Sexual and asexual reproduction of the holothurian Stichopus chloronotus (Echinodermata): a comparison between La Réunion (Indian Ocean) and east Australia (Pacific Ocean)

Summary

Stichopus chloronotus (Brandt, 1835) is one among nine aspidochirotide holothurian species known to reproduce both sexually by broadcast spawning and asexually by transverse fission. New data on the sexual cycle of this species in La Réunion are presented here and information available on sexual and asexual reproduction in this species is summarised. Sexual reproduction on La Réunion shows a distinct seasonality with a main spawning period in the warm season (November-February). The spawning period the Great Barrier Reef appears to be at the same time. Some intriguing deviations from unity in sex-ratio, usually biased towards more male individuals, have been observed in both geographic regions (sex ratio at La Reunion 31:1). New data on the asexual reproduction of this species in La Réunion confirm the high rates of fission. The peak of asexual reproduction in both the Indian and Pacific Ocean was observed in winter (June-July). Thus, asexual reproduction in this species occurs outside the season for sexual reproduction. The rate of asexual reproduction appears to vary between sample locations. However, results of population genetic studies on S. chloronotus (Uthicke et al., 1999; Uthicke et al., 2001) indicated that in most populations investigated a maximum of about 60% of all individuals may be derived from sexual recruitment. Cluster analyses on genetic distances between populations grouped populations within Oceans together, with the exception of one sample from a nearshore reef of the GBR. Although genetic differences between the two regions exist, these are relatively small regarding the large geographic distance. We conclude that asexual reproduction in S. chloronotus is important to maintain local population sizes, but that larval exchange between populations mediated by sexual reproduction is important for colonisation of new areas and to provide connectivity between populations. Here, we present the first synthesis of these phenomena for a holothurian species.     

Asexual reproduction, evisceration, and regeneration in holothurians (Holothuroidea) from Nha Trang Bay of the South China Sea

Peculiarities of asexual reproduction, evisceration, and regeneration were studied in 13 holothurian species of the orders Dendrochirotida and Aspidochirotida from Nha Trang Bay of the South China Sea. Asexual reproduction by fission has been described for the first time for Cladolabes schmeltzii. It has been shown for the first time that transected C. schmeltzii and Colochirus robustus successfully regenerate not only their anterior, but also their posterior structures. It was found that Pseudocolochirus violaceus was able to regenerate the anterior part of the body and to eject viscera through the anus. The modes of evisceration and regeneration of the gut have been elucidated for ten species of aspidochirotids. It has been shown that the intestine of Holothuria scabra forms from two anlagen rather than from a single one, as previously believed.     

A comparative study of the population biology of the American immigrant triclad Dugesia tigrina (Girard) in two British lakes

The population biology of the American immigrant triclad Dugesia tigrina was investigated in two British eutrophic lakes: Colemere, England, harbours an asexually reproducing population and Llyn Coron, North Wales, a population that reproduces both sexually and asexually. Monthly samples of triclads were taken from the undersides of stones in both lakes, and from ceramic tiles and plastic trays in Colemere and Llyn Coron, respectively, over two years. In both populations, body size-structure decreased slightly over winter, with an absence of very large and very small animals. Individual growth occurred in spring, and over summer the proportion of large and small individuals declined and increased, respectively. During September to November, size-structure was fairly stable. Increases in the size structure of the populations were associated with higher temperatures and an increased food supply; stability in size structure during the autumnal post-reproductive period, when temperatures were favourable for growth, to the occurrence of intraspecific competition for food; and decreases in size structure to lower temperatures during the winter. In both populations the density of triclads increased in summer to a peak in autumn, thereafter declining to a nadir in spring. The numerical peak in autumn was due to recruitment from reproduction, and the subsequent decline to deaths following the occurrence of intraspecific competition for food in late autumn, some invertebrate predation and winter mortality. Asexual reproduction (fission) started in June and finished during August in both populations. Laboratory experiments indicated that the occurrence and rate of fission is influenced by temperature and the amount of available food. The critical temperature for the initiation and cessation of fission lay between 14 and 16 °C in laboratory studies, and in the field fissioning started as temperatures approached 15 °C. In Llyn Coron, cocoon deposition commenced in June, peaked in July with only a very few produced in August. Triclads collected from the field outside these months could not be induced to lay cocoons in the laboratory. Laboratory experiments showed that cocoons were deposited at temperatures of 17.5, 20, and 25 °C, but not at 12.5 °C. Thus, in the field, cocoon production started when temperatures approached 15 °C in June, but had ceased whilst temperatures were still in excess of 15 °C in late August. Termination of cocoon dsposition is associated with the disappearance of large triclads in excess of 20 mm², below which animals are not sexually mature; disappearance of large animals was due to fissioning, death after sexual reproduction, and probably shrinkage due to severe intraspecific competition for food. Laboratory experiments indicated that the Colemere population had, potentially, greater fission production than the Llyn Coron population. Despite this, the numerical size of the Colemere and Llyn Coron populations increased seven-fold and eleven-fold, respectively, over the reproductive period. Whether or not this difference in reproductive potential between the populations will continue is speculative; the introduction of D. tigrina to Llyn Coron is relatively recent and the population may still be expanding to reach the carrying capacity of the habitat. Its high reproductive output must have helped its successful invasion of the lake.     

