Facultative semelparity in capelin Mallotus villosus (Osmeridae)-an experimental test of a life history phenomenon in a sub-arctic fish

Two alternative reproductive modes are present in fishes and reflect the age-specific mortality encountered through ontogenesis. Life-history hypotheses suggest that semelparity (i.e. death after a single reproductive event) evolves when the ratio of juvenile to adult survival is relatively high. Conversely, a relatively low ratio of juvenile to adult survival will favour iteroparity (i.e. death after two or more reproductive events). Fisheries management associates capelin (Mallotus villosus) spawning with mass mortality and semelparity even though life history models developed for this species suggest that females may follow an iteroparous trajectory. Capelin may spawn either inter-tidally on the beach or offshore in deeper, ocean waters but post-spawning survival and potential iteroparity has been notoriously difficult to assess in natural populations. Through a series of aquarium experiments we tested post-spawning survivability in a beach spawning and an ocean spawning population. The findings demonstrate that capelin which spawn offshore are absolute semelparous (death of both genders) while beach spawning capelin are iteroparous irrespective of sex. Beach spawning capelin regenerated ripe gonads from one spawning season to the next and provides the first conclusive evidence that capelin is physiologically capable of an iteroparous reproductive mode. The potential physical and biological processes which generate certain reproductive patterns in capelin are summarized and discussed in relation to life history hypotheses. We suggest that capelin is a facultative semelparous species in which dynamic changes within the semelparity-iteroparity continuum may occur as a result of subtle interactions between the spawning habitat, physical forcing, and predatory pressure.     

The timing of spawning in capelin (Mallotus villosus Müller) at a coastal location in eastern Newfoundland

We tested three hypotheses concerning the timing of spawning for a circumpolar species, capelin (Mallotus villosus), for which timing of larval emergence is known to be synchronized by physical conditions. The first hypothesis, developed from previous studies, was that spawning would be synchronized by upwelling events. Initial results from Middle Cove Beach in eastern Newfoundland indicated that spawning was not synchronized with upwelling. We next hypothesized that spawning was a function of several environmental variables. Results from logistic regression indicated that neither single-factor nor multi-factor models could explain the timing of spawning. Single variables could predict spawning in some years but no variable could reliably predict the time of spawning year after year. Finally, we hypothesized that the probability of spawning increased as a set of significant variables approached preferred levels. For capelin at Middle Cove, the set of variables that influence capelin spawning were identified as wave height, sea surface roughness and capelin abundance in the water. Thus only a combination of variables explained the timing of spawning for capelin. Preferred conditions for capelin spawning were wave heights less than 20 cm at the beach, a sea surface with a slight ripple, and an intermediate rank abundance of capelin in the water corresponding to hundreds to thousands of individuals. Capelin abundance alone was not a useful predictor. During the course of the study we observed a shift in the dates that capelin arrived and spawned at the beach. During 1987–1990 capelin spawned at Middle Cove Beach during June, but in more recent years (1991–1993) capelin did not arrive or spawn until July.     

Beach-spawning fishes, terrestrial eggs, and air breathing

Many fishes have independently evolved beach spawning with oviposition at the water's edge. These include intertidal, subtidal, and estuarine, as well as a few freshwater, species. Their spectacular reproductive behavior at the boundary of water and land has focused attention on adults, but they emerge either briefly or not at all. The need for air breathing is more apparent in the eggs, and the reasons for emergence are more applicable to eggs than to the adults of most beach-spawning fishes. There is little evidence of air breathing in the adults, unless they are regularly emerged at other times as well. Conversely, eggs metabolize in air and show substantial emergence tolerance. We consider beach spawning a form of parental care in fishes. The adults place eggs so they will be emerged into air during part or all of incubation, providing increased temperatures, oxygen availability, and protection. Beach spawning provides habitat segregation at different points in the life history, with air emergence early in the life cycle and a return to water at hatching. The parents take great risks to spawn at the water's edge to give their offspring the most advantageous beginning in life.     

