Reproductive cycles of tropical sea cucumbers (Echinodermata: Holothuroidea) in southern Taiwan

Reproductive cycles of Afrocucumis africana (Dendrochirotida), Actinopyga echinites, Holothuria leucospilota, H. cinerascens, H. difficilis (Aspidochirotida), Synaptamaculata, Opheodesoma grisea, Patinapta taiwaniensis and Polycheira rufescens (Apodida), representing three orders of intertidal holothurians in southern Taiwan, were determined by gonad index and histological examination from March 1990 through September 1991. All nine species of holothurians have annual spawning periods lasting 2 to 4 mo in spring or summer. The early spawning of H. cinerascens and P. rufescens (suspension feeders) suggests that their feeding mode is related to food resources and may influence the reproductive period. In the direct-developing dendrochirotid (suspension feeder), gonad development occurs in cool months, and gametes are released at the beginning of warm months. In indirect-developing aspidochirotid and apodid (deposit feeder), gamete release occurs in late spring or summer and appears to be correlated with summer phytoplankton growth. The holothurians in the present study display spawning periodicity and duration similar to those of temperate species. Four species of holothurians lengthened spawning season with decreased latitude.     

Reproductive cycle of two commercial species of sea cucumber (Echinodermata: Holothuroidea) from Caribbean Panama

The reproductive status of the holothuroid species Isostichopus badionotus (Selenka, 1867) and Holothuria mexicana (Ludwig, 1875) was studied over 16 months in Bocas del Toro (Panama), from November 1999 to February 2001. Sexual reproduction was evaluated by the gonad index method, and by histology of gonad development. In addition, population structure was assessed based on sex ratio, minimum reproductive size, and length and weight distributions of males and females. The sex ratio in both species was 1:1, with a unimodal population distribution composed mainly of mature individuals. The minimum reproductive length and weight were 13-20 cm and 150 g, respectively, for both species, although reproductive individuals 10 cm in length were also found. A consistently higher gonad index was observed in H. mexicana, due to a high proportion of mature females and males and high gonad indices in most monthly samples. Gametogenesis and spawning patterns seemed to occur throughout the year, with periods of enhanced activity. Two periods of maximum reproductive activity were tentatively identified: July-November for I. badionotus and February-July for H. mexicana, but neither species had a single, sharply defined annual spawning event. Further work on these exploited holothuroids should examine the relationships between reproduction and environmental factors and between reproductive status and recruitment.     

Reproduction of the commercial sea cucumber Holothuria scabra (Echinodermata: Holothuroidea) in the Solomon Islands

Over a 3-year period (1996-1998), reproduction of the commercial sea cucumber Holothuria scabra (Jaeger, 1833) was investigated in the Solomon Islands to determine the spawning pattern and whether gametogenesis is continuous or seasonal. The gonad consisted of a single cohort of tubules that developed uniformly. Macroscopic examination of the gonads revealed that mature gametes were present throughout the year. Individuals with gonads at different stages of maturity were present in most samples. Partly spawned gonads were prevalent in females, whereas mature gonads were prevalent in males. The time at which the peak gonad index was recorded differed among years. Although gametogenesis was continuous, with a potential for prolonged gamete release, a period of enhanced spawning occurred during the dry season, from September to December. Maximum gonad indices were reached prior to and during this period of enhanced spawning. Histology revealed that gametogenesis reinitiated in partly spawned gonads, resulting in the presence of gametes at different stages of development in the gonad. The uniform growth of gonad tubules indicated that H. scabra does not conform to the progressive tubule recruitment model described for holothurian oogenesis. Continuous reproduction in H. scabra and prolonged availability of mature gametes would facilitate use of this species for aquaculture.     

L-Lactate dehydrogenase in the longitudinal muscle of the sea cucumber Sclerodactyla briareus (Echinodermata: Holothuroidea)

The infaunal holothurian Sclerodactyla briareus (Thyone briareus) is able to tolerate exposure to hypoxic conditions for over 2 days. Since the in vitro anaerobic degradation of glucose-U-C¹⁴ by longitudinal muscle preparations leads to an accumulation of labeled lactic acid, it is apparent that lactate dehydrogenase plays a key role during anoxia. Disc electrophoresis resolved one major band of lactate dehydrogenase (LDH) activity in longitudinal muscle extracts. Muscle extracts of s. briareus oxidized L-lactate only, as is the case with most other echinoderms. The apparent Michaelis constants for lactate oxidation and pyruvate reduction are dissimilar from values reported for other marine invertebrates. The LDH activity in this holothurian is higher than the activities reported for other marine invertebrates with the exception of some active, large arthropods. Substrate inhibition of LDH maximal activity occurs at substrate concentrations (pyruvate) exceeding 10 mM, and then to only a minor extent. The characteristics of lactate dehydrogenase from the longitudinal muscle of S. briareus support the hypothesis that it functions to maintain glycolytic flux during prolonged periods of exposure to anoxic or hypoxic conditions.     

