Lunar Periodicity Research Articles

Goliath grouper Epinephelus itajara sound production and movement patterns on aggregation sites

Sound production by goliath grouper Epinephelus itajara was characterized on 2 aggre- gation sites in the Gulf of Mexico off the southwest coast of Florida, which are likely to be spawning sites, based on the presence of fish with ripe gonads. Goliath grouper produced predominately low- frequency single-pulse sounds with dominant frequencies around 60 Hz. Long-term acoustic record- ings documented that sounds were most frequently produced between 01:00 and 03:00 h. Sound pro- duction had a lunar periodicity, with reduced levels occurring for several days around the full moon. A single goliath grouper was implanted with an acoustic telemetry transmitter that indicated the depth of the fish. This fish remained on the aggregation site for all but 1 d of the 2 mo record and was located near the bottom (46 m) for the majority of the time. Several forays to shallower depths were detected, most of which occurred near midnight and 03:00 h. These short-duration shallow-water forays could possibly indicate spawning ascents. The combination of passive acoustics and active acoustic telemetry indicates that efforts to document spawning should be concentrated around mid- night. The prolific sound production of goliath grouper will allow large spatial and temporal scale mapping and monitoring of aggregation sites.

The lunar cycle: a cue for amphibian reproductive phenology?

Lunar cycles give rise to cues that can be recognized by animals, including changes in light intensity, geomagnetism and gravity. Many environmental variables affect reproductive timing in amphibians and we tested the hypothesis that lunar cycles provide one of the cues for amphibian breeding phenology. For several species of anurans, the number of individuals arriving, amplexed or spawning at breeding sites in Italy and the U.K. were recorded each day over several breeding seasons. Data on various aspects of reproductive phenology were also collated from the published literature, for several anuran and urodele species. Large arrival, amplexus and spawning events were more frequent around the full moon than the new moon in anurans, although the date that the first spawn was observed showed no lunar periodicity. Anurans could be responding directly to lunar light, or could have a lunar-synchronized endogenous cycle. First sightings and peak arrivals of urodeles occurred more frequently around new and full moons, but less frequently during the third quarter of the lunar cycle, while departure dates did not show lunar periodicity. Newts could be using gravitational and/or geomagnetic changes related to the lunar cycle to time their arrivals. Synchronization of reproduction in this way may function to maximize spawning success by ensuring the temporal and spatial proximity of breeding adults, or by reducing predation on individuals. Few studies of amphibian breeding phenology consider lunar phase and our results have important implications for the prediction of amphibian mass movements and conservation strategies.

Lunar periodicity and the timing of river entry in Atlantic salmon Salmo salar

Historical catch records of Atlantic salmon Salmo salar from three rivers discharging to the Baltic Sea in an area free from tides and from strong effects of the moon on illumination were analysed to investigate whether timing of S. salar river entry was associated with lunar cycles directly. Although a significant effect of lunar phase on river entry was detected, with more fish entering rivers around the full moon than other phases, the effect of the lunar cycle was very small compared with other sources of variation. Hence, the biological role of lunar cycle as a determinant of the timing of S. salar runs in the investigated populations was negligible, suggesting that lunar cycle per se does not play a role in the timing of S. salar river entry.

Spawning of the Temperate Sea Cucumber, Australostichopus mollis (Levin)

Abstract The spawning of sea cucumbers is related to the interaction of environmental cues and reproductive maturity. Groups of Australostichopus mollis were collected every 2 wk during the summer reproductive season from mid‐October to early February. They were observed for spawning in the hatchery during heat‐shock trials conducted 3–5 C above ambient seawater temperature. Lunar periodicity existed with spawning being most prominent in the week following a full moon. In the week prior to a spawning event, there was also a decrease in ambient incoming seawater temperature. More than 75% individuals spawned during most trials in which spawning occurred. In total, 40% of the 270 individuals spawned during the reproductive season. Reliable spawners were females with a yellow gonad color and large numbers of vitellogenic oocytes, and males with large numbers of spermatocytes and an absence of motile spermatozoa. Furthermore, the percentage germinal vesicle breakdown of oocytes exposed to starfish radial nerve extract compared to seawater was greater for the more orange‐colored gonad of nonspawners. Gonad color is useful in determining the likelihood of spawning over a 2‐wk period in the presence of a cue. Sea cucumbers held for short periods in the hatchery during the reproductive season maintain a natural rhythm of spawning that can be monitored using visual indices and augmented using heat shock.