Hope springs eternal in the starfish gonad: preserved potential for sexual reproduction in a single-clone population of a fissiparous starfish

Among echinoderms, asexual reproduction by fission occurs in few species. This strategy is considered a temporary response to stressful conditions and usually alternates with sexual reproduction events; thus, monoclonal populations are extremely rare. The occurrence of a single-clone population of the starfish Coscinasterias tenuispina at Llançà (NW Mediterranean) allowed us to study intra-clonal variation of the reproductive cycle during a two-year study. The few developed gonads (all male) were found in winter months, coinciding with the minimum photoperiod (ρ = ?0.82; P < 0.001) and lowest temperatures (ρ = ?0.75; P < 0.001), only in best-fed individuals, indicating that food availability influences individual ability for gonad development. Fissiparity happened throughout all the sampled period, but its rate increased with warm temperatures (ρ = 0.68; P < 0.0001). In contrast to what has been reported in other species, no correlation between fission rates and population density was found. The population was maintained over time by asexual reproduction and remained monoclonal. Although sexual reproduction has probably not occurred in this all-male population for a long time, the ability to yearly produce mature gonads is retained by some individuals, indicating that potential to reproduce sexually may be preserved, even in the case of strictly asexual populations.     

The annual gametogenic cycle of the sea anemone Metridium senile from the Gulf of Maine

A year-long study was conducted to quantify the reproductive cycle of the clonal sea anemone, Metridium senile, an important member of the benthic community in the Gulf of Maine (GOM). M.senile is an abundant sessile invertebrate that forms identifiable clonal aggregations that are maintained by pedal laceration but individuals can also reproduce sexually. Specimens were collected monthly from a shallow (< 10 m) subtidal site and the reproductive cycle of male and female anemones was described on a seasonal basis using histological preparation of the gonads and light microscopy. Gametogenesis was determined for both sexes and showed that females undergo spawning during the seasonal transition from summer to fall, while males have mature sperm within testicular cysts in the winter, spring, and summer. Environmental data recorded at the study site shows that the spawning period occurs during a period of peak water temperature (August-September), and rapid gametogenesis occurs during periods of high food availability (April). The low percentage of reproductively mature anemones and the dominance of asexual reproduction in this population are believed to be the result of the high flow regime at this site.     

Population Growth in Planaria Dugesia tigrina (Gerard) : Regulation by the absolute number in the population

Planaria reproduce by transverse fission. Isolated worms increase in number exponentially, while social animals at the same density are inhibited in terms of numerical increase, but over a 25 day period undergo a larger increase in mass. Isolated posterior fission products reproduce faster than isolated anterior fission products. Regulation of population growth is independent of density over a 16-fold range and regulatory factors cannot be demonstrated in the medium. Regulation of population growth depends on direct contact between animals. Fission period varies from individual to individual and from period to period for a given individual. Doubling time is related to the absolute number of individuals comprising the population as follows: P_N = (P_M · N)/(K + N), where P_N is the doubling period of a population of N individuals, P_M is the doubling time of an infinitely large population, N is the number of individuals in the population, and K is the number of individuals in a population the period of which is one-half P_M. At 22°–24°C P_M is estimated to be 43.3 days and K is 1.87 individuals. A model system assumes that inhibitor flows through the population from animal to animal from the slowest to the fastest animal in the population thus acting to synchronize population increase as well as to determine the rate of population growth. A possible source of the inhibitor is discussed.     

