Gametogenic and reproductive cycles of the sea anemone, <Emphasis Type="Italic">Entacmaea quadricolor</Emphasis>

Host sea anemones are ecologically important as they provide habitat for obligate symbiotic anemonefish in many areas of the Indo-Pacific. Despite their importance, no information is available on their gametogenic cycles. This study aimed to address this lack of knowledge by determining the gametogenic cycles of Entacmaea quadricolor. Gonad samples were taken from January 2003 to February 2005 at North Solitary Island, Solitary Islands Marine Park, Australia using a specially developed non-lethal field biopsy sampling technique. Sampling was done 17 times during the study period, with 15–20 individuals being sampled on each occasion. Samples were examined prior to fixation, and then histologically sectioned to determine the reproductive activity of each individual. Female anemones were significantly more abundant than males, and had asynchronous oocyte development both within and among individuals. Male anemones showed a single annual cycle of spermary growth, development and spawning. Data from the 26-month study indicated that spawning occurred in the austral summer and autumn between January and April, which coincided with the observed spawning periods that have previously been documented for this species in outdoor flow-through seawater tanks at the study location. The biopsy sampling technique used during this study provides an opportunity to gain a more thorough understanding of the gametogenic cycles and sexual pattern of host sea anemones throughout their distribution.     

The gametogenic cycle of<Emphasis Type="Italic"> Octopus vulgaris</Emphasis> (Mollusca: Cephalopoda) as observed on the Atlantic coast of Andalusia (south of Spain)

The present study reports the gametogenic cycle of the common octopus, Octopus vulgaris Cuvier, 1797 in the Atlantic coast of Andalusia between May 2001 and May 2002. A total of 673 specimens of total weight ranging from 30 to 3,732 g were analysed. The gonad development was defined by means of histological methods and gonadosomatic indexes. Four gametogenic stages were identified in males (I immature, II maturing, III mature, IV spawning) and in females (I immature, II maturing, III pre-spawning, IV spawning). The sex ratio obtained was not significantly different from 1:1 (P>0.01). Mature males were found during the whole year, September being the month when the highest rate of sexually active individuals occurred (48%). In females, the gametogenic cycle commenced in December and ended in November, and spawning occurred between April and October, with two maximum peaks in August and September (48% in each). Size at sexual maturity was 850 g of total body weight for males and 1,250 g of total body weight for females. Males mature earlier than females.Communicated by S.A. Poulet, Roscoff     

Seasonal reproduction of the brachiopod Frieleia halli and the scaphopod Cadulus californicus at bathyal depths in the deep sea

Two benthic species of invertebrates from the physically seasonless bathyal depths of the San Diego Trough off southern california USA showed highly synchronous reproductive cycles. Although the common pattern in the deep-sea benthos seems to be year-round reproduction, these two species are exceptions. The brachiopod Frieleia halli Dall spawned between January and April (1971) and the scaphopod mollusc Cadulus californicus Pilsbry and Sharp in late summer between July and October. Furthermore, F. halli. has maintained a predictable annual gametogenic cycle for three years (1970–1972). Several factors are suggested as possibly important in synchronizing their reproductive cycles, but no single environmental cue can be conclusively demonstrated as a definite influence.     

The reproductive cycle of the sea urchin Arbacia lixula in northwest Mediterranean: potential influence of temperature and photoperiod

We studied the reproductive cycle of the sea urchin Arbacia lixula in a subtidal population from northeast Spain over four years using a gonadosomatic index (GSI) and gonad histology. Our results show that the GSI of A. lixula follows a seasonal cycle which peaks in May–July and attains its lowest values in October–November every year. The time course of the GSI matched closely the photoperiod cycle. We also found a remarkable inter-annual variability in the maximum value of GSI, which correlated with mean water temperature during the gonad growth period (winter and spring). Gonad histology was also in agreement with a single gametogenic cycle per year in this species. We explored the application of circular statistics to present and analyse gonadal development data, which allowed us to adequately handle the high intra-individual variability detected, with several developmental stages commonly found within the same gonad. The picture that emerged is one of a gametogenic timing driven by photoperiod, while the amount of reproductive output is determined by temperature. This is coherent with the tropical origin of the species and lends support to recent warnings about an increase in the abundance of this species in the Mediterranean as a result of global warming, with associated increased impact potential in sublittoral communities.     

