Ephemeral spawning aggregations in the Mediterranean sardine, <Emphasis Type="Italic">Sardina pilchardus</Emphasis>: a comparison with other multiple-spawning clupeoids

Using previously published histological data on multiple, monthly samples of Sardina pilchardus collected in the central Aegean and Ionian Seas (September 1999–August 2000, and November 2000–February 2001), the Mediterranean sardine was treated as a case study to investigate the biological characteristics of ephemeral spawning aggregations in multiple-spawning clupeoids. Actively spawning (Day₀) females in the Mediterranean sardine, i.e., the daily class of spawners caught a few hours prior, during, or after the spawning act, were shown to separate spatially from late (Day₁₊) spawners and non-spawning females, taking with them a large proportion of conspecific males which were also in advanced spawning condition and in better somatic condition compared to the remaining population. In addition, information from 28 stocks of multiple-spawning clupeoids from a wide range of geographic locations, belonging to 14 species and 2 families (Engraulidae and Clupeidae), was reviewed and analyzed pertinent to the formation of ephemeral spawning aggregations. Results from the latter analysis indicated similar patterns of spatial segregation of Day₀ spawners in the reviewed clupeoid stocks as in the Mediterranean Sardine, which strongly suggested that the formation of ephemeral spawning aggregations is a common behavioral trait among multiple-spawning clupeoids. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Esterase gene frequencies and temperature relationships in the New Zealand snapper Chrysophrys auratus

Esterase and glucosephosphate isomerase loci were examined in different year classes of the snapper Chrysophrys auratus Forster from the Hauraki Gulf in New Zealand and compared with temperatures during the immediate post-spawning period, the time when snapper larvae suffer high mortality. Year classes spawned in warm years have a low frequency of the Est-4² allele and year classes from cold years a high frequency of Est-4². Gpi-1² frequencies showed no significant change between warm and cold years. Annual fluctuations in allele frequencies within stocks may account for the observed excess of esterase homozygotes in other marine teleosts.     

Reproductive dynamics of endeavour prawns, Metapenaeus endeavouri and M. ensis, in Albatross Bay, Gulf of Carpentaria, Australia

 The spawning patterns of two penaeid prawns, Metapenaeus endeavouri (Schmitt) and M. ensis (De Haan), were examined from data collected at 45 stations between March 1986 and March 1992. An index of population fecundity based on the abundance, proportion and fecundity of sexually mature females was used as a measure of spawning output of the prawn stock. The population fecundity index for M. ensis was higher than that for M. endeavouri. The monthly population fecundity index for M. endeavouri varied markedly among years, while that for M. ensis was consistent among years. Spawning of M. endeavouri occurred year-round, while that of M. ensis was concentrated mainly in spring (September to November). For M. endeavouri, a minor spawning, derived from a relatively small number of summer spawners, occurred in the 20 to 30 m offshore waters in summer. In early summer (after May), the major spawning group consisted of large females from the winter-spawning cohort, and the spawning area shifted to depths of 30 to 60 m. In winter (July), the major spawning, derived from the winter-spawning cohort, occurred at depths of 20 to 40 m. For M. ensis, the major spawning, derived from the spring-spawning cohort, was observed in depths <50 m and was concentrated particularly in inshore waters (<20 m) in spring. In autumn, the spawning output was mainly from the autumn-spawning cohort, which comprised but a small number of individuals. In winter, the major spawning group again consisted of the large females from the spring-spawning cohort, and spawning increased in the oceanic waters (>50 m). These results suggest that mature female M. endeavouri and M. ensis move offshore (>40 m) by May and July, respectively, and return to shallow waters (<35 m) in July and November, respectively. The monthly reproduction patterns of both species in the “effective spawning” area showed that the major spawning season for M. endeavouri is August to October and that for M. ensis is September to December. Received: 19 February 1999 / Accepted: 18 June 2000     

Male characteristics, sperm traits, and reproductive success in winter-spawning Celtic Sea Atlantic herring, Clupea harengus

