of and Keer-Garcõ a 1992) and its high survival probability. the species at Isla Espõ ritu Santo were 5 to 7 years old The life history characteristics of this are (Fig. 9), meaning they were recruited between 1989 and those of a K-strategist; I. fuscus has low mortality and 1993, years when the ®shery was active. It is probable growth rates, a late start of sexual maturity, large size that individuals were too small to be captured then and and great longevity (Conand 1988). The common ap- consequently they survived. This ®nding suggests that pearance of these traits in a species is only the conse- the current age and size structure of the local population quence of several active agents working together (Jensen of I. fuscus re¯ects the e€ects of human activities. 1997), needing no particular explanation for their com- Another important consideration related to age is mon occurrence. that individuals attain sexual maturity at age ®ve (Fig. 9). Taking into account that the number of adult Acknowledgements The Direccio n de Estudios de Posgrado e holothurians was much reduced in the southern gulf in Investigacio n del Instituto Polite cnico Nacional, and Comisio n Nacional para el Conocimiento y Uso de la Biodiversidad (Project the early 1990s because of ®shing mortality, it is possible FB315/H216/96) granted funds for this work . The Comisio n de that a sizeable portion of the local population is now Operacio n y Fomento de Actividades Acade micas fellowship was producing gametes for the ®rst time in the decade. If this awarded to F. Garcõ a-Domõ nguez, and the Programa Nacional conclusion is correct, an increase in local population size para la Formacio n de Investigadores (PIFI-IPN) and the Consejo Nacional de Ciencia y Tecnologõ a (Number 82643) scholarships to may become apparent at Isla Espõ ritu Santo and prob- M.D. Herrero-Pe rezrul. ably elsewhere in America in the coming years. In the southern gulf, a subtropical area, Isostichopus fuscus attains ®rst reproduction at small weights (367 g, Fig. 5). In the tropical western Paci®c, other commercial References aspidochirotes reach their ®rst sexual maturity at sizes Anonymous (1997) Successful production of juvenile sand®sh >500 g dry weight (Conand 1981, 1982, 1990) and Holothuria scabra by ICLARM in the Solomon Islands. Beà che- along the northern Paci®c coast of Baja California, de-mer Inf Bull 9: 3±4 Me xico (31° N), Parastichopus parvimensis reaches ma- Atkinson D, Sibly RM (1997) Why are organisms usually bigger in turity at 160 g (Pe rez Plascencia 1995). These data, al- colder environments? Making sense of a life history puzzle. though still minimal, point to an inverse gradient Trends Ecol Evolut 12: 235±239 Bakus JG (1973) The biology and ecology of tropical holothurians. between ®rst-maturity weight and latitude (and possibly In: Jones OA, Endean R (eds) Biology and geology of coral sea surface temperature), a tendency which provides an reefs. Vol. 2. Academic Press, New York, pp 325±367 interesting line of future investigation regarding man- Birkeland C (1989) The in¯uence of echinoderms on coral-reef agement of resources as important as holothurians. communities. In: Jangoux M, Lawrence JM (eds) studies. Vol. 3. Balkema, Rotterdam, pp 1±79 In marine species mortality rate is related to asymp- Boolootian RA (1966) Reproductive physiology. In: Boolootian totic length and to age at maturity, which, in turn, RA (ed) Physiology of Echinodermata. John Wiley and Sons represent a group of parameters dependent on size Interscience, New York, pp 561±614 (Jensen 1997; Sparre and Venema 1995). The estimated Bulteel P, Jangoux M, Coulon P (1992) Biometry, bathymetric distribution and reproductive cycle of the holothurid Holothuria natural mortality of Isostichopus fuscus at Isla Espõ ritu tubulosa (Echinodermata) from Mediterranean seagrass beds. Santo (M = 0.51, Fig. 10) is among the lowest rates Publ Staz zool Napoli (I: Mar Ecol) 13: 53±62 known for commercial taxa (Table 3), which indicates Cameron JL, Fankboner PV (1986) Reproductive biology of the that the species may be more resistant to natural factors sea cucumber Parastichopus californicus (Stimpson) (Echi- that cause death, like predation. There are just a few nodermata: Holothuroidea). I. Reproductive periodicity and spawning behavior. Can J Zool 64: 168±175 species known to feed on holothurians (Birkeland 1989; Camhi M (1995) Industrial ®sheries threaten ecological integrity of Wiedemeyer 1994), but none live in the eastern Paci®c, a the Gala pagos Islands. Conserv Biol 9: 715±724 531

Caso ME (1967) Morfologõ a interna y ecologõ a de Stichopus fu- Giese CA, Pearse JS (1974) Reproduction of marine invertebrates. scus Ludwig. An Inst Biol Univ Me x (Ser Cienc Mar) 37: 175± Vol. 1. Academic Press, New York 182 Hamano T, Amio M, Hayashi KI (1989) Population dynamics of Chao SM, Chien CP, Alexander PS (1994) Reproduction and Stichopus japonicus Selenka (Holothuroidea: Echinodermata) in growth of Holothuria atra (Echinodermata: Holothuroidea) at an intertidal zone and on the adjacent subtidal bottom with two contrasting sites in southern Taiwan. Mar Biol 119: 565± arti®cial reefs for Sargassum. Suisanzoshoku 37: 179±186 570 Hammel JF, Himmelman JH, Dufresne L (1993) Gametogenesis Conand C (1981) Sexual cycle of three commercially important and spawning of the sea cucumber Psolus fabricii (Duben and holothurian species (Echinodermata) from the lagoon of New Koren). Biol Bull mar biol Lab, Woods Hole 184: 125±143 Caledonia. Bull mar Sci 31: 523±543 Harriot VJ (1982) Sexual and asexual reproduction of Holothuria Conand C (1982) Reproductive cycle and biometric relations in a atra Jaeger at Heron Island Reef, Great Barrier Reef. Aust Mus population of Actinopyga echinites (Echinodermata: Ho- Syd Mem 16: 53±66 lothuroidea) from the lagoon of New Caledonia, western Harriot VJ (1985) Reproductive biology of three congeneric sea tropical Paci®c. In: Lawrence JM (ed) Proc. Int. Echinoderm cucumber species, Holothuria atra, H. impatiens and H. edulis, Conf. Tampa Bay. Vol. 1. Balkema, Rotterdam, pp 437±442 at Heron Reef, Great Barrier Reef. Aust J mar Freshwat Res Conand C (1988) Comparison between estimations of growth and 36: 51±57 mortality of two stichopodid holothurians: Thelenota ananas Herrero Pe rezrul MD, Reyes Bonilla H, Garcõ a Domõ nguez F and Stichopus chloronotus (Echinodermata: Holothuroidea). In: (1998) Casual hermaphroditism in gonochoric Isostichopus fu- Choat JH et al. (eds) Proc. 6th Int. Coral Reef Symp. Vol. 2. scus (Ludwig, 1875) (Echinodermata: Holothuroidea) in the Symposium Executive Committee, Townsville, pp 661±665 southern Gulf of California, Mexico. Bull mar Sci 63(3): 611± Conand C (1990) The ®sheries resources of Paci®c island countries. 615 Part 2. Holothurians. FAO Fish Tech Pap 272.2: 1±143 Hyman LH (1955) The invertebrates: Echinodermata, the coelo- Conand C (1993a) Ecology and the reproductive biology of mate bilateria. McGraw Hill, New York Stichopus variegatus, an Indo Paci®c coral reef sea cucumber Jensen AL (1997) Origin of the relationship between K and Linf and (Echinodermata: Holothuroidea). Bull mar Sci 52: 970±981 synthesis of relationships among life history parameters. Can J Conand C (1993b) Reproductive biology of the holothurians from Fish aquat Sciences 54: 987±990 the major communities of the New Caledonian Lagoon. Mar Kastendiek J, Muscat A (1982) Aspects of the biology of the sea Biol 116: 439±450 cucumber Parastichopus parvimensis: a developing commercial Conand C (1997) Are holothurian ®sheries for export sustainable? ®shery. Univ South Calif Sea Grant Inst Prog A Rep 1: 63±66 In: Lessios HA, MacIntyre IG (eds) Proc. 8th Int. Coral Reef Krishnaswamy S, Krishnan S (1967) A report on the reproductive Symp. Vol. 2. Smithsonian Tropical Research Institute, Balboa, cycle of the holothurian Holothuria scabra Jaeger. Curr Sci 6: Panama, pp 2021±2026 155±156 Costelloe J (1985) The annual reproductive cycle of the holothurian Lawrence JM (1987) A functional biology of echinoderms. Croom Aslia lefevrei (Dendrochirota: Echinodermata). Mar Biol 88: Helm, London 155±165 Lessios HA (1990) Adaptation and phylogeny as determinants of Costelloe J (1988) Reproductive cycle, development and recruit- egg size in echinoderms from the two sides of the Isthmus of ment of two geographically separated populations of the den- Panama. Am Nat 135: 1±73 drochirote holothurian Aslia lefevrei. Mar Biol 99: 535±545 Levitan RD (1993) The importance of sperm limitation to the Day RW, Quinn GP (1989) Comparisons of treatments after an evolution of egg size in marine invertebrates. Am Nat 141: 517± analysis of variance in ecology. Ecol Monogr 59: 433±463 536 Ebert TA (1978) Growth and size of the tropical sea cucumber Maluf LY (1988) Composition and distribution of the central Holothuria (Halodeima) atra Jaeger, at Eniwetok Atoll, Mar- eastern Paci®c echinoderms. Nat Hist Mus Los Angel Cty Tech shall Islands. Pacif Sci 32: 183±191 Rep 2: p 242 Ebert TA, Russell MP (1993) Growth and mortality of subtidal red Mosher C (1982) Spawning behavior of the aspidochirote ho- sea urchins (Strongylocentrotus franciscanus) at San Nicolas lothurian Holothuria mexicana Ludwig. In: Lawrence JM (ed) Island, California, USA: problems with models. Mar Biol 117: Proc. Int. Echinoderm Conf. Tampa Bay. Balkema, Rotterdam, 79±89 pp 467±468 Encarnacio n-Dimayuga R, Keer-Garcõ a S (1992) Compuestos con Norma O®cial Mexicana (1994) Determinacio n de las especies y actividad antimicrobiana de organismos marinos. Revta Soc subespecies de ¯ora y fauna silvestre terrestres y acua ticas en mex Cienc farmac 22: 33±41 peligro de extincio n, amenazadas, raras y las sujetas a pro- Engstrom AN (1980) Reproductive cycles of Halodeima ¯oridana teccio n especial, y que establece especi®caciones para su pro- Holothuria mexicana and their hybrids (Echinodermata: teccio n. NOM-059-ECOL-1994, Diario O®cial de la Holothuroidea) in southern Florida, USA. Int J Invert Reprod Federacio n, Me xico, pp 2±59 2: 237±244 Ong Che RG, Go mez ED (1985) Reproductive periodicity of Ho- Fajardo Leo n MC, Michel Guerrero E, Singh Cabanillas J, Ve lez lothuria scabra Jaeger at Catalan, Batangas, Philippines. Asian Barajas JA, Masso Rojas A (1995) Estructura poblacional y mar Biol 2: 21±30 ciclo reproductor del pepino de mar Isostichopus fuscus en Pauly D, Morgan GR (eds) (1987) Length-based methods in ®sh- Santa Rosalõ a, B.C.S., Me xico. Cienc Pesq 11: 45±53 eries research. ICLARM-Kuwait Institute for Scienti®c Re- Fajardo Leo n MC, Ve lez Barajas A (1996) Pesquerõ a del pepino de search, Sicily mar. In: Casas-Valdez MC, Ponce-Dõ az G (eds) Estudio del Pauly D, Sambilay V, Opitz S (1993) Estimates of relative food potencial pesquero y acuõ cola de Baja California Sur. Vol. 1. consumption by ®sh and invertebrate populations required for SEMARNAP/ CICIMAR, LaPaz, Me xico, pp 151±165 modeling the Bolinao reef ecosystem, Philippines. In: Chris- Fiedler PC (1992) Seasonal climatologies and variability of eastern tensen V, Pauly D (eds) Trophic models of aquatic ecosystems. tropical Paci®c