Reproductive cycle of the chiton Chiton iatricus and environmental control of its gonad growth

The annual reproductive cycle of the chiton Chiton iatricus was studied for the period from September, 1977 to December, 1978. Gametogenesis is initiated in the November – December period followed by rapid gonadal growth up to March. Breeding season of C. iatricus extends up to the beginning of August. Though the emission of the gametes halts in August, the gonad never enters into the quiescent phase owing to the time required for the gametogensis. The examination of correlation between the reproductive events during the annual reproductive cycle and existing environmental factors suggests that multiple environmental factors are involved in the control of different phases of gonad growth. The collected data are discussed in the light of the reproductive physiology of C. iatricus.     

Influence of habitat on the reproductive biology of the deep-sea hydrothermal vent limpet <Emphasis Type="Italic">Lepetodrilus fucensis</Emphasis> (Vetigastropoda: Mollusca) from the Northeast Pacific

Habitat selection by the hydrothermal vent limpet, Lepetodrilus fucensis, in Northeast Pacific hydrothermal vent ecosystems, may influence its reproductive output, as it occupies habitats with varying physico-chemical conditions that reflect the availability of nutritional resources. Histological techniques were used to determine size at first reproduction, gametogenesis, reproductive output, and fecundity in relation to shell length (SL), through examination of the gonads of male and female L. fucensis, collected from five different hydrothermal vent habitat types with different temperature anomalies and hydrothermal fluid flow vigour: vigorous (VIG), diffuse (DIF), tubeworm bushes (TWB), peripheral (PER), and senescent areas (SEN). Both male and female L. fucensis exhibited early maturity, with the first reproductive event occurring at 3.8 and 3.9 mm shell length, respectively. All stages of gamete development were present in the gonads of males and females, suggesting continuous gametogenesis and asynchronous reproduction in this species. Gametogenic maturity of limpets did not vary among actively venting habitats (VIG, DIF, TWB, and PER), but was significantly lower in males and females from SEN habitats. Mean oocyte diameter was largest in females from VIG habitats, and smallest in females from SEN habitats, than in those from the other habitats (DIF, TWB, and PER). Females from actively venting habitats also had greater actual fecundity than those from senescent habitats. While the gametogenic pattern of L. fucensis appears phylogenetically constrained, selection of actively venting habitats by L. fucensis maximizes its reproductive output. The multiple feeding strategies of L. fucensis may allow for a constant supply of energy to be allocated to reproduction in any habitat except senescent vents. Early maturity, high fecundity, and continuous production of gametes suggest a reproductive strategy characteristic of an opportunistic species, and may be contributing to the extremely abundant populations of L. fucensis observed in the Northeast Pacific vent ecosystem.     

Sexual reproduction in Acropora (Isopora) (Coelenterata: Scleractinia)

In contrast to the seasonal gamete and planula production of Acropora (Isopora) palifera on Heron Island reef (Lat. 23° S), populations on Lizard Island reef (Lat. 14° S), sampled in 1979, 1981 and 1983, and Salamaua and Busama reefs (Lat. 7° S), sampled from 1980 to 1983, planulated year-round. Intensive sampling of colonies at Salamaua and Busama showed that gametes ripened at two-month intervals and that up to six cycles of gametes and larvae could be produced by an individual colony. Gametes of only a portion of the population — usually close to 50% — ripened each month. The Salamaua population, on average, produced fewer and smaller planulae than the Heron Island population during each two-monthly reproductive cycle. Hypotheses correlating the annual periodicity of breeding in marine animals with latitudinal variation of temperature were tested. In general, the time of breeding in A. palifera at Heron Island reef is much more restricted than theories based on latitudinal variations of water temperature would predict. It is hypothesized that, in the near subtropical environment of Heron Island reef, this species has evolved a life-history strategy that limits the amount of energy allocated to reproduction and allocates more energy to growth.     

Ovary structure and oogenesis in Cirratulus cirratus (Polychaeta: Cirratulidae)

Oogenesis in polychaetes has, in most species, two main phases: a coelomic phase during which vitellogenesis occurs, and an ovarian phase. Details of the latter are known in very few species. Efficient reproduction requires coordination between these two phases of oocyte differentiation. The ovaries of Cirratulus cirratus (O. F. Müller) occur 2/segment throughout the fertile region of the body; 5 main stages of oocyte differentiation can be recognised on them: stem cells, oogonia, premeiotic oocytes, early oocytes and terminal oocytes. A quantitative study of the composition of the ovary throughout the reproductive cycle shows that the ovary size is approximately constant, but that the percentage of cells in the terminal oocyte stage is reduced to zero prior to spawning. This stage in oocyte differentiation is therefore a critical one, at which oogenesis may be arrested. The ovary alternates between a proliferative phase when the terminal oocytes are present, and a non-proliferative phase when they are absent. The overall rate of germ cell production for each ovary is low, less than 1 cell/ovary/day, and the, ovary tissue turnover time is greater than 2 years. A qualitative model describing the production of oocytes is presented, and the implications of the low rate of germ cell production are discussed. A low rate of germ cell proliferation, as in Cirratulus cirratus, implies that the rate of oocyte output into the coelom will be controlled by factors influencing the later stages of ovarian oocyte differentiation.     

Analysis of blood chemistry and flow cytometry of gonadal cell cycle during reproductive cycle of Anabas testudineus

The population of climbing perch, Anabas testudineus, an important food fish in India, is presently under threat and has been declared endangered. A narrow range of environmental conditions for successful reproduction of the species was previously ascertained in breeding experiments. In this study, the role of physiological parameters including plasma glucose, total protein, cholesterol, and glycogen content in liver and ovary were determined with respect to the reproductive cycling stages. Flow cytometric analysis of cell cycle of ovary and testis in relation to reproductive cycle was also analyzed. In both the sexes, plasma glucose and plasma protein changed significantly during breeding cycle. Plasma cholesterol levels were reduced markedly during spawning. Liver and ovarian glycogen levels showed significant variation during reproductive cycling. Flow cytometric study revealed that the hypoploid and synthesis phase were altered significantly with breeding cycle in ovarian and testicular cells. Data indicate that the biochemical parameters indicative of the fish reproduction capacity are influenced by environmental conditions. Thus, climatic changes may therefore potentially induce biochemical alterations that may exert detrimental effects on fish reproduction and subsequent population decline.     

Reproduction and condition of female Octopus mimus (Mollusca: Cephalopoda)

The relationship between reproduction and condition was studied in a 15 mo sample of 919 maturing, mature and post-spawning female Octopus mimus (388 to 3714 g) caught in Iquique (North Chile). O. mimus is a semelparous species, with reproduction taking place all year round. Investment in reproductive tissues was, on average, 9.9% of mature female body weight, independent of season. However, somatic growth during maturation was dependent on season and varied between 26 and 63% of the whole-body growth in weight. The condition of females did not vary markedly until spawning, although seasonal variations were apparent, winter being the most unfavourable. Condition deteriorated dramatically after spawning, during parental care of the eggs. During this period, somatic-tissue depletion, mainly from the muscles, was >25% of the total body weight of mature females. The fecundity of O. mimus was probably limited by the costs associated with parental care of the eggs.     

Observations on the biochemical changes in gonads and other organs of Uca annulipes,Portunus pelagicus and Metapenaeus affinis (Decapoda: Crustacea) during the reproductive cycle

The fluctuations in biochemical constituents such as water, nitrogen, non-protein nitrogen, protein, lipid and glycogen in gonad, muscle and hepatopancreas have been followed in 3 decapod crustaceans, Uca annulipes (Latreille), Portunus pelagicus (Linnaeus) and Metapenaeus affinis (Milne-Edwards). The water and ash content of the entire body show no systematic fluctuation in relation to the annual reproductive cycle. The water content of the ovary diminishes as it matures. In the ovary of these crustaceans, the lipid fluctuated greatly in relation to the reproductive cycle. The maturing ovary contains more lipid than an immature or spent ovary per unit tissue weight. The changes in the biochemical constituents in the testis are not so pronounced as in the ovary, since the testicular cycle is often drawn-out and almost continuous in these crustaceans. There is an inverse relationship between water content and lipid content of the hepatopancreas; the greater the fat content, the lesser the water content. The hepatopancreas in these crustaceans is apparently a storage organ and contains much lipid and glycogen. At the height of the breeding season, when gonad production is intense, there is an indication of the mobilisation of at least a part of the lipid from hepatopancreas to gonad.Dissertation for the award of a Doctorate Degree of the Kerala University.Formerly the Marine Biological Laboratory.     