The relationship between sperm characteristics and reproductive success was examined in male herring, Clupea harengus L. Males were categorised as being first-time or repeat spawners on the basis of their age; they were also grouped according to whether their sperm were immediately active and exhibited forward motion on contact with seawater (FM) or had little or only vibratory motion (VM). Unlike the Pacific herring C. pallasii Valencienes, Atlantic herring sperm is usually motile on contact with seawater. The age, weight and gonadosomatic index (testes mass as a percentage of somatic mass = GSI) were measured and used as characteristics for individual fish. Sperm traits measured were (1) adenosine triphosphate (ATP) concentration, (2) sperm count, (3) duration of sperm motility. Reproductive success for each male was estimated from the fertilisation rate and from the length of larvae at hatching. Fertilisation rates for all fish were generally >80%. The ATP concentration of non-activated spermatozoa was negatively correlated with fertilisation rate. Among repeat spawners, fish with higher GSIs produced larvae that were larger at hatching. Although VM sperm fertilised eggs at rates equivalent to fertilisation by FM sperm, the larvae produced by VM sperm were significantly smaller at hatching. Larval length tended to increase in parallel with the duration of sperm motility, but the relationship was not significant in these tests. The results did not indicate any age or size pattern to spawning readiness in male herring. Sperm that are not yet ready to be shed are not fully motile on contact with seawater, but are still capable of fertilising eggs that hatch successfully. There is likely to be a progression of males which come into spawning readiness within a spawning shoal; therefore it is possible that paternal influences would result in a progressive decrease in larval size over the spawning period in winter-spawning Celtic Sea herring. Received: 22 November 1997 / Accepted: 8 June 1998     

Reproductive biology of deep-water calanoid copepods from the Arctic Ocean

Reproductive modes and egg production were studied in 15 species of meso- and bathypelagic copepods from nine Calanoida families in the Arctic Ocean. During shipboard incubation, females of seven species released eggs freely into the water and females of three species produced membrane-bound egg sacs. One species, Aetideopsis rostrata, produced a mass of eggs looking like an egg sac, but the “sac” lacked a membrane and disintegrated within 2 h. Females of four additional species were encountered with membrane-bound egg sacs in the preserved samples. In most families, only one reproductive mode, either egg-carrying (the Euchaetidae, Augaptilidae), or broadcast spawning (the Heterorhabdidae, Spinocalanidae, Scolecitrichidae, Tharybidae, Bathypontiidae) was observed. In contrast, different genera of the Aetideidae family demonstrated different reproductive modes, with broadcast spawning predominant in the benthopelagic species, and both broadcast spawning and egg-brooding in the planktonic species. Clutch size and egg diameter varied widely between species in both broadcast spawners and egg-brooders. In broadcast spawners, the clutch size varied from 1 to 95 eggs female⁻¹, while the average egg diameter ranged from 152 to 440 μm. The clutch size for egg brooders varied between 3 and 82, while average egg diameter varied from 258 to 732 μm. Deep-water broadcast spawners produced much larger eggs compared to surface-dwelling broadcast spawning species. This larger egg size may result in a reduction, or elimination, of feeding during naupliar stages, thereby improving the survival potential of deep-water species.     

Ecological and genetic aspects of reproductive isolation by different spawning times in<Emphasis Type="Italic"> Acropora</Emphasis> corals

In Okinawa, Japan, we found several species of the coral genus Acropora that spawn 1.5-3 h earlier than other mass-spawning acroporids. In six early-spawning species, gamete bundles appear on the surface of the colony ("setting") about 1 h before sunset, whereas setting occurs about 1 h after sunset in the more common late mass spawners. These early spawners are divided further into two sub-groups: three species that release their gametes within 1 h after setting and three that release their gametes 1.5-2 h after setting. DNA phylogenetic analyses show that each of these groups forms an independent genetic clade. These genetic relationships suggest that different spawning times form the basis of reproductive isolation among these broadcast-spawning corals. Late spawning appears to be the ancestral state, and the shift of spawning to earlier times may have played a role in the speciation process in these sympatric species.     

Age and growth of the lanternfish Lampanyctodes hectoris (Myctophidae) from eastern Tasmania,Australia

The age, growth and mortality of the lanternfish Lampanyctodes hectoris (Gunther) were investigated by examining the otoliths, length-frequency data, and seasonal abundance of fish collected from continental slope waters of eastern Tasmania between April 1984 and June 1985. Although L. hectoris can live to 3 yr old, it has a high annual mortality (79%) and few live past their first year. Growth, described here by a variation of the Von Bertalanffy model, takes place mainly in the first six months of life and only during late spring and summer. The hypothesis of daily deposition of primary growth increments in myctophids was supported by comparing the back-calculated birth dates of daily-aged individuals of L. hectoris with the spawning season of this species.     

Reproductive cycle of the brachiopodTerebratulina retusa on the west coast of Scotland

The reproductive cycles of two populations of the Recent articulate brachiopodTerebratulina retusa (Linnaeus) are described, based on samples taken between October 1985 and October 1986. Stereological analysis of the gonads revealed a single synchronised spawning event between late November and the end of January in the Firth of Lorn. In a second population, in Loch Fyne, spawning took place repeatedly throughout the spring and summer, with greatest spawning activity occurring in the late autumn.T. retusa from Loch Fyne were approximately three times more fecund than those from the Firth of Lorn. Productivity in the Clyde Sea area is approximately five times higher than in Firth of Lorn and higher fecundities and spawning frequencies of the Loch Fyne population are attributed, in part, to greater food availability. The initiation of gametogenesis appears to be mediated by the mobilisation of reserves stored in the outer mantle epithelium during the winter. Primary productivity increases dramatically in the spring and gametogenesis shows a corresponding increase.     

Gonad development and the planulae of the temperate Australian soft coral Capnella gaboensis

Capnella gaboensis Verseveldt, 1977 was sampled at four sites in Sydney Harbour, during 1981–1984. This soft coral has an annual cycle of gonad development, with gonad number reaching a peak in May several weeks prior to spawning, and gonad size reaching a peak in May–June at spawning. The gonads develop during the warm months, and colonies spawn their gametes in late autumn and early winter. Gonad development is neither synchronous within colonies nor within populations, possibly reflecting the protracted nature of spawning. The histology of the developing oocytes and spermaries is described in detail C. gaboensis is a surface-brooder. The planulae are similar in structure to the larvae of other octocorals. The larvae are benthic, settling quickly upon suitable substratum, metamorphosing into polyps with mouths, tentacles and spicules, approximately one week after settling.     

Reef coral reproduction in the eastern Pacific: Costa Rica,Panama, and Galapagos Islands (Ecuador)

Reproductive ecology of two major reef-building corals in the eastern Pacific [Pocillopora damicornis (Linnaeus) andPocillopora elegans Dana] was investigated between 1984 and 1990 in Costa Rica, Panama (Gulf of Chiriqui and Gulf of Panama), and the Galapagos Islands (Ecuador) following the 1982–83 El Niño disturbance. Mature spermatocytes and oocytes were found in both species and were usually present in the same polyp in nearly equal ratios. Numerous zooxanthellae were observed in mature, unfertilized oocytes. Although spawning in field populations was not observed, it is likely that both pocilloporids are simultaneous hermaphroditic spawners, as evidenced by the disappearance of mature gametes after full moon. This is in contrast with most known pocilloporid corals that brood and release planula larvae. Corals were reproductively most active in the thermally stable environments of Costa Rica and the Gulf of Chiriqui (Panama) where 32 to 90% of all colonies contained gametes. In the moderately varying thermal conditions in the Galapagos Islands, 16 to 40% of colonies contained gametes, and in the pronounced seasonal upwelling environment of the Pearl Islands (Panama) only 6 to 18% of colonies contained gametes. Year-round reproduction occurred in Costa Rica and the Gulf of Chiriqui, whereas reproduction was confined to warm periods in the seasonally varying environments of the Galapagos Islands and the Gulf of Panama. Pocilloporid corals in Costa Rica and the Gulf of Chiriqui demonstrated lunar spawning activity, with mature gametes present a few days before and after full moon. Some limited spawning may have occurred also at new moon. While frequent gamete maturation has been demonstrated in this study, the relatively low rates of larval recruitment occurring on eastern Pacific coral reefs disturbed by the 1982–83 El Niño suggest that the recovery of important frame-building corals could be greatly prolonged.     