Development and metamorphosis of two psolid sea cucumbers,Psolus chitonoides andPsolidium bullatum,with a review of reproductive patterns in the family Psolidae (Holothuroidea: Echinodermata)

Reproduction and development of two psolid sea cucumbers in waters of the San Juan Archipelago, Washington, were studied from April 1981 through August 1984. Spawning inPsolus chitonoides Clark andPsolidium bullatum Ohshima in the laboratory and in the field waters of the San Juan Archipelago, Washington, occurred from February through may, with heaviest spawning in April and May. The egg ofPsolus chitonoides was bright red in color and 627µm in diameter;Psolidium bullatum released eggs that were golden yellow in color and 330µm in diameter. Maximum measured fecundities (spawned eggs) forPsolus chitonoides andPsolidium bullatum were 34 700 and 3 074, respectively. Developmental schedules were similar in both species. Early cleavages were equal, radial, and holoblastic; slightly subequal cleavage was common inPsolus chitonoides. The gastrula elongated to form a uniformly ciliated larva and the vestibule first appeared as a ventral crescent-shaped depression, after which the larva decreased in length and formed three posterior ridges that encircled the early doliolaria. Just prior to settlement, there was loss of cilia between the three ridges and on the posterior end of the early doliolaria, leaving three ciliary rings that are characteristic of the dendrochirote doliolaria larva. Vertical swimming ensued, and five primary tentacles protruded through the vestibule, with occasional attachment to the substratum using the primary tentacles. Upon settlement, two primary podia emerged and all external ciliation was lost except among tentacular papillae and on the end of tube feet. Timing of appearance and of loss of ciliary rings suggest that the rings function in vertical swimming and substratum selection behaviors. Metamorphosis involved the following simultaneous events: (1) resorption of the preoral lobe, (2) formation of large, dorsal, calcareous ossicles, (3) flattening of the trivium, and (4) proliferation of ventral tube feet on Ambulacral Radii B and E to form the sole. Reproduction in the family Psolidae is reviewed. The large proportion of brooders in this family appears to be related to small size, the possession of protective armor and sole, and geographic distribution (mainly in Antarctica). Lecithotrophic doliolaria larvae with three ciliary rings are produced by large northern psolids.     

Structural and functional peculiarities of the digestive system of Cucumaria frondosa (Echinodermata: Holothuroidea)

The fine structure of the intestinal epithelium of Cucumaria frondosa has been examined. The digestive cells possessed some specific ultrastructural peculiarities which testify to their participation in the transport of substances and in the processes of intracellular and cavitary digestion. The main units of the intestinal epithelium appear to be multifunctional digestive cells in which the phenomenon of compartmentalization among the organelles' groups, intended to carry out various functions, occurs. The heterogeneity of the structure of populations of the digestive cells is explained. Both primitive and progressive features of the structure of the digestive tract of C. frondosa are indicated.     

Reproduction of the intraovarian brooding apodid Leptosynapta clarki (Echinodermata: Holothuroidea) in British Columbia

Reproduction in the viviparous apodid sea cucumber Leptosynapta clarki was examined in Grappler Inlet, Bamfield, Vancouver Island, Canada from July 1989 through July 1991. The reproductive cycle of L. clarki is annual with gonad growth during the summer months. Male sea cucumbers spawn during November and December and internally fertilize, through as yet undetermined means, the oocytes within the ovary. Embryonic development is rapid, so that within 2 wk fertilized eggs reach the pentactula stage. Pentactulae have an open mouth and anus and actively move in the ovarian tubules feeding on droplets and fluid derived from the resorption of unfertilized eggs. Histological examination of gametogenesis shows similar development to that found in non-brooding holothurians. However, the protandric sex change observed in some male L. clarki after spawning and changes to the overian wall structure prior to fertilization are previously undescribed in sea cucumbers.     

