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     

Egg production of the marine,planktonic copepod,Calanus pacificus Brodsky: Laboratory observations

When acclimated to a continuous, superabundant food supply and constant temperature, Calanus pacificus Brodsky females produce eggs at a weight-specific rate ranging from 0.13 · day^?1 at 8°C to 0.21 · day^?1 at 15°C. Maximum weight-specific egg production rates do not change with seasonal changes in female body size. The relationship between egg production rate and food concentration is hyperbolic, with threshold and critical concentrations that are high relative to other species for which data are available. Food concentration and temperature influence spawning frequency (i.e., the time required for oocytes to mature) much more than the number of eggs in a single spawning event (i.e., clutch size). Clutch size is significantly related to female body size.     

A multi-generation Calanus finmarchicus culturing system for use in long-term oil exposure experiments

Crustacean zooplankton form the keystone link between primary producers and fish stocks along the Norwegian shelf and in the southern part of the Barents Sea. We have established a multi-generation cultivation system for zooplankton in order to perform future experiments on the biological effects of drilling discharges from the offshore petroleum industry. A population of the cold-water species, Calanus finmarchicus, was collected in March 2004 and maintained in a static system of 100 l polypropylene containers through all stages (Eggs-CVI). The population exhibited an average developmental time of 105 days which corresponds to realistic sub-Arctic to Arctic conditions (water temperatures = 5 °C (spring) and 8 °C (late summer)). A series of experiments was performed to examine copepod egg production as a function of different food sources and feeding concentrations. Only minor differences in egg production were observed for C. finmarchicus females fed with varying concentrations of the two diatom species Chaetoceros socialis and Thalassiosira weissflogii. In a separate experiment, the response to food availability was examined over time by tracking egg production and fecal pellet production (used as an indicator of food ingestion). Both hatching success and food ingestion were positively correlated with the food concentrations offered to adult females. Through this work we have demonstrated that C. finmarchicus populations can be maintained in the laboratory through multiple generations. In addition, methods to control egg production through changes in food availability have been established making it feasible to control the start date of exposure experiments or the timing of the collection of eggs to initiate a new generation.     

Reproductive patterns of Calanus finmarchicus at the Norwegian midshelf in 1997

Gonad stage, mean clutch size, prosome length, oil sac volumeand feeding activity of adult female Calanus finmarchicus werestudied from preserved samples collected at two transects inthe Norwegian Sea from February to October 1997. The patternof co-ordinated changes in gonad maturity and egg clutch sizesuggested that two generations were produced annually in thestudy region. The main period of reproduction, judging fromproportion of females with mature gonads and mean clutch size,occurred in April, followed by less pronounced peaks in Juneand July. Gonad stage and the oil sac volume were negativelycorrelated, suggesting that gonad development was, at leastpartly, fuelled by reserve lipids. Individual clutch size (estimatedas the number of mature oocytes per female) was highly variable,ranging from 10 to 104 during the studied season. Feeding activityat the shelf stations was usually higher than at oceanic stations,and was higher at the southern transect than the northern, causingearlier maturation over the shelf, and in the south. The distinctlypronounced spring generation was probably synchronized by thetermination of the overwintering phase, while the summer generation,which depends on the variable feeding conditions of the habitat,was less synchronized.     

La reproduction de Temora stylifera: ses implications anatomiques en relation avec le facteur 'nutrition'

The culture of copepods under different feeding regimes hasallowed us to determine the effects of food availability onegg laying. In Temora stylifera spawning appears to be modifiedby the food resources of the adult. Conditions encountered duringdevelopment have little effect on spawning. The life span offemales is reduced by high food availability. In such casesthe sex organs are hypertrophied, the oviducts being distendedby the large oocytes. The ovary is little affected by changesin food availability, while the size of the oviducts variesin relation to feeding. The size of the genital system is reducedin older females. Variations in food concentration induce variationsof several days in the time required for egg laying. A rapidmaturation of the oocytes, combined with nutrition and the availabilityof food permits Temora stylifera to optimize egg laying.     

