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Sexual Satellites, Moonlight and the Nuptial Dances of Worms: The Influence of the Moon on the Reproduction of Marine Animals
Abstract
The evidence that the moon has a profound effect on the timing of reproductive activities of marine animals is compelling. Some moon phase related spawning events are revealed by the constant phase relationship between the timing of once per year spawning events and the lunar phase as in the highly synchronised breeding of the palolo worm Palola viridis and the Japanese crinoid Comanthus japonicus In other cases there is a repeated lunar cycle of reproductive activity and again the marine worms provide many good examples. The breeding of the palolo worm involves the highly synchronised release of what are in effect detached sexual satellites and the timing of this has annual (solar year), lunar, daily and tidal rhythm components. In a similar way, the onset of sexual maturation and participation in the nuptial dance of Platynereis dumerilli has strong lunar components. Sexual reproduction is the culmination of a process of sexual maturation that takes many months for completion and the mechanisms by which moon phase relationships are imposed on this process must have been selected for by mechanisms relating to reproductive success. The polychaetes provide excellent models for investigation of both the selective advantage and the physiological processes involved in reproductive synchrony. We have recently shown that the spawning of the lugworm Arenicola marina has lunar components and we conclude that an interaction between solar and lunar signals is widespread in the timing of reproduction in marine animals. Carl Hauenschild was the first to demonstrate the existence of a free-running circa-lunar rhythm in marine animals using captive populations of Platynereis dumerilli His experiments also provided clear evidence for the influence of moonlight (light at night) as the zeitgeber for this rhythm. This implies a high level of sensitivity to light, and the operation of appropriate endogenous biological rhythms. Using Nereis virens we have demonstrated a high level of sensitivity to low intensity solar light signals in relation to rhythmic processes with the properties similar to the circadian and photoperiodic mechanisms of terrestrial organisms. The spawning of N. virens is also believed to have lunar components reflecting the complex influences of the sun and the moon in the marine domain, where influences of the moon and sun are more equal. We suggest that evolution of biological rhythmicity that can be entrained to either lunar or solar systems arose in the marine domain. Recent advances in understanding the molecular components of the circadian clock system suggest that a search for a common molecular mechanism for both lunar and solar related biological rhythms in marine organisms might be very fruitful.
... As yet an alternative reproductive strategy, stolonization has evolved in non-nereidid polychaetes and can be regarded as a special case of epitoky. This mode of reproduction avoids the risk of losing the reproductive potential by predation before the spawning event (Fischer, 1999): only the posterior part of the animal transforms into an epitokous form containing ripe gametes, detaches from the atokous anterior part and enters a short pelagic phase as "sexual satellite" (Bentley et al., 2001). The autotomized segments start swarming on their own and carry out reproduction, while the anterior atokous part of the animal starts regenerating the lost segments and produces new epitokous stolons at the next spawning period. ...
... The autotomized segments start swarming on their own and carry out reproduction, while the anterior atokous part of the animal starts regenerating the lost segments and produces new epitokous stolons at the next spawning period. The most famous example is the Palolo worm Palola (Eunice) viridis (Gray, 1847;Hauenschild et al., 1968) whose breeding is highly synchronized and has annual, lunar, daily, and tidal rhythm components (Bentley et al., 2001). Stolonization is also common in the Syllidae (for a review, see Franke, 1999). ...
... Other polychaetes (many syllids) form epitokous stolons through schizogamy, where only the posterior body is modified to produce an epitoke (Nygren 1999;Rouse & Pleijel 2001). Synchronized spawning is thought to maximize the likelihood of fertilization for broadcast swarmers (Rouse & Pleijel 2001), and for many epitokous polychaetes, the precise synchronization of swarming and spawning is linked to specific lunar phases (Aiyar & Panikkar 1937;Clark 1961;Wilson 1991;Bentley et al. 1999). ...
... For over a century, there have been many accounts in the polychaete literature of nocturnally swarming polychaetes, especially those forming large epitokal swarms comprised of species from the families Eunicidae, Nereididae, and Syllidae (Browne 1900;Horst 1904;Mayer 1908;Moore 1908;Clark 1961;Bentley et al. 1999;Pamungkas and Glasby 2015). Epitokes have also been recorded in the families Amphinomidae, Dorvilleidae, Glyceridae, Goniadidae, Ophelleidae, Phyllodocidae, and Scalibregmatidae (Chamberlain 1919;Allen 1957;Clark 1954;Glasby et al. 2000;Pleijel & Rouse 2006). ...