Novel vocal repertoire and paired swimbladders of the three-spined toadfish,Batrachomoeus trispinosus: insights into the diversity of the Batrachoididae

Toadfishes (Teleostei: Batrachoididae) are one of the best-studied groups for understanding vocal communication in fishes. However, sounds have only been recorded from a low proportion of taxa within the family. Here, we used quantitative bioacoustic, morphological and phylogenetic methods to characterize vocal behavior and mechanisms in the three-spined toadfish, Batrachomoeus trispinosus. B. trispinosus produced two types of sound: long-duration 'hoots' and short-duration 'grunts' that were multiharmonic, amplitude and frequency modulated, with a dominant frequency below 1 kHz. Grunts and hoots formed four major classes of calls. Hoots were typically produced in succession as trains, while grunts occurred either singly or as grunt trains. Aside from hoot trains, grunts and grunt trains, a fourth class of calls consisted of single grunts with acoustic beats, apparently not previously reported for individuals from any teleost taxon. Beats typically had a predominant frequency around 2 kHz with a beat frequency around 300 Hz. Vocalizations also exhibited diel and lunar periodicities. Spectrographic cross-correlation and principal coordinates analysis of hoots from five other toadfish species revealed that B. trispinosus hoots were distinct. Unlike any other reported fish, B. trispinosus had a bilaterally divided swimbladder, forming two separate swimbladders. Phylogenetic analysis suggested B. trispinosus was a relatively basal batrachoidid, and the swimbladder and acoustic beats were independently derived. The swimbladder in B. trispinosus demonstrates that toadfishes have undergone a diversification of peripheral sonic mechanisms, which may be responsible for the concomitant innovations in vocal communication, namely the individual production of acoustic beats as reported in some tetrapods.

Endogenous Activity Rhythms of Larval Fish Assemblages in a Mangrovefringed Estuary in North Brazil

In Caete Estuary, the decrease of larval abundance downstream was attributed to reduced retention, since ebb tide densities prevailed mainly in the middle and lower estuary during the rainy season due to increased freshwater out- flow. Anchovia clupeoides, Stellifer microps and Guavina guavina were most abundant in the late dry season on flood tides in the upper estuary, whereas ebb tide densities of these species prevailed in other regions. Environmental fluctua- tions associated with lunar periodicity, such as tidal amplitude, may account for weekly variability of recruitment and re- production of some fish species. A. clupeoides showed increased spawning activity during first quarter moon, whereas new moon phases seemed to be reproduction periods of Cynoscion acoupa. Vertical migration was not employed by the most abundant species to enable river retention, since larval densities of these species were not significantly higher at the bottom on ebb tides, except for C. acoupa and Stellifer rastrifer. This result may be related to system turbulence or to the dominance of younger stages unable to migrate vertically at the time of sampling. Lateral movement to the river bank is proposed as a possible retention mechanism. Diel effects on larval abundance related to trophic activity and gear avoid- ance.

Using mobile phone telemetry to investigate the haul-out behaviour of harbour seals Phoca vitulina vitulina

Information on the haul-out behaviour of pinnipeds is essential for increasing the accu- racy of population estimates necessary for the effective conservation of protected species, as well as improving survey design. The haul-out behaviour of 10 harbour seals Phoca vitulina L. in southwest Ireland was examined using a novel telemetry system based on global systems for mobile communi- cations technology. The data on the haul-out patterns of tagged individuals were examined using generalised additive modelling to determine potential factors of influence, such as the tide, the time of day and the time of year. The behaviour varied among seals, with time ashore reaching a maxi- mum during post-moult in October and decreasing to a minimum in February. A strong tidal in- fluence on haul-out behaviour was evident. Tagged seals hauled out more frequently at low tide. There was variation between individuals in the influence of time of day on haul-out behaviour. A cyclic pattern with lunar periodicity was evident in seals tagged in October, and the pattern varied between tidal periods. There was an overall large variation in patterns of behaviour over the tagging period, both between individuals and between tidal periods for each individual. This cautions against making inferences on the haul-out behaviour of the 'population' based on the behaviour of a small number of tagged individuals. The present study provides detailed information, heretofore unavail- able, on the haul-out behaviour of individual harbour seals and on the behaviour of the species in Ireland, and it has important implications for population assessment for conservation purposes across the species' entire geographical range.