Reproductive biology and biochemical composition of the brooding echinoid <Emphasis Type="Italic">Amphipneustes lorioli</Emphasis> on the Antarctic continental shelf

The bathyal West Antarctic Peninsula (WAP) shelf experiences intense seasonal variability in primary production, with summer phytoplankton blooms yielding intense pulse of phytodetritus to shelf sediments. Echinoderms form a conspicuous proportion of the deposit-feeding megabenthos on the shelf and of these Amphipneustes lorioli was the most abundant irregular echinoid. To explore the reproductive response of A. lorioli to this seasonal production cycle, A. Lorioli was sampled at one location on the WAP shelf during four separate cruises between March 2000 and March 2001. Reproductive patterns were determined by histological analyses of gonad tissue, and elemental (CHN) analyses were used to estimate the nutritional and energetic status of the body tissues. Histological analysis of the brooding echinoid A. lorioli suggested a quasi-continuous gametogenic pattern in both the ovaries and the testes. Biochemical analysis of the gonads and the gut tissues were consistent with a continuous gametogenic cycle, showing no significant changes in the biochemical composition of the tissues among seasons. Size-frequency distributions of the embryo and juvenile echinoids within the adults’ brood pouches revealed a synchronous recruitment of embryos and juveniles in specific cohorts between different adult specimens. Whilst this occurrence of different cohorts of the developing brood may be an adaptation to limited brood space, there may also be an external factor influencing the synchrony between adult individuals. Nonetheless, a continuous gametogenic cycle and the lack of seasonal variation in the biochemical composition of gonad and gut tissues suggest that this deposit-feeding irregular urchin is exploiting a persistent sediment food bank in WAP shelf sediments throughout much of the year.     

Reproductive cycle of the endemic cassiduloid<Emphasis Type="Italic"> Cassidulus mitis</Emphasis> (Echinoidea: Cassiduloida) on the Brazilian coast

Cassidulus mitis Krau, 1954 is an endemic species from Rio de Janeiro, Brazil. To study the reproductive cycle of this species, samples were collected at Praia Vermelha, in Guanabara Bay, from October 1998 to April 2000. The sex ratio for C. mitis was 1:1, and reproduction occurred throughout the year. The gonadal index of males was greater than that of females. Five gametogenic stages were identified in males: early growth, premature, mature, partially spawned and early growth with a partially spawned stage. There were no spent or recovery stages such as those seen in females. Females had six gametogenic stages: recovery, early growth, premature, mature, partially spawned and spent stage; there was no early growth with a partially spawned stage as there was in males. The mean oocyte diameter was 382 m (SD=49 m), and the mean number of juveniles per female was 100 individuals (SD=108). The anterior gonads were frequently smaller than the posterior ones, and there were differences in the gametogenic stages between the anterior and posterior gonads. First sexual maturation occurred in individuals with a diameter of 17 mm. The intestinal wet weight was two- to threefold higher than the test wet weight. This may indicate that C. mitis uses its intestine as a weight belt to avoid displacement from the substratum.Communicated by P.W. Sammarco, Chauvin     

Reproductive energetics,endocrinology and population dynamics of Nephtys caeca and N. hombergi

An investigation of gametogenetic cycles and spawning success in populations of Nephtys caeca and N. hombergi from the River Tyne estuary, North Shields, England, in relation to production of gonadotrophic (GH) and spawning hormones (SH) has been made, based on data collected from 1978–1984. The data show that a consistent pattern of gametogenesis and efficient spawning occurs in populations of N. caeca in north-east England, but that the reproductive cycle of N. hombergi is erratic. Premature oosorption and gametogenic failure in this latter species is associated with a low level of GH production. Following high levels of GH production, gravid females sometimes fail to spawn owing to the non-release of SH. The reproductive energetics and reproductive success of N. caeca and N. hombergi are described in relation to the observed patterns of endocrine activity and the consequent changes in population structure.     

