Predictable and unpredictable spawning events: in situ behavioural data from free-spawning coral reef invertebrates

Summary

We describe the spawning behaviour and some aspects of spawning periodicity in a diverse group of marine invertebrates, principally echinoderms, but including sponges, anthozoans, molluscs, and polychaetes. Our observations were made both opportunistically and on a systematic basis between 1978 and 1992 on the central and northern Great Barrier Reef. Spawning was predictable in some of the species observed, for example Bohadschia argus, Euapta godeffroyi, and Stichopus variegatus (Holothuroidea), which exhibited regular lunar and diel periodicity. Others, such as Holothuria coluber, Actinopyga lecanora, and Bohadschia graffei (Holothuroidea), Acanthaster planei (Asteroidea), Hyotissa hyotis and Arca spp. (Bivalvia) exhibited no clear lunar or diel periodicity in spawning behaviour. Mass heterospecific spawnings which involved several species, often from different phyla, were commonly observed. The species participating were usually those with unpredictable spawning patterns and while the species involved were diverse there were also occasions when spawning involved species from the same genera. Fertilization rates were measured in situ for the predictable spawner Bohadschia argus and were found to vary between 0–96% depending on the circumstances of the spawnings. Fertilization rates for the unpredictable spawners showed similar variability; Holothuria coluber and Actinopyga lecanora ranged from 9–83%.     

Timing matters: species‐specific interactions between spawning time,substrate quality,and recruitment success in three salmonid species

Substratum quality and oxygen supply to the interstitial zone are crucial for the reproductive success of salmonid fishes. At present, degradation of spawning grounds due to fine sediment deposition and colmation are recognized as main factors for reproductive failure. In addition, changes in water temperatures due to climate change, damming, and cooling water inlets are predicted to reduce hatching success. We tested the hypothesis that the biological effects of habitat degradation depend strongly on the species‐specific spawning seasons and life‐history strategies (e.g., fall‐ vs. spring‐spawners, migratory vs. resident species) and assessed temperature as an important species‐specific factor for hatching success within river substratum. We studied the species‐specific differences in their responses to such disturbances using egg‐to‐fry survival of Danube Salmon (Hucho hucho), resident brown trout (Salmo trutta fario), and migratory brown trout (Salmo trutta lacustris) as biological endpoint. The egg incubation and hatching success of the salmonids and their dependence on temperature and stream substratum quality were compared. Hatching rates of Danube salmon were lower than of brown trout, probably due to higher oxygen demands and increased interstitial respiration in spring. Increases in maximum water temperature reduced hatching rates of resident and migratory brown trout (both fall‐spawners) but were positively correlated with hatching rates of Danube salmon (a spring‐spawner). Significantly longer incubation periods of resident and migratory brown trout coincided with relatively low stream substratum quality at the end of the egg incubation. Danube salmon seem to avoid low oxygen concentrations in the hyporheic zone by faster egg development favored by higher water temperatures. Consequently, the prediction of effects of temperature changes and altered stream substratum properties on gravel‐spawning fishes and biological communities should consider the observed species‐specific variances in life‐history strategies to increase conservation success.     

The effect of nicotine on sperm-Egg interaction in the sea urchin: Polyspermy and electrical events

We have studied some of the effects of nicotine on sea urchin eggs, spermatozoa, and their interaction using electrical recording techniques and fertilization-rate experiments. Pretreating eggs with nicotine enhances the fertilization rate, whereas this drug has an inhibitory effect on spermatozoa. Pulse-treated eggs or eggs fertilized in the presence of nicotine give rise to attenuated step depolarizations, which may be attributed to a decrease in membrane resistance (Rm) of the egg or, in the latter case, to an alteration to the spermatozoon. Concurrently, with the change in the step depolarization there is a reduction in amplitude of the fertilization potential (FP) suggesting that the cortical reaction is in some way altered. Nicotine has no effect on the Rm of fertilized eggs or oocytes, where there are no cortical granules. We suggest that nicotine alters the cortex of sea urchin eggs–possibly by causing a partial dissolution of cortical granules–which renders the eggs more receptive to spermatozoa. The reductions in amplitude of the step depolarization and the FP are consequences of this alteration.     