Gonad morphology,oocyte development and spawning cycle of the calanoid copepod <Emphasis Type="Italic">Acartia clausi</Emphasis>

Information on gonad morphology and its relation to basic reproductive parameters such as clutch size and spawning frequency is lacking for Acartia clausi, a dominant calanoid copepod of the North Sea. To fill this gap, females of this species were sampled at Helgoland Roads from mid March to late May 2001. Gonad structure and oogenesis were studied using a combination of histology and whole-body-analysis. In addition, clutch size and spawning frequency were determined in incubation experiments, during which individual females were monitored at short intervals for 8 and 12 h, respectively. The histological analysis revealed that the ovary of A. clausi is w-shaped with two distinct tips pointing posteriorly. It is slightly different from that of other Acartia species and of other copepod taxa. From the ovary, two anterior diverticula extend into the head region, and two posterior diverticula extend to the genital opening in the abdomen. Developing oocytes change in shape and size, and in the appearance of the nucleus and the ooplasm. Based on these morphological characteristics, different oocyte development stages (OS) were identified. Mitotically dividing oogonia and young oocytes (OS 0) were restricted to the ovary, whereas vitellogenic oocytes (OS 1–4) were present in the diverticula. The development stage of the oocytes increased with distance to the ovary in both, anterior and posterior diverticula. Most advanced oocytes were situated ventrally, and their number varied between 1 and 18, at a median of 4. All oocyte development stages co-occur indicating that oogenesis in A. clausi is a continuous process. These morphological features reflect the reproductive traits of this species. In accordance with the low numbers of mature oocytes in the gonads, females usually produced small clutches of one to five eggs. Clutches were released throughout the entire observation period at intervals of 90 min (median) resulting in mean egg production rates of 18–28 eggs female⁻¹ day⁻¹.     

Reproductive traits of the small Patagonian octopus Octopus tehuelchus

This study evaluated the reproductive features of Octopus tehuelchus in three coastal environments of San Matías Gulf (Patagonia). Monthly samples of O. tehuelchus were used to estimate size at maturity, compare seasonal changes in oocyte size frequency distributions between sites as well as oocyte number and size between female maturity stage and sites. Females in Islote Lobos had a smaller size at maturity than females in San Antonio Bay and El Fuerte, probably as a consequence of a generally smaller body size. Males in San Antonio Bay were smaller at maturity than females. O. tehuelchus is a simultaneous terminal spawner. Fecundity (expressed as number of vitellogenic oocytes in ovary) was lower in Islote Lobos, and an increase in oocyte number in relation to female total weight was found. Females in San Antonio Bay had the largest oocytes, which may indicate higher energy reserves for the embryo and therefore higher juvenile survival. There was a close relationship between reproduction, growth and condition, represented as size at maturity, number and size of vitellogenic oocytes and period of maturity and spawning. Given the local variation in some reproductive features of O. tehuelchus, studies should focus on the environmental factors, which bring about this variation, and on how it affects the dynamics of local populations.     

Effect of temperature,food and individual variability on the embryonic development time and fecundity of <Emphasis Type="Italic">Arctodiaptomus salinus</Emphasis> (Copepoda: Calanoida) from a shallow saline pond

Organisms living in temporary and shallow wetlands are adapted to survive in very fluctuating and unpredictable conditions and might help us to understand life cycle strategies and plasticity in the context of global warming. Despite the importance of Arctodiaptomus salinus in these systems, little is known about the effect of temperature on its population dynamics. Through an individual-based experimental protocol, we studied the effect of this factor and food on its reproduction. This approach has revealed a large range of variability in reproductive parameters in all the experimental conditions. Temperature positively affected egg production and negatively longevity, but did not affect clutch size. Under unsuitable food conditions, the clutch size decreased and the inter-clutch period increased, and when the food conditions improved, the number of eggs increased gradually in every clutch. Eggs from the same clutch hatched synchronously. In contrast, there were significant differences between the hatching times of clutches from different females and between those of the same female. The observed individual variability increased when temperature moved away from the medium values. The thermal tolerance threshold for A. salinus development might be around 25–29°C. Since water pond is close to this thermal limit for long periods of time, an increment of temperature because of global warming might have dramatic consequences on this population. The individual-based experimental approach of this study provides useful information to construct realistic individual-based models, which will help us to better understand the population-level consequences of individual variability in A. salinus reproduction.     

