Reproductive traits and relative gonad expenditure of the sexes of the free spawning Chiton articulatus (Mollusca: Polyplacophora)

ABSTRACT

Reproductive studies of an intertidal free-spawning population of Chiton articulatus (Mollusca: Polyplacophora) from Puerto Angel, Oaxaca, Mexico were undertaken during 2011. We used gonad histology and gonadal indices to assess the relative gonad expenditure of the sexes (RGES) and other reproductive traits, accounting for individual and seasonal variation within this population. At this location, C. articulatus is gonochoric, without sexual dimorphism, except internally by gonad colour (testis is ‘salmon’ coloured and ovary olive green). Annual and monthly sex ratios (m/f) do not differ significantly from 1:1. Highest population-level gonadosomatic index (GSI) corresponded to maximum (peak) ripe stage (i.e. maximum gonad investment), with a first peak in May with a high value (8.4 ± 0.5) and a second peak during August-September with a lower value (4.7 ± 0.3). GSI fluctuated throughout year implying that gonad expenditure may be seasonally constrained, but with overall synchrony between sexes of ripe and spawning stages. July to December was the main reproductive season with some facultative spawning occurring off-season. Ripe and spawning RGES did not differ between sexes, suggesting that either sperm competition is intense and/or that sperm limitation is high. Early spawning individuals may quickly replenish their gametes for a second phase of gamete release later.

Abbreviations: RGES: relative gonad expenditure of the sexes; GSI: gonadosomatic index; GDS: gonad developmental stages; MiMI: microscopic maturity index; SST: sea-surface temperature.     

Reproductive cycle and reproductive output of the sea urchin Loxechinus albus (Echinodermata: Echinoidea) from Beagle Channel, Tierra del Fuego, Argentina

Reproductive cycle, frequency and duration of spawning, energetic content of gonads, and reproductive output of the common green sea urchin Loxechinus albus were analyzed in the Beagle Channel (Tierra del Fuego) between May 2004 and May 2005. Gonad indices (GI, percentages of gonad mass in total body mass) were significantly higher in March, April, July, and August than in November and May, thus showing a negative correlation with the photoperiod. Highest GI values of mature individuals were observed in August, and spawning occurred from September to December. In females, the mass-specific energy content of gonads (ECG) was highest in spawned gonads and lowest in mature ones, while in males ECG values were higher in immature stage and lower in premature and mature stages. High ECG values can be explained by the abundance of nutritive phagocytes. Both ECG and total gonad energy content (TECG) were higher in females than in males. Mean reproductive output was 7.28% for females and 6.15% for males (expressed as the difference between mean GI of mature and spawned gonads) and 25.02 kJ for females and 19.26 kJ for males (expressed as the difference between mean TECG of mature and spawned gonads).     

Seasonal changes in energy allocation to somatic and reproductive body components of the common cold temperature sea urchin <Emphasis Type="Italic">Loxechinus albus</Emphasis> in a Sub-Antarctic environment

Monthly variations in the somatic indexes and energetic content of organs were investigated in Loxechinus albus from the Beagle Channel. Samples were collected monthly from May 2004 to May 2005. Lantern and test indexes did not vary significantly. A major peak of gonad index (GI) was observed in winter (sexual maturation period), with a strong declination in November suggesting a spawning period in spring. In coincidence a shortening of feeding activities was expressed by the lower values of gut index (Gut I), suggesting that the gut is a storage organ. The values of gonad energetic content (GEC) and total gonad energetic content (TGEC) showed minimum values in winter (ripe stage) and the maximum in spring (spawned stage). The TGEC reached higher monthly average values (50–200 kJ) than total gut energetic content (TGuEC) (20–40 kJ). These differences indicate that the gonads constitute the most important store organs in L. albus. Moreover, organic stores are built up in the gonads after spawning, and then utilized during gamete production.     