The influence of population density on fission and growth of Holothuria atra in natural mesocosms

Investigation of the population dynamics, asexual reproduction (fission) and growth of holothuroids has been impeded by the difficulty of tagging individuals. We conducted the first tests on the interactions between population density, fission and growth of holothuroids in experimental populations placed in natural mesocosms (microatolls) at One Tree Reef (OTR), Great Barrier Reef. Similarly sized Holothuria atra were translocated to the microatolls in low (LDT) and high (HDT) density treatments. We hypothesised that holothuroids in lower density treatments would have more resources per individual and that this would promote higher frequencies of asexual reproduction and smaller individuals. The seasonal pattern of fission was similar in natural (unmanipulated) and experimental populations, with the maximum number of fission products occurring in winter and spring. The overall density of the LDT (0.19 ind. m^- 2) and HDT (0.59 ind. m^- 2) did not vary over time. This ‘steady state’ suggested that some fission products died and that asexual reproduction compensated for overall mortality and emigration. There was no difference in sediment chlorophyll pigments between treatments indicating that the different densities of H. atra did not affect benthic microalgal biomass. The percentage of fission products was greater in the LDT than the HDT but this difference was not statistically significant, providing some support for the hypothesis that H. atra in the LDT exhibit a higher fission rates. At the end of the experiment H. atra in LDT were significantly longer and heavier than in HDT. H. atra surpassed their initial deployment weight and length after 13 months in the LDT by 115.2% and 45.2% respectively and in the HDT 86.9% and 24.6% respectively, changing from the small to the large phenotype known for this species. This differential growth may be linked to habitat stability and high benthic productivity and demonstrates the phenotypic plasticity of holothuroids and potential to achieve ‘Optimum Individual Size’ with respect to environmental conditions. Our results will assist in finetuning conceptual models on asexual reproduction and future experimental studies on the phenomena of fission and plastic growth in holothuroids.     

The extent of asexual reproduction in sponges of the genus Chondrilla (Demospongiae: Chondrosida) from the Caribbean and the Brazilian coasts

In this study, we estimated the extent of asexual reproduction and genotypic diversity at the intra- and interspecific levels in sponges of the genus Chondrilla in the Caribbean and along the coast of Brazil. Allozymes were used to identify the genotypes of specimens of Chondrilla in each location. The four species studied displayed a large variation in the extent of clonal reproduction and genotypic diversity, with the two species from the Bahamas having a greater proportion of asexually produced individuals than those along the coast of Brazil. Conspecific Brazilian populations of Chondrilla sp. had large differences in clonality: the population from a heterogeneous environment and under the influence of a strong upwelling had little clonality (7%), whereas the population located 350 km south along the coast, in a more homogeneous and temporally stable environment, had a five-fold larger (39%) proportion of asexually derived individuals. Finally, we were able to confirm that, besides fission, the genus Chondrilla displays a second mode of asexual reproduction, by fragmentation of teardrop shaped individuals.     

Seasonal aspects of life cycles in Calathus melanocephalus and C. micropterus (Coleoptera, Carabidae) in the northern taiga

The seasonal dynamics of the activity and the demographic structure of Calathus melanocephalus and C. micropterus populations were studied in the northern taiga of Arkhangelsk Province. The period of adult activity lasts from early June to mid-or late September with the maximum surface activity observed in the middle of summer. In C. melanocephalus, mature individuals are recorded from early June to early September, and in C. micropterus, during the entire season. The data on seasonal changes of the demographic structure of the population demonstrate that in the northern taiga, these species probably possess a biennial life cycle with summer reproduction. The geographical variability of the demographic structure of populations and of life cycles of two species of the genus Calathus was demonstrated. Northwards from the south, the period of activity decreases and the period of reproduction increases and shifts from autumn to the middle of summer. A hypothesis was formulated, according to which in the species studied the annual life cycle in the central part of the range is replaced by the biennial cycle in the north.     