Reproduction and annual gametogenic cycle in Nephtys hombergii and N. caeca (Polychaeta: Nephtyidae)

The gametogenic cycles of Nephtys hombergii Audouin et M. Edw. and N. caeca Fabricius are described. Both species are polytelic (=discrete, iteroparous) and breed in their second and subsequent years. They spawn in May in the Tyne estuary. After spawning, N. hombergii retains a large number of gametocytes, which are ultimately resorbed. A new generation of gametocytes is proliferated by September and mature gametes accumulate during the winter months. Gametic development is not well synchronised.     

Annual reproductive cycle of the green sea urchin, Strongylocentrotus droebachiensis, in differing habitats in Nova Scotia, Canada

We monitored the reproductive cycle of Strongylocentrotus droebachiensis (OF Müller) between April 1993 and August 1995 in kelp beds, barren grounds and grazing fronts at both a wave-exposed and a sheltered site along the Atlantic coast of Nova Scotia. Gonad index and histological analyses showed that S. droebachiensis has an annual reproductive cycle that is synchronous across sites and habitats, and between females and males. Spawning occurs in March/April of each year but a small proportion of sea urchins in the study populations also spawned in fall 1995. During most of the year, sea urchins in kelp beds and grazing fronts have a higher gonad index than those in barren grounds. Gonad indices also tended to be higher at the wave-exposed than the sheltered site. Interannual variability in peak gonad index was significant in the barren grounds at the wave-exposed site and in the grazing front at the sheltered site. The gametogenic cycle is characterized by six stages based on the abundance of nutritive and germinal/gametic cells. Nutritive phagocytes are abundant after spawning and replaced by increasing numbers of germinal and gametic cells as the gametogenic cycle progresses. The temporal patterns of abundance of each cell type were similar among habitats indicating that the gonads were qualitatively similar despite large differences in gonadal mass. The quantity of gut contents (ratio of food volume to body volume) was similar among habitats, but the quality (percentage of organic material) tended to be higher in kelp beds and grazing fronts than in barren grounds suggesting that differences in gonad index of S. droebachiensis in different habitats are related to differences in diet. The high density of sea urchins in grazing fronts combined with their high fecundity suggests that they make the greatest contribution, per unit area, to the overall larval pool. Received: 20 May 1997 / Accepted: 21 January 1998     

Reproduction,recruitment and fragmentation in nine sympatric species of the coral genus Acropora

Multispecies assemblages of the coral genus Acropora occur commonly throughout the Indo-Pacific Ocean. Nine species from such an assemblage comprising 41 species of Acropora, at Big Broadhurst Reef on the Great Barrier Reef, were studied during 1981–1983. Similarities and differences in reproductive modes and timing, oocyte dimensions and fecundity, recruitment by larvae and by fragments, and mortality were recorded. All species had an annual gametogenic cycle, were simultaneous hermaphrodites, and had the same arrangement of gonads in polyps. In six species, most colonies released gametes on the same night of the year, in early summer, during a mass spawning event involving many coral genera. A seventh species had colonies spawning at this as well as other times of the year. Another species spawned in late summer, and gametes were not observed to mature in the last species. Eggs were very large (601 to 728 m geometric mean diameter) and fecundity of polyps low, compared with other corals; no reduction in oocyte numbers occurred during oogenesis. Reef-flat species had slightly bigger and fewer eggs than reef-slope species. All species recruited by larvae, but four also multiplied by fragmentation, either year-round or during occasional rough weather. Yearround fragmenters had few larval recruits; non-fragmenters had many, and a rough-weather fragmenter had an intermediate number of larval recruits. It was concluded that larval recruitment largely determined species composition, and that reduced larval recruitment was responsible for sparse distribution of fragmenting species. Subsequent mortality in some species and increase by fragmentation in others probably determined relative abundances.     