Reproductive cycle of the commercially harvested sea urchin (Paracentrotus lividus) along the western coast of Portugal

Harvested populations of the sea urchin (Paracentrotus lividus) from the northwestern (Carreço) and southwestern (Aljezur) coasts of Portugal were surveyed to describe the species reproductive cycle and assess possible relationships with geographical location and seawater temperature. Individuals were sampled monthly to analyze gonad histology, mean gonadal index (GI), and gonadosomatic index (GSI) during 2 consecutive years (November 2010–November 2012). Both populations presented an annual reproductive cycle, with synchronous gonad maturation and gamete release between sexes. Gonad maturation occurred throughout autumn–winter, followed by a single but prolonged spawning season during spring–summer. The duration of the spawning season displayed a latitudinal gradient likely related to the north–south increasing trend in seawater temperature, with the northwestern population (Carreço) exhibiting a shorter spawning period compared to the southwestern population (Aljezur). The timing and duration of the spawning season was compared with several populations throughout the distributional range of P. lividus in the Atlantic Ocean and Mediterranean Sea. In the population from Carreço, the size at first sexual maturity (test diameter = 35.9 mm) was considerably smaller than the minimum conservation reference size (MCRS) of 50 mm test diameter legally established for P. lividus. This study confirms that sustainable exploitation depends on harvesters’ awareness of and compliance with the MCRS and provides useful information for the eventual establishment of a closed season in the harvesting of P. lividus.     

Temperature-dependent regulation of reproduction in the diving beetle Dytiscus sharpi (Coleoptera: Dytiscidae)

The effects of temperature on the mating behavior, gonad development, germ cell maturation, and egg spawning of the predaceous diving beetle Dytiscus sharpi (Coleoptera; Dytiscidae), were investigated. By field observations, we found that mating behavior started in October and occurred more frequently from November to December. Under our laboratory breeding conditions, we observed almost the same seasonal variation in mating behavior. We found that temperatures lower than 20 degrees C were required to trigger mating behavior. We also found the same temperature threshold triggered gonadogenesis as well as spermatogenesis. Furthermore, for females, exposure to lower temperatures (<8 degrees C) during the winter was required for egg maturation and spawning in spring; that is, there was a second threshold for successful female reproduction. We conclude that the termination of summer reproductive diapause of D. sharpi is regulated in a temperature-dependent manner, thus effecting the adaptation of D. sharpi to southern warm habitats.     

Estimating gonadal development using a non-destructive measurement of ovarian length in live Tasmanian striped trumpeter, Latris lineata (Forster, 1801)

Sexually mature female striped trumpeter Latris lineata (Forster, 1801) were sampled monthly for two spawning seasons until the start of gonadal recrudescence, and then fortnightly until ovulations ceased. Oocyte size and ovarian length, measured by inserting a semi-rigid biopsy catheter to the full extent of insertion, were recorded at each sample time. Ovarian length was expressed as proportion of fork length to provide a gonad index (GI). In non-ovulating females, there was little change in GI throughout the year. However, in ovulating females, GI increased from 18.3 five months before the first spawning season to 27.6 at the peak of the season in October, decreasing to 19.1 the following May and then increasing again to a maximum of 31.1 the following October, in concert with annual changes in reproductive condition. There was a positive linear correlation between GI and oocyte size during the period of oocyte growth ( r  = 0.75, n = 302). Based on the range of GI values for each stage in oocyte development (primary, cortical alveoli, vitellogenic, maturing and hydrated), GI was 90% accurate at assessing fish as pre-vitellogenic and 83% accurate at assessing fish as undergoing final oocyte maturation. This study demonstrated that measurement of GI by catheterization provides a rapid and non-destructive method for assessing maturational status of striped trumpeter broodstock.     

Estimation of gonad volume, fecundity, and reproductive stage of shovelnose sturgeon using sonography and endoscopy with application to the endangered pallid sturgeon

Most species of sturgeon are declining in the Mississippi River Basin of North America including pallid (Scaphirhynchus albus F. and R.) and shovelnose sturgeons (S. platorynchus R.). Understanding the reproductive cycle of sturgeon in the Mississippi River Basin is important in evaluating the status and viability of sturgeon populations. We used non‐invasive, non‐lethal methods for examining internal reproductive organs of shovelnose and pallid sturgeon. We used an ultrasound to measure egg diameter, fecundity, and gonad volume; endoscope was used to visually examine the gonad. We found the ultrasound to accurately measure the gonad volume, but it underestimated egg diameter by 52%. After correcting for the measurement error, the ultrasound accurately measured the gonad volume but it was higher than the true gonad volume for stages I and II. The ultrasound underestimated the fecundity of shovelnose sturgeon by 5%. The ultrasound fecundity was lower than the true fecundity for stage III and during August. Using the endoscope, we viewed seven different egg color categories. Using a model selection procedure, the presence of four egg categories correctly predicted the reproductive stage ± one reproductive stage of shovelnose sturgeon 95% of the time. For pallid sturgeon, the ultrasound overestimated the density of eggs by 49% and the endoscope was able to view eggs in 50% of the pallid sturgeon. Individually, the ultrasound and endoscope can be used to assess certain reproductive characteristics in sturgeon. The use of both methods at the same time can be complementary depending on the parameter measured. These methods can be used to track gonad characteristics, including measuring Gonadosomatic Index in individuals and/or populations through time, which can be very useful when associating gonad characteristics with environmental spawning triggers or with repeated examinations of individual fish throughout the reproductive cycle.     

Specific gravity and vertical distribution of sprat eggs in the Baltic Sea

During peak spawning of sprat Sprattus sprattus in the Baltic Sea in May–June egg specific gravity averaged ± s . d . 1·00858 ± 0·00116 g cm⁻³ but was significantly higher in the beginning and significantly lower towards the end of the spawning season. A close relationship was found between egg diameter and egg specific gravity ( r ² = 0·71). This relationship, however, changed during the spawning season indicating that some other factor was involved causing the decrease in specific gravity during the spawning period. The vertical egg distribution changed during the spawning season: eggs were distributed mainly in the deep layers early in the season, occurred in and above the permanent halocline during peak spawning, and above the halocline towards the end of the spawning season. Consequently, poor oxygen conditions in the deep layers and low temperatures in layers between the halocline and the developing thermocline may affect egg development. Thus, opportunities for egg development vary over the spawning season and among spawning areas, and depending on frequency of saline water inflows into the Baltic Sea and severity of winters, between years.     

The choice of oviposition site and the effects of density and oviposition timing on survivorship in<Emphasis Type="Italic"> Rana japonica</Emphasis>

In species that lack parental care and whose larvae are restricted to a given space throughout development, choice of egg-laying or reproductive sites often greatly influences fitness. Furthermore, reproductive success of individuals may be affected not only by conditions of the breeding area but also by the time when they start to breed, because intraspecific variation in the timing of breeding may result in asymmetric competition between larvae. We addressed these issues in an experimental and field study of the Japanese brown frog, Rana japonica. We tested whether the survival success of larvae decreased with an increase in the number of deposited egg masses and with a greater delay in oviposition. We found that the number of egg masses and timing of oviposition together significantly predicted larval survival per clutch. Moreover, we observed the natural oviposition of R. japonica to examine the prediction that if the density of larvae and the timing of oviposition affect survivorship of larvae, R. japonica will avoid depositing eggs in pools in which egg masses have already been deposited. We found that for small pools only, R. japonica tended to favor oviposition at unoccupied pools (those lacking egg masses and larvae) in the spawning season. For large pools, however, adults favored those already occupied by egg masses in the spawning period. The density of egg masses and tadpoles or the timing of oviposition may have less effect on spawning or the survival of tadpoles in large pools than in small pools.     

Biochemical composition of the Atlantic bonito Sarda sarda from the Aegean Sea (eastern Mediterranean Sea) in different stages of sexual maturity

The content (% wet mass) in water, ash, lipid, crude protein, DNA and RNA of different tissues was determined during sexual maturation of bonitos Sarda sarda from the Aegean Sea. A total of 220 specimens were collected in the following stages of sexual maturity: immature, resting, developing, mature, spawning and spent. Highest lipid levels in the white muscle, red muscle and liver were measured in immature specimens, while lowest levels were found in spawning bonitos. The gradual percentage of lipid reduction from immature to spawning bonitos was relatively higher in the liver (females 71·2% and males 64·4%) than in the white (females 59·2% and males 53·5%) and red (females 62·1% and males 51·7%) muscle. Lipid levels in the gonads increased gradually from the immature to spawning stage. The decrease of lipid in the somatic tissues was more intense in females than in males, and gonadal lipid content was higher in females than in males. There was a strong reverse correlation between water and lipid percentage in all tissues. Protein content decreased significantly only in spawning bonitos. The percentage of protein reduction from immature to spawning stage was relatively higher in males than in females in both white (females 3·4% and males 4·6%) and red (females 4·6% and males 5·1%) muscles. Protein content in the liver was significantly lower than in the other tissues, being highest in mature females. Gonadal protein content in females increased with maturation and decreased after spawning. The content in ash exhibited considerable stability. The RNA:DNA ratio exhibited a similar pattern of variation in both muscles. The RNA:DNA ratio increased during gonadal development gradually from the developing to spent stage. It was concluded that in S. sarda during gonadal development, there was an increase in gonadal lipid accompanied by a decrease in somatic tissue lipid reserves. Thus, reproductive inactive bonitos have more lipid in their edible part and a higher nutritional value than active ones.     