Distribution and abundance of eggs of Labidocera aestiva (Copepoda: Calanoida) in the bottom sediments of Buzzards Bay,Massachusetts, USA

Grain-size composition of the sea-bed and density of eggs of Labidocera aestiva in bottom sediments in Buzzards Bay were determined at approximately monthly intervals from March 1983 through April 1984. The results of this study, together with those of Marcus (1984), show that during the fall and winter periods of 1982–1984 the proportion of eggs of L. aestiva occurring in the surficial sea-bottom sediments declined and the proportion of eggs in the deeper sediment layers increased. High positive correlations (r ²=0.72 and 0.92) were observed during the early fall 1983 between egg abundance and the proportion of the total sediments represented by the mud fraction. During late fall, winter, and early spring 1983–1984, the coefficients of determination were much lower. Physical criteria (e.g. sedimentation and transport characteristics) can be used to accurately predict the distribution and abundance of recently spawned eggs on the sea-bottom.     

Glucosephosphate isomerase genotype frequencies,homozygous excess and size relationships in the sand flounder Rhombosolea plebeia

Genetic variation was studied at two polymorphic loci for 3 yr (November 1978–February 1982) in juvenile sand flounder (Rhombosolea plebeia) in Wellington Harbour, New Zealand. The Gpi-1 locus showed a heterogeneity in genotype frequencies, but this was not clearly related to season or to fish length. At the Gpi-2 locus, genotype frequencies were dependent upon length and showed a significant excess of homozygotes in juveniles but not in adults. This latter phenomenon has been reported previously in several species of marine molluscs, and so may be common to marine organisms producing large numbers of pelagic larvae. Reasons for the excess of homozygotes are discussed, and it is suggested that assortative mating is the most likely explanation and that this is an area of marine population genetic research which has been over-looked.     

Life history of the golden ring cowry Cypraea annulus (Mollusca: gastropoda) on Okinawa Island,Japan

Two mark-recapture studies, regular population censuses, field observations, and laboratory culture were used to study the life history of the tropical marine gastropod Cypraea annulus Linnaeus, 1758 from Cape Maeda, Okinawa Island, from April 1984 to March 1986. In the field, the average rate of increase in shell length of marked juvenile snails was 1.0±0.3 mm wk^-1 (N=13), with a maximum of 1.5 mm wk^-1 (initial shell length 10.6 to 17.2 mm). In the laboratory, the maximum growth rate of juveniles was 3.0 mm wk^-1 with food ad libitum. Snails with primordial teeth on the shells grew at a rate of 0.1 to 0.5 mm wk^-1 for about 2 wk. The adults continued to grow at a similar rate for an additional 3 to 6 wk, and ceased detectable growth when some females started spawning egg masses. In the littoral zone on Okinawa Island, snails reproduced throughout the year. Egg masses brooded by three females (shell length 17.4 to 21.3 mm) in the field contained 90 000 to 133 000 ova. In the laboratory, brooding periods of three females lasted 6,8, and 9 d. The estimated average frequency of spawning was 5 egg masses female^-1 yr^-1. The mean shell length of adult females (20.3 mm) was significantly larger than that of adult males (19.6 mm). The life-history strategy of C. annulus is characterized by rapid growth, high fecundity, and repeated spawning throughout the year.     