Sperm motility and longevity in the giant cuttlefish, Sepia apama (Mollusca: Cephalopoda)

The sperm kinetics and fertilisation literature in marine invertebrates is heavily biased toward free-spawning species. Nonetheless, many species (e.g. cephalopods) transfer and/or fertilise gametes in confined external spaces or internally, creating very different selective pressures on sperm storage, sperm longevity and hence sperm competition. Here we report the results of an investigation into the effects of sperm age, water temperature and sperm concentration on sperm motility in the giant cuttlefish (Sepia apama). Significant positive correlations were found between percent motility and sperm concentration, and between sperm motile speed and sperm concentration. Mean percent motility of cuttlefish sperm suspension was still 9% eight hours after being released from the spermatophore and diluted into filtered seawater at 12°C (ambient field temperature during the spawning season). Sperm resuspended from spermatangia taken from (mated) females in the field were motile for up to 100 hours. When spermatophores were stored at 4°C motility was still observed in resuspended sperm after two months. Our results show that spermatangia and spermatophores can retain and release live sperm for long periods. The observed longevity of sperm in S. apama greatly increases the potential for sperm competition in this species.     

Egg production in the arrow squid Nototodarus gouldi (Cephalopoda: Ommastrephidae), fast and furious or slow and steady?

The process of reproductive maturation and egg release was examined in the temperate shelf squid Nototodarus gouldi. The energy allocation between somatic and reproductive growth from juvenile to mature adult was investigated throughout the life span to determine the underlying energetic strategy adopted by individuals. The relative weight of the mantle, fin and digestive gland remained unchanged during ovarian development, with no significant correlations found between the mantle length (ML)-gonad residuals and the ML-mantle (r=0.01, P>0.05), ML-fin (r=0.07, P>0.05) and ML-digestive gland (r=0.07, P>0.05) residuals. This suggested that energy was not being diverted away from somatic growth during sexual development, and consequently neither muscle nor digestive gland was being utilised as an energy store. Since squid in all maturity stages contained some food in their stomachs (e.g. 66.7% of mature animals), it is likely that the cost of maturation in this species is largely being met by food intake. The energy investment in reproductive tissues was relatively low (mean gonado-somatic index for mature individuals was 9.29% - 0.40%), indicating that only small amounts of energy were being allocated to reproduction at anyone point in time, which is characteristic of a multiple-spawning strategy. Furthermore, oviduct weight was not correlated with body size (r=0.256, P>0.05), suggesting that eggs are not stored for a single release. In all except one individual, ovary weight was consistently heavier than oviduct weight, suggesting that the ovary is not being depleted of oocytes as mature ova move into the oviducts. Additionally, the ovaries of mature females contained a range of oocyte sizes with discrete peaks, indicating a continued production and development of oocyte cohorts. The presence of some individuals with stretched empty oviducts is further evidence that the reproductive strategy of N. gouldi is slow and steady, with eggs possibly being released in discrete batches over a period of time.     

Substrate catabolism related to reproduction in the bay scallop Argopecten irradians concentricus,as determined by O/N and RQ physiological indexes

Weight specific rates of oxygen consumption carbon dioxide production, and ammonia-N excretion, measured for a Florida population of the bay scallop Argopecten irradians concentricus between May and September, 1982 and October and November, 1983 were significantly correlated (P<0.0005) to environmental factors that co-varied seasonally with metabolic shifts related to reproduction. Mean O/N and CO₂/O₂ (RQ) molar ratios indicates that scallop energy metabolism varied over the course of the reproductive cycle. Resting stage individuals (May-early June) had RQ values close to 0.7, indicative of a predominantly lipid-based metabolism. During the initial stages of gametogenesis (late June-early July) scallops catabolized primarily carbohydrate, as evidenced by maximum O/N (>22) values and RQ values close to 1.0 RQ values >1.0 indicated a possible carbohydrate to lipid conversion during the period of cytoplasmic growth (late July-early September). As gametes matured and spawning commenced (late September-November), metabolism became primarily protein based, as indicated by O/N and RQ values around 9.0 and 0.8, respectively. This pattern of substrate catabolism supports existing data on the storage and utilization of specific energy reserves with respect to reproduction in this species.     

