Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria

Many corals which engage in symbioses with dinoflagellates from the genus Symbiodinium (zooxanthellae) produce offspring which initially lack zooxanthellae. These species must choose their symbionts from numerous genetically distinct strains of zooxanthellae co-occurring in the environment. In most cases, symbiosis onset results in an association between a specific host coral and a specific strain of algal symbiont. This is the first study to examine host-symbiont specificity during symbiosis onset in a larval cnidarian, and the first to examine such events in a scleractinian of any life stage. We infected planula larvae of the solitary Hawaiian scleractinian Fungia scutaria with both homologous zooxanthellae, freshly isolated from F. scutaria adults, and heterologous zooxanthellae, isolated from Montipora verrucosa, Porites compressa, and Pocillopora damicornis, three species of scleractinians which co-occur with F. scutaria. We found that homologous zooxanthellae were better able to establish symbioses with larval hosts than were heterologous isolates, by two separate measures: percent of a larval population infected, and densities of zooxanthellae per larva. We also measured algal densities in larvae over a 4-day period until the onset of settlement and metamorphosis. We found no changes in zooxanthella population densities, regardless of zooxanthella type or the light environment in which they were incubated. Strong infection of host larvae with homologous algae compared to heterologous algae suggests that there is a specificity process which occurs sometime during the early stages of infection between the partners, and which results in the establishment of a specific symbiosis.     

Aspects of the spawning of western Atlantic butterflyfishes (Pisces: Chaetodontidae)

Synopsis The status of knowledge of spawning among the five shallow waterChaetodon species in the western Atlantic is reviewed. Spawning has been observed for three species in Puerto Rico, St. Croix and the Bahamas, with possible courtship in a fourth.Chaetodon aculeatus spawned near the time of sunset over objects on the reef as single female/male pairs or as two females and one male, with pair spawning in rapid succession. Spawning occurred during much of the lunar month from February to April and it is uncertain whether any lunar periodicity to spawning exists. Male-male aggression was noted. Spawning sites (coral heads) were alternated daily and it is likely that females spawn only once every two days. A single female produced as many as 2090 eggs in a single spawning.Chaetodon capistratus spawned during much of the lunar month from February to April. It spawned about 5 min afterC. aculeatus, occasionally using the same sites, and alternated sites daily. A female produced as many as 3710 eggs in one spawning.Chaetodon striatus spawned from February to April but it is unknown if it has any lunar spawning cycle. No predation attempts by piscivores on spawning adults were seen. Predation byMelichthys niger on eggs ofC. striatus occurred. No egg predation was observed forC. aculeatus andC. capistratus. With an assumed four month reproductive season, alternate day spawning and observed egg production values,C. aculeatus andC. capistratus produce respectively about 100 000 and 200 000 eggs per large female per year. The reproductive strategy of smaller species may be to produce moderate numbers of eggs per day over a spawning season of at least a few months while larger species may produce more eggs per day for a shorter period.     

Timing of spawning and early development of Palythoa tuberculosa (Anthozoa, Zoantharia, Sphenopidae) in Okinawa, Japan

The spawning behavior and early embryogenesis of Palythoa tuberculosa (Anthozoa, Zoantharia) were observed in August 2009 off Okinawa Island, Japan. P. tuberculosa released zygotes just after high tide around new moon nights. The mean diameter of zygotes was 365.6 ± s.d.14.8 μm, and zygotes did not contain any symbiotic algae (zooxanthellae). About 2 h after spawning, the first cleavage furrow appeared on one side of the zygotes, although it was uncertain when eggs were fertilized. After second cleavage, the arrangement of blastomeres was pseudospherical. At 9 h after spawning, the embryo became a concave-convex dish shape, then gastrulation occurred and the blastopore was formed. Seven-day old larvae were ellipsoid and about 700 μm long, with an open mouth at one end. Two weeks after spawning, the larvae developed a longitudinal band of long cilia (= ventral ciliate band) that is characteristic of zoanthella larvae. In P. tuberculosa, larvae show a non-radial body plan and then metamorphose to almost-radial (in outward appearance) polyps after settlement. These results may support a hypothesis that a common ancestor of Cnidaria had a bilateral body plan that has been secondarily lost in some extant cnidarians.     