Population genetics of the fissiparous holothurian Stichopus chloronotus (Aspidochirotida) on the Great Barrier Reef, Australia

 Population genetic structure was studied in one nearshore and two offshore populations of Stichopus chloronotus, a common holothurian species on Indo-Pacific coral reefs. Genetic variation at five polymorphic loci was examined using allozyme electrophoresis. The nearshore population consisted almost exclusively of male individuals, and more males than females were found in all populations studied. Deviations of heterozygosity from that predicted under Hardy-Weinberg equilibrium indicated that asexual reproduction occurred in all populations. Estimates of the level of asexual reproduction using the ratios of the number of sexually produced individuals to sample size, observed genotypic diversity to expected genotypic diversity, and number of genotypes to sample size confirmed that this reproductive mode was more important at the nearshore reef compared to the two offshore reefs. There were large differences in genotypic frequencies between males and females. F-statistics on clonal genotypic frequencies were not statistically significant between populations for neither females or males, suggesting high dispersal of larvae between reefs. A higher mortality of females during larval or early post-settlement stages, or reduced dispersal capability of female larvae are the most likely reasons for biased sex ratios. Accepted: 23 November 1998     

Population dynamics of Stylaria lacustris (Linnaeus, 1767) (Oligochaeta,Naididae) in Los Talas,Argentina

Population dynamics of Stylaria lacustris were analyzed over 2 years in a pond located at Los Talas, Argentina. In both years, the peak in abundance, due to intense asexual reproduction, fell at the end of winter, and was followed by mature individuals. The species was not collected during summer. Temperature was the main factor regulating the population through both sexual and asexual reproduction. In the second year, density was lower and correlated with a lower water level and a reduced vegetation development. Individuals were randomly distributed in periods of high abundance and contagious when density was low. Generation time was 15 days.     

Asexual reproduction and somatic growth of the fissiparous sea star Allostichaster polyplax in New Zealand

Allostichaster polyplax is a fissiparous (capable of reproducing asexually by fission) sea star found in intertidal and shallow subtidal habitats in New Zealand and Australia. A localized population of A. polyplax occurred at a density of 2.7?individuals?m^?2 in an intertidal boulder field at Otago Harbour, South Island, New Zealand. The percentage of sea stars undergoing fission, recorded from January 2010 to March 2011, peaked in January (midsummer) in both years. The frequency of fission decreased for larger sea stars (mean arm length, R?>?25?mm), suggesting an ontogenic shift from asexual to sexual reproduction. Effects of fission (i.e. arm regeneration) and food availability (small gastropods) on growth, storage and sexual reproduction were examined in a factorial laboratory experiment. There was no effect of arm regeneration or food on total arm growth. Storage capacity, measured as pyloric caeca index (PCI), was greater in full-armed than regenerating sea stars, and greater in fed than starved individuals. Fed individuals had a similar PCI as field-collected ones. Gonads were observed in two individuals (males) in the full-armed and fed treatment. Fission did not occur during the experiment. Feeding rate on snails was greater for full-armed than regenerating sea stars. Water temperature had a weak positive effect on the feeding rate of regenerating sea stars. Our findings suggest that fission and subsequent growth of ramets can sustain demographically stable and geographically isolated populations of A. polyplax. The role of sexual reproduction in population dynamics and connectivity of this species (and fissiparous sea stars in general) remains equivocal and requires further research on genetic differentiation within and among populations.     

The distribution of Naididae (Oligochaeta) in the littoral zone of selected lakes in North Wales and Shropshire

SUMMARY. The distribution of twenty species of Naididae found in seventeen lakes in North Wales and Shropshire is described. Fewer species were observed in the mountain lakes in Snowdonia in comparison to the more productive lakes of Anglesey and Shropshire.
Substrate was an important factor influencing the distribution of naids within lakes, A small number of sexually mature individuals was found in more productive lakes in the summer and autumn months. Sexually mature individuals of Stylaria lacustris were cultured in the laboratory; the population doubled its numbers, by asexual reproduction, in 12 days at 15°C. In Llyn Coron a natural population of S. lacustris doubled its numbers in 40 days. The gut contents of S. lacustris consisted of periphyton.     

Biomass variation and reproductive phenology of Gracilaria gracilis in a Patagonian natural bed (Chubut, Argentina)

The biomass variation and the reproduction of the natural Gracilaria gracilis bed in Bahía Bustamante (Patagonia, Argentina) were analyzed for 2 years, with the aim of determining the present situation of the population for an updated status overview; establishing the relevant features of the temporal variation in both biomass and reproductive states in relation to environmental factors, epiphytes and associated algae; and assessing carpospore availability for future spore-culture development. Field measurements and sampling were performed monthly between March 2006 and February 2008. In both years, G. gracilis biomass presented marked seasonal variations, with a minimum in winter and a maximum in late spring and in summer. During both years, coexistence of the three life-cycle phases was found, with dominance of tetrasporophytes. Two data sets from individuals originated from sexual reproduction (tetraspores and carpospores) and from asexual reproduction by thallus fragmentation were analyzed separately. In the fragmentation fraction, tetrasporophyte frequencies remained higher than those for gametophytes. However, in the spore-originated fraction, a generation ratio close to 0.5 was observed. Female gametophytes bearing cystocarps were always present, with a maximum in summer and autumn. Biological data were related to environmental factors by means of canonical correspondence analysis (CCA). The first year was characterized by higher biomass values of G. gracilis and Undaria pinnatifida, lower epiphytism, larger Gracilaria thalli and greater proportion of mature tetrasporophytes and gametophytes. The second year was characterized by a high proportion of Gracilaria vegetative thalli and high epiphyte density. The best time to obtain spores from cystocarpic thalli would be in summer and early autumn.     

Reproductive biology of Philodryas patagoniensis (Snakes: Dipsadidae) in south Brazil: male reproductive cycle

The male reproductive cycle of Philodryas patagoniensis in south Brazil was described through morpho‐anatomical and histological analysis of individuals deposited in zoological collections. Spermatogenesis occurred during late autumn–winter (June–September) and spermiogenesis occurred in spring–summer (October–March). The volume of the testes was smaller (quiescent) in winter, while the tubular diameter and the epithelial height of the seminiferous tubule were larger in summer (January–March). The ductus deferens presented spermatozoa all over the year and had no seasonal variation in diameter. The length of the kidney was larger in winter–spring (July–December), although the tubular diameter and epithelium height of the sexual segment of the kidney (SSK) were larger only in winter (July–September). Total testicular regression was observed in late autumn (May), simultaneously with the peak in SSK. Therefore, at the individual level, males exhibit a discontinuous cyclical reproduction. Considering the population level, the reproductive cycle is seasonal semisynchronous, with most of the individuals showing a reproductive peak in spring–summer (October–March). Here, we present evidence to support the importance of the microscopic approach to reproductive cycle studies. Finally, we discuss the intrinsic and extrinsic factors influencing P. patagoniensis reproductive patterns.     

Making the most of the old age: Autumn breeding as an extra reproductive investment in older seabirds

The extrinsic and intrinsic factors affecting differing reproductive strategies among populations are central to understanding population and evolutionary ecology. To evaluate whether individual reproductive strategies responded to annual patterns in marine productivity and age‐related processes in a seabird we used a long term (2003–2013), a continuous dataset on nest occupancy and attendance at the colony by little penguins (Eudyptula minor) at Phillip Island (Victoria, Australia). We found that concurrent with a secondary annual peak of marine productivity, a secondary peak in colony attendance and nest occupancy was observed in Autumn (out of the regular breeding season in spring/summer) with individuals showing mating‐like behavior. Individuals attending this autumn peak averaged 2.5 years older than those individuals that exclusively bred during spring/summer. Rather than being a naïve response by younger and inexperienced birds misreading environmental cues, our data indicate that the autumn peak attendance is an earlier attempt to breed by older and more experienced penguins. Therefore, we provide strong support for the fundamental prediction of the life‐history theory of increasing investment in reproduction with age to maximize lifetime fitness as future survival prospects diminish and experience increases.     