Multiple spawning in several commercial fish species and its consequences for fisheries management, cultivation and experimentation

The strategy of multiple spawning is examined in several commercially important species—in particular turbot, Scophthalmus maximus (L.); halibut, Hippoglossus hippoglossus (L.); cod, Gadus morhua L.; and northern anchovy, Engraulis mordax Girard. Aspects of special relevance to fishery science and commercial and experimental cultivation are discussed. These include changes in batch fecundity and egg size as the spawning season progresses; the timing and methodology of fecundity estimations; ovulatory/spawning rhythms; the effect of temperature on the ageing rate of retained ovulated oocytes and the interovulatory period; ovulation prediction in hand-stripped broodstocks to facilitate the collection of good quality, freshly ovulated eggs, and the effect of maternal stress on the ovulatory/spawning rhythm. The implications of these phenomena are discussed in terms of recommended practices for the culturist, experimentalist and fisheries scientist.     

Migration and spawning energetics of the anadromous sea lamprey,Petromyzon marinus

Synopsis Energy expended in migration and reproduction was determined from measurements of caloric concentration and body and gonodal weight for nontrophic sea lampreys collected from different sites along the St. John River, New Brunswick. The estimated cost of locomotion in swimming the 140 km which separates the estuary from the spawning redds was 300 and 260 kcal for males and females respectively. Acutal distance which lampreys swam as well as mean swimming speed were estimated from a linear regression equation relating energy expenditure for locomotion and body weight. Energy expenditure for breeding was considerably greater than that catabolized throughout the upstream migration.     

Monogamy,spawning and skin-shedding of the sea moth,Eurypegasus draconis (Pisces: Pegasidae)

Synopsis The Red Sea seamoth, Eurypegasus draconis, has a social structure that involves close pair-bonding with a monogamous mating system. The occurrence of 61 specimens, 95.1% paired, were recorded in the Gulf of Aqaba, during summers 1989 and 1990. Fourteen pairs were tagged and seven of them were seen again at least once. Cumulative location maps for tagged individuals showed that they were not territorial or site-attached, home ranges of pairs overlapped, they had low mobility, and occurred in low densities. Dissections and histological analyses showed that pairs (n = 12) were heterosexual and all individuals were sexually mature. E. draconis is sexually dimorphic. Females (n = 13) have significantly larger carapace volumes than males (n = 13). In aquaria, pairs spawned repetitively at dusk. At the peak of a spawning rise they released pelagic eggs from which embryos hatched in 24–29h at 27.2°C. Unpaired individuals probably have little opportunity to meet and mate. Close pair-bonding that ensures the availability of a mate, probably evolved as a style for increasing reproductive success in these small fish that occur in low density. E. draconis sheds its skin in one piece every 1 to 5 days.     

Distribution of Nephrops norvegicus (L.) larvae in the western Irish Sea: an example of advective control on recruitment

Results of a survey of Nephrops norvegicus larvae conductedin the western Irish Sea during May 1984 are discussed. Thelarval distributions show a pronounced tongue of high numbersextending southward from the muddy area where they are hatched.The inferred density-driven circulation at the time of the surveyis consistent with the southward transport of larvae. BecauseN.norvegicus requires a muddy substrate for successful larvalsettlement, the processes which influence the circulation mayprovide an important control on the level of recruitment.     