Seasonality, lunar periodicity of settlement and microhabitat association of juvenile humpback red snapper Lutjanus gibbus (Lutjanidae) in an Okinawan coral reef

Snappers (Lutjanidae) are one of the important fisheries resources in tropical and subtropical waters. However, there have been few studies clarifying the ecology of newly settled juvenile snappers. The aims of the present study were to clarify the seasonality and lunar periodicity of the larval settlement, and the microhabitat association of newly settled juveniles for Lutjanus gibbus in an Okinawan coral reef. Fifteen coral patches were chosen and underwater visual surveys were conducted during a 2-year period. The larval settlement of the species mainly occurred between May and October during the 2-year survey period. In terms of lunar periodicity of the settlement, the newly settled juveniles were mainly found between the last quarter moon and new moon during the main settlement season. Back calculations of settlement dates based on otolith microstructure showed that most juveniles settled during the last quarter moon and new moon. Stepwise multiple regression analyses revealed that the newly settled juveniles were mainly found on coral patches with a large number of holes on the top of the coral patch and this tendency was mainly consistent during the study period. The volume of holes at the base of coral patches had also a positive effect on the abundance of newly settled juveniles in some cases. The results of the present study suggest that larval settlement has a strong seasonal and lunar periodicity, and newly settled juveniles select coral patches with available refuge spaces.

Timing of planulation by pocilloporid corals in the northwestern Philippines

We determined the lunar, seasonal, and diel timing of larval release in several species in the scleractinian family Pocilloporidae at Bolinao in the northwestern Philippines. All of the species exhibited remarkable lunar periodicity in planula release, with distinct timing in the lunar calendar. Despite confinement of peak larval release between the first quarter and full moons in 4 species (Pocillopora damicornis, P. verrucosa, Stylophora pistillata, and Seriatopora guttatus), only the 2 Pocillopora species experienced significant overlap in release times. Disparate lunar timing, on the other hand, was exhibited by the 3 Seriatopora species (new moon for S. caliendrum, last quarter moon for S. hystrix, and full moon for S. guttatus) during warm-dry months, although during seasons with low planulation rates the timing for the former 2 species seemed to overlap. Generally, lunar reproductive patterns in each species were seasonally consistent despite strong variations in larval output. The highest rates of planulation were recorded during the warm-dry months (March to May) and the lowest during the warm-wet months (June to October), except for P. damicornis, in which the lowest rate occurred during the cool-dry months (November to February). The timing of release in P. damicornis is mainly during the dark period of the diel cycle, with a peak at ca. 02:30 h. This report highlights the variation in timing of planulation among closely related coral species and compares temporal planulation data in the Philippines, which lies within the Indo-West Pacific center of coral diversity, to available data on brooding pocilloporid corals from other biogeographic regions.

Diurnality and nocturnality in nonhuman primates: comparative chronobiological studies in laboratory and nature

Looking for differences in circadian clock characteristics of diurnal and nocturnal nonhuman primates, this article summarizes results of chronobiological studies carried out in various nocturnal, diurnal, and cathemeral prosimian and anthropoid primate species under controlled laboratory conditions, under seminatural conditions, and in the wild. In almost all circadian parameters investigated, no differences were discernible between the two main chrono-ecotypes, either in circadian period length and the influence upon it of after-effects, of light intensity, and ambient temperature, or in the PRC, re-entrainment behavior, rhythm splitting, and internal desynchronization. Diurnal and nocturnal or cathemeral species differed only in the phase of artificial or natural LDs to which their circadian activity phase was adjusted as well as in the characteristics of masking activity upon the rhythms produced by the direct inhibiting or enhancing effects of light. Pronounced lunar periodicity—observed in the activity rhythm of nocturnal neotropical owl monkeys, genus Aotus, in seminatural and natural environments as well as in wild cathemeral Malagasy lemurs, genus Eulemur—is shown to result from masking effects of moonlight. In captive Eulemur fulvus albifrons, a change from dark-active over cathemeral to light-active behavior, without concurrently changing the circadian phase-setting of activity to D, was produced by direct masking effects of a stepwise reduction of darktime luminosity on an LD 12:12 cycle. Long-term activity recordings carried out in wild diurnal Malagasy sifakas (Propithecus verreauxi) and cathemeral redfronted lemurs (Eulemur fulvus rufus), as well as in wild nocturnal owl monkeys (Aotus a. azarai) of the North Argentinean Chaco, yielded in all species distinct bimodal long- and short-day activity patterns with pronounced peaks during dusk and dawn. Applying Pittendrigh's two-oscillator concept to these results, it is hypothesized that the differences in chrono-ecotype behavior may result from variations in internal coupling and external phase-setting of morning and evening oscillators (m, e) to dawn and dusk, interacting with direct masking effects of light.