Early development of zooxanthella-containing eggs of the corals Pocillopora verrucosa and P. eydouxi with special reference to the distribution of zooxanthellae

Some hermatypic corals spawn eggs that contain zooxanthellae. We followed development of zooxanthella-containing eggs of two such species, Pocillopora verrucosa and P. eydouxi. We also documented changes in the distribution pattern of zooxanthellae during development. Oocytes of both species took up zooxanthellae 3 to 4 days before spawning. At first, zooxanthellae were evenly distributed in oocytes, but they later moved to the hemisphere that contained the germinal vesicle. After fertilization, early cleavage events were holoblastic, progressing by furrow formation. The first cleavage furrow started at the hemisphere that contained zooxanthellae, dividing the zooxanthellate complement of the zygote about equally into the two blastomeres. The second division divided each blastomere into one zooxanthellae-rich cell and one with few zooxanthellae. With continued cell division, blastomeres containing zooxanthellae moved into the blastocoel. The blastocoel disappeared at about 5 h after the first cleavage, and the central region of the embryo was filled with cells containing either zooxanthellae or lipid droplets, forming a stereogastrula. Our results suggest that only blastomeres that had been determined to develop into gastrodermal cells receive zooxanthellae during cleavage. This determination appears to take place, at the latest, by the second cell division at the four-cell stage.     

Sexual reproduction and larval settlement of the zooxanthellate coral Alveopora japonica Eguchi at high latitudes

Sexual reproduction and larval settlement of Alveopora japonica Eguchi were studied at its northernmost distribution in Tokyo Bay (34°58'03'N, 139°46'05'E), where the annual sea temperature ranges from 13 to 27 °C. Alveopora japonica is a hermaphroditic brooding coral with oocytes and spermaries developing on separate mesenteries of the polyp. The oocytes first appeared in October, maturing in late August to early September of the following year, whereas the spermaries were first observed in May, and matured in approximately 4 months. The oocytes reached ca. 800 µm in diameter. Planulae containing zooxanthellae in their endoderm were released during the daytime in September and October. Well-developed planulae were able to settle and metamorphose within 7 h. The polyps started budding about 3 weeks after settlement, and took 3 years to grow to maturity. The population examined was sexually reproductive, indicating that A. japonica maintains local populations in Tokyo Bay by sexual reproduction.     

Settlement induction of Acropora palmata planulae by a GLW-amide neuropeptide

Complex environmental cues dictate the settlement of coral planulae in situ; however, simple artificial cues may be all that is required to induce settlement of ex situ larval cultures for reef re-seeding and restoration projects. Neuropeptides that transmit settlement signals and initiate the metamorphic cascade have been isolated from hydrozoan taxa and shown to induce metamorphosis of reef-building Acropora spp. in the Indo-Pacific, providing a reliable and efficient settlement cue. Here, the metamorphic activity of six GLW-amide cnidarian neuropeptides was tested on larvae of the Caribbean corals Acropora palmata, Montastraea faveolata and Favia fragum. A. palmata planulae were induced to settle by the exogenous application of the neuropeptide Hym-248 (concentrations ≥1 × 10⁻⁶ M), achieving 40–80% attachment and 100% metamorphosis of competent planulae (≥6 days post-fertilization) during two spawning seasons; the remaining neuropeptides exhibited no activity. Hym-248 exposure rapidly altered larval swimming behavior (<1 h) and resulted in >96% metamorphosis after 6 h. In contrast, M. faveolata and F. fragum planulae did not respond to any GLW-amides tested, suggesting a high specificity of neuropeptide activators on lower taxonomic scales in corals. Subsequent experiments for A. palmata revealed that (1) the presence of a biofilm did not enhance attachment efficiency when coupled with Hym-248 treatment, (2) neuropeptide-induced settlement had no negative effects on early life-history developmental processes: zooxanthellae acquisition and skeletal secretion occurred within 12 days, colonial growth occurred within 36 days, and (3) Hym-248 solutions maintained metamorphic activity following storage at room temperature (10 days), indicating its utility in remote field settings. These results corroborate previous studies on Indo-Pacific Acropora spp. and extend the known metamorphic activity of Hym-248 to Caribbean acroporids. Hym-248 allows for directed and reliable settlement of larval cultures and has broad applications to the study and rehabilitation of threatened Acropora populations in the Caribbean.     

Effect of lunar periodicity on the locomotor activity of silver-stage Japanese eel,Anguilla japonica

Lunar periodicity has been thought to influence the onset of the spawning migration of anguillid eels. In this study, we measured daily locomotor activity of 8 silver-phase Japanese eels Anguilla japonica in outdoor tanks to examine the effect of lunar periodicity on their activity and the following seaward migration. The activity of silver eels was highest around the new moon during the early part of the experiment, which is the ordinary season of seaward migration in Japan. The observed patterns of activity may reflect the importance of the lunar cycle for the onset of the spawning migration in anguillid eels.     