Study of the spawning area of the Northern anchovy in the Gulf of California from 1990 to 1994, using satellite images of sea surface temperatures

The influence of the water temperature on the distribution andabundance of eggs of the Northern anchovy in the Gulf of Californiawas analyzed. Data on sea surface temperatures (SST) were combinedwith the analyses of patterns of eggs of plankton collectedon the five cruises carried out from 1990 through 1994, duringthe spawning season of the Northern anchovy. The principal spawningarea of this species is between the northern point of Angelde la Guards Island and     

Extreme temperatures,foundation species,and abrupt ecosystem change: an example from an iconic seagrass ecosystem

Extreme climatic events can trigger abrupt and often lasting change in ecosystems via the reduction or elimination of foundation (i.e., habitat‐forming) species. However, while the frequency/intensity of extreme events is predicted to increase under climate change, the impact of these events on many foundation species and the ecosystems they support remains poorly understood. Here, we use the iconic seagrass meadows of Shark Bay, Western Australia – a relatively pristine subtropical embayment whose dominant, canopy‐forming seagrass, Amphibolis antarctica, is a temperate species growing near its low‐latitude range limit – as a model system to investigate the impacts of extreme temperatures on ecosystems supported by thermally sensitive foundation species in a changing climate. Following an unprecedented marine heat wave in late summer 2010/11, A. antarctica experienced catastrophic (>90%) dieback in several regions of Shark Bay. Animal‐borne video footage taken from the perspective of resident, seagrass‐associated megafauna (sea turtles) revealed severe habitat degradation after the event compared with a decade earlier. This reduction in habitat quality corresponded with a decline in the health status of largely herbivorous green turtles (Chelonia mydas) in the 2 years following the heat wave, providing evidence of long‐term, community‐level impacts of the event. Based on these findings, and similar examples from diverse ecosystems, we argue that a generalized framework for assessing the vulnerability of ecosystems to abrupt change associated with the loss of foundation species is needed to accurately predict ecosystem trajectories in a changing climate. This includes seagrass meadows, which have received relatively little attention in this context. Novel research and monitoring methods, such as the analysis of habitat and environmental data from animal‐borne video and data‐logging systems, can make an important contribution to this framework.     

Reproduction and recruitment of sympatric fish species on an intertidal rocky shore

The reproductive cycle of seven common species (Gobius paganellus, Gobius bucchichi, Gobius cobitis, Parablennius sanguinolentus, Salaria pavo, Tripterygion tartessicum and Symphodus roissali) on rocky shores in the Gulf of Cadiz and their relationship with the sea surface temperature (SST) is analysed. Partial data on Scorpaena porcus are also given. Fecundity of these short lifespan species shows a positive linear correlation between the number of oocytes and an increase in female size. Spawnings are concentrated in the first 7 months of the year. An analysis of reproductive growth with respect to SST shows that water temperature in the winter months affects the timing of the onset of reproduction in most species. Recruitment is takes place throughout the year, but a temporal segregation within different families occurs in their spawning as well as recruitment.     

The effect of flooding on the recruitment of reed marsh and tall forb plant species

Recruitment of plant species in wetlands dominated by Phragmites australis often results in a zonation of two vegetation types. A development of reed marshes takes place in the shallow flooded parts where the dominant P. australis becomes accompanied by interstitial marsh species. The vegetation on higher elevations becomes dominated by tall forbs. We investigated whether this zonation is related to the effects of flooding on the recruitment of component species of both vegetation types. All but one species had maximum germination at field capacity and germination was strongly reduced in drier soils and flooded soils. Nearly all seedlings of reed marsh species, irrespective of whether they initially supported two or six true leaves, survived eight weeks of total inundation. Survival of tall forbs was however significantly decreased by inundation. At both seedling stages a considerable number of Cirsium arvense lost their leaves when submerged, but all plants were able to recover when drained. Eupatorium cannabinum suffered extra mortality when transferred from flooded to drained conditions, whereas only young seedlings of Epilobium hirsutum died. Of all investigated species E. hirsutum was the only one with a significantly increased stem length after one week of submergence. Root porosities did not differ between reed marsh species and tall forbs but stem porosities of the reed marsh species Mentha aquatica and Lycopus europaeus were significantly higher than those of the tall forbs C. arvense and E. cannabinum. It was concluded that both reed marsh species and tall forbs require lowered water levels for germination. Flooding during the seedling stage will assign species to their position on the elevation gradient. Reed marsh species establish at lower elevations because they are best able to survive flooding and because their higher stem porosities allows them to withstand higher levels of partial submergence.     