Passive acoustic detection of grouper sound production

Passive acoustic recordings were used to study the behavior of red hind (Epinephelus guttatus) at spawning aggregation sites off of Puerto Rico and Mona Island, and goliath grouper (Epinephelus itajara) and red grouper (Epinephelus morio) on the West Florida Shelf. The sounds produced by each species were unique, low-frequency pulsed sounds and associated with reproductive-related behavior. Male red hind produced sounds composed of a series of pulses that graded into a tonal-like sound, mostly during territorial patrolling. Long-term acoustic recorder (LARS) data from the west coast of Puerto Rico and Mona Island showed similar diel periodicities of sound production of red hind, but had different monthly peaks in sound production. Goliath grouper sounds consisted of low-frequency individual pulses (50-100 Hz) that are consistent with sounds produced by a large fish, and showed lunar periodicity in sound production. Peaks in sound production occurred nightly after midnight, but sounds were also produced throughout the day. Sound production and spawning by red grouper was recorded using a remotely operated vehicle (ROV) at depths of 80-100 m. Passive acoustic techniques can provide synoptic, long-term time series of sound production associated with reproductive activities of soniferous species at widely spaced sites.

A Lunar Clock Changes Shielding Pigment Transparency in Larval Ocelli of Clunio marinus

Living in the tidal zones of the sea requires synchronization with the dominant environmental influences of tidal, solar, and lunar periodicity. Endogenous clocks anticipate those geoclimatic changes and control the respective rhythms of vital functions. But the underlying mechanisms are only partly understood. While the circadian clocks in animals are investigated employing neurobiological, molecular, and genetic approaches, clocks with a lunar periodicity have been studied with reference to development and behavior only. Sites of their pacemakers, zeitgeber receptors, and coupled endocrine components are unknown. Here, a lunar‐rhythmic change of shielding pigment transparency in the larval ocelli of the intertidal midge Clunio marinus is demonstrated for the first time as a possible access to the neurobiology of lunar timing mechanisms. We studied third instar larvae (Vigo strain) throughout the lunar cycle by light‐ and electron-microscopy as well as by x‐ray fluorescence analysis for the identification of the pigment. Moonlight detection is a prerequisite for photic synchronization of the lunar clock. The larval ocelli of Clunio putatively may function as moonlight receptors and are also controlled by the circalunar clock itself, hence being primary candidates for tracing input and output pathways of the lunar pacemaker. Additionally, the demonstration of a reversible optical change of shielding pigment transparency in Clunio is a novel finding, not reported so far in any other animal species, and reveals a mechanism to enhance photosensitivity under the condition of very dim light. It represents a remarkable change of a sense organ from an imaging device to a radiometer. Its restriction to the developmental stage susceptible to lunar timing elucidates a unique sensory strategy evolved at the level of sensory input. It also raises basic questions about the biochemistry of optically active pigments, like melanin, and their intracellular control.

Ammonoid growth rhythms

Determination of ammonite growth rate and longevity is an intriguing but difficult problem. Doguzhaeva (1982) made an exciting contribution through her study of ‘growth rings’ and their distribution on a variety of ammonite shells. She postulated a fortnightly or lunar monthly periodicity for chamber formation and a daily periodicity for growth line secretion on the outer shell. Before these suppositions become doctrine, however, a measure of skepticism seems warranted. Some of the relevant remarks run over familiar ground and were raised in response to Kahn & Pompea (1978), who assumed that growth increments on the outer shell of Nautilus are daily and septal deposition lunar monthly. Criticisms of their work focused on the nature of their data and the lack of a basis for the initial time assumptions (Jones & Thompson 1979; Saunders & Ward 1979). These criticisms apply to Doguzhaeva's study because her approach is similar and because Nautilus is the best living analog for ammonite growth.