Fission and its effect on population structure of Holothuria atra (Echinodermata: Holothuroidea) in Taiwan

Populations of Holothuria atra Jaeger occurring at Wanlitung and Nanwan were sampled monthly at spring tide from March 1990 to February 1992 in southern Taiwan. At Wanlitung, small individuals with evidence of fission and regeneration were abundant in shallow tidepools on the wide reef flats (density: 98±40 ( ± SD) 100 m^-2, body weight: 6 to 182 g). At Nanwan, large individuals with no evidence of fission were sparse in deep tidepools and narrow flats [density: 0.24±0.07 ( ± SD) 100 m^{- 2}, body weight: 351 to 1400 g]. At Wanlitung, fission occurred throughout the year with an average monthly fission frequency of 4.5%, peaking at 18% in September 1990 and 16% in August 1991. Fission was accomplished by revolving, twisting, and stretching of the body, resulting in two unequal fragments. The minimal weight of 3007 individuals measured during 1 yr at Wanlitung was 6 g. All ten individuals weighing 6 to 9 g ( ± SD = 6.7 ± 1.1) 100 m^{- 2} showed evidence of regeneration from fission products. Nine large individuals (>500 g) transferred from Nanwan to Wanlitung and 50 small individuals (<100 g) transferred from Wanlitung to Nanwan in February 1991 showed no evidence of fission during the following year. Fission occurs in small individuals living in shallow tidepools, suggesting that fission probably is triggered by a stressful environment resulting from solar radiation at the unusually low water level of spring tide. Fission of H. atra at Wanlitung results in a population consisting of small individuals.     

Investigations on brood protection inPsolus dubiosus (Echinodermata: Holothuroidea) from Antarctica in spring and autumn

Brood protection in the holothurianPsolus dubiosus Ludwig and Heding, 1935 was investigated in the Antarctic zone of permanent packice, an environment with an extreme seasonality in planktonic activity. Yearly reproductive cycles on the continental shelf of this area have been poorly investigated. Brooded juveniles of this species were found for the first time between the retracted tentacles of adult females at two different localities in the southeastern Weddell Sea, sampled in spring (October 1986) and autumn (February 1984). Mean lengths of the juveniles of each brooding female showed significant differences within each sample. However, there was no detectable difference in size of the juveniles between the two seasons. The results are discussed as an uncoupling of the dynamics of the early life history of these benthic invertebrates in space and time from processes in the euphotic layer of the Southern Ocean. The species investigated follows the general trend of some Antarctic invertebrates towards a non-pelagic development.     

Reproduction and growth of Holothuria atra (Echinodermata: Holothuroidea) at two contrasting sites in southern Taiwan

Reproductive periods and growth of two populations of Holothuria atra Jaeger distinctly different in body size at two sites of southern Taiwan were determined. Individuals examined in the present study were collected between march 1990 and February 1992. At Nanwan (21° 57N, 120° 45E), large individuals (351 to 1400 g wet wt) spawned from June to September. At Wanlitung (22°N, 120° 42E), a small proportion of frequently dividing individuals (<190 g wet wt) have mature gonads in May, June and September, but histological examination revealed no sign of spawning. Sexual recruits, defined as small individuals <5 g wet wt without sign of regeneration, were not found at either site during this 2-yr study. After the peak of fission at Wanlitung, 40% of the population showed signs of external regeneration. At Nanwan, small individuals transferred from Wanlitung grew from 6 g (n=6) to 166±8 g within 8 mo, and from 48±4 g (n=50) to 324±16 g within 1 yr, with a 6.8-fold biomass increase in 1 yr. At Wanlitung, the monthly average body weight of H. atra is between 33 and 62 g, apparently due to frequent fission, and the biomass increased only 2.9-fold in 1 yr. In southern Taiwan, sexual reproduction of H. atra occurs in large individuals. Asexual reproduction, occurring in small individuals, is the chief mechanism for population maintenance and increase, but it may decrease sexual reproductive potential.     

Reproductive cycle of the sea urchin Holopneustes purpurascens (Temnopleuridae: Echinodermata)

This study documents the annual reproductive cycle of the Temnopleurid echinoid Holopneustes purpurascens near Sydney. H. purpurascens reached sexual maturity between 11 and 26 mm diameter and was gonochoristic. The sequence of oogenesis was similar to previously described echinoids. However, the proportion of eggs at each stage showed no temporal pattern in abundance, suggesting that vitellogenesis is continuous throughout the year. Spermatogenesis was also similar to other echinoids and showed a significant increase in the proportion of partially spawned testes in spring, followed by a similar increase in the proportion of partially spawned testes in late spring and summer. Gonad indices showed a peak in weight from late winter to mid-spring (9.10ǃ.47 for females; 6.28ǂ.43 for males; mean-SE), then a decline for both sexes. Although spawning was variable over time, there was a peak in the proportion of spawning from late winter to early summer that correlated with the observed peaks in gonad indices and gametogenic cycles. The demographic implications of this reproductive pattern are that new recruits can enter the population through synchronous spawning during the breeding period, and smaller haphazard spawning events at other times of the year.     