Reproductive periodicity of the scleractinian coral Lophelia pertusa from the Trondheim Fjord, Norway

Between 2002 and 2008, samples of the cold-water scleractinian coral Lophelia pertusa were collected from the Trondheim Fjord in Norway to examine reproductive periodicity. Collections were made from three locations: Tautra, (63°35.36′N, 10°31.23′E at 40–70 m), Stokkbergneset (63°28.18′N, 09°54.73′E at 110–500 m), and Røberg (63°28.88′N, 09°59.50′E at 250 m). Populations of L. pertusa from the Trondheim Fjord initiated oogenesis in January and spawning occurred from late January to early March the following year. Gametogenic cycles of the female L. pertusa samples overlapped by approximately 2 months, with oogonia visible in January, but this was not evident in the males. This paper provides the most complete gametogenic cycle to date and spawning observations for this important structure-forming species. The results from fjord populations are compared with published and preliminary data from other regions and are discussed in the context of regional differences in physical and biological variables, particularly food supply. Differences in gametogenic cycles within a single species provide a rare opportunity (especially in deep-sea species) to examine potential drivers of reproduction.     

Influence of temperature and food availability on the ecological energetics of the giant scallop Placopecten magellanicus

Scallops (Placopecten magellanicus) were collected in 1981–1983 from two water depths at a location in Newfoundland, Canada, where temperature and food conditions associated with shallower water have been shown to be more favourable for somatic growth and gamete production. To gain insight into the seasonal energy balance for this species, metabolic and clearance rates were measured monthly under ambient temperature conditions and natural seston levels. Stereological techniques were used to determine the gamete volume fraction in the gonad in order to establish the annual reporductive cycle. The less favourable conditions associated with deeper water were relfected in reduced rates of gamete development, but the diameter of spawned eggs and the timing of spawning appeared unaffected by poorer conditions in the natural environment. Estimates of scope for growth were low or negative during the winter, but consistently high during the spring bloom, corresponding to a period of rapid gamete maturation. Somatic weight declined in both populations as gamete development proceeded but increased again during periods of low gametogenic activity, suggesting a close relationship between energy available for growth and the reproductive cycle. Oxygen uptake and clearance rate varied seasonally in relation to ambient temperature and food conditions, all of which appeared to be interrelated in a complex fashion with the energy demands of gametogenesis.     

Genetic and nutritional control of the gametogenic cycle in Mytilus edulis

Individuals of Mytilus edulis were collected from two populations in easterm Long Island Sound, USA, at 6 wk intervals from January 1982 to February 1983, and the hypothesis that nutrient availability controls the timing of gametogenic events in this mussel was tested using genetic variants at the Lap locus. In eastern Long Island Sound, Lap genotypes differ in the net rate of nitrogen accumulation. A highly significant difference in reproductive cycle among genotypes occurred in a population of M. edulis where Lap genotypes differ in nitrogen budget. Genotypes with lower rates of nutrient accumulation delayed the reproductive cycle by approximately six weeks relative to genotypes with high rates of nutrient accumulation. No significant difference in reproductive cycle occurred at a locality where Lap genotypes do not differ in nitrogen budget. These data indicate that nutritional status can exert significant control over the timing of gametogenesis in M. edulis. Differences in reproductive cycle among Lap genotypes provide a mechanism of non-random mating among genotypes which may result in heterozygote deficiencies at this locus.     

Very slow development in two Antarctic bivalve molluscs,the infaunal clam <Emphasis Type="Italic">Laternula elliptica</Emphasis> and the scallop <Emphasis Type="Italic">Adamussium colbecki</Emphasis>

