Role of the tidal cycle in the gonadal development and spawning of the tropical wrasse Halichoeres trimaculatus

Many wrasses on coral reefs exhibit daily spawning that peaks around daytime high tides. In this study, we examined tidal-related ovarian development in the threespot wrasse, Halichoeres trimaculatus, a species common on coral reefs in the Indo-Pacific Ocean. When the fish were collected in the morning at different tidal phases, the gonadosomatic index (GSI) and ovarian histology changed; concomitant with increases in GSI towards high tide, a clutch of the most advanced oocytes developed from vitellogenic to maturation stages. Ovulated eggs and post-ovulated follicles (POF) existed in most ovaries around high tide, but only POF remained around ebb tide, suggesting that spawning occurred during or after high tide. We noticed that tidal-related spawning was considerable in the morning and that most ovaries collected on the afternoon high tide exhibited post-spawning features. This suggests that certain labrid species possess plasticity with regard to their spawning time and utilize potent environmental cues to ensure their reproductive success. When pieces of ovary were incubated with precursor steroids, high conversion of testosterone to 17beta-estradiol occurred during high and ebb tides, while that of 17alpha-hydroxyprogesterone to 17alpha,20beta-dihydroxy-4-pregnen-3-one and 17alpha,20beta,21-trihydroxy-4-pregnen-3-one was observed during low and flood tides. Incubation of pieces of ovary with human chorionic gonadotropin resulted in similar fluctuations in the steroid hormones with tidal phase. Production of these steroid hormones correlated with oocyte development in the ovaries and was probably regulated by gonadotropin. These results demonstrate that the daily cycle is fundamental for oocyte development, and that the tidal cycle is superimposed on this process.     

Aspects of the spawning of labrid and scarid fishes (Pisces: Labroidei) at Enewetak Atoll,Marshall Islands with notes on other families

Synopsis Spawning of 32 species of Labridae and 13 species of Scaridae was seen at Enewetak Atoll, Marshall Islands. Most spawned on a reef bisecting the main ocean-lagoon passage which had strong tidal currents. Others spawned on lagoon reefs and in Halimeda beds. Polygynous haremic, lek-like and promiscuous mating systems were found which were species specific. Data on reproductive patterns, sexual dichromatism, sexual dimorphism, seasonality and spawning behavior were determined. Many spawned during the day in a time-phase dependent pattern from near sunrise to sunset. Scarid spawning began at slack high water or after when currents were starting to move out of the lagoon. Labrid spawning usually started about 30 min later with some continuing up to 2 h after high tide. With high tide before sunrise, scarid spawning began 30–50 min after sunrise as the current started flowing over the reef. With high tide near sunset, spawning occurred with an incoming current. Most labroids spawned on all phases of the moon. Acanthuridae (6 spp), Caesionidae (1 sp.) and Zanclidae (1 sp.) spawned after high tide at the same time as labroids. Pomacanthidae (5 spp.) spawned only shortly before sunset without reference to tidal currents. Fishes producing pelagic eggs at the lagoon-ocean channel spawned (1) at or slightly after high tide (44spp.), (2) in late afternoon without reference to tide (6 spp.) or (3) after slack low water (1 sp. ). Spawning style can vary within a single species in different environments. Despite the presence of many piscivores, no successful predation on spawning adults was seen. Predation on newly released eggs was uncommon. Labrichthys unilineata and Anampses twistii attempted to defend their eggs for a few sec after release. Attacks by piscivores on spawning adults on tropical reefs occur once per 100–1000 spawnings. Most are wary when preparing to spawn and prespawning behavior is easily interrupted. The risk from piscivores goes down and spawning ascent speed decreases with increasing size of spawners. Egg predation by zooplanktivores is less for pair spawners than group spawners possibly due to less conspicuous gamete clouds and times of spawning. Increasing height of egg release, speed and length of the spawning ascent, and trajectory alteration of ascending adults are believed to make it more difficult for zooplanktivores to locate eggs after release. For labrids, permanent full sexual dichromatism was found among haremic, lek-like and promiscuous mating systems. Species with temporary full dichromatism, permanent and temporary partial dichromatism and monochromatism were haremic. Smaller scarids were believed to have lek-like, and larger species haremic, mating systems. Smaller scarids had male looping behavior and post spawning displays, plus faster spawning ascents and different locations for egg release than larger ones. Eggs of 21 labrids were spherical or nearly spherical, ranging from 0.55–0.80 mm in diameter, and most had one oil globule. Among 7 is scarids, 6 had spindle-shaped eggs ranging from 1.25 ×0.50 mm 2.14× 0.48 mm while one had a nearly spherical egg. One scarid egg lacked an oil globule.     