Seasonality of coral reproduction in the Dampier Archipelago,northern Western Australia

Coral spawning in Western Australia (WA) occurs predominantly in the austral autumn in contrast to the Great Barrier Reef (GBR) on Australia’s east coast where most spawning occurs in spring. Recent work, however, suggests a second spawning period in northern WA with at least 16 Acropora spp spawning in spring or early summer. This discovery has initiated a re-examination of reproductive seasonality in northern WA, particularly on inshore reefs adjacent to large development projects, such as the site of this study in Mermaid Sound, in the Dampier Archipelago. Three locally abundant taxa, Porites spp, Pavona decussata and Turbinaria mesenterina were sampled monthly from September 2006 to May 2007 to determine sexuality, the mode of reproduction and the time of gamete maturity. All three taxa were gonochoric broadcast spawners. Porites spp. colonies were mature in November and December, P. decussata in March and April. In contrast, most colonies of T. mesenterina contained mature gametes for up to 5 months beginning in November, suggesting either individuals are releasing gametes on multiple occasions, or they retain mature gametes for more than 1 month. Field surveys to determine the reproductive status of the remaining coral assemblage were conducted prior to the full moon in October 2006 and March 2007. Only four species contained mature gametes in October 2006. In contrast, 55 species contained mature gametes in March 2007. We conclude that the major spawning season of corals on shallow-inshore reefs in the Dampier Archipelago is autumn, although taxa that spawn in spring and summer include Porites spp., Acropora spp. and possibly T. mesenterina that are numerically dominant at many of these sites. Consequently, management initiatives to limit the exposure of coral spawn to stressors associated with coastal development may be required in up to five months per year.     

Reproductive cycle,larval development,juvenile growth and population dynamics of Patiriella pseudoexigua (Echinodermata: Asteroidea) in Taiwan

A field study was conducted at Wanlitung, southern Taiwan, in 1986–1089, to determine the reproductive cycle, development mode, growth rate and population dynamics of the small seastar Patiriella pseudoexigua (Dartnall), which occurs in highly stressful and disturbed intertidal pools in this area. An inverse relationship between gonad index and pyloric-caccum index was only recorded immediately prior to spawning. A short, well-synchronized seasonal spawning occurs in October. When reared at 25 °C, lecithotrophic larvae develop directly, lack a bipinnaria stage, and metamorphose completely on the seventh day after fertilization. The growth curves of field juveniles are linear, those of laboratory-reared juveniles are sigmoid. Juveniles appear in tide pools in spring-early summer of each year. Adults spawn mainly in late fall, enabling spawning to occur in time for the larvae to benefit from the environmentally favorable winter season. Populations in high-tidal pools decrease in later summer, but remain more stable in lowtidal pools and lagoons.     

Reef coral reproduction in the Abrolhos Reef Complex, Brazil: the endemic genus Mussismilia

The current contribution deals with the reproductive biology of a genus endemic to Brazil –Mussismilia Ortmann, 1890 – including all three species of the genus: M. braziliensis (Verrill, 1868), M. hartti (Verrill, 1868), and M. hispida (Verrill, 1902), which occur sympatrically in the studied area, the Abrolhos Reef Complex, Brazil. Sexuality patterns, modes of reproduction, synchrony and spawning periods are reported, and were determined by histological examination of material. All three species started to develop female and male gametes over different periods in the same breeding season. The three species are probably broadcast spawners, since no embryos or planulae were observed in any species at any given time of the year. Each reproductive cycle lasted approximately 11 months. Oogenesis and spermatogenesis started in different periods, with spermaries appearing in approximately the eighth month of ovary development and lasting about 3 months. Reproductive cycles were annual. Spawning probably occurred in consecutive months in each species. In M. braziliensis, spawning presumably happened between March and the middle of May in 1996 and 1997. Evidence suggested that spawning events of M. hispida took place between the end of April and mid-June. M. hartti may have spawned between September and November. The data presented here suggested that all studied species have at least one exclusive spawning period, asynchronically with the others. A possible exception may be the simultaneous (or close) spawnings of M. braziliensis and M. hispida in May. It is suggested that asynchrony in spawning periods among species may reduce the chance of hybridization, gamete waste and the competition for settlement surfaces. The occurrence of extended spawning periods for each species may also reduce the risks of reproductive failure, due to temporary adverse conditions. Received: 8 December 1998 / Accepted: 15 July 1999     