Sexual reproduction of three coral species from the Mexican South Pacific

Our understanding of the reproductive biology of corals from the Mexican southeastern Pacific is limited, and consequently, the role of reproduction in structuring coral communities is unclear. As a first attempt to understand the importance of sexual reproduction in structuring and maintaining of the coral communities from this region, we documented the reproductive cycles over 2 years (2003–2004) in three main reef-building corals species in the region. Pocillopora damicornis was shown to be hermaphroditic with asynchronous gamete development observed only in 2004; P. gigantea was characterized as both gonochoric and cosexually hermaphroditic. Absence of mature gametes was documented in both species, and an observation may be attributed to the 2003 El Niño Southern Oscillation event, which may have inhibited reproductive maturation via thermal stress. Porites panamensis was gonochoric with asynchronous development, and planulae were generally brooded. The presence of mature gametes and planulae in P. panamensis polyps suggests that this species is an important contributor to local and, likely, regional recruitment of this species. Further research should seek to identify important source populations for these coral recruits and document the exchange of larvae between coral populations of the Mexican Pacific.     

Larval reproduction in the ctenophore Mnemiopsis mccradyi (order Lobata)

Dissogony was observed in normal and experimentally manipulated individuals of Mnemiopsis mccradyi in February–April, 1985. The normal oral-aboral length at which sexual reproduction begins in M. mccradyi is 30±5 mm; however, some larvae, of 1.5 to 2.8 mm (oralaboral length), produce viable gametes. During the present study, not all individuals from a particular spawning which were kept in the same conditions became reproductive at an early age. The age at which larval reproduction began varied between individuals. The length of time over which individuals spawned varied considerably — some spawned only once, while others spawned repeatedly. Only the gonads located under the adesophageal ctene rows (and not those associated with the adtentacular rows) produced gametes during the early reproductive period. After larvae stopped spawning, the gonads regressed and the larvae grew to large lobate stages. Individuals which became sexually reproductive as larvae also became sexually reproductive during lobate stages.     

Multiple spawning events and sexual reproduction in the octocoral Sarcophyton elegans (Cnidaria: Alcyonacea) on Lizard Island, Great Barrier Reef

Sarcophyton elegans is a common symbiotic (zooxanthellate) octocoral species in the shallow waters of the Great Barrier Reef (GBR). Study of a population at Lizard Island (14°40′S, 145°28′E) on the GBR from October 1991 to January 1994 revealed that, as is typical of tropical alcyonarian corals, S. elegans is a gonochoric broadcast spawner with a 1:1 sex ratio. Sexual reproduction was closely correlated with colony size, with first reproduction at 13-cm basal stalk circumference for females and 12 cm for males. Oogenesis took 19–24 months, with a new cycle commencing every year, and spermatogenesis took 10–12 months. The majority of gametes were released during the annual austral mass coral spawning event after the full moon in November, but gametes were also released after the full moon in each month between August and February. All autozooid polyps participated in reproduction, but those at the outer edge of a colony released their gametes first. During subsequent months, the polyps closer to the center of the colony released their gametes. This is a novel strategy of gamete release, reported here for the first time, which accommodates the demands of feeding and reproduction in a different way than other corals where individual polyps have separate feeding or reproductive roles. Colonies upstream in the prevailing current spawned up to 1 month earlier than those downstream and ceased 1 month earlier. The mechanism controlling this spatial differentiation in spawning time, repeatedly observed over three seasons, is unknown. Sarcophyton elegans appears to have a dual strategy of providing protection for its gametes by releasing most of them concurrently with the single, annual mass spawning of a large number of cnidarians, while also hedging its bets by individual colonies spawning a fraction of their gametes over an extended period of 6 months.     

Östrogenartige wirkungen von bisphenol a auf vorderkiemenschnecken (Mollusca: Gastropoda: Prosobranchia)