Life history correlates and extinction risk of capital-breeding fishes

We consider a distinction for fishes, often made for birds and reptiles, between capital-breeding and income-breeding species. Species that follow a capital-breeding strategy tend to evolve longer intervals between reproductive events and tend to have characteristics that we associate with higher extinction risk. To examine whether these ideas are relevant for fishes, we assembled life history data for fish species, including an index of extinction risk, the interval between spawning events, the degree of parental care, and whether or not the species migrates to spawn. These data were used to evaluate two hypotheses: (1) fish species with a major accessory activity to spawning (migration or parental care) spawn less often and (2) fish species that spawn less often are at greater risk of extinction. We tested these hypotheses by applying two alternative statistical methods that account for phylogenetic correlation in cross-taxon comparisons. The two methods predicted average intervals between spawning events 0.13–0.20 years longer for fishes with a major accessory activity. Both accessories, above-average parental care and spawning migration, were individually associated with longer average spawning intervals. We conclude that the capital-breeding paradigm is relevant for fishes. We also confirmed the second hypothesis, that species in higher IUCN extinction risk categories had longer average spawning intervals. Further research is needed to understand the relationship between extinction risk and spawning interval, within the broader context of life history traits and aquatic habitats. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Guest editors: S. Dufour, E. Prévost, E. Rochard & P. Williot Fish and diadromy in Europe (ecology, management, conservation)     

Adaptive significance of the formation of multi-species fish spawning aggregations near submerged capes

Background

Many fishes are known to spawn at distinct geomorphological features such as submerged capes or “promontories,” and the widespread use of these sites for spawning must imply some evolutionary advantage. Spawning at these capes is thought to result in rapid offshore transport of eggs, thereby reducing predation levels and facilitating dispersal to areas of suitable habitat.

Methodology/Principal Findings

To test this “off-reef transport” hypothesis, we use a hydrodynamic model and explore the effects of topography on currents at submerged capes where spawning occurs and at similar capes where spawning does not occur, along the Mesoamerican Barrier Reef. All capes modeled in this study produced eddy-shedding regimes, but specific eddy attributes differed between spawning and non-spawning sites. Eddies at spawning sites were significantly stronger than those at non-spawning sites, and upwelling and fronts were the products of the eddy formation process. Frontal zones, present particularly at the edges of eddies near the shelf, may serve to retain larvae and nutrients. Spawning site eddies were also more predictable in terms of diameter and longevity. Passive particles released at spawning and control sites were dispersed from the release site at similar rates, but particles from spawning sites were more highly aggregated in their distributions than those from control sites, and remained closer to shore at all times.

Conclusions/Significance

Our findings contradict previous hypotheses that cape spawning leads to high egg dispersion due to offshore transport, and that they are attractive for spawning due to high, variable currents. Rather, we show that current regimes at spawning sites are more predictable, concentrate the eggs, and keep larvae closer to shore. These attributes would confer evolutionary advantages by maintaining relatively similar recruitment patterns year after year.     

Sperm competition affects male behaviour and sperm output in the rainbow darter

Rainbow darters, Etheostoma caeruleum, are promiscuous fish with moderate rates of group spawning (between one and five males may simultaneously mate with one female). In this study, I examined male sperm output and male willingness to spawn under different levels of sperm competition intensity. One male and one female were allowed to spawn in an aquarium where they had visual and olfactory access to one of four treatments: four males, one male, zero males, or one female. Theory predicts that males should reduce sperm output when there are more than the average number of males at a group spawning (four-male treatment) and should increase sperm output when there are fewer than average males at a group spawning (one-male treatment). Mean sperm output did not differ among treatments. However, males released more sperm when spawning in the presence of competing males (four-male and one-male treatments pooled) than when spawning in the absence of competing males (zero-male and one-female treatments pooled). Males were also most likely to forego spawning opportunities when sperm competition intensity was high. Furthermore, male willingness to spawn was size dependent. Large males were more likely to forego spawning opportunities under high sperm competition intensity. Large males may be better off waiting for future spawning opportunities when there is a lower potential for sperm competition intensity.     