Coral spawning in the western Pacific Ocean is related to solar insolation: evidence of multiple spawning events in Palau

Coral reproductive schedules have long been related to concomitant increases in regional sea surface temperature (SST). Yet, corals also mass spawn in the tropics, where SSTs vary little throughout the year. Here we show that the rise toward and fall from solar insolation maxima, which is the electromagnetic energy incident on the surface of the earth, coincide with coral spawning events in tropical Palau. Two insolation maxima (a consequence of the vernal and autumnal equinoxes) in the tropics lead to multiple spawning events per year. SSTs are poor predictors of coral spawning in the tropics. Multiple spawning events increase the rate of genetic recombination, which in turn may facilitate the likelihood of speciation and explain, in part, the high coral diversity in the tropics. We also show that mass spawning coincides with near-maximum solar insolation (5.0–7.2 kWh/m²/day) events from 33°N to 30°S in the western Pacific Ocean, and should be considered as one of the primary variables driving coral reproductive cycles.     

The role of chemical signals in the spawning induction of polychaete worms and other marine invertebrates

Extracts of gonad, body fluid and spawning water (into which gametes have been released by the process of spawning) were tested for the presence of spawning-inducing activity (SIA) on both sexes of the polychaetes Nereis succinea (Frey and Leuckhart) and Platynereis dumerilii (Audouin and Milne-Edwards). Gonadal and body fluid extracts from Asterias rubens (L.) and Echinus esculentus (L.) (echinoderms), Arenicola marina (L.) (polychaete), Clupea harengus (L.) (teleost) and body fluid and spawning water of Nereis virens (Sars) (polychaete) all exhibit SIA on male N. succinea. C. harengus extract from male gonads also had SIA on male P. dumerilii. Phytoplankton monoculture extracts were also tested. The cryptomonad (Rhodomonas baltica) (Karsten) had SIA on male P. dumerilii, and the diatom Phaeodactylum tricornutum (Bohlin) had some activity on Mytilus edulis (L.). The active fraction of R. baltica is chromatographically similar to uric acid (the natural sperm-release pheromone produced by females of P. dumerilii) [Nature 382 (1996) 214], but has a different retention time and UV absorbance spectra on reverse phase HPLC. Conspecific extracts of spawning water and gonadal material did not have SIA on the same and opposite sex in A. marina and N. virens. The role of chemical signals in marine invertebrates is discussed in relation to their mode of spawning.     

Predation by vertebrates and invertebrates on the seeds of five canopy tree species of an Amazonian forest

We studied the pre-germination loss of seeds to invertebrate and vertebrate seed predators of 5 species of Amazonian trees (Astrocaryum macrocalyx—Palmae; Bertholletia excelsa—Lecithydaceae; Calatola venezuelana—Icacinaceae; Dipteryx micrantha—Leguminosae (Papilionoidae); Hymenaea courbaril-Leguminosae (Caesalpinoidae)). These five species were selected from a large tree flora on several criteria. All possess large (3–10 cm) well-protected seeds that might plausibly be attractive to mammalian seed predators. The reproductive biology of three of the species, or close congeners, had been studied elsewhere in the Neotropics (Astrocaryum, Dipteryx, Hymenaea); one is important to the economy of southeastern Peru (Bertholletia); and one, despite large and apparently edible seeds, appeared to suffer no pre-germination loss to predators (Calatola). We conducted the research in mature forests in the Manu National Park of southeastern Peru where mammal densities are unperturbed by human activities. Densities of adult trees of the five species in our area range from very high (>30 per ha: Astrocaryum) to very low (1 per ha: Hymenaea).Loss of seeds to all causes, and to mammalian seed predators in particular, was determined for seeds placed in 2-square meter mammal exclosures and in open controls located at 10 m (near) and 50 m (far) from a large mature individual of the target species (with minor variations in the design for Astrocaryum and Calatola). The exclosures were of two types: impermeable—designed to exclude all mammals, but not invertebrate seed predators, and semipermeable—designed to admit small (<500 g), but not large mammals. Experimental and control plots were stocked with apparently viable seeds during the dry-wet transition period (October–November) and scored one year later.A significant distance effect (higher predation near vs far from a large conspecific adult) was found in only one of the species (Astrocaryum), the only one to be attacked with high frequency by invertebrate seed predators. The absence of any detectable distance effect attributable to mammals suggests that mammals, over the course of a year, thoroughly search the forest floor for seeds. Invertebrates may thus be responsible for most pre-germination distance (density) effects. With respect to the treatments, we found three qualitatively distinct results: seeds of three species (Astrocaryum, Bertholletia, Dipteryx) were significantly protected by the impermeable, but not semipermeable exclosures, implicating small mammals in seed loss; the seeds of one species (Hymenaea) were significantly protected by exclosures of both types, implicating large mammals; and the seeds of one species (Calatola) exhibited 100% survival, whether or not protected by exclosures.The importance of large mammals as seed predators is generally underestimated in these experiments because semipermeable exclosures may serve as foraging reserves for small mammals. Finally, we noted no relationship between the intensity of mammalian seed predation (as suggested by the survival of unprotected seeds) and the abundance of adults of the five species in the environment. The diversity of results obtained for the five species reveals that large-seeded tropical trees may display a wide range of demographic patterns, and points to the likely importance of post-germination bottlenecks in the population biology of many species, even those that may experience severe pre-germination seed loss.     