Within a Federal Environmental Agency research project to develop a biological test for hormone-mimetic compounds using the freshwater snail Marisa cornuarietis, the effects of the suspected xenoestrogenic substance bisphenol A (BPA), not only on freshwater but also on marine prosobranch snails, were investigated. For the laboratory experiments the ramshorn snail Marisa cornuarietis and the ovoviviparous snail Potamopyrgus antipodarum were considered as freshwater species and two marine prosobranchs, the netted whelk Nassarius reticulatus and the dog whelk Nucella lapillus, were additionally employed. N. reticulatus, as a typical sediment-living species, was exposed via artificial sediments, while the three other prosobranchs were exposed via water. The test series with Marisa cornuarietis covered a nominal concentration range between 1 and 100 μg BPA/l in a 5 month experiment with adult snails and a complete life cycle test for 12 months. Additionally, a third test in the nominal range between 0.05 and 1 μg BPA/l (measured: 0.0079–0.404 μg/l) was performed with adults snails for 6 months. In these experiments, BPA induced a complex syndrome of physiological and morphological alterations in female Marisa referred to as the induction of ‘superfemales’. Affected specimens were characterised by the formation of additional female organs, an enlargement of the accessory pallial sex glands, gross malformations of the pallial oviduct section resulting in an increased female mortality, and a massive stimulation of oocyte and spawning mass production. For these tests, an LOEC of 48.3 ng/l, an NOEC of 7.9 ng/l and an EC₁₀ of 13.9 ng/l were calculated. Superfemales occurred also in the BPA exposure experiment with the other snail species, but comparable oviduct malformations as in Marisa were not found, probably due to species differences in the gross anatomical structure of the pallial oviduct. During the 9 week test with Potamopyrgus antipodarum in the nominal concentration range between 1 and 100 μg/l, BPA induced an enhancement of embryo production even in the sexual repose phase of the reproductive cycle. A characteristic inverted U-type concentration response relationship was found. Nassarius reticulatus was exposed via BPA-spiked artificial sediments (nominal concentration range: 10–1000 μg/kg dry wt.) for 3 months. BPA exhibited a significant and concentration dependent uterotrophic effect which could be detected not only by an enlargement but also by a weight increase of the accessory pallial gland complex in the pallial oviduct section. Adult Nucella lapillus were tested for three months in the laboratory in a nominal concentration range between 1 and 100 μg BPA/l. Superfemales in the dog whelk were also characterised by enlarged accessory pallial sex glands and an enhancement of egg production, but the test compound also affected the males in this species. A lower percentage of exposed specimens had ripe sperm stored in their vesicula seminalis and male Nucella exhibited a reduced length of penis and prostate gland when compared to the control. Because statistically significant effects were observed already at the lowest nominal test concentration (1 μg/l), it can be assumed that even lower concentrations may have a negative impact on the snails. The results show that prosobranch snails are affected by BPA at lower concentrations compared to other systematic taxa in the animal kingdom. Consequently, it has to be claimed that the results of these experiment have to be considered for the current EU risk assessment for BPA in order to achieve a sufficient protection of wildlife in aquatic ecosystems.     

The reproduction of some littoral molluscs from Macquarie Island (Sub-Antarctic)

The reproduction of 9 species of littoral molluscs from the sub-Antarctic Macquarie Island was examined. The mode of larval development is reported for all species, and the reproductive patterns for 7 are described from collections taken monthly over a period of 1 year. Two species release gametes for external fertilization, whereas the other 7 have non-pelagic development via brooding or the laying of egg cases; some of these findings were deducted from examination of gonads rather than by direct observation. Features of reproduction important in any correlation between a littoral animal's reproduction and its habitat are discussed, and relationships between pelagic and non-pelagic development of the Macquarie molluscs and (a) distribution in the local environment and (b) habitat are drawn. The widely recognised correlation between species having a non-pelagic development and small number and large size of eggs is considered as a method for predicting the type of larval development (in terms of pelagic versus non-pelagic) from an examination of the ovary. It is suggested that further data on modes of development could be obtained from specimens of marine invertebrates collected throughout southern latitudes and that such data would enhance zoogeographical interpretations.     

Fecundity and reproductive effort in Ophryotrocha labronica (Polychaeta: Dorvilleidae)

Reproductive effort in terms of fecundity and energy allocation was studied in Ophryotrocha labronica La Greca and Bacci, 1962 a small, semicontinuous iteroparous species. In O. labronica fecundity is more or less constant throughout life, and the total fecundity of the 64 couples examined in this experiment only declined by 12% from the first to the last spawning. No linear relationship was found between fecundity and body size.␣The energy content of germinal and somatic tissues was determined by differential scanning calorimeter. The␣reproductive effort and a reproductive index based on the fifth spawning were evaluated to compare the␣patterns of energy allocation of a semicontinuous iteroparous species with semelparous and annual iteroparous species. The reproductive index ranged from 0.20 to 0.77, with an average of 0.480. The average reproductive effort was 0.840, ranging from 0.60 to 0.96. These figures highlight the enormous amount of energy that O. labronica allocates to reproductive tissues. Received: 23 July 1997 / Accepted: 20 October 1998     