Bacterial diversity of the sediments transiting through the gut of Holothuria scabra (Holothuroidea; Echinodermata)

This work analyzes bacterial diversity of sediments transiting through the gut of Holothuria scabra which is an important bioturbator in tropical shallow waters. This edible holothurian species has a social and economic importance for coastal populations in many developing countries. Bacterial biodiversity was analyzed by sequencing the 16S rRNA of bacterial cultures and clones. DAPI and FISH methods were used to determine and compare the number of bacteria found in the various gut compartments. A total of 116 phylotypes belonging to the γ-Proteobacteria (60.5 %), α-Proteobacteria (24.5 %), Bacteroidetes (6 %), Actinobacteria (2.75 %), Fusobacteria (1.75 %), Firmicutes (1.75 %), Cyanobacteria (1.75 %) and δ-Proteobacteria (1 %) were identified. The number of bacteria is significantly greater (1.5×) in the foregut than in the ambient sediments. The number of bacteria significantly decreases in the midgut and remains stable until defecation. Some γ-Proteobacteria, especially Vibrio, are less affected by digestion than other bacterial taxa. The season has an impact on the bacterial diversity found in the sediments transiting through the gut: in the dry season, γ-Proteobacteria are the most abundant taxon, while α-Proteobacteria dominate in the rainy season. Vibrio is the most frequent genus with some well-known opportunistic pathogens like V. harveyi, V. alginolyticus and V. proteolyticus. Findings show that sediment-associated microbial communities are significantly modified by H. scabra during their transit through the gut which supports the view that holothurians play a substantial role in the structuring of bacterial communities at the sediment–seawater interface.     

Functional effects of the hadal sea cucumber <Emphasis Type=Italic>Elpidia atakama</Emphasis> (Echinodermata: Holothuroidea,Elasipodida) reflect small-scale patterns of resource availability

Holothuroidea represent the dominant benthic megafauna in hadal trenches (~6,000–11,000 m), but little is known about their behaviour and functional role at such depths. Using a time-lapse camera at 8,074 m in the Peru–Chile Trench (SE Pacific Ocean), we provide the first in situ observations of locomotory activity for the elasipodid holothurian Elpidia atakama Belyaev in Shirshov Inst Oceanol 92:326–367, (1971). Time-lapse sequences reveal ‘run and mill’ behaviour whereby bouts of feeding activity are interspersed by periods of locomotion. Over the total observation period (20 h 25 min), we observed a mean (±SD) locomotion speed of 7.0 ± 5.7 BL h⁻¹, but this increased to 10.9 ± 7.2 BL h⁻¹ during active relocation and reduced to 4.8 ± 2.9 BL h⁻¹ during feeding. These observations show E. atakama translocates and processes sediment at rates comparable to shallower species despite extreme hydrostatic pressure and remoteness from surface-derived food.     

Genetic variance in Ophiomusium lymani (Ophiuroidea: Echinodermata) from lower bathyal depths in the Rocklall Trough (northeast Atlantic)

Specimens of the deep-sea brittle-star Ophiomusium lymani were collected from six sites in the Rockall Trough (northeast Atlantic_. Four monomorphic and four polymorphic loci were detected, with up to 75 individuals screened at any one locus. The results showed little difference in allele frequencies between sites and, consequently, estimates of genetic identity indicated no significant genetic differentiation between the populations sampled. Deficits of heterozygotes were observed at all polymorphic loci, but the deficiencies were only significant at the phosphoglucose isomerase locus from two locations. The deficit of heterozygotes was not the same across loci, suggesting that inbreeding is not the cause of the excess homozygosity. No relationship between heterozygosity and depth was observed.     

On the distribution and variability of the Indo-Pacific sea star Asterina wega (Echinodermata: Asteroidea) in the Mediterranean sea

The distribution of the Mediterranean populations of Asterina wega Perrier is described. Four populations were found to differ in size of animals and regeneration rate. The possible migratory pattern is duscussed.     