Crevice spawning behavior in Dionda dichroma,with comments on the evolution of spawning modes in North American shiners (Teleostei: Cyprinidae)

The crevice spawning behavior of Diondadichroma is described for the first time, andcompared to spawning behavior in the genusCyprinella. The evolution of crevice spawningwith respect to other spawning behaviors ofNorth American shiners is examined usingexplicitly phylogenetic hypotheses for thisgroup. We present evidence that broadcastspawning is plesiomorphic and all otherspawning behaviors are independently derived. There is evidence that crevice spawning hasevolved independently at least three timeswithin the shiner clade. There is no supportfor an evolutionary transition between eggclustering and crevice spawning. Nestassociation, spawning on habitat prepared byother species, has also evolved multiple timeswithin this clade. Evolution of spawning inshiners is best described by phylogeneticstasis with several independent origins ofspecialized spawning stragegies.     

Disturbance of freshwater habitats by anadromous salmon in Alaska

High densities of habitat modifiers can dramatically alter the structure of ecosystems. Whereas spawning sockeye salmon (Oncorhynchus nerka) dig nests that cover over 2 m² and are at least 20 cm deep, and can spawn at high densities, relatively little attention has been devoted to investigating the impacts of this disturbance. We hypothesized that this temporally and spatially predictable bioturbation has large impacts on the coastal aquatic habitats used by sockeye. We experimentally investigated the impacts of disturbance caused by spawning sockeye in two streams and two lakes in Alaska by excluding salmon from 2.25 m² plots where they traditionally spawn. We sampled exclusions and control plots before, during, and after spawning. During sockeye spawning, fine sediment accumulated in areas where sockeye were excluded from spawning. In addition, sockeye spawning significantly decreased algal biomass by 80% compared to exclusion plots. We found mixed effects of spawning on the invertebrate assemblage. Tricladida and Chironomidae densities increased by 3x in exclusion plots relative to control plots in one creek site. However, for most taxa and sites, invertebrate densities declined substantially as spawning progressed, regardless of experimental treatment. Habitat modification by spawning salmon alters both community organization and ecosystem processes.     

Genetic, spatial, and temporal components of precise spawning synchrony in reef building corals of the Montastraea annularis species complex

When organisms release gametes into the sea, synchrony must be precise to increase fertilization and decrease hybridization. We tagged and genotyped over 400 spawning corals from the three species in the Montastraea annularis species complex. We report on the influence of species, individuals, and genotypes on timing of spawning from 2002 through 2009. During their annual spawning event M. franksi spawns on average 2 h after sunset, whereas M. annularis and M. faveolata spawn 3.5 h after sunset. Only M. franksi and M. annularis have compatible gametes. Individual colonies of the same genotype spawn at approximately the same time after sunset within and across years (within minutes), but different genotypes have significantly different spawning times. Neighboring colonies, regardless of genotype, spawn more synchronously than individuals spaced further apart. At a given distance, clone-mates spawn more synchronously than nonclone-mates. A transplant experiment indicates a genetic and environmental influence on spawn time. There is strong, but not absolute, concordance between spawn time, morphology, and genetics. Tight precision in spawning is achieved via a combination of external cues, genetic precision, and perhaps conspecific signaling. These mechanisms are likely to influence reproductive success and reproductive isolation in a density-dependent manner.     

Macroscopic and histological analyses of gonads during the spawning season of Chionodraco hamatus (Pisces,Channichthyidae) off Terra Nova Bay,Ross Sea,Southern Ocean

A macroscopic and histological analysis of gonads was carried out during the spawning season of the high-Antarctic channichthyid Chionodraco hamatus in the western Ross Sea. Samples were collected between December and February during several years in the coastal waters of Terra Nova Bay. Gonad maturity stages were described for males and females according to macroscopic and histological scales. Using multi-year data, the estimated length at first spawning of females was about 35 cm TL, very similar to that obtained indirectly for males. Similar to many other high-Antarctic fish, C. hamatus is a summer spawner. The greater part of the stock was indeed in spawning condition between December and February, although a large proportion of females large enough to spawn probably did not spawn in that season. The present data confirm that C. hamatus, as is typical for Antarctic fish, probably spawns a single batch of oocytes once a year. In addition, vitellogenesis is a slow process that extends over at least 1 year. Discrepancies between the macroscopic and histological appearance of gonads were found. These were associated mainly with spent and resting females (maturity stages 5 and 2, respectively). This study demonstrates the importance of histological analysis of gonads in order to confirm the results of the macroscopic analyses routinely carried out in studies of reproductive biology. This is of particular importance in determining size at maturity and spawning stock biomass, for assessment purposes.     