Reproductive cycle of the brooding echinoid Abatus cordatus (Echinodermata) in Kerguelen (Antarctic Ocean): changes in the organ indices,biochemical composition and caloric content of the gonads

Variations in organ indices, organic levels, organic and caloric contents of the gonads of the brooding echinoid Abatus cordatus (Verrill), collected in the Morbihan Gulf (49°30′S; 70°E) were studied over a 1 yr period (March 1978 to January 1979). In both sexes, a clear annual cycle was discernable for organ indices, and for organic and caloric contents. In contrast, the protein levels in the gonads varied moderately, while the levels of lipid and carbohydrate remained almost constant. This peculiarity sets A. cordatus apart from nearly all other echinoids characterized by an annual reproductive cycle. The male and female gonad indices change synchronously. The gonad indices double during maturation, reflecting variations in the germinal tissue. In both sexes, the maximal gonad index (at the end of March) coincides with the onset of the spawning season. The average male gonad index is 50% higher than that of the female. This difference is related to the restriction of coelomic space in the female due to development of the brood pouches. At maturity, the lipid and carbohydrate levels in the ovary are 2.8 and 2.1 times greater, respectively, than the levels in the testis, the latter having a 25% higher protein level. This disparity in organic levels reflects mainly the differences in germinal tissue composition. The female reproductive effort is higher than that of the male. The spawn energy output of a standard individual is 200 cal for a male and 228 cal for a female. The unusually lower gonad index of the female is compensated for by higher lipid and carbohydrate levels, giving the ovary a 40% higher calorific value.     

Sexual reproduction in the coral Pocillopora verrucosa (Cnidaria: Scleractinia) in KwaZulu-Natal, South Africa

The mode of reproduction in Pocillopora verrucosa Ellis and Solander, 1786 varies between geographically isolated regions. This scleractinian coral is common along the KwaZulu-Natal coast, and its reproductive mode and period of reproduction were assessed using histological preparations. The study was undertaken from 1992 to 1994 and showed that P. verrucosa is a simultaneous hermaphrodite and broadcast spawner in KwaZulu-Natal. Gametogenesis occurs from October to January, with the gametes maturing simultaneously so that spawning can be synchronised at new moon in January (mid-summer). Zooxanthellae are present in the mature oocytes. Received: 10 September 1997 / Accepted: 6 July 1998     

Reef coral reproduction in the equatorial eastern Pacific: Costa Rica, Panamá, and the Galápagos Islands (Ecuador). VII. Siderastreidae, Psammocora stellata and Psammocora profundacella

Two zooxanthellate, scleractinian species present in the equatorial eastern Pacific, Psammocora stellata and Psammocora profundacella, were examined in terms of their reproductive biology and ecology at four study sites, non-upwelling (Ca?o Island, Costa Rica, and Uva Island, Panamá), upwelling (Gulf of Panamá, Panamá), and seasonally varying thermal environments (Galápagos Islands). Both species were gonochoric broadcast spawners lacking zooxanthellae in mature ova. Mature gametes and spawned gonads are present around full moon; however, no spawning was observed naturally or in outdoor aquaria. Mature gametes occurred in P. stellata at Ca?o Island for nearly 6?months, and year round at Uva Island, both non-upwelling sites. Reproductively active colonies occurred mostly in the warmer months in the Gulf of Panamá and Galápagos Islands. In the Galápagos Islands, where collecting effort was greatest for P. profundacella, mature gametes were also most prevalent during the warm season. Annual fecundity was high in both species, 1.3–1.8?×?10⁴?ova?cm^?2?year^?1 in P. stellata and 1.2–2.0?×?10⁴?ova?cm^?2?year^?1 in P. profundacella. Compared to other eastern Pacific corals, P. stellata was relatively resistant to ENSO-related bleaching and mortality, especially populations inhabiting deep (12–20?m) coral communities. Rapid recovery and persistence of Psammocora spp. can be attributed to several factors: (a) relative resistance to bleaching, (b) deep refuge populations, (c) broadcast spawning, (d) protracted seasonal reproduction, (e) high fecundity, and (f) asexual propagation.