Integrate-and-fire models of insolation-driven entrainment of broadcast spawning in corals

The circa-annual cycle of gametogenesis produces mature gametes at the spawning “season” for successful mass spawning of broadcast corals. We develop a bioenergetic integrate-and-fire model that reveals how annual insolation rhythms can entrain the gametogenetic cycles in tropical hermatypic corals to the appropriate spawning season, since photosynthate is their primary source of energy. In the presence of short-term fluctuations in the energy input, a feedback regulatory mechanism is likely required to achieve coherence of spawning times to within one lunar cycle, in order for subsequent signals such as lunar and diurnal light cycles to unambiguously determine the “correct” night of spawning. The feedback mechanism can also provide robustness against population heterogeneity that may arise due to genetic and environmental effects. We solve the integrate-and-fire bioenergetic model numerically using the Fokker–Planck equation and use analytical tools such as rotation number to study entrainment.     

Mass spawning of corals on a high latitude coral reef

Evidence is presented that at least 60% of the 184 species of scleractinian corals found on reefs surrounding the Houtman Abrolhos Islands (Western Australia) participate in a late summer mass spawning. These populations are thus reproductively active, despite most species being at the extreme southern limit of their latitudinal range (28° 29°S). In the present study, coral mass spawning occurred in the same month on both temperate (Houtman-Abrolhos) and tropical (Ningaloo) reefs of Western Australia, despite more than two months difference in the timing of seasonal temperture minima between the two regions. This concurrence in the month of spawning suggests that temperature does not operate as a simple direct proximate cue for seasonal spawning synchrony in these populations. Seasonal variation in photoperiod may provide a similar and more reliable signal in the two regions, and thus might be more likely to synchronize the seasonal reproductive rhythms of these corals. Also there is overlap in the nights of mass spawning on the Houtman Abrolhos and tropical reefs of Western Australia, despite significant differences in tidal phase and amplitude between the two regions. This indicates that tidal cycle does not synchronize with the night(s) of spawning on these reefs. Spawning is more likely to be synchronised by lunar cycles. The co-occurrence of the mass spawning with spring tides in Houtman Abrolhos coral populations may be evidence of a genetic legacy inherited from northern, tropical ancestors. Micro-tidal regimes in the Houtman Abrolhos region may have exerted insufficient selective pressure to counteract this legacy.     

Lunar synchronization of the monthly reproductive rhythm in the sea urchin Centrostephanus coronatus Verrill

The monthly reproductive rhythm in the diadematid sea urchin Centrostephanus coronatus Verrill at Santa Catalina Island, California, was studied in the summer of 1973 and the results are compared with data for the summer of 1969. In the summer of 1973 the more extreme spring tides coincided with the new moon, while in the summer of 1969 the more extreme spring tides coincided with the full moon. The reproductive rhythm in both years was closely synchronized with lunar phases and not with the monthly tidal cycles; spawning occurred near the third lunar quarter in both years. These observations suggest that this monthly reproductive rhythm is synchronized by monthly changes in moonlight, and not by monthly tidal changes.     

Apparent semi-lunar spawning rhythmicity in a brackish cardinalfish

The purpose of the present study was to examine the lunar-related spawning rhythmicity of the amboina cardinalfish Apogon amboinensis, which is a euryhaline species inhabiting mangrove creeks in the Indo-Pacific area. During the reproductive season, the gonado-somatic index increased towards and peaked within a week of the first and last quarter moon. Histological observations of the ovaries also showed development of yolk-laden oocytes towards the first and last quarter moon; postovulatory follicles, an indicator of spawning, appeared around these lunar phases. Fish with immature oocytes in the ovary were also collected in the same lunar phases, suggesting that at least two fish populations with different oocyte development stages exist at any given time. The levels of two steroid hormones secreted from the ovarian pieces into a culture medium with human chorionic gonadotropin were measured using enzyme-linked immunosorbent assay (ELISA). The level of oestradiol-17β increased around the new and full moon periods. On the other hand, 17α,20β-dihydroxy-4-pregnen-3-one levels increased around the first and last quarter moon, suggesting that the fish are actively undergoing vitellogenesis and final oocyte maturation around the respective lunar phase. These results suggest that with the 1 month ovarian development process, A . amboinensis exhibits a semi-lunar spawning pattern with peaks around the first and last quarter moon. When A . amboinensis were reared under laboratory conditions without the tidal stimuli, mouth-brooding was initiated in 13 of 20 males within a week of the first and last quarter moon. The possibility of a lunar-related endogenous rhythm in A . amboinensis is discussed.     

Hormones and reproduction in scleractinian corals

Most broadcast spawning scleractinian corals synchronously release gametes during a brief annual spawning period. In southern Taiwan, the mass spawning of scleractinians occurs in lunar mid-March. The exact cues triggering this annual phenomenon remain unclear. A scleractinian coral, Euphyllia ancora has been selected as a model for the hormones and reproduction studies. Testosterone (T) and estradiol (E2) in free and glucuronided forms were identified and consistently detected in coral polyps throughout the year. Peak levels of free E2, glucuronided E2 and T were obtained in the coral tissue just prior to spawning. The presence of specific aromatase activity was demonstrated in coral tissue. Higher concentrations of free E2 than glucuronided E2 were detected in the coral tissue throughout the year. In contrast, higher levels of glucuronided E2 than free E2 and glucuronided T were found in seawater during mass coral spawning. Furthermore, immunoreactivity and biological activity of immunoreactive gonadotropin-releasing hormone (irGnRH) was detected and quantified in coral tissue. Coral extracts (irGnRH) and mammalian (m)GnRH agonist had a similar dose-dependent effect on luteinizing hormone (LH) release in black porgy fish pituitary cells (in vitro). Peak levels of irGnRH were detected during the spawning period. In in vivo experiments, mGnRH agonist time- and dose-dependently stimulated aromatase activity, as well as the levels of T and E2 in free and glucuronided forms in coral. In conclusion, our data suggest that irGnRH and glucuronided E2 may play important roles in the control of reproduction and mass spawning in corals.     

Coral spawn timing is a direct response to solar light cycles and is not an entrained circadian response

Broadcast spawning corals release gametes into the oceans with extraordinarily accurate timing. While the date of spawning is set by the lunar cycle, the hour/minute of spawning is set by the solar cycle. In this report, we describe experiments that test whether the time of spawning is regulated by an entrained biological clock or whether it is directly controlled by the solar cycle. Montastraea franksi samples were collected on the morning of the predicted spawning. Fragments from colonies were kept under three different lighting conditions and spawning monitored. The three conditions were sunset times of 0, 1 or 2 h earlier than normal. Fragments from the same colony spawned differently under these three conditions, with an early sunset causing a corresponding early shift in spawning. These results indicate that spawn timing is not controlled by a circadian rhythm and that it is directly controlled by local solar light cycle.     

Circadian clock gene expression in the coral Favia fragum over diel and lunar reproductive cycles

Natural light cycles synchronize behavioral and physiological cycles over varying time periods in both plants and animals. Many scleractinian corals exhibit diel cycles of polyp expansion and contraction entrained by diel sunlight patterns, and monthly cycles of spawning or planulation that correspond to lunar moonlight cycles. The molecular mechanisms for regulating such cycles are poorly understood. In this study, we identified four molecular clock genes (cry1, cry2, clock and cycle) in the scleractinian coral, Favia fragum, and investigated patterns of gene expression hypothesized to be involved in the corals' diel polyp behavior and lunar reproductive cycles. Using quantitative PCR, we measured fluctuations in expression of these clock genes over both diel and monthly spawning timeframes. Additionally, we assayed gene expression and polyp expansion-contraction behavior in experimental corals in normal light:dark (control) or constant dark treatments. Well-defined and reproducible diel patterns in cry1, cry2, and clock expression were observed in both field-collected and the experimental colonies maintained under control light:dark conditions, but no pattern was observed for cycle. Colonies in the control light:dark treatment also displayed diel rhythms of tentacle expansion and contraction. Experimental colonies in the constant dark treatment lost diel patterns in cry1, cry2, and clock expression and displayed a diminished and less synchronous pattern of tentacle expansion and contraction. We observed no pattern in cry1, cry2, clock, or cycle expression correlated with monthly spawning events suggesting these genes are not involved in the entrainment of reproductive cycles to lunar light cycles in F. fragum. Our results suggest a molecular clock mechanism, potentially similar to that in described in fruit flies, exists within F. fragum.     