Natural spawning of a Hawaiian sea urchin,Tripneustes gratilla

Observations of natural spawning events are rare but critically important for the field of fertilization ecology. For broadcast spawners, knowing the natural behavior of spawning, including proximity of animals and the timing of spawning, is essential for informing spawning experiments and directing future study. Here we describe a natural spawning event that took place on the island of Maui in the winter of 2010. Groups of Tripnuestes gratilla were observed to spawn in the late afternoon shortly after a local high tide that was a lower high of a mixed, semidiurnal tide cycle. Urchins appeared to increase the probability of fertilization by ascending to the local high points of the reefs and spawning within groups of 2–5. Although the majority of the urchins that spawned were T. gratilla, two individuals of Echinothrix diadema were observed to spawn at the same time, raising questions about potential hybridization in the wild.     

Recent local adaptation of sockeye salmon to glacial spawning habitats

Salmonids spawn in highly diverse habitats, exhibit strong genetic population structuring, and can quickly colonize newly created habitats with few founders. Spawning traits often differ among populations, but it is largely unknown if these differences are adaptive or due to genetic drift. To test if sockeye salmon (Oncorhynchus nerka) populations are adapted to glacial, beach, and tributary spawning habitats, we examined variation in heritable phenotypic traits associated with spawning in 13 populations of wild sockeye salmon in Lake Clark, Alaska. These populations were commonly founded between 100 and 400 hundred sockeye salmon generations ago and exhibit low genetic divergence at 11 microsatellite loci (F _ST < 0.024) that is uncorrelated with spawning habitat type. We found that mean P _ST (phenotypic divergence among populations) exceeded neutral F _ST for most phenotypic traits measured, indicating that phenotypic differences among populations could not be explained by genetic drift alone. Phenotypic divergence among populations was associated with spawning habitat differences, but not with neutral genetic divergence. For example, female body color was lighter and egg color was darker in glacial than non-glacial habitats. This may be due to reduced sexual selection for red spawning color in glacial habitats and an apparent trade-off in carotenoid allocation to body and egg color in females. Phenotypic plasticity is an unlikely source of phenotypic differences because Lake Clark sockeye salmon spend nearly all their lives in a common environment. Our data suggest that Lake Clark sockeye salmon populations are adapted to spawning in glacial, beach and tributary habitats and provide the first evidence of a glacial spawning ecotype in salmonids. Glacial spawning habitats are often young (i.e., <200 years old) and ephemeral. Thus, local adaptation of sockeye salmon to glacial habitats appears to have occurred recently.     

Spawning ecology of Japanese surf smelt, Hypomesus pretiosus japonicus (Osmeridae), in Otsuchi Bay, northeastern Japan

The spawning habits of Japanese surf smelt, Hypomesus pretiosus japonicus (Japanese name chika), were studied from 1992 to 1995 at Akaiso Beach in Otsuchi Bay off the Pacific coast of northern Honshu. Investigations were conducted in relation to time, tidal rhythm, sand grain size on the spawning ground, and sex and age of spawners. Spawning occurred from late March to early May with its peak at the spring tide period during full moon in April. Before dark, fish gathered to school from 1–3 m depth, and 10–20 m off the shoreline of the spawning beach. Just before dark, they repeatedly approached the shoreline and stayed near the shoreline to spawn just after dark. In the spawning process, three intervals, i.e. aggregation, approach, and spawning, were recognized and these intervals are thought to be functionally connected. Mating occurred in a unit or group formed by one female and several males. During 1992–1995, except for 1994, spawning took place in a restricted region of the beach where backwash was stronger than other areas, and most sand grains were more than 1 mm in diameter and coarser than those of other areas. Although spawning was observed near the shoreline (34 to 120 cm tide level), most of the eggs were dispersed by backwash and each became attached to a few sand grains close to a step formed at 1–2 m depth off the spawning site. Spawners were composed mainly of age 0+ fish and some 1+ fish. Males usually outnumbered females on the spawning ground. Their spawning styles are discussed in relation to their ecology and habitat.     