Chemical defense in the eggs and embryos of antarctic sea stars (Echinodermata)

Fifteen species of reproductively mature echinoderms (11 sea stars, 3 sea urchins, 1 sea cucumber) were collected from McMurdo Sound, Antarctica, during austral spring and summer of 1985 and 1986; eggs and embryos were obtained, and were tested for ichthyonoxicity using the common marine killifishFundulus grandis as a model predator. Chemical deterrents occurred in the large, yolky eggs of the pelagic lecithotrophic sea starPerknaster fuscus and the planktotrophic sea starPorania antarctica. Brooded embryos of the sea starsDiplasterias brucei andNotasterias armata were also noxious. Significant ichthyonoxicity was not detected in the remaining 7 species of sea stars, 3 sea urchins, and 1 sea cucumber. Chemical deterrents were generally effective at concentrations below a single egg or embryo per agar test-pellet. Although chemicals found in these eggs and embryos are noxious to an allopatric fish, they may not be noxious to sympatric fish.     

Reproduction of the commercial sea cucumber Holothuria whitmaei [Holothuroidea: Aspidochirotida] in the Indian and Pacific Ocean regions of Australia

Seasonal trends in the gonad index (GI) of two widely separated populations of black teatfish, Holothuria whitmaei (formerly included in Holothuria nobilis), were investigated between Pacific (Great Barrier Reef) and Indian Ocean (Ningaloo Reef) coral reefs of Australia. Reproductive activity followed a similar annual trend, with the GI of both populations peaking typically between April and June. Macroscopic and histological analysis of Ningaloo Reef specimens revealed that large germinal tubules, positioned centrally on the gonad basis, progressed through four maturity stages: growing (II); mature (III); partly spawned (IV); and spent (V). Growing tubules dominated the central region of the gonad basis between January and March, followed by an increase in the number of mature tubules throughout the GI peak (April–June). The progressive appearance of partly spawned and spent tubules between June and October suggests that spawning in H. whitmaei continues intermittently over an extended period throughout the austral winter. The examination of the gonad structure of sexually mature male and female specimens identified five tubule size classes in total (C₁ to C₅), each of differing physical and gametogenic status. In females, smaller C₁ tubules located at the anterior edge of the gonad basis contained pre- to early vitellogenic oocytes. Larger C₂ and C₃ tubule cohorts, positioned centrally on the gonad basis, contained mid- to late-stage vitellogenic oocytes. Smaller C₄ and C₅ tubules, located at the posterior edge, contained only relict oocytes. Similar physical and gametogenic differences were apparent between tubule cohorts in male specimens. We propose that these results, together with evidence of incomplete gonad resorption over the austral summer, indicate that gonad development in H. whitmaei conforms to the predictions of the Tubule Recruitment Model (TRM). The TRM is reported rarely among tropical aspidochirotes, and results presented here (1) provide the first direct evidence of this model in H. whitmaei, and (2) confirm that this species is one of the few winter-spawning tropical invertebrates.     

Costs of extended brood protection in the Antarctic sea star, Neosmilaster georgianus (Echinodermata: Asteroidea)

Changes in size, morphology, and biochemical composition in adults and embryos of a brooding sea star, Neosmilaster georgianus (Sladen), were studied in a population adjacent to Anvers Island, Antarctic Peninsula (64°46′S; 64°04′W) during the austral spring, 1991. Five morphological stages of development were designated in 24 broods, and for each the weight and biochemical composition of the brooding adults and their embryos were determined. Between Stage 1 and 2, the dry weight (dw) and organic weight (ow) of the embryo did not change. From Stage 2 to 3, the dw and ow increased significantly by 10%. Stage 2 and 3 embryos were in clusters of a few (2 to 10) to as many as 40 individuals. In the smaller clusters, individual embryos were attached by tissue cords to another, sometimes atrophied, brood member. In the larger clusters, they were attached to a central mass of tissue containing remnants of embryos. We interpret these interactions as a form of cannibalism which may account for the weight gains between Stage 2 and 3. During Stages 4 and 5, as juvenile form was approached, the dw and ash weight of the young increased significantly and the ow decreased significantly. The calculated energy content for the juvenile (Stage 5) was not significantly different from the energy content of the earliest undifferentiated stage (Stage 1), an indication that most of the organic matter in the egg is the primary contribution to the large juvenile. In brooding females, pyloric caeca indices declined by 52% from Stage 1 to Stage 5 and pyloric energy stores declined by 63% due to proportionately equivalent declines in protein and lipid. The ovary index was low and increased only slightly during brood protection, while the size of the largest oocytes remained approximately 23% that of ova. Energy stores in the pyloric caeca of brooding N. georgianus thus become depleted over a long period of incubation during which the adults apparently starve. This may delay oocyte development and ultimately limit the frequency of individual reproduction. Received: 15 September 1998 / Accepted: 9 March 1999