Response of the larger protozooplankton to an iron-induced phytoplankton bloom in the Polar Frontal Zone of the Southern Ocean (EisenEx)

The responses of larger (>50 μm in diameter) protozooplankton groups to a phytoplankton bloom induced by in situ iron fertilization (EisenEx) in the Polar Frontal Zone (PFZ) of the Southern Ocean in austral spring are presented. During the 21 days of the experiment, samples were collected from seven discrete depths in the upper 150 m inside and outside the fertilized patch for the enumeration of acantharia, foraminifera, radiolaria, heliozoa, tintinnid ciliates and aplastidic thecate dinoflagellates. Inside the patch, acantharian numbers increased twofold, but only negligibly in surrounding waters. This finding is of major interest, since acantharia are suggested to be involved in the formation of barite (BaSO 4), a palaeoindicator of both ancient and modern high-productivity regimes. Foraminifera increased significantly in abundance inside and outside the fertilized patch. However, the marked increase of juveniles after a full-moon event suggests a lunar periodicity in the reproduction cycle of some foraminiferan species rather than a reproductive response to enhanced food availability. In contrast, adult radiolaria showed no clear trend during the experiment, but juveniles increased threefold, indicating elevated reproduction. Aplastidic thecate dinoflagellates almost doubled in numbers and biomass but also increased outside the patch. Tintinnid numbers decreased twofold, although biomass remained constant because of a shift in the size spectrum. Empty tintinnid loricae, however, increased by a factor of two, indicating that grazing pressure on this group mainly by copepods, intensified during EisenEx. The results show that iron-fertilization experiments can shed light on the biology and the role of these larger protists in pelagic ecosystem, which will improve their use as proxies in paleoceanography.

Reproductive periodicity and steroid hormone profiles in the sex-changing coral-reef fish, Plectropomus leopardus

The reproductive biology of coral trout, Plectropomus leopardus, from the Great Barrier Reef (Australia) was investigated by correlating gonadal condition with plasma levels of gonadal steroids. Female fish were found to be regressed from mid-summer to early spring, after which rapid and cyclical increases in gonado-somatic index (IG), maximum oocyte diameter (MOD) and plasma concentrations of estradiol-17β and testosterone were detected. Male fish, in contrast, commenced recrudescence slightly earlier in winter and responded with less dramatic increases in both IG and plasma concentrations of testosterone and 11-ketotestosterone. The mode of oocyte development was multiple group-synchronous, and cyclical fluctuations in reproductive parameters (IG, MOD and gonadal steroid concentrations) were synchronized with new-moon lunar phases. It is likely, therefore, that individual P. leopardus have the capacity to spawn on multiple occasions, with lunar periodicity. However, evidence suggests that early bouts of reproduction may be more important in terms of reproductive investment than subsequent bouts later in the same season. It is concluded that patterns of gametogenesis and steroidogenesis in P. leopardus are similar to the patterns displayed by other tropical groupers, suggesting that management regimes and propagation protocols developed for these fishes may also be appropriate for use with P. leopardus.

Semilunar spawning periodicity in brackish damsel Pomacentrus taeniometopon

Lunar-related spawning periodicity of the brackish damsel Pomacentrus taeniometopon was investigated by changes in gonadosomatic index (GSI) and ovarian histology. During the spawning season, GSI increased toward the week of the first and last quarter moon. Concomitant with increases in GSI, oocytes laden with yolk developed from the new/full moon to the first/last quarter moon. Postovulatory follicles appeared in the ovary around and after the first/last quarter moon. These results suggest that P. taeniometopon is a semilunar spawner and repeats spawnings twice a month with lunar periodicity during the spawning season. When the fish were reared under laboratory conditions without periodicity of tide, the spawning of P. taeniometopon occurred sporadically. It is likely that the fish uses tidal stimuli in the natural habitat to entrain reproductive activities.