Deepwater broadcast spawning by Montastraea cavernosa, Montastraea franksi, and Diploria strigosa at the Flower Garden Banks, Gulf of Mexico

Broadcast spawning by corals is a tightly synchronized process characterized by co-ordinated gamete release within 30–60 min time windows once per year. In shallow water corals, annual water temperature cycles set the month, lunar periodicity the day, and sunset time the hour of spawning. This tight temporal regulation is critical for achieving high fertilization rates in a pelagic environment. Given the differences in light and temperature that occur with depth and the importance of these parameters in regulating spawn timing, it has been unclear whether deeper coral can respond to the same environmental cues that regulate spawning behaviour in shallower coral. In this report, a remotely operated vehicle was used to monitor coral spawning activity at the Flower Garden Banks at depths from 33 to 45 m. Three species Montastraea cavernosa, Montastraea franksi, and Diploria strigosa were documented spawning within this depth range. All recorded spawning events were within the same temporal windows as shallower conspecifics. These data indicate that deep corals at this location either sense the same environmental parameters, despite local attenuation, or communicate with shallower colonies that can sense such spawning cues.     

Lunar and daily spawning rhythms of Senegal sole Solea senegalensis

A periodicity of 29 days was observed in spawning rhythms in Senegal sole Solea senegalensis , with an acrophase around the last quarter and the new moon. In both spring and autumn, a very marked nocturnal spawning rhythm was registered, with spawning beginning after dusk and the acrophase occurring around 2300 hours. When the photoperiod was artificially extended (from 10L:14D to 14L:10D), S. senegalensis synchronized to the new photoperiod: spawning took place after the new 'dusk', the beginning gradually shifting from 2100 to 2300 hours and the acrophase from 2325 to 0032 hours. Under continuous light conditions, fish sustained rhythmicity for 2 days, with an acrophase at 2249 hours, which suggested the existence of an endogenous pacemaker controlling the daily spawning rhythm. These findings provided new insights for better understanding the reproductive physiology of this species and for optimizing the timing protocols of egg collection and larvae production in S. senegalensis aquaculture.     

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.     

Effects of moonlight exposure on plasma melatonin rhythms in the seagrass rabbitfish, Siganus canaliculatus

Influences of light-dark (LD) cycle and moonlight exposure on plasma melatonin rhythms in the seagrass rabbitfish, Siganus canaliculatus, a lunar synchronized spawner, were determined by time-resolved fluoroimmunoassay (TR-FIA). When the fish were exposed to a natural LD (12:12) cycle, plasma melatonin levels exhibited a clear daily rhythm, with higher levels at midnight and lower levels during the day. These rhythms were not evident under either constant light (LL) or constant dark (DD) conditions. Plasma melatonin levels under LL condition were low and high under DD condition. These results indicate that plasma melatonin rhythms are driven by LD cycle in this species. When the fish were exposed to the 4 lunar phases, plasma melatonin levels around the new moon were significantly higher than during the first quarter moon and the full moon. Exposure to experimental new moon and full moon conditions caused significant increases and decreases of plasma melatonin levels, respectively. The synchronous rhythmicity of melatonin levels in the plasma support the hypothesis that the seagrass rabbitfish perceives moonlight intensity and responds with secretion of melatonin into the bloodstream.     