Nocturnally swarming polychaetes were sampled over a ten-year period (2007–2017) in shallow waters of the Virgin Islands National Park, St. John, United States Virgin Islands. While sampling was qualitative and conducted over different years, months and lunar phases, some patterns were noted in the emergence of swarming polychaetes. Three families (Nereididae, Opheliidae, and Syllidae) had members that swarmed on most nights, while reproductive epitokes from two families appeared only during specific lunar phases: Goniadidae around the full moon and Phyllodocidae around the new moon. Additional polychaete families represented included Amphinomidae, Dorvilleidae, and Scalibregmatidae, whose members swarmed during the waning or waxing lunar phases. This overview offers new information about the timing of reproductive swarming in Caribbean polychaetes and suggests some connections between lunar phases and the swarming of different families.
... sekitar pukul 04.00-05.00. Pengamatan terhadap beberapa spesies cacing laut seperti Palolo viridis, Comanthus japonicus dan Platynereis dumerilli menunjukkan bahwa pergerakan ini memiliki korelasi yang kuat dengan cahaya berintensitas rendah yang berasal dari pergantian fase bulan (Bentley et al., 1999). Terhadap cacing laut Platynereis dumerii, Zantke et al. (2013) menemukan bahwa terdapat gengen yang berperan dalam mengatur ritme sikardian seperti ini di antaranya: clock, period, pdp1, dan timeless yang terlokalisasi pada bagian otak depannya (forebrain). ...
Nusa Tenggara Timur (NTT) merupakan salah satu provinsi kepulauan di Indonesia yang menyimpan kekayaan alam dan potensi pariwisata yang tak kalah luar biasa eksotismenya. Salah satu potensi alam biotik yang unik di daerah ini adalah cacing laut Nyale yang terdapat di perairan kabupaten Sumba Barat. Cacing ini memiliki keunikan tersendiri karena memiliki tampilan morfologis yang berwarna-warni serta hanya muncul ke permukaan air sekali dalam setahun. Secara budaya, kemunculannya di perairan pesisir pantai ini harus diikuti pula oleh suatu ritual yang dipimpin oleh para ketua adat yang disebut Rato dan menjadi salah satu atraksi wisata yang menarik banyak wisatawan baik dalam maupun luar negeri. Cacing ini juga dimanfaatkan oleh masyarakat lokal baik sebagai pangan maupun obat. Akan tetapi, kajian ilmiah terhadap cacing laut yang berada di daerah ini masih sangat minim dilakukan khususnya terkait analisis kandungan nutrisinya. Dalam penelitian ini, sampel cacing Nyale diambil dari perairan pantai Wanokaka pada bulan Maret 2022 dan dilanjutkan ke analisis proksimat. Parameter yang diukur adalah kadar air, kadar abu, protein kasar, lemak kasar, serat kasar, BETN dan aktivitas antioksidan. Hasil analisis memperoleh kadarnya secara berturut-turut adalah 6.22%, 10.41%, 52.34%, 9.61%, 0.51%, 27.13% dan 53.59%. Hasil ini menunjukkan bahwa cacing ini dapat dijadikan sebagai pangan alternatif bersumber protein yang dapat menggantikan sumber-sumber protein lainnya seperti ikan, daging, telur, tahu dan tempe. Diharapkan hasil dari penelitian ini dapat semakin memberikan informasi-informasi baru terkait cacing ini yang dapat membantu peningkatan aspek pendidikan, riset/penelitian, pariwisata, pangan & nutrisi, serta konservasi & pelestarian lingkungan terkhususnya di daerah kabupaten Sumba Barat, NTT.
... Moonlight cycles entrain spawning synchronization [12][13][14] . ALAN from coastal developments disrupts these cycles presenting a potential threat to coral reproduction 15 . ...
Coral broadcast spawning events - in which gametes are released on certain nights predictably in relation to lunar cycles - are critical to the maintenance and recovery of coral reefs following mass mortality. Artificial light at night (ALAN) from coastal and offshore developments threatens coral reef health by masking natural light:dark cycles that synchronize broadcast spawning. Using a recently published atlas of underwater light pollution, we analyze a global dataset of 2135 spawning observations from the 21st century. For the majority of genera, corals exposed to light pollution are spawning between one and three days closer to the full moon compared to those on unlit reefs. ALAN possibly advances the trigger for spawning by creating a perceived period of minimum illuminance between sunset and moonrise on nights following the full moon. Advancing the timing of mass spawning could decrease the probability of gamete fertilization and survival, with clear implications for ecological processes involved in the resilience of reef systems.