Tree stems and tides – A new approach and elements of reflexion (reviewed paper)

In the context of chronobiological research on trees, a high-sensitivity device was developed to measure low-potential electric currents along the bole of two trees growing under open conditions. Rhythmic variations of the(bio-)electric potentials are found, linked on the one hand to daily photoperiods and on the other to lunar periodicities,depending on the physiological phase of the trees.

Spawning events in small and large populations of the green sea urchin Strongylocentrotus droebachiensis as recorded using fertilization assays

During the winter and spring of 2002 and 2003, we used time-integrated fertilization assays to monitor sperm availability in three populations of the green sea urchin Strongylocentrotus droebachiensis in Maine: a naturally occurring population of >40,000 urchins and two smaller groups (<1,000) of transplanted urchins isolated from other aggregations. Episodes of sperm release coincided in two populations 10 km apart, suggesting that urchins were responding to a widespread environmental signal. We observed significant lunar periodicity in sperm release events for both of these populations. However, extensive spawning as shown by fertilization rates near 100% and a dramatic drop in gonad mass only occurred in the large natural population around the onset of thermal stratification and the spring phytoplankton bloom. By contrast, in the two small populations we observed low fertilization rates and little or no change in gonad mass. We speculate that a subset of males in these populations responded to a common external spawning signal, but that mass spawning is more likely to occur in large, dense populations where sperm concentrations reach high enough levels to trigger spawning in less responsive urchins.

Lunar periodicity of planula release in the reef-building coral Stylophora pistillata

Stylophora pistillata is a dominant stony coral on reefs in the Red Sea, but the levels and periodicity of planula release in this coral are not well understood. We examined patterns of planula release by colonies under laboratory conditions in outdoor tanks at Eilat during 1998, then tagged and returned the corals to the adjacent reef. In 2003, we re-collected them and re-estimated their planula release patterns. In both years, the number of planula larvae released per night varied widely between colonies, and did not correlate with coral colony volume or diameter. Planula release rate per live coral volume was 5.6-fold lower in 2003 than in 1998, while coral volume increased 5.5-fold during this period. In both years, colonies of S. pistillata released planula larvae on a lunar cycle dur- ing the 4 mo of peak planulation (March to June). Peak release was on Night 6 following the full moon each month during 1998 and on Night 2 during 2003, with most planulation occurring between Nights 1 and 12. Collection of released planulae from randomly selected colonies of S. pistillata in the field during both years revealed the same lunar cycle of planula release as under laboratory condi- tions. In field colonies, the number of planulae released per coral was 3-fold lower in 2003 than in 1998. The observed reduction in planula release between years in the field parallels documented declines in coral recruitment and reef growth at Eilat, and may have resulted, in part, from anthro- pogenic impacts to local reefs. Added effects of coral aging in tagged experimental colonies may have caused the larger observed reduction in planula release observed under laboratory conditions. The proximate factors that regulate the above lunar periodicity of planulation are thought to include night irradiance patterns and tidal cycles, which also may be linked to gametogenesis cycles. Lunar periodicity ultimately may have developed to enhance the dispersal of released propagules during neap or spring tides, or to maximize fertilization of gametes through tight synchronization of coral reproduction among colonies.

Annual cycle of clupeiform larvae around Gran Canaria Island, Canary Islands

AbstractThe distribution and abundance of fish larvae was studied along the eastern and southern shelf of Gran Canaria Island (Canary Islands) from July 2000 to June 2001. Oblique bongo hauls were carried out fortnightly during the daytime, coinciding with days of full and new moon. During February, the area was sampled every 2–5 days. About 17.3% of the ichthyoplanktonic community was composed of clupeiform larvae: 92.9% of these larvae were Sardinella aurita, whereas 4.7% and 2.4% were respectively Engraulis encrasicolus and Sardina pilchardus. Sardinella aurita larvae appeared during the whole year with two periods of maximum abundance: June to September and December to February. During the full moon their abundance was on average 38.5% (±6.8%) of their numbers during the new moon, showing a clear lunar periodicity. Engraulis encrasicolus larvae appeared from November to March, also coinciding with the new moon. Sardina pilchardus larvae only appeared during two short periods, both coinciding with filaments shed from the African coastal upwelling which reached the island. This fact confirms the transport of fish larvae from the upwelling area off northwest Africa to the Canary Islands, promoting a genetic flow among both sites.