Semilunar spawning cycle of the humbug damselfish Dascyllus aruanus

A very distinct semilunar spawning cycle was found in a population of the damselfish Dascyllus aruanus on the coral reefs of Sesoko Island, Okinawa. Spawning occurred from June to September, only in the early morning, during a period of 2–4 days immediately before or around the time of the new and full moon. Males cared for the eggs deposited on the substrate for 2.5 days until hatching. Hatching occurred just after sunset, i.e., at the high tide of spring tide; the strong ebb current then would rapidly disperse the newly hatched larvae offshore. Females tended to synchronize spawning in a male's nest, also because multiple clutches in a nest would be more likely to survive until hatching. Thus, the distinct semilunar spawning cycle may favor females in reducing mortality of both eggs and larvae. Received: July 9, 1999 / Accepted: January 29, 2000     

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.     

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.     

Multispecies spawning sites for fishes on a low‐latitude coral reef: spatial and temporal patterns

Spawning sites used by one or more species were located by intensively searching nearshore coral reefs of Kimbe Bay (New Britain, Papua New Guinea). Once identified, the spawning sites were surveyed repeatedly within fixed 5 m radius circular areas, for > 2000 h of observations ranging from before dawn to after dusk spanning 190 days between July 2001 and May 2004. A total of 38 spawning sites were identified on the seven study reefs distributed at an average of one site every 60 m of reef edge. Pelagic spawning was observed in 41 fish species from six families. On three intensively studied reefs, all 17 spawning sites identified were used by at least three species, with a maximum of 30 different species observed spawning at a single site. Spawning was observed during every month of the study, on all days of the lunar month, at all states of the tide and at most hours of the day studied. Nevertheless, the majority of species were observed spawning on proportionately more days from December to April, on more days around the new moon and in association with higher tides. The strongest temporal association, however, was with species‐specific diel spawning times spanning < 3 h for most species. While dawn spawning, afternoon spawning and dusk spawning species were differentiated, the time of spawning for the striated surgeonfish Ctenochaetus striatus also differed significantly among sites. The large number of species spawning at the same restricted locations during predictable times suggests that these sites are extremely important on this low‐latitude coral reef.     

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.     

Annual variation in the timing of coral spawning in a high-latitude environment: influence of temperature

This study was conducted at a high-latitude location (32°N; Kochi, Japan), where annual seawater temperatures show large fluctuations due to the meandering of the Kuroshio Current, providing a unique opportunity to examine the influence of temperature on coral reproduction. Annual spawning of individual colonies of four reef coral species-two Acropora species (Acropora hyacinthus and A. japonica) and two faviid species (Favites pentagona and Platygyra contorta)-was monitored in situ for 4 years in 2006-2009. The spawning of the four species always occurred around the last quarter moon in the local summer, July or August, irrespective of high annual variations in seawater temperatures (from 23.7 to 29.5 °C) and weather during the spawning period. However, the exact timing of spawning during the spawning period varied among the years and was correlated with the cumulative seawater temperature during the late period of gametogenesis (0-3 months before spawning). When seawater temperatures were higher, spawning occurred in the earlier spawning month (July) and vice versa, except in A. hyacinthus, which always spawned in July. In the case of the two Acropora species, higher (lower) temperatures led to spawning earlier (later) in the lunar cycle. Seawater temperature may have an influence on gametogenesis, causing the shift in spawning timing.     

Synchronous reproduction of corals in the Red Sea

Multi-species synchronous spawning was first described on reefs off the east and west coast of Australia. In contrast, locally abundant species in the northern Red Sea and the central Pacific have little overlap in the time of reproduction. Consequently, the idea developed that high levels of spawning synchrony both within and among species was largely confined to Australian reefs. Here, we show that gamete maturity in colonies of the genus Acropora was highly synchronous in the Red Sea. In early April 2008, at two locations separated by 300 km, 13 of 24 species sampled had mature colonies, and a further 9 species had immature colonies. In late April–early May 2008, all colonies sampled had no oocytes, indicating colonies had spawned a few days after the full moon of 20 April 2008. Similarly, in 2009, 99% of colonies from 17 species at Hurghada were mature in late April, and all were empty in early May. Spawn slicks suggested many of these colonies had released gametes three night prior to the full moon on 8 May 2009. This level of synchrony in gamete maturity is among the highest ever recorded and similar to that typically recorded in Acropora assemblages on Australian reefs. While further work is required to document the night of gamete release, these data strongly suggest that high levels of spawning synchrony are a regular feature of these Red Sea coral assemblages and that multi-species spawning occurs on or around the full moon in April and/or May.     

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.     