Taxonomic Status and Reproduction Dynamics of the Non-Indigenous Cercopagis in the Gulf of Riga (Baltic Sea)

Overwintering population of Cercopagis is represented by resting eggs which hatch generally in May. Although representatives of the first parthenogenetic generation (the spring form individuals) differ morphologically from individuals of the subsequent generations (the summer form individuals) and could be keyed to a separate species – Cercopagis (Apagis) ossiani – our analysis confirm that there is only one Cercopagis species in the Gulf of Riga: Cercopagis pengoi. Notable seasonal dynamics was observed for the gamogenetic mode of reproduction, being strongly associated with the total population density. Gamogenetic females develop since the end of June and reach the maximum absolute abundance in July whereas their proportion is generally the highest in fall. The gamogenetic absolute fecundity drops to the lowest level late July but increased afterwards until the late August. One resting egg was, an average, found in 45.4%, two in 53.4% and three in 1.2% of females. Parthenogenetic fecundity was significantly higher in May–June compared to other months studied. Brood pouch of parthenogenetic females was found to contain 11.6 ± 1.0 and 10.2 ± 0.3 embryos in the spring and summer form individuals, respectively. Variation in the two modes of reproduction and fecundity is probably solely not controlled by temperature, but also by food availability and population density.     

Differences in larval dynamics of golden mussel <Emphasis Type="Italic">Limnoperna fortunei</Emphasis> between dam reservoirs with and without an aeration system

The golden mussel Limnoperna fortunei is a freshwater bivalve that adheres to water intake facilities, leading to problems of several kinds. Biofouling problems have been increasing recently in East Asia and South America, and the planktonic stage of this species is considered to play an important role in its dispersal. We investigated the larval dynamics of L. fortunei in two reservoirs, Lake Ohshio and Lake Takenuma, which are connected by a headrace channel. An aeration system for water quality conservation was present in the former reservoir but not in the latter. Larval density in Lake Ohshio was more than 10,000 individuals/m³ with a maximum of 80,000 individuals/m³ in summer. The density in Lake Takenuma was much lower, with a maximum of around 200 individuals/m³. Water temperature (WT) and dissolved oxygen (DO) concentration were almost uniform regardless of water depth in Lake Ohshio because of destratification due to continuous aeration. Summer WT and DO in the lake were considered to be suitable for survival and reproduction of L. fortunei. On the other hand, stratification was found for WT and DO in Lake Takenuma throughout the summer. The low WT and DO found in the deep areas of the lake in summer were considered to be not suitable for survival and reproduction of this species. Thus, the population of L. fortunei larvae differed widely even in two adjoining lakes, and WT and DO are considered to be critical factors, especially for reproduction.     

Millipedes faced with drought: the life cycle of a Mediterranean population of Ommatoiulus sabulosus (Linnaeus) (Diplopoda,Julida, Julidae)

Growth, development and life-cycle duration of the millipede Ommatoiulus sabulosus (f. aimatopodus) were studied in a Mediterranean shrubland of southern France and compared with previous data from northwest Europe. Changes in the proportions of stadia during the course of the year were analysed in several generations. The results show that stadia VII and VIII are consistently reached after the first year of growth, and stadia IX and X after the second year. First reproduction may occur at the age of two years in males reaching maturity at stadium X, but not until the age of three in those reaching maturity at stadia XI and XII. Reproduction cannot occur until at least the age of three in females, which carry mature eggs from stadium XI onwards. In comparison with more northern populations, life-cycle duration is not shorter in the Mediterranean population but there are marked differences in its phenology: the breeding period is in autumn, so that juveniles of stadia II to VI are never faced with the summer drought, and larger individuals are mostly inactive in summer; moreover, all individuals moult once every winter. The results illustrate how julid millipedes of humid temperate regions could respond to higher temperatures and drier summer conditions in the context of climate change.     

Long-term variation in dates of mass spawning of cod Gadus morhua callarias (Gadidae) in the southeastern part of the Baltic Sea

Long-term data on the numbers of eggs of cod Gadus morhua callarias in ichthyoplankton and the seasonal variation of their distribution in the Gdansk Deep of the Baltic Sea are considered. The spring peak of spawning was observed for the years 1948–1954 and 1960–1964; the spring-summer peak for 1968–1977; and the summer peak for 1955–1959 and 1995–2001. Maximum egg numbers of cod were recorded from the late 1940s to the early 1950s; minimums were recorded in the late 1980s and the late 1990s. The decrease in the numbers of cod eggs in the ichthyoplankton, in general, coincided with a decrease in the proportion of spawners maturing at the beginning of the season of mass reproduction and a decrease in the oxygen content in the near-bottom layer of the Gdansk Deep. It is suggested that a shift of the spawning peak of cod from spring to summer is related to a decrease in the volume of near-bottom waters providing favorable conditions for the reproduction of this population.