Lunar synchronization of testicular development and steroidogenesis in rabbitfish

Lunar synchronization of testicular development in the golden rabbitfish, Siganus guttatus, was assessed by measuring changes in sperm motility and conditions in the seminal plasma, and by in vitro production of steroid hormones in testicular fragments and sperm preparations. The duration and percentage of sperm motility was low 1 week before spawning (the new moon), but increased significantly on the day of spawning (the first lunar quarter). During the first lunar quarter, the osmolality decreased, but Ca(2+) concentration increased in the seminal plasma. These results suggest that spermiation occurs rapidly towards the specific lunar phase. Testicular fragments and sperm preparations were incubated with human chorionic gonadotropin (hCG) and two precursor steroid hormones, 17alpha-hydroxyprogesterone (17alpha-OHP) and testosterone (T), during the two lunar phases. The production of 11-ketotestosterone (11-KT) increased significantly when the testicular fragments were incubated with hCG at the first lunar quarter, while incubation of sperm preparations with 17alpha-OHP during the same moon phase resulted in a significant increase in 17alpha,20beta-dihydroxy-4-pregnen-3-one (DHP) production in the medium. These results suggest that 11-KT is produced in the somatic cells of the testis under the influence of gonadotropin, and that sperm can convert 17alpha-OHP to DHP. Additionally, steroidogenic activity was considered to increase toward the specific lunar phase. The synchronous increase in testicular activity supports the hypothesis that lunar periodicity is a major factor for the testicular development of S. guttatus.     

Effects of light dynamics on coral spawning synchrony

Synchrony of spawning in many hermatypic corals, typically a few nights after the full moon, is putatively dependent on solar and lunar light cycles in conjunction with other possible cues such as tides and temperature. We analyze here the contributions of separate components of light dynamics, because the effects of twilight and lunar skylight on coral spawning synchrony have previously been conflated and the alternative hypothesis that these components have differential contributions as proximate cues has not been tested. Moonlight-dependent changes in spectra during twilight, rates of decreasing twilight intensities, and changes in lunar photoperiod were experimentally decoupled using programmed light-emitting diodes and compared for their separate effects on spawning synchrony in Acropora humilis. Effects on synchrony under the control of synthetic lunar cues were greatest in response to changes in lunar photoperiod; changes in light intensities and spectra had lesser influence. No significant differences among treatment responses were found at the circa-diel time scale. We conclude that spawning synchrony on a particular lunar night and specific time of night is a threshold response to differential periods of darkness after twilight that is primarily influenced by lunar photoperiod and secondarily by discrete optical components of early nocturnal illumination.     

Lunar phase-dependent expression of cryptochrome and a photoperiodic mechanism for lunar phase-recognition in a reef fish, goldlined spinefoot

Lunar cycle-associated physiology has been found in a wide variety of organisms. Recent study has revealed that mRNA levels of Cryptochrome (Cry), one of the circadian clock genes, were significantly higher on a full moon night than on a new moon night in coral, implying the involvement of a photoreception system in the lunar-synchronized spawning. To better establish the generalities surrounding such a mechanism and explore the underlying molecular mechanism, we focused on the relationship between lunar phase, Cry gene expression, and the spawning behavior in a lunar-synchronized spawner, the goldlined spinefoot (Siganus guttatus), and we identified two kinds of Cry genes in this animal. Their mRNA levels showed lunar cycle-dependent expression in the medial part of the brain (mesencephalon and diencephalon) peaking at the first quarter moon. Since this lunar phase coincided with the reproductive phase of the goldlined spinefoot, Cry gene expression was considered a state variable in the lunar phase recognition system. Based on the expression profiles of SgCrys together with the moonlight's pattern of timing and duration during its nightly lunar cycle, we have further speculated on a model of lunar phase recognition for reproductive control in the goldlined spinefoot, which integrates both moonlight and circadian signals in a manner similar to photoperiodic response.     

Ontogeny of the circadian system governing ecdysial rhythms in a holometabolous insect, Diatraea grandiosella (Pyralidae)

ABSTRACT. Three eclosion rhythms of Diatraea grandiosella Dyar (Lepidoptera, Pyralidae) showed different phase relationships to the LD cycle, different degrees of synchronization and different sensitivity to a brief light perturbation. Egg hatching occurred mainly at dawn, whereas pupation and adult emergence occurred mainly at dusk. The egg hatching was the most synchronized rhythm of the three, pupation the least. The egg hatching rhythm was more sensitive to a brief light perturbation than was the adult emergence rhythm. A light pulse in the middle of the night caused greater disturbance in the egg hatching rhythm than did a pulse placed in the early night. The three rhythms persisted in both DD and LL. LL free-running rhythm gradually became desynchronized and broke down at the third cycle. The phase relationships reveal difficulties in applying the 'external coincidence model' to this species' photoperiodic response.     

Physiological aspects of sound communication in crickets (Gryllus campestris L.)

Summary An extremely elaborate performance, involving endogenous timing with both tidal and lunar frequencies, has been recorded in the locomotor activity of an adult specimen of the intertidal isopod,Excirolana chiltoni. During two months of observation, under constant, non-tidal conditions, this animal showed a persistent tidal rhythm in its swimming activity. Bursts of activity were initially well synchronized with times of tide crest on the shore. The average free-running period of the tidal rhythm was about 24 h 55 min, i.e. about 5 minutes longer than the average period of the tides; thus, the loss of synchrony with the concurrent tides was very gradual. The amount of activity per burst showed a conspicuous pattern of variation, a periodic amplitude modulation which paralleled, in detail, the complex lunar cycle of changes in height of high tide. The free-running period of the bimodal, circa-lunar rhythm of amplitude modulation was one or two days longer than the natural 29-day lunar cycle of tide heights.Each feature of this recording has been qualitatively replicated in activity records from other individuals of this species. Freshly-collectedExcirolana generally show spontaneous bursts of activity at times of tide crest, bursts which are repeated as a persistent tidal rhythm, the period of which commonly departs by only a few minutes from that of the natural tidal cycle. Superimposed on the tidal rhythm is an endogenous monthly pattern of amplitude modulation, which alters the amount of activity per burst. This circa-lunar rhythm has a free-running period between about 26 and 33 days, and generally leads to maximum activity on days of highest of high tides. The net result of the tidal and lunar rhythms is an activity pattern which permits the isopods to recapitulate, in great detail, certain significant ecological aspects of the mixed, semi-diurnal tidal regime of California.The experimental data are not compatible with the hypothesis that uncontrolled environmental factors, such as vibrations from waves, were responsible for the rhythmic behavior of the animals. Neither do the data support the hypothesis that beats between the observed tidal rhythm and a hidden daily or circadian rhythm were responsible for the observed circa-lunar rhythm. Furthermore, the pattern of the circa-lunar rhythm cannot be accounted for by a single monthly oscillation in the excitability of the animals, such as might be mediated by changes in the level of an excitatory or inhibitory hormone in the circulatory system.     

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.     

Lunar synchronization of testicular development and plasma steroid hormone profiles in the golden rabbitfish

Weekly changes in the gonadosomatic index (I_G) of male golden rabbitfish Siganus guttatus showed two peaks corresponding with the new moons in June and July. The testes developed synchronously toward the first lunar quarter in June and July. After the second spawning, the sperm duct and the seminiferous tubules were occupied by residual spermatozoa and spermatogonia, respectively. Weekly changes of plasma testosterone, 11-ketotestosterone and 17,20β-dihydroxy-4-pregnen-3-one coincided with those of testicular activity. They reached their peaks 1 week before spawning coinciding with the peaks of I_G and testicular development. These cyclical changes in plasma steroid hormones suggest that lunar periodicity is a major factor that synchronizes testicular activity of S. guttatus .