The distribution and prevalence of sponges in relation to environmental gradients within a temperate sea lough: inclined cliff surfaces

Abstract. Sponge communities on inclined cliff surfaces (40°) at Lough Hyne Marine Nature Reserve, Co. Cork, Ireland were sampled at five sites (four inside the lough and one on the adjacent Atlantic coast). Each site varied in sedimentation rate and flow regime. Sites ranged from turbulent (with negligible sedimentation) to very low flow (< 3 cm⁻¹) and highly sedimented regimes. Sponge species showed variation between sites and depth. The greatest difference in sponge communities was observed between the most turbulent and most sedimented sites. The distinct zonation patterns, present at all sites, were most pronounced at the highly sedimented sites. Encrusting forms constituted a high proportion of the sponges at all sites. However encrusting species found at the turbulent site were different to those at the sedimented sites. Arborescent species were common, mainly at the sedimented sites within Lough Hyne. Distributions of sponge species are considered with respect to morphological adaptation, competition and physiological adaptation. The distributions of sponge species on inclined surfaces are also compared with those on vertical cliff faces.     

The distribution and prevalence of sponges in relation to environmental gradients within a temperate sea lough: vertical cliff surfaces

Abstract. The prevalence and distribution of sponges was surveyed on vertical cliff surfaces at Lough Hyne Marine Nature Reserve, Co. Cork, Ireland. The number of sponge species was recorded at 6-metre depth intervals at four sites within Lough Hyne, and at one site on the adjacent Atlantic coastline to examine differences in abundance and zonation patterns. Sites ranged from an exposed turbulent regime to sheltered, sedimented environments. Individual species showed different distributions and prevalence between sites and with increasing depth. Greatest differences were observed between the most- and least-disturbed sites. Distinct sponge zonation patterns were evident at all sites sampled. Twenty-five species were considered dominant at all five sites with the remaining 48 species considered rare. Only four of the 25 most-dominant species occurred at the site experiencing the most turbulent flow conditions, whereas 12 species were found at the site of unidirectional fast flow. At sites of moderate to slight water movement and high sedimentation, between 18 and 24 of the most dominant species were present. Encrusting forms constituted high proportions of sponge communities at all five sites sampled (although consisting of different species). At sites of turbulent and unidirectional fast flow massive forms also dominated whereas at the least turbulent sites, where sedimentation was high, arborescent sponges were abundant. Few species showed exclusive distribution to a single depth and site, but there was some degree of correlation between species distributions and abiotic factors such as sedimentation rate and flow regimes. Sponge distributions and densities are discussed with respect to the suitability of species' morphologies to particular environments, intra-specific and inter-specific competition and physiological adaptations that enable them to survive in different habitats.