Embryos of the large infaunal clam Laternula elliptica and the scallop Adamussium colbecki, from Antarctica, were cultured over an 18-month period. Their development rates were extremely slow, taking 240 and 177 h, respectively, to reach the trochophore stage. This is ×4 to ×18 slower than related clams and scallops from temperate latitudes. The relationship between temperature and development rate for bivalve molluscs shows the expected slowing with reduced temperature (Q ₁₀ in the range 2–4) for temperate and tropical species. However, the slowing at polar latitudes is much stronger than at warmer waters, and all of the limited data for Antarctic species are well above the Arrhenius plot for the overall bivalve data, and the Q ₁₀ value for Antarctic to cool temperate species is 11.8, well outside the expected range for biological systems. Either the relationships describing the effects of temperature on the kinetics of biological systems do not apply to Antarctic bivalve molluscs, or some other factor that cannot be compensated for becomes important at low temperature. In the laboratory, L. elliptica embryos stayed viable in very sticky egg capsules for up to 18 months without hatching. However, even the disturbance of removing eggs using a pipette ruptured some egg capsules allowing embryo release. Gametogenesis in Antarctic marine invertebrates is almost universally slowed compared to temperate species, with nearly all cases documented requiring more than 1 year to complete oogenesis. The only exception so far appears to be A. colbecki, which has a 1-year gametogenic cycle. The data here indicate that it has been unable to adapt embryonic development in a similar way, and we are not aware of any exceptions to the markedly slowed development at low temperature rule.     

Reproduction in five species of crinoids at Lizard Island,Great Barrier Reef

Reproduction in five species of crinoids [Himerometra bartschi (A. H. Clark), H. robustipinna (P. H. Carpenter), Cenometra bella (Hartlaub), Colobometra perspinosa (P. H. Carpenter), and Oligometra serripinna (P. H. Carpenter)] was studied at Lizard Island, Queensland, over 24 mo, from April 1981 to March 1983 (except for O. serripinna —June 1981 to March 1983). All five species of crinoids were dioecious, although a few instances of synchronous hermaphroditism were noted in H. bartschi, C. perspinosa, and O. serripinna. Gonad morphology and the sequence of developmental stages were similar in each species. Within individuals, gametogenesis was synchronous in gonads both along and between arms, except in some proximal and distal genital pinnules in which gonads never matured. Within a species, there was a degree of synchrony of gametogenesis in a sample, but the level of gametogenic activity varied considerably between years. A high level of continuous reproductive activity was observed in H. bartschi, H. robustipinna, Cenometra bella, and Colobometra perspinosa from about mid-summer to early/mid-winter, while O. serripinna probably had a bimodal reproductive cycle with peaks around February and June. There was a significant 1:1 male:female sex ratio in the populations sampled, and unsexable individuals were significantly smaller (as determined by maximum arm length) than either sexable males or females.     

Reproduction and development of the blue coralHeliopora coerulea (Alcyonaria: Coenothecalia)

Up to the present time, the reproductive cycle and larval development ofHeliopora coerulea, living fossil and sole member of the alcyonarian order Coenothecalia, have been undescribed. Populations ofH. coerulea studied on the Great Barrier Reef between 1984 and 1989 were found to have separate sexes and an annual gametogenic cycle. Mature eggs were large (>800µm diam), and their development was initiated internally. There appeared to be a lunar or semi-lunar periodicity in reproductive behaviour, with brooding of larvae commencing around either full or new moon. Development proceeded via superficial cleavage and a solid stereoblastula. Subsequent development took place on the surface of the colony, within a temporary brood-space created by protracted distension of the polyps. Larvae lacked zooxanthellae and were brooded for between 6 and 14 d prior to leaving the colony. Reproduction and development reflected the taxonomic affinities ofH. coerulea, but brooding and embryological development also appeared to be constrained by its morphology. Reproductive and larval characteristics ofH. coerulea may offer a partial explanation of the current biogeographic range ofH. coerulea.     

Population differences in gonad and pyloric caeca cycles of the New Zealand seastarSclerasterias mollis (Echinodermata: Asteroidea)

Inshore and offshore populations ofSclerasterias mollis (Hutton, 1872) were sampled on the outer continental shelf off the Otago Peninsula, New Zealand, and their nutritional and reproductive cycles are described from 1985–1986. Histological changes in the gonads are generally typical of other asteroids. The gametogenic cycle takes 12 mo. The gonad and pyloric caeca indices in both females and males had an inverse relationship.S. mollis accumulates nutrients in the pyloric caeca during summer and early autumn. The gonads develop in the autumn and winter. Offshore seastars were much larger and had significantly higher gonad and pyloric caeca indices than inshore individuals. These differences in body sizes and organ indices arise from differences in food availability and/or population density.     