Spawning patterns in the leopard grouper, <Emphasis Type="Italic">Mycteroperca rosacea</Emphasis>, in comparison with other aggregating groupers

We documented the spawning patterns of the leopard grouper, Mycteroperca rosacea, from April to June 2005 in the central Gulf of California, Mexico to draw comparisons with other aggregate-spawning groupers and provide information useful for management of their fishery. Adults formed spawning aggregations of 150 to >700 individuals at specific sites, and spawning occurred daily at these sites from late April through early June. Courtship occurred throughout the day, but spawning was restricted to the evening hours. Adults spawned in groups of 6–40 fish, and pair-spawning was not observed. The group-spawning behavior of adults and the gonosomatic indices of mature males (maximum = 7.2%) suggest that sperm competition was present. The site-specificity of leopard grouper spawning aggregations and diel spawning period were typical of most aggregating groupers, and the size and structure of these aggregations was similar to other species in the genus Mycteroperca. Leopard grouper behavior patterns were unusual in that spawning aggregations persisted for extended periods, spawning was not synchronized with the lunar cycle, and adults aggregated during non-spawning periods. The extensive duration and site-specificity of spawning aggregations and the propensity of M. rosacea to form aggregations year-round increases the vulnerability of the species to overfishing. Policies that limit harvest from these aggregations are needed to improve the management of leopard grouper fisheries in the Gulf of California.     

Allozyme electrophoresis demonstrates that the scleractinian coral Montipora digitata is two species

Allozyme electrophoresis at five loci was used to clarify the species status of two morphs of the scleractinian coral Montipora digitata (Dana, 1846), using specimens collected from three locations off the Queensland coast between October 1991 and April 1993. The two morphs, occurring sympatrically, were distinguished by one fixed gene difference at Locus LT-2 and frequency differences at three other loci, indicating reproductive isolation between them. Populations of both morphs were generally in Hardy-Weinberg equilibrium, suggesting that sexual reproduction does occur. Despite sampling designed to reduce the chance of collecting clonemates, the genetic diversity ratio (G _O:G_E) indicated that asexual reproduction also occurs. This is in agreement with the known modes of reproduction for this species. There was significant genetic differentiation between populations of one of the morphs of M. digitata. This could have been influenced by greater degrees of asexual reproduction in this morph, selection within sites, or variation in larval survival and recruitment patterns. Relatively low F _st (differentiation among populations) values found for a broadcast spawning species during this study are in accordance with the hypothesis that brooded planulae are adapted for rapid settlement, whereas planulae produced by broadcast spawners are adapted for widespread dispersal.     

The reproductive ecology of the invasive ascidian, <Emphasis Type="Italic">Styela clava,</Emphasis> in Auckland Harbour,New Zealand

The ascidian Styela clava, native to the north-west Pacific, is an invasive species affecting New Zealand’s marine ecosystems, biodiversity and aquaculture operations. To provide detailed information on the reproductive biology of S. clava in New Zealand for post-border biosecurity management, long-term seasonal patterns of gametogenesis were determined from May 2006 to May 2008 in Auckland’s Waitemata Harbour (36°49′20″S, 174°45′85″E). Of particular interest was whether the critical 15°C threshold spawning temperature for reproduction observed in the Northern Hemisphere applied here to the first Southern Hemisphere study. S. clava gametogenesis followed a regular seasonal cycle with ripe gametes appearing as early as September and persisting to June; this time frame corresponds to the period when sea surface temperatures in the region first reach 15°C and with spawning occurring mainly during late summer to early autumn. From photoperiod manipulation, it was determined that spawning occurred at approximately 18:20. The extended reproductive period and a short generation time in the Waitemata Harbour provides a lengthy opportunity for S. clava to spread. Findings are discussed in relation to S. clava’s post-border management.