surface waters. NOAA tech Rep NMFS 109: 1± ICLARM Conf. Proc. 26. ICLARM, Manila, pp 236±251 34 Pe rez Plascencia G (1995) Crecimiento y reproduccio n del pepino Foster GG, Hodgson AN (1995) Annual reproductive cycles of de mar Parastichopus parvimensis en la Bahõ a de Todos Santos, three sympatric species of intertidal holothurians (Echinoder- Baja California, Me xico. M.Sc. thesis, Universidad Auto noma mata) from the coast of the eastern Cape Province of South de Baja California, Me xico Africa. Invert Reprod Dev 27: 49±59 Powell JR, Gibbs JP (1995) A report from Gala pagos. Trends Ecol Gayanillo FC, Sparre P, Pauly D (1996) FAO-ICLARM stock Evolut 10(9): 351±354 assessment tools (FiSAT). FAO Computerized Information Reyes Bonilla H (1993) Biogeogra®a y ecologia de los corales Series (Fisheries), No. 8, FAO, Rome hermatipicos (Anthozoa: Scleractinia) del Paci®co de Me xico. 532

In: Salazar Vallejo SI, Gonza lez NE (eds) Biodiversidad marina Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W.H. Freeman and y costera de Me xico. Commisio n Nacional de la Biodiversidad Company, New York (CONABIO)/Centro de Investigaciones de Quintana Roo Sonnenholzner J (1997) A brief survey of the commercial sea cu- (CIQRO), Cheturnal, pp 207±222 cumber Isostichopus fuscus (Ludwig, 1875) in the Gala pagos Ricker WC (1975) Computation and interpretation of biological Islands. Beà che-de-mer Inf Bull 9: 11±15 statistics of ®sh populations. Bull Fish Res Bd Can 191: 1±382 Sparre P, Venema SC (1995) Introduccio n a la evaluacio n de re- Sewell MA (1992) Reproduction of the temperate aspidochirote cursos pesqueros tropicales. FAO Doc. Tec. Pesca 306/1. Stichopus mollis (Echinodermata: Holothuroidea) in New Zea- DANIDA-FAO, Rome land. Ophelia 2: 103±121 Strathmann RR (1985) Feeding and nonfeeding larval development Sewell MA, Bergquist PR (1990) Variability in the reproductive and life-history evolution in marine invertebrates. A Rev Ecol cycle of Stichopus mollis (Echinodermata: Holothuroidea). Syst 16: 339±361 Invert Reprod Dev 17: 1±7 Tuwo A, Conand C (1992) Reproductive biology of the ho- Shelley C (1985) Growth of Actynopyga echinites and Holothuria lothurian Holothuria forskali (Echinodermata). J mar biol Ass scabra (Holothuroidea: Echinodermata) and their ®shery po- UK 72: 745±758 tential (as Beà che-de-mer) in Papua, New Guinea. In: Gabrie C Tyler PA, Billet DSM (1987) The reproductive ecology of ela- et al. (eds) Proc. 5th Int. Coral Reef Congr. Vol. 5. Antenne sipodid holothurians from the North East Atlantic. Biol Museum ± EPHE, Moorea, French Polynesia, pp 297±302 Oceanogr 4: 273±296 Singh Cabanillas J, Ve lez Barajas A (1996) La pesquerõ a del pepino Tyler PA, Muirhead A, Gage JD, Billet DSM (1985) Reproductive de mar Isostichopus fuscus en la costa oriental de Baja Cali- biology of the deep-sea holothurians Laetmogone violacea and fornia Sur y propuestas de regulacio n. Cienc Pesq 12: 13±18 Benthogone rosea (Elasipoda: Holothuroidea). Mar Ecol Prog Smiley S (1988) The dynamics of oogenesis and the annual ovarian Ser 23: 269±277 cycle of Stichopus californicus (Echinodermata: Holothuroidea). Wiedemeyer WL (1994) Biology of small juveniles of the tropical Biol Bull mar biol Lab, Woods Hole 175: 79±93 holothurian Actynopyga echinites: growth, mortality and habi- Smiley S, Cloney RA (1985) Ovulation and a ®ne structure of the tat preferences. Mar Biol 120: 81±93 Stichopus californicus (Echinodermata: Holothuroidea) fecund Zann L, Brodie J, Berryman C, Nagasima M (1987) Recruitment, ovarian tubules. Biol Bull mar biol Lab, Woods Hole 169: 342± ecology, growth and behavior of juvenile Acanthaster planci (L.) 364 (Echinodermata: Asteroidea). Bull mar Sci 41: 561±575