Perception and possible utilization of moonlight intensity for reproductive activities in a lunar-synchronized spawner, the golden rabbitfish

Rabbitfishes are known to spawn synchronously around the species-specific lunar phase. It is considered that they perceive and utilize cues from the moon in order to be synchronized gonadal development and spawning with the lunar cycle. Using the golden rabbitfish, Siganus guttatus, which spawns synchronously around the first quarter moon during the reproductive season, we measured the fluctuation of melatonin levels and examined the response of the fish to moonlight intensity. Daily fluctuation of melatonin concentration in the blood of golden rabbitfish showed low levels during daytime and high levels during night-time, suggesting that melatonin functions in the perception and utilization of photoperiod. Plasma melatonin concentration at the new moon was higher than that at the full moon. When the fish were exposed to moonlight at midnight of the both moon phases, the melatonin concentrations decreased to the control levels. These results show that the fish possibly perceive moonlight intensity and plasma melatonin fluctuates according to 'lightness' at a point of night. At the first spawning period (experiment was started one month before the spawning), the fish reared under natural conditions spawned at the expected spawning dates, whereas the fish reared under the constant darkness and lightness of night did not spawn. At the second spawning period (experiment was started 2 weeks before the spawning), the fish reared under the conditions of natural and constant darkness of night spawned but not that of constant lightness of night. It is possible that night conditions are related to synchronous gonadal development and spawning in the golden rabbitfish.     

Presence of cleaner wrasse increases the recruitment of damselfishes to coral reefs

Mutualisms affect the biodiversity, distribution and abundance of biological communities. However, ecological processes that drive mutualism-related shifts in population structure are often unclear and must be examined to elucidate how complex, multi-species mutualistic networks are formed and structured. In this study, we investigated how the presence of key marine mutualistic partners can drive the organisation of local communities on coral reefs. The cleaner wrasse, Labroides dimidiatus, removes ectoparasites and reduces stress hormones for multiple reef fish species, and their presence on coral reefs increases fish abundance and diversity. Such changes in population structure could be driven by increased recruitment of larval fish at settlement, or by post-settlement processes such as modified levels of migration or predation. We conducted a controlled field experiment to examine the effect of cleaners on recruitment processes of a common group of reef fishes, and showed that small patch reefs (61–285 m²) with cleaner wrasse had higher abundances of damselfish recruits than reefs from which cleaner wrasse had been removed over a 12-year period. However, the presence of cleaner wrasse did not affect species diversity of damselfish recruits. Our study provides evidence of the ecological processes that underpin changes in local population structure in the presence of a key mutualistic partner.     

Anti-egg predator behaviors of the small angelfish Centropyge ferrugatus (Pomacanthidae)

Synopsis Predation on eggs of the angelfish, Centropyge ferrugatus, was observed in the coral reefs of Sesoko Island, Okinawa, Japan. This angelfish released pelagic eggs in pairs at sunset after slow ascents. Of 99 matings of this angelfish, an omnivorous damselfish Amblyglyphidodon curacao approached in 25, and fed on the released eggs in eight cases. The spawning angelfish never attacked the egg-predators. Pairs of this angelfish avoided the egg-predators by delaying mating for several minutes during courtships, and by frequent changes of spawning sites. Of the 25 matings targeted by the egg-predators, the angelfish successfully avoided predation in 17 cases. Eight matings were failures mainly due to lack of any attempt to elude the predator, suggesting that the delayed matings on multiple spawning sites are effective anti-egg predator behaviors.     

Rhythmic egg-release in Littorina littorea (Mollusca: Gastropoda)

Batches of female Littorina littorea from four estuarine sites were kept in aquaria throughout their breeding season (December to July), some permanently submerged in circulating sea-water and others in a regime of simulated semi-diurnal tides of constant small amplitude. Females without the tidal experience released few eggs with little relation to the lunar month. Those in the tidal regime released more than four times the total number of eggs and released far more in periods of new and full moon than in periods of half-moon. Over the whole season, release was 1–5–3–25 times faster (at different sites) during full and new moon but the difference was more accentuated at the height of the season in February to early March and in early May. While individual females differed considerably and there were minor variations between the four sites, it is concluded that a two-weekly rhythm relates egg release to the spring-neap tide cycle and that this rhythm requires a tidal cycle of immersion and emersion for its maintenance. The special significance of such a rhythm for a species with pelagic eggs and larvae in an estuary is discussed.     

Spawning of the colonial coral <Emphasis Type="Italic">Cladocora caespitosa</Emphasis> (Anthozoa,Scleractinia) in the Southern Adriatic Sea

Data on sexual reproduction of scleractinian coral species living in temperate zones, particularly in the Mediterranean Sea, are quite scarce. This paper describes sexual reproduction of the colonial coral Cladocora caespitosa from Veliko jezero (Mljet Island) in the Adriatic Sea. Spawned orange eggs and white sperm bundles were observed on the coral bank of C. caespitosa two nights before the full moon (20 June 2005) coinciding with increasing water temperature and correlated with the lunar cycle. Spawning was observed during five nights, involving about 30% of the colonies from the coral bank. Different colonies on the bank released only one type of gamete during the reproductive period. The diameter of the sperm bundles ranged from 100 to 200 μm (average 163 μm; SD = 47.08), while the female gametes diameter ranged from 300 to 500 μm (average 416 μm; SD = 73.12).     