Variation in larval properties of the Atlantic brooding coral <Emphasis Type="Italic">Porites astreoides</Emphasis> between different reef sites in Bermuda

Recent research has documented phenotypic differences among larvae released from corals with a brooding reproductive mode, both among species and within broods from a single species. We studied larvae released from the common Atlantic coral Porites astreoides in Bermuda to further evaluate phenotypic variability. Inter-site differences were investigated in larvae from conspecifics at a rim and patch reef site. Larvae were collected daily for one lunar cycle from several colonies per site each year over 5 yr. Larval volume varied with reef site of origin, with colonies from the rim reef site producing larger larvae than colonies from the patch reef site. This inter-site variation in larval size could not be explained by corallite size and may be a response to different environmental conditions at the sites. Larvae from both reef sites also varied in size depending on lunar day of release over 4 yr of study. Regardless of site of origin, smaller larvae were released earlier in the lunar cycle. Over 1 yr of study, lipid and zooxanthellae content and settlement success after 48 h covaried with larval size. However, there may be a trade-off between larger larvae and reduced fecundity. Overall, larvae released from colonies from the rim reef site were larger and had greater settlement success than those from colonies from the patch reef site. This study documents larval phenotypic variability and a distinct inter-site difference in larval ecology among conspecifics within the same geographic area, which may have implications for recruitment success, population dynamics, and resilience.     

Diel and lunar spawning periodicity of the hawkfish Paracirrhites forsteri (Cirrhitidae) on the reefs of Kuchierabu-jima Island, southern Japan

We observed spawning behavior of the hawkfish Paracirrhites forsteri on reefs of southern Japan. Spawning generally occurred after sunset, prior to the full and new moon with semi-lunar spawning peak periodicity. No egg predation was observed in spawning after sunset, and high tide often occurred at dusk in the lunar phases. Thus, diel timing and lunar synchronicity may increase larval survival. We found that the mating activity tended to start earlier in the day during early mating season than during mid-to-late mating season. The advantages of the earlier start of mating activity were also examined in relation to adult biology contexts.     

Lunar spawning in Siganus canaliculatus

A major spawning of the seagrass rabbitfish Siganus canaliculatus occurred 4 days after the new moon in both May and June 1993, and 7 days after the new moon in 1994. The gonadosomatic index ( I _G) and serum vitellogenin (VTG) levels fluctuated according to the lunar cycle; IG and VTG levels showed peaks at around the new moon and the waning moon, respectively, suggesting that spawning of this species is synchronized with the lunar cycle. Vitellogenic oocytes appeared on day 2 after the first spawning and were fully mature on day 30. When a greater percentage of the most advanced oocytes attained the tertiary yolk stage, they formed a batch and separated from the adjacent group of smaller pre-vitellogenic oocytes, indicating that S. canaliculatus is a multiple spawner with an ovary belonging to the group-synchronous type of oocyte development. Batch fecundity, assessed using batches of oocytes at and after the tertiary yolk stage, ranged from c. 0·52 to 2·56 million eggs. The relationship between batch fecundity (F) and fork length (1) can be represented as F=0·0536854L^5·07292.     

Effects of delayed settlement on post-settlement growth and survival of scleractinian coral larvae

Demographic connectivity requires both the dispersal of individuals between sub-populations, and their subsequent contribution to population dynamics. For planktonic, non-feeding marine larvae, the capacity to delay settlement enables greater dispersal distances, but the energetic cost of delayed settlement has been shown to adversely impact post-settlement fitness in several taxa. Here, we assess whether delayed settlement influences mortality rates or growth rates for the first 6 weeks following settlement of the scleractinian coral, Acropora tenuis. Coral larvae that were settled at 2, 4, and 6 weeks after spawning, and then deployed in the field, showed negligible effects of delayed settlement on post-settlement survival and time to initial budding for colony formation. Between-cohort differences in budding rate appeared to be explained by temporal variation in the post-settlement acquisition of zooxanthellae. The potential for coral larvae to remain in the pelagic zone for increased periods of time with little to no effect on post-settlement survival and growth suggests that the capacity for delayed settlement is likely to have meaningful demographic consequences for broadcast-spawning reef-building corals, and that the predicted trade-off between delayed settlement and post-settlement fitness is less applicable to reef-building scleractinian corals than other taxa with non-feeding larvae.     

Spawning timing of the cleaner wrasse, Labroides dimidiatus, on a warm temperate rocky shore

We observed spawning behaviors of the haremic cleaner wrasse Labroides dimidiatus at a rocky reef in southern Japan. Females released pelagic eggs daily from June to September after a spawning ascent by pairs. When the high tide occurred between noon and evening (quarter moon to new or full moon), they spawned around the time of the tide providing fast offshore currents. For the rest of the lunar cycle, spawnings occurred during late afternoon independent of the state of the tide at the time of day. This spawning pattern is quite different from that of conspecifics on coral reefs that always spawn around the high tide at all lunar stages to avoid potential egg predators. The wrasse ascended high in the water column, probably because of its predator-immune characters as a cleaner. The steep slope of the study site seemed to contribute to releasing gametes far above aggregating planktivores. Thus, gametes were not subject to heavy predation. Current direction might not always affect survival of spawned pelagic eggs on the temperate reefs so crucially as it does on coral reefs. We conclude that spawning during unfavorable tidal conditions during the daytime may be better than spawning during the best tidal condition in the crepuscular period when predation pressure on adults will be high. Intraspecific variation in the timing and location of spawning of the wrasse may result from different conditions for larval survival. Received: February 6, 2000 / Revised: June 16, 2000 / Accepted: July 17, 2000     

Diel spawning periodicity of red snapper Lutjanus campechanus in the northern Gulf of Mexico

Ovaries of red snapper Lutjanus campechanus were examined histologically to determine rates of oocyte maturation, diel spawning periodicity and whether lunar cycle influenced spawning rhythm. Hydration of red snapper oocytes began during the mid‐morning hours; c . 5 h was necessary for oocytes to become fully hydrated and ovulation occurred no more than 5 h after oocytes attained full hydration. Appearance of fresh postovulatory follicles after 1330 hours and the absence of hydrated oocytes after 1830 hours signified that red snapper spawning occurred during this 5 h period. In addition, evidence of a peak in spawning was seen near 1600 hours. Postovulatory follicles degenerated within a 24 h time period. A lunar spawning cycle was not evident.     

Experimental infection of aposymbiotic gorgonian polyps with zooxanthellae

The planula larvae and young polyp stages of the West Indian gorgonian Pseudopterogorgia bipinnata (Verrill) do not have symbiotic zooxanthellae. Planulae were allowed to settle in water free of any algae and presented with a number of strains of dinoflagellates. Motile forms of these algae were attracted to the polyps and in some cases were seen to swim into the polyp's open mouth. Successful infection was obtained only with Gymnocdinium (probably microadriaticum (Freudenthal)). Algae of the genus Amphidinium were apparently not able to infect polyps. The differences in transmission of zooxanthellae in symbiotic animals are discussed.     

Spawning frequency, fecundity, egg weight and spawning type of silver pomfret, Pampus argenteus (Euphrasen) (Stromateidae), in Kuwait waters

Silver pomfret, Pampus argenteus, were collected by fishing with drift gillnets on one spawning ground in Kuwait waters during 1998–2000. Fish size frequency, sex ratio, maturation cycle, spawning frequency, fecundity and egg weight were assessed. The length–weight relationship differed between sexes whereby females were significantly bigger than males. Spawning started in mid‐May and continued until early October. During this time the water temperature ranged from 26.0 to 32.8°C, salinity was ? 39.0‰ and water depth ranged between 5 and 12 m. Large females spawned earlier than young spawners and the overall percentage of males during the spawning period was 70.3%. Spawning occurred after 13.00 h, with peak spawning between 15.00 and 18.00 hours during outgoing tide. Mean daily spawning frequency amounted to 63.2%. Spawning activity was found to be associated with the lunar cycle and spawnings were concentrated during the first and third quarters of the moon period, indicating a semilunar reproduction cycle. It was concluded that a female would spawn at least six times during the season. No change was observed in relative fecundity during the peak spawning season (June–August). Average relative batch fecundity was 176.3 eggs g^?1 somatic weight (SW), corresponding to a relative total fecundity of 1058 eggs g^?1 SW, which is 1.5 times higher than estimates obtained from counting the standing stock of oocytes. Bigger fish produced heavier eggs and the egg weight decreased as the spawning season progressed. Based on gonadal cycles, oocyte size frequency distribution and total fecundity, we concluded that silver pomfret is a multiple batch spawner with indeterminate fecundity.     