Oogenesis and gonad maturation in the copepodCalanus finmarchicus and the prediction of egg production from preserved samples

 Oogenesis and gonad development of Calanus finmarchicus during the winter spring transition in a fjord in Northern Norway were studied. A combination of observations on whole animals (macroscopic), taking advantage of their transparency, and histological sections was used to establish a system of gonad maturation stages, to describe the spawning cycle and to estimate egg production rates from preserved samples. During their development, oocytes change their shape and size, the morphology of the nucleus, and the appearance of the ooplasm. Four oocyte development stages were identified and related to a macroscopic system of four gonad developmental stages (GS) that can be applied to whole stained animals. During gonad development, the macroscopic morphological modifications of the gonads are mainly manifested in an increase in number and size of the oocytes and their distribution in diverticula and oviducts. The maturation processes during the spawning cycle (the period between egg depositions) were described from histological sections of females preserved at regular intervals after egg deposition. The macroscopic GS did not vary during the spawning cycle. This GS was a highly significant indicator for females, which spawned within 24 h after collection at 5°C. Another histological indicator for the last third of the spawning cycle is the appearance of distinct chromosomes, which, however, are only seen in histological sections. For the prediction of egg production rate of a Calanus population, in addition to the number of females spawning, knowledge of clutch size and the interval of clutch deposition is required. Clutch size was determined by counting the number of the oocyte stages to be released during the next spawning event in serial sections of the gonads. There was no significant difference in clutches laid by the females during 5 days before preservation. From the observations it seems that GS 4 predicts females that are ready to spawn within the minimum spawning interval characterisitic for a given temperature. If this holds true, it should be possible to predict in situ egg production rates solely from preserved samples. Received: 18 August 1995/Accepted: 6 January 1996     

Spatio‐temporal variability in reproductive ecology of sand flathead,Platycephalus bassensis,in three Tasmanian inshore habitats: potential implications for management

Temporal and spatial variability in gonad development, duration of spawning period, and size/age at maturity were investigated in sand flathead, Platycephalus bassensis. A 3‐year study (2001–2003) revealed that variation in gonad weight with somatic weight was a function of an interaction between season and study location (Coles Bay, Georges Bay, and Tamar River estuary). Highest gonad weight was recorded in Coles Bay in early summer, which in comparison to Georges Bay, was approximately 50% higher and occurred 3 months later. Tamar River mature individuals were reproductively inactive during the spawning season. The proportion of mature individuals at different stages of maturity differed significantly among the three locations across all times. Coles Bay individuals were reproductively active from October to March, while in Georges Bay females with hydrated oocytes were seen in September but were absent from the population by November. Interannual variation in initiation and duration of spawning activity was evident in each location. Apart from male size at maturity, for both sexes the size and age at maturity (L₅₀) was higher in Georges Bay compared to Coles Bay. The results emphasize the necessity of temporal and spatial management based on population differences in reproductive ecology.     