Mass spawning of Caesio teres (Pisces: Caesionidae) at Enewetak Atoll,Marshall Islands

Synopsis Mass spawning of Caesio teres occurred between March and August, 1983 on a reef emerging from deep water just inside the East Channel of Enewetak Atoll, Marshall Islands. Aggregations and spawning were observed from one day before until three days after the full moon. Spawning aggregations were not observed during the new or quarter moons. Spawning commenced after high tide, when the current began to flow out the pass from lagoon to ocean. The spawning aggregation of close to 1000 individuals migrated to the spawning site. Spawning occurred when the aggregate ascended to near the water's surface. Subgroups dashed horizontally within the aggregate, releasing a highly visible gamete cloud. Predation on spawning adults was not observed. Predation on spawned eggs was noted. The eggs of C. teres are described. Mid-Pacific Research Laboratory, Enewetak Atoll, Republic of the Marshall Islands Present address: Motupore Island Research Station, P.O. Box 320, University of Papua New Guinea, Papua New Guinea     

Phenotypic Plasticity in the Reproductive Behavior of Female Sand Tilefish, Malacanthus plumieri

Female sand tilefish (Malacanthus plumieri) inhabiting a deep channel in the fringing reef at Glover's Atoll, Belize (channel females) spawned planktonic eggs more frequently than those occupying the shallow sand‐rubble slopes adjacent to patch coral reefs inside the atoll lagoon (reef‐slope females). We tested five non‐exclusive hypotheses to explain habitat differences in female spawning frequency. We found no evidence that spawning frequency variation was a consequence of differences in food availability, variation in male fertility, or the intensity of predation on spawned eggs. On reef slopes, barracuda stalked tilefish near their benthic burrows, whereas these piscivores attacked channel tilefish by diving suddenly from higher in the water column. Differences in the hunting behavior of barracuda suggested that the behavior of tilefish females might be influenced by temporal variation in predation risk (risk allocation hypothesis). Consistent with this hypothesis, reef‐slope females had a much higher frequency of retreats to burrows in response to barracuda, spent more time burrowing and ventured less far from these refugia in response to a simulated predatory threat. As predicted by the risk allocation hypothesis, reef‐slope females also had lower and more variable frequencies of foraging bites, and shorter and more variable travel distances to forage than channel females. Estimated mortality from predation was over nine times higher in channel tilefish. Consistent with the hypothesis that investment in current vs. future reproduction is influenced by rates of adult mortality (mortality risk hypothesis), channel females invested more supplemental energy in egg production whereas reef‐slope females invested more in growth. Our results indicate that behavioral and life‐history traits of female tilefish show phenotypic plasticity depending upon the nature and intensity of localized predation risk.     

New insights into patterns of coral spawning on Western Australian reefs

On reefs around Australia, coral mass spawning typically occurs during the austral spring (October/November) on the east coast, and during autumn (March/April) on the west coast. However, to investigate the incidence of a secondary spawning event in spring on the west coast, the reproductive state of corals was assessed on two reefs. The results indicated that of the 29 species of Acropora investigated, multiple colonies of 11 species spawned in late spring or in early summer, in contrast to previous reports of spawning during autumn. Additionally, of four species that were followed through time at one reef, two spawned in both spring and autumn, however, individual colonies had only one gametogenic cycle. Within a single site, conspecific colonies were reproductively isolated and may not interbreed, potentially representing the initial stage of sympatric speciation in these populations.     

Female spawning migrations of the protogynous wrasse,Halichoeres marginatus

Spawning sites and spawning migration paths of tagged females of the protogynous wrasse,Halichoeres marginatus, were studied on the shallow reefs at Kuchierabu-jima Island, Japan. Males set up mating territories above prominent rocks on the offshore reef slope in the late afternoon, and pair-spawned with females, which had migrated there from their home ranges located in inshore areas. Small females migrated to the spawning sites near their home ranges, whereas large females migrated to various spawning sites located within a wide area, including downcurrent sites. Spawning at the downcurrent sites favors transport of eggs offshore, thereby increasing the female’s fitness. The spawning sites where an individual had spawned as a female were subsequently used for mating after it had changed sex. It is suggested that the wide migration of females to various spawning sites, enables the storing up of information on those sites, which later helps in the acquisition of mating territories after changing sex.