Factors regulating the breeding and foraging activity of a tropical opisthobranch

This study investigated the influence of environmental factors on the foraging cycle, breeding activity, settlement and growth of the opisthobranch Hydatina physis using laboratory trials and field observations. Results showed that H. physis follows a nocturnal circadian rhythm mediated by photic intensity and modulated by food availability. The adults foraged between 1900 and 0530 h, with an activity peak between 2000 and 2200 h, and remained inactive and burrowed in the sand during the day. This pattern was clearly influenced by cloud cover, rain and laboratory manipulated light:dark cycle. The reproduction of H. physis was primarily influenced by the lunar cycle. For 4 consecutive months, hermaphroditic reciprocal copulation, preceded by pre-copulatory courtship behaviour, occurred at night 5–7 d before the full moon. Spawning occurred 3–5 d later for up to 5 consecutive nights, the egg mass gradually decreasing in size with each spawning. An overcast sky or rain prevented or delayed both copulation and egg release. Settlement of veligers was largely influenced by the nature of the substrate. In multiple-choice experiments, settlement occurred predominantly on sand containing cirratulid polychaetes. The juveniles reached ca. 3.9 mm in shell length after 5.5 months growth.     

Moonlighting? - Consequences of lunar cues on anuran reproductive activity

While the influence of environmental variables, particularly temperature and rainfall, on the breeding behavior of amphibians is widely recognized, relatively few studies have addressed how the moon affects amphibian behavior. Yet, the lunar cycle provides several rhythmic temporal cues that animals could use to time important group events such as spawning, and the substantial changes in light levels associated with the different moon phases may also affect the behavior of nocturnal frogs. Using seven years of field observation data, we tested for lunar effects on the reproductive activity of male and female Eastern Gray Treefrogs (Hyla versicolor). We found that chorusing and breeding activity was statistically more likely to occur around the first quarter of the moon and during intermediately bright nights, but that reproductive activity also occurred during various other times during the lunar cycle. We discuss these findings in relation to the two main hypotheses of lunar effects on animals: predator avoidance and temporal synchronization of breeding.     

Laboratory culture and evaluation of the tubeworm Ficopomatus enigmaticus for biofouling studies

Ficopomatus enigmaticus, a euryhaline tube-building polychaete worm with a subtropical to temperate distribution, is an increasingly problematic fouling organism. In this study, laboratory protocols for maintaining adult broodstock, destructive spawning, larval culture and a settlement bioassay were developed. The method routinely yielded approximately 200 larvae per spawning adult. The mean number of eggs released by females was 1517 and the mean number of spermatozoids per male was 4.425?×?10⁶. Fertilisation success, using an initial concentration of 2.5?×?10⁶ spermatozoids and 45?eggs?ml^?1, was 76% after a contact time of 60?min. The first cleavage occurred after 20?min and the trocophore larval stage was attained by 18?h. Metatrochophores were observed 4?d post-fertilisation and were competent to settle 1?day later. The proportion of larvae that settled after 48?h was surface-dependent: 10.24% on glass, 1.39% on polystyrene and 11.07% on a poly(dimethylsiloxane) elastomer. The presence of a biofilm on glass increased the rate of settlement 7-fold compared to clean glass.     

Aggregation and spawning of the humphead wrasse Cheilinus undulatus (Pisces: Labridae): general aspects of spawning behaviour

The humphead wrasse Cheilinus undulatus formed resident spawning aggregations daily after high tide at specific locations along the seaward edge of the Palau barrier reef. The location and extent of one aggregation site remained consistent for 6 years with no physical features distinguishing it from adjacent areas. Spawning was documented most months and probably occurred year round with possible seasonal and lunar variation. Spawning males arrived first at the site, followed by females and potentially small primary males. The aggregation female to male sex ratio was estimated to be between 6:1 and 10:1. A maximum of 15 males and 100–150 females were observed at the site. A male courtship posture with the anal fin pointed, the caudal fin folded down and the dorsal fin folded against the body was maintained while swimming a few metres off the bottom in view of females. When ready to spawn females rose up as the posturing male passed and the pair released gametes in a relatively sedate fashion near the surface along the shelf break. No attempted predation on spawning adults was seen. Egg predation after spawning was uncommon. On days with early to mid‐day high tides the spawning period started 2·0–2·5 h after high tide when the speed of lagoon–ocean tidal currents peaked and lasted c. 1 h. On days with later afternoon high tides, spawning occurred sooner after high tide and before current speeds peaked. Other fishes with planktonic eggs spawned at the site as pairs or small groups in a rough succession after high tide with C. undulatus, the last species to spawn.