Aspects of the biology of grey mullet, Mugil cephalus L., adult populations of a coastal lagoon in Sri Lanka

The biology of grey mullet, Mugil cephalus L., adult populations in a coastal lagoon in Sri Lanka is presented. The percentage of grey mullet catches increased with increasing salinity. The larger fish were found in the deeper areas and the relationship of total length to depth was L = 8.4602e^{0.0058 D} where L = total length and D = depth (cm). The overall female to male ratio was 0.95 : 1.0 and seasonal variation in the sex ratio is considered to be caused by the differential timing in the spawning migrations of the two sexes. Males mature at 34.0 cm and females at 31.5 cm. The main spawning season was between January and May and it is hypothesized that the breeding season is geared to utilize the favourable time period, for growth of fry, in the lagoon. Grey mullet sheds its eggs in batches. Fecundity varied from 0.45 to 4.2 million in fish ranging in length from 32 to 56 cm and in weight from 0.7 to 2.2 kg. Fecundity was significantly correlated to body length and weight and gonad weight.     

Eel protection measures within the Manapouri hydro-electric power scheme,South Island,New Zealand

Variation in developmental rate from fertilization to swim-up, and body size at swim-up, may affect the growth and survival of young-of-the-year fish. Fish egg size (diameter) is often positively correlated to adult female size, but whether increased egg size equates to higher egg nutrient content and subsequently improved embryo/larval performance, remains unclear. Artificially fertilized northern pike eggs from individual females (total length 400–800 mm) were cultured under temperature controlled laboratory conditions to test the hypothesis that female body size positively influences egg size and the amount of specific nutrients (carbon, nitrogen, phosphorus, and fatty acids) allocated to eggs. We further hypothesized that greater egg nutrient content would positively influence egg survival, developmental rate, and the size of swim-up fry. These hypotheses were investigated in the context of two different northern pike spawning strategies (early season tributary vs. late season deep shoal spawning). Nutrients were allocated conservatively in northern pike eggs, showing very little variation in nutrient concentrations, but the total mass of all egg nutrients increased linearly with egg dry mass. Neither egg dry mass nor nutrient content (concentration or mass), were related to either egg diameter or female body size. The mass of individual egg nutrients was, however, strongly correlated with egg dry mass (r ² range 0.62 to 0.99 for individual nutrients) and positively related to the total length of swim-up fry (r ² = 0.58). The eggs of late spawning pike had significantly greater dry mass (average = 3.02 mg/egg) and developed more rapidly to swim-up (average = 17.89 days) than did those of early spawners (average = 2.28 mg/egg, 19.05 days). Our results indicate that egg quality may be best assessed by egg dry mass, which was correlated with greater nutrient mass and increased swim-up fry body length, as opposed to egg diameter or female body size which showed no correlation to egg nutrient composition and egg/larval performance. Guest editors: J. M. Farrell, C. Skov, M. Mingelbier, T. Margenau & J. E. Cooper International Pike Symposium: Merging Knowledge of Ecology, Biology, and Management for a Circumpolar Species     

Variations in clutch and egg sizes in the amphidromous goby <Emphasis Type="Italic">Rhinogobius</Emphasis> sp. CB along a river course and within a spawning season

Rhinogobius sp. CB is a common amphidromous goby in Japan. I investigated egg and clutch sizes along a river course and within a spawning season in the Aizu River, Kii Peninsula, Japan. Clutch size within the same female size did not differ along the course of the river, but decreased from early to later in the spawning season. Egg size within the same female size decreased from early to later in the spawning season and from the upper to the lower reaches. These results mean energy resources allocated to the ovary decreased seasonally and locally. Several factors are presented to explain these variations, such as female somatic conditions, a tradeoff between reproduction and growth, food availability, water temperature, and presence of competitive species. Some factors explaining the seasonal and local variations in egg size, such as water temperature and food availability for offspring, are also presented. Egg size correlated well with female size. The trend in egg size variation with female size seems to be an adaptation for their migrating pattern, as larvae from larger female, which tended to inhabit the upper reaches, would have a greater endurance against starvation during their migration to the sea.     