... Additionally, circalunar clocks synchronize reproduction within a population, maximizing the chances of successful fertilization. This aspect is most important for broadcast spawners, which release their gametes into the open water (e.g., corals [27] or annelids [28] ). Particularly in tropical oceans, with no seasonality to synchronize reproduction, lunar rhythms are very common. ...
Circalunar clocks, which allow organisms to time reproduction to lunar phase, have been experimentally proven but are still not understood at the molecular level. Currently, a new generation of researchers with new tools is setting out to fill this gap. Our essay provides an overview of classic experiments on circalunar clocks. From the unpublished work of the late D. Neumann we also present a novel phase response curve for a circalunar clock. These experiments highlight avenues for molecular work and call for rigor in setting up and analyzing the logistically complex experiments on circalunar clocks. Re-evaluating classic experiments, we propose that (1) circalunar clocks in different organisms will have divergent mechanisms and physiological bases, (2) they may have properties very different from the well-studied circadian clocks and (3) they may have close mechanistic and molecular relations to seasonal rhythms and diapause.
... Platynereis' life cycle exhibits several interesting features and encompasses three phases separated by metamorphosis events (Fischer and Dorresteijn 2004) (Figure 13.2). Like many other marine animals, such as corals, sea urchins and even fishes, Platynereis sexual maturation and reproduction are synchronized with the natural moon phases (Bentley et al. 1999). This fascinating biological characteristic of lunar-controlled reproductive periodicity, regulated thanks to an endogenous oscillator, is called a circalunar life cycle (Tessmar- Raible et al. 2011;Raible et al. 2017). ...
... It has been suggested that spawning activities in many jellyfish species are inherently linked to diel periodicity of light (Purcell & Madin, 1991;. The moon light intensity has also been reported to have an impact on the spawning of fish (Horký et al., 2006;Ikegami et al., 2014;Krumme et al., 2015), invertebrates (Nascimento et al., 1991;Bentley et al., 1999;Camargo et al., 2002) and local shrimp species (Ramarn et al., 2014). ...
Jellyfish or scyphozoan blooms are known to negatively impact human welfare. However, there is a lack of baseline ecological data or knowledge regarding the scyphozoans in Malaysia which could be used to mitigate these impacts, as well as effectively exploit and manage a fast-growing fishery. Thus, the overall aim of the present study is to verify the scyphozoan diversity in Malaysian waters, and specifically, to explicate the environment, biology and ecological role of the scyphozoans in Klang Strait. The study was conducted via a nation-wide survey of 15 sites in Peninsular Malaysia (January 2011 – June 2015) based on opportunistic samplings, and a monthly sampling regime supplemented with intensive diel (24-hr) and lunar-phase samplings by using commercial bag nets in the Klang Strait. Additional samples examined from May 2010 to December 2010 were part of Dr. Mohammed Rizman Idid’s scientific collection. Scyphozoan abundance, population growth and mortality, reproduction and trophodynamics were investigated. To date, a total of 20 species of scyphozoans in Malaysian waters has been verified. Conjoint or co-occurring mangrove-mudflat habitats have the highest species richness (9 species) among the various coastal habitats in Peninsular Malaysia. The Klang Strait’s mangrove-mudflat habitat is represented by eight species. The overall scyphozoan abundance in the area tends to be higher during the wetter northeast monsoon (heavy rainfall), but decreases during the drier southwest monsoon (less rainfall). The temporal variability in scyphozoan abundance is subjected to the local hydrological regime (salinity, dissolved oxygen, temperature, turbidity and pH) that varied with the regional meteorological events (monsoon and rainfall pattern). During the rainy or wet period, scyphozoan abundances across the water column are generally higher during the daytime than at night. There is evidence of flood-tide horizontal transport of scyphozoan especially by the swift currents during spring tide. Following their ingression into the nearshore areas, some species may actively swim against the offshore ebb current or engage in vertical migration to maintain their position and form aggregations near coastlines. The population of Phyllorhiza punctata and Cyanea sp. (the dominant species) in the Klang Strait perform continuous spawnings and juvenile (medusa) recruitments throughout the year, with one or two peaks observed during the northeast and southwest monsoon. The parameters (K and Loo) of the von Bertalanffy Growth Function and total mortality estimated using the software for both P. punctata and Cyanea sp. are generally similar with that of other scyphozoan populations, although the estimated lifespans of these two species (40 and 32 months, respectively) appear to be greater than that of temperate species. Scyphozoan species in the Klang Strait are zooplankton predators. They can be grouped as specialized copepod feeders (P. punctata, Rhopilema esculentum, Lychnorhiza malayensis, Rhopilema hispidum), copepod and macrozooplankton feeder (Cyanea sp.) and mixed plankton feeder (Lobonemoides robustus). Stable isotope analysis indicates that the scyphozoans mainly derive their primary or basal carbon source from microphytobenthos (65%) and phytoplankton (32%) with little from mangrove (4%). The scyphozoan fauna thus play an important ecological role in the transfer of trophic energy and materials from the benthos to pelagic water, as well as from nearshore to offshore waters.