The migration of spawning stocks of graylingThymallus thymallus, in Lake Mjøsa, Norway

Synopsis The migration of grayling was studied in Lake Mjøsa and 13 of its tributaries in which grayling spawn. The study demonstrate that grayling spawn in creeks in May/June and leave for Lake Mjøsa shortly after spawning to return the next spring. Once mature, the grayling spawn every year. Grayling mix in the lake and are found at a mean distance of 11.9 km from the estuary of their spawning creek in September. Grayling embryos hatch in June and the juveniles stay in the tributaries until September/October. Grayling spend the winter months in the lake. Out of 1599 grayling tagged in tributaries during the spawning season, 240 of 284 recaptures (84.5%) were made in subsequent spawning seasons in the same tributary in which they were first tagged. Forty-four grayling were recaptured in adjacent tributaries. These results demonstrate that, despite the fact that all grayling leave the tributaries and mix in the lake, there is a high precision of homing. It is suggested that the grayling population in lake Mjøsa is composed of stocks using specific tributaries for spawning.     

Sex-specific spawning behavior and its consequences in an external fertilizer

Identifying the target of sexual selection in externally fertilizing taxa has been problematic because species in these taxa often lack sexual dimorphism. However, these species often show sex differences in spawning behavior; males spawn before females. I investigated the consequences of spawning order and time intervals between male and female spawning in two field experiments. The first involved releasing one female sea urchin's eggs and one or two males' sperm in discrete puffs from syringes; the second involved inducing males to spawn at different intervals in situ within a population of spawning females. In both, fertilization success was measured as the fraction of eggs fertilized and the paternity share of each male. The results indicate that spawning after females imposes a cost on males but only during sperm competition. Further, the optimal interval between the initiations of male and female spawning depends on degree of sperm competition, distance between males and females, and water velocity. The results show that sex differences in spawning timing of marine invertebrates can be explained on the basis of the differential costs and benefits of spawning out of synchrony with the other sex and that the result of sexual selection on external fertilizers may be behavioral rather than morphological differentiation of the sexes.     

Atlantic capelin (Mallotus villosus) tetranucleotide microsatellites

Twelve microsatellite loci developed for Atlantic capelin (Mallotus villosus) using magnetic bead hybridization enrichment for tetranucleotide microsatellites revealed five loci composed of single repeat elements and six composed of complex repeats. Forty‐four beach‐spawning females from three different northwestern Atlantic Newfoundland beach‐spawning populations were screened at each locus. Loci were polymorphic (two to 59 alleles per locus) and all but two exhibited high heterozygosity (0.86–1). The loci are considered suitable for addressing questions related to fine‐scale population structure, spawning fidelity and survivorship/kinship issues.     

Maturation and Reproductive Biology of Female Wild Carp, Cyprinus carpio, in Victoria, Australia

The reproduction of carp Cyprinus carpio L. (Family: Cyprinidae), from Victorian waters in Australia, is studied with detailed analysis of gonad maturation, spawning season, fecundity and oocyte diameter. Results show that carp has a high annual fecundity (AF) (0.12–1.54 million oocytes per fish), which is positively correlated with caudal fork-length (L, mm) and total weight (W, kg) but not age. The relationships between length or weight and AF were statistically significant and best described with the simple linear or quadratic regressions. Mean relative fecundity was 0.163 million eggs kg^–1 whole weight. Egg size was estimated from oocyte diameter in carp from eight stocks. Egg size was proportional to maternal size but not age. Seasonal trends in gonadosomatic indices, together with the changes in the macroscopic and microscopic condition of ovaries, demonstrated that spawning generally peaks during spring–early summer, but also occurs through until autumn and can even start in late winter at some sites. In Victoria, this species is a multiple spawner with asynchronous oocyte development and a protracted spawning season. Stocks generally contain both females that spawn once, and females that spawn repeatedly, within a spawning season. Implications for management for the control of feral carp stocks are discussed.     