Sexual Maturation, Annual Reproductive Cycle, and Spawning Periodicity of the Shore Scorpionfish, Scorpaenodes littoralis

The ovarian structure, sexual maturation, annual reproductive cycle, and spawning periodicity of the shore scorpionfish, Scorpaenodes littoralis, in Uchiura Bay, central Japan, were examined using specimens collected between May 1995 and March 1998 and fishes reared in laboratory. The ovarian stroma and blood vessels run longitudinally through the center of each ovarian lobe. The ovarian peduncles radiate from the central stroma. During the spawning season, gelatinous material is secreted from the epithelia of both the ovarian peduncle and ovarian wall, and the epithelia show morphological changes accompanying the ovarian maturation cycle. The minimum standard length at maturity was 55.2mm for males and 40.2mm for females. Males with mature testes were collected from March to November. Females in the mature or post spawning stages were collected between May and October, when the mean gonadosomatic indices were also high. This indicates that the spawning season of this species occurs between May and October. Four successive types of oocytes were grouped in the mature ovary, comprised of mature, late and early vitellogenic and previtellogenic oocytes respectively, suggesting that this species is a multiple spawner. Four captive females spawned repeatedly at intervals of 2–8 days over a prolonged period (4–8 months); a 2-day spawning interval was the most common for all females. This suggests that female S. littoralis have a 48-h spawning cycle in captivity.     

Non-copulatory spawning and female participation during early egg care in a marine sculpinHemilepidotus gilberti

The reproductive behavior of a marine sculpin,Hemilepidotus gilberti, was observed in the aquarium. The behavioral sequence comprised fight for terriotory, courtship and fight for females, spawning and caring for the egg mass. Females very slowly deposited eggs enclosed with viscous ovarian fluid onto the substrate. Almost all the eggs contained in the ovary were released in a single spawning, its completion requiring 21–22 min. Territorial males emitted of spawning. Sneaking by neighboring males followed subsequently. This was the first observation of non-copulatory spawning among marine sculpins. Females cared for the eggs for severl days after spawning, and then male alone care continued until hatching (47–49 days after spawning). Participation by females in egg caring is likely to be caused by their spawning only once during the spawning season and the consequent lack of urgency for post-spawning feeding.     

Cyclical Changes in the Ovary of the Hagfish Eptatretus burgeri (Cyclostomata)

Abstract The development of eggs and the degeneration of ovulated follicles in Eptatretus burgeri was studied over a period of one year. It was found that small resting eggs with a diameter of about 1.5 mm continue to grow in November. By the spawning season in October of the following year, the follicles attain a length of about 24 mm. Only one fertilized egg containing an embryo of 7.5 mm length was obtained. The ratio of males to females was found to vary throughout the year. The annual increase of body length in correlation to ovarian development in the hagfish is calculated to be 4 to 5 cm.     

Biochemical composition of the ovarian fluid and its effects on the fertilization capacity of turbot Scophthalmus maximus during the spawning season

This study investigated the biochemical composition of ovarian fluid and its effect on the fertilization capacity of turbot Scophthalmus maximus during the spawning season. The fertilization rate and pH of ovarian fluid varied throughout the spawning season, with the highest values recorded at the mid‐season. Positive correlations were found between the fertilization rate and the ovarian fluid pH. The composition of major inorganic ions (Na⁺, K⁺, Ca²⁺ and Cl^?) showed no significant changes during the spawning season. Alkaline phosphatase (AKP) activity was significantly higher during mid‐season than other seasons. The lowest levels of protein, acid phosphatase (ACP) and aspartate aminotransferase (AAT) were in the ovarian fluid released at the mid‐season. Moreover, significant relationships were observed between the fertilization rate and the levels of protein, ACP, AKP and AAT. These observations suggest that the biochemical profile of ovarian fluid affects the insemination microenvironment as well as the fertilization capacity of S. maximus eggs. Determination of such profiles may prove to be a useful strategy to improve S. maximus breeding techniques.     

Some aspects of the reproductive biology of Spratelloides gracilis (Schlegel) in the Ysabel Passage, Papua New Guinea

Fecundity, length at first spawning, spawning seasonality and ovarian development of Spratelloides gracilis were determined by examining preserved ovaries from fish captured over a 5-year period. Fecundity ( F ) was estimated from the number of eggs in the most advanced ovarian mode and was related to fish length ( L ) by the function: log_e F =3.764 log_eL-7.308, and to weight ( W ) by: log_eW= 1.210 log_eW+7.337. Spawning was observed in most months of the year without any recognizable pattern between the years. Ova diameter frequencies were bimodal but the smaller mode remained stationary regardless of the position of the larger mode. This was interpreted as evidence that individual fish may spawn only once. From data on egg length versus fish length and gonad index versus fish length it was estimated that fish were first capable of spawning at 45 mm (fork length).