... Environmental factors play a critical role in regulating both sexual and asexual reproduction for many marine invertebrates (Yamahira, 2004;Naylor, 2013). Temperature changes have been shown to trigger gametogenesis and to induce asexual events in widespread taxa (Sastry, 1966;Beauchamp, 1992;Olive et al., 1998;Ettinger-Epstein et al., 2007;Cardone et al., 2010;Epherra et al., 2015), and lunar cycles have been linked to spawning activities for many organisms (Fromont and Bergquist, 1994;Tanner, 1996;Bentley et al., 2001;Mercier et al., 2011). Nutrient availability has also been positively correlated with gametic and larval density (Thompson, 1983;Snell, 1986;Bronstein and Loya, 2015), as sexual reproduction requires an organism to have energy available for gamete production and, particularly, yolk investment to oocytes (vitellogenesis). ...
Marine organisms that rely on environmental cues for reproduction are likely to experience shifts in reproductive phenology and output due to global climate change. To assess the role that the environment may play in the reproductive timing for temperate sponges, this study examined sexual and asexual reproduction in New Zealand sponge species (Tethya bergquistae and the Tethya burtoni complex) and correlated reproductive output with temperature, chlorophyll-a concentration, and rainfall. Histological analyses of sponges collected monthly (from February 2015 to February 2017) revealed that these sponges are oviparous and gonochoristic and that they sexually reproduce annually during the austral summer. Both monthly collections and in situ monitoring revealed that Tethya spp. asexually bud continuously, but with greater intensity in the austral spring and summer. Temperature was positively associated with both sexual reproduction and budding, with seasonal cues appearing important. Future shifts in the environment that alter such cues are expected to affect population dynamics of these sponges.
Population blooms of scyphozoan jellyfish in tropical shallow water regions can fuel localized fisheries but also negatively impact human welfare. However, there is a lack of baseline ecological data regarding the scyphozoans in the region, which could be used to manage a fast-growing fishery and mitigate potential impacts. Thus, this study aims to investigate the temporal factors driving the distribution of scyphozoan community along the environmental gradients under different monsoon seasons, rainfall periods, moon phases, and diel-tidal conditions in the Klang Strait located in the central region along the west coast of Peninsular Malaysia, where bloom events are increasing. Scyphozoan samples were collected using commercial bag nets during a 19-month survey. Temporal variations in species abundance and composition were evident and related to the local environmental parameters (salinity, dissolved oxygen, temperature, turbidity, and pH) that varied with the regional monsoon events, although these effects appeared to be species-specific. Phyllorhiza punctata, Acromitus flagellatus, Lychnorhiza malayensis, and Rhopilema esculentum were more abundant during the wetter northeast monsoon (NEM) while the abundance of Chrysaora chinensis and Lobonemoides robustus increased during the drier southwest monsoon (SWM). During the wet period of NEM, scyphozoan abundance was generally higher during the daytime than night-time. The regional monsoon regime and local hydrological events account for jellyfish abundance in the nearshore area with concurrent threats to coastal tourism and power plants, as well as benefits to fisheries especially during the NEM.