Population structure and reproductive biology of two sympatric hydrothermal vent polychaetes,Paralvinella pandorae and P. palmiformis

The alvinellid polychaetes Paralvinella pandorae Desbruyères and Laubier and P. palmiformis Desbruyères and Laubier occur at deep-sea hydrothermal vents along the Juan de Fuca and Explorer Ridges in the northeast Pacific Ocean. The population structure and reproductive biology of both species were studied in samples taken from three vent sites during six cruises in 1983 and 1984. Size-frequency analyses of two P. pandorae populations produced unimodal histograms, suggesting continuous or semi-continuous juvenile recruitment; in a third population two possible size classes were evident. Histograms of P. palmiformis displayed size-class peaks, which most likely reflected periodic recruitment of juveniles. Both species are gonochoric and gametes develop free in the coelom. Due to the simultaneous presence of a full range of gametogenic stages in P. pandorae populations, including spermatozoa in males, and to the continuous or semi-continuous recruitment pattern suggested by the size-frequency histograms, continuous reproduction is proposed for this species. In P. palmiformis a discrete, possibly synchronized, breeding cycle is thought to occur. Although maximum fecundity of P. pandorae is very low, continual reproduction over a long period of time could enhance its reproductive potential. The estimate of maximum fecundity for P. palmiformis is comparable to estimates for other polychaetes that undergo non-planktotrophic larval development. Maximum observed oocyte size was 215 and 260 m in P. pandorae and P. palmiformis, respectively. It is proposed that P. pandorae broods its young, while P. palmiformis probably undergoes demersal lecithotrophic larval development. The continual production of brooded young by P. pandorae could maintain a vent population, but severely limit dispersal to other vents. Demersal lecithotrophic larvae of P. palmiformis could repopulate vents, and potentially be carried by bottom currents to other vent sites.     

Reproductive periodicity in the euryalinid snake star Astrobrachion constrictum in a New Zealand fiord

The euryalinid snake star Astrobrachion constrictum (Farquhar), a normally deep-water species, exists within SCUBA diving range in New Zealand flords, and thus presents a unique opportunity for study. A population of A. constrictum in Doubtful Sound was investigated from February 1990 to July 1994 to determine the reproductive cycle. Unlike most ophiuroids, the gonads of A. constrictum are positioned along the aboral coelom in the proximal portion of the arms. The proximal 2 to 3 cm of the arms of individuals were thus removed on an approximately monthly basis for histological examination of the gonads. Image analysis was used to determine oocyte size-frequency distributions. A gonad index was calculated for each individual based on the ratio of cross-sectional area of the gonads to cross-sectional area of the arm. Maturity indices were calculated based on stage of development of the gonads of each individual. A. constrictum has a period of enhanced breeding activity in April–June, after which both the gonad and maturity indices decline. The increase in gametogenic activity during these months was correlated with rising sea temperature within the fiord. Although the females showed an annual pattern of gonad development, oogenesis was continuous throughout the year, with oocytes at different stages of development present in the gonads. Males also showed continuous spermatogenesis and, although the same annual pattern of gonad development was evident as seen in the females, it was less marked. The presence of females with large oocytes and ripe males throughout the study indicates that breeding in the Doubtful Sound population is prolonged, and possibly continuous, as found in many deep-sea ophiuroids.     

Sexual reproduction in solitary corals: Synchronous gametogenesis and broadcast spawning in Paracyathus stearnsii

Samples of the temperate solitary coral Paracyathus stearnsii Verrill, 1869 were collected monthly or bimonthly from January 1977 to September 1978 off the California coast. This species is gonochoric and reproduces only sexually. Females produce a large number of small eggs (ca. 10⁵ per polyp) in gametogenic synchrony and both sexes spawn between February and May. A small planktonic planula (ca. 160 m long) develops following external fertilization. Broadcast spawning with planktonic development may be more common than previously assumed in scleractinians, and includes both lecithotrophic and planktotrophic larvae.