A snapshot of the population structure of Branchiostoma lanceolatum in the Racou beach, France, during its spawning season

A methodology for inducing spawning in captivity of the lancelet Branchiostoma lanceolatum has been developed recently with animals collected at the Racou beach, in the southern coast of France. An increasing amount of laboratories around the world are now working on the evolution of developmental mechanisms (Evo-Devo) using amphioxus collected in this site. Thus, today, the development of new aquaculture techniques for keeping amphioxus in captivity is needed and the study of the natural conditions at which amphioxus is exposed in the Racou beach during their spawning season becomes necessary. We have investigated the amphioxus distribution, size frequency, and population structure in the Racou beach during its natural spawning season using multivariate methods (redundancy analysis and multiple regression). We found a clear preference of amphioxus for sandy sites, something that seems to be a general behaviour of different amphioxus species around the world. We have also estimated the amphioxus growth rate and we show how the animals are preferentially localized in shallow waters during April and June.     

The effect of alternative mating tactics on the fertilization success of a hermaphroditic seabass

In the simultaneously hermaphroditic marine fish, Serranus subligarius, male role individuals are known to pair spawn, group spawn and streak spawn. While the effects of these common mating tactics on mating success in the male role have been well studied, their consequences for the reproductive success of the individuals taking the female role have received little attention. To investigate those consequences, I observed mating behaviors and quantified fertilization success in natural and experimental settings during the summers of 2005-2008 at three sites with different local population densities. I observed focal individuals in 15-min increments and recorded the total number of spawns, number of streak spawns, size of participating spawners, and fertilization rate. The occurrence of small-sized individuals in the local population is associated with higher frequencies of streaking behavior; these small fish are most often first-year individuals reaching sexual maturity late in the spawning season (August/September). Spawns that included one or more streak spawners had a significantly lower average fertilization rate (89?%) than pair spawns without a streak spawner (97?%). This pattern was confirmed with a field manipulation experiment in which spawning events that included streakers again showed lower fertilization rates (93?%) than spawning events that did not include streakers (98?%). These lower fertilization rates occurred despite the fact that spawns that included multiple males produced, on average, 20?% more sperm than produced in spawns with only a single male. These results indicate that females incur a significant fitness cost when streakers invade a spawning event, a cost not attributable to sperm limitation or any direct effects on the female.     

Quantitative observations of predation during spawning rushes of the labrid fishThalassoma cupido at Miyake-jima,Japan

A rapid upward spawning rush is a nearly universal phenomenon among reef fishes that spawn pelagic eggs. Although spawning rushes have long been considered to have evolved as a defense against egg predators and/or attacks on the spawning fishes by piscivores, these hypotheses have never been tested in the field. We analysed piscivore attacks during three motor patterns associated with group spawning of the labrid fishThalassoma cupido at Miyake-jima, Izu Islands, Japan. Egg predation on group spawnings was also quantified. Of 206 piscivore attacks on spawning fishes by seven predator species, 17.1 (83.1%) occurred during 461 spawning rushes (1/2.7 spawning rushes). No attacks were successful during spawning rushes, and only four kills were made in 206 attacks summed from all three motor patterns associated with spawning, amounting to a piscivore success rate of only 1.9 %. In contrast, gametes from 90 of 213 spawnings (42.3 %) were consumed by nine species of planktivorous fishes. Spawning fish seemed not to recognize egg predators and made no attempt to avoid them, often spawning in the midst of waiting aggregations of damselfishes. Our data indicate that the rapidly of the spawning rush ofT. cupido serves as an excellent defense against piscivores, but is ineffective against egg predators. Evidence is presented from observations of seven other species suggesting that spawning ascents provide little protection against water column egg predators in predator-rich environments.