Life on earth has evolved under constant environmental changes; in response to these changes, most organisms have developed an endogenous clock that allows them to anticipate daily and seasonal changes and adapt their biology accordingly. Light cycles synchronize biological rhythms and are controlled by an endogenous clock that is entrained by environmental cues. Light is known to play a key role in the biology of symbiotic corals as they exhibit many biological processes entrained by daily light patterns. In this study, we aimed at determining the effect of constant dim light on coral's perception of diel and monthly cycles. Our results show that under constant dim light corals display a loss of rhythmic processes and constant stimuli by light, which initiates signal transduction that results in an abnormal cell cycle, cell proliferation, and protein synthesis. The results emphasize how constant dim light can mask the biological clock of Acropora digitifera.
In many marine invertebrates, such as the nereid polychaetes, sex pheromones ensure the coordinated release of gametes by both sexual partners. The question of species-specificity of chemical cues and the scale of their distribution in the marine environment evolves when one considers the wide overlap in multispecies and multiphyla spawning. Behavioural and electrophysiological assays with several nereid species, such as Platynereis dumerilii, Nereis succinea, N. virens and N, japonica, confirm the existence of heterospecific activity of coelomic fluid. The nuptial dance, as well as the release of gametes, are elicited when individuals are exposed to coelomic fluid of another nereid species. We, therefore, discuss the function of sex pheromones in nereid polychaetes and their role in the timing of reproduction in relation to other environmental cues.
The senior author has used the eggs of the pelagic form of Nereis limbata in studies on fertilization for several years. During the seasons of 1911 and 1912 collections were made each night by the junior author, and records were kept which reveal considerable uniformity in swarming periods in accordance with the phases of the moon. In addition advantage was taken of the opportunity to study certain other features of breeding behavior. These observations are brought together in a paper partly for the sake of such general interest as they may possess and partly for the information of those who may have occasion to use this form for investigations. The animals may be taken after sunset on certain nights, in general during the â€oe¿¿ dark of the moon,†• in the months of June, July, August and September. They appear swimming near the surface of the water very soon after sunset, and may be attracted by the light of a lantern and readily caught with a small hand net. The swarming usually begins with the appear ance of a few males, readily distinguished by their bright red' anterior segments and white sexual segments, darting rapidly through the water in curved paths in and out of the circle of light cast by the lantern. The much larger females then begin to appear, usually in smaller numbers, swimming laboriously through the water. Both sexes rapidly increase in numbers during the next fifteen minutes,' and in the case of a large swami there may be hundreds of males in sight at one time, though the number of females to be seen at one time rarely exceeds ten or a dozen.' In about 45 minutes the numbers begin to decrease andi 1 At the height of some runs, as for instance, on the evenings of June 12, July 5 to 8, and August 6â€"io. 1912 (see curves 6. 7 and z). great numbers of females. appeared. On one occasion at least a liter of females was secured in ten minutes, several being caught with each sweep of the net. Within the circle of the light on. such nights as many as fifty females may be seen at once.
The reproductive cycles of the majority of marine invertebrates are strongly seasonal with highly synchronised patterns of spawning. It has become accepted that a distinction can be made between proximate factors and ultimate factors in the causation of seasonal reproduction. We briefly review these concepts and the hypotheses that have been developed about the nature of the ultimate factors that cause the fitness benefit and that 'explain' the adaptive significance of seasonal reproduction. We use a model based on the life history of the polychaete Nereis virens and demonstrate that seasonal reproduction may have impacts on adult components of fitness (i.e. reproductive value at age of first maturity), as well as on fertilisation rate and survival to age at first maturity. The results are discussed in the context of the programme PNDR and the related UK Natural Environment Research Council thematic programme 'Developmental Physiology of Marine Organisms (NERC-DEMA). (C) 2000 Ifremer/CNRS/IRD/Editions scientifiques et medicales Elsevier SAS.
The relationship between the phase of the moon and the emergence of the epitokous segments of the palolo worm Eunice viridis Gray has been known to the natives of the Samoan Islands for centuries. They predict the date and time of day when the emergence occurs so that they can be ready to catch the worms. This phenomenon is one of the best known examples of lunar periodicity. It was first described scientifically at the end of the last century. My own investigations concern the occurrence of the worms in the reef, in which they gnaw long tunnels through the massive blocks of coral limestone at levels characterized by the occurrence of symbiotic algae. Apparently the algae are the main sources of nutrition for the worms. The casting off of the epitokous segments occurs at the third quarter of the moon in October or November. An analysis of known dates on which the swarms of worms have appeared permitted a precise method of prediction to be formulated. The causality of this periodicity is discussed.