On the environmental control of oocyte maturation in a plethodontid salamander

Summary The relationship between condition and oocyte maturation was experimentally studied in Plethodon cinereus. Gravid females with immature oocytes were collected in September and maintained on different feeding regimes for 180 days. An index of salamander condition was derived. There was no significant relationship between the number of maturing oocytes and condition of the salamander at the end of the experiment, but oocyte size was signifiantly related to condition. A significant regression relationship was found for oocyte number and initial body weight, suggesting that condition may affect oocyte number early in the reproductive cycle. The implications of environmental induction of oocyte number for affecting clutch size and fitness are discussed.     

Not putting all their eggs in one basket: bet‐hedging despite extraordinary annual reproductive output of desert tortoises

Bet‐hedging theory makes the counter‐intuitive prediction that, if juvenile survival is low and unpredictable, organisms should consistently reduce short‐term reproductive output to minimize the risk of reproductive failure in the long‐term. We investigated the long‐term reproductive output of an Agassiz's desert tortoise (Gopherus agassizii) population and conformance to a bet‐hedging strategy of reproduction in an unpredictable but comparatively productive environment. Most females reproduced every year, even during periods of low precipitation and poor germination of food plants, and the mean percentage of reproducing females did not differ significantly on an annual basis. Although mean annual egg production (clutch size × clutch frequency) differed significantly among years, mean clutch size and mean clutch frequency remained relatively constant. During an El Niño year, mean annual egg production and mean annual clutch frequency were the highest ever reported for this species. Annual egg production was positively influenced by maternal body size but clutch size and clutch frequency were not. Our long‐term results confirm earlier conclusions based on short‐term research that desert tortoises have a bet‐hedging strategy of producing small clutches almost every year. The risk of long‐term reproductive failure is minimized in unpredictable environments, both through time by annually producing multiple small clutches over a long reproductive lifespan, even in years of low resource availability, and through space by depositing multiple annual clutches in different locations. The extraordinary annual reproductive output of this population appears to be the result of a typically high but unpredictable biomass of annual food plants at the site relative to tortoise habitat in dryer regions. Under the comparatively productive but unpredictable conditions, tortoises conform to predictions of a bet‐hedging strategy of reproduction with relatively small but consistent clutch sizes. Published 2015. This article is a U.S. Government work and is in the public domain in the USA, Biological Journal of the Linnean Society, 2015, 115 , 399–410.     

The reproductive biology of Euchaeta antarctica Giesbrecht (Copepoda: Calanoida) at South Georgia

The reproductive biology of the predatory calanoid copepod Euchaeta antarctica Giesbrecht was investigated in two interconnected fjord systems at South Georgia. Counts of the number of spermatophores attached to adult females and the number of egg sacs encountered, indicated probable peaks of reproduction in summer and winter. Patterns of spermatophore placement were examined and compared with data for E. norvegica (Boeck) from boreal waters. Elemental analysis indicated a high proportion of carbon and a low proportion of nitrogen in adult females and egg sacs from both sites.High winter carbon levels in adults seem related to their predatory feeding habits allowing high food intake throughout the year whereas in egg sacs it probably reflects extended development times and/or non-feeding naupliar stages.Mean adult female and egg clutch dry weights were higher in Cumberland East Bay during winter than in Moraine Fjord during summer. These differences are discussed in the context of relationships between fjord morphology and production levels.     

Effects of salinity, temperature and individual variability on the reproduction of Eurytemora affinis (Copepoda; Calanoida) from the Seine estuary: A laboratory study

The brackish water copepod Eurytemora affinis is the most abundant copepod species in the low salinity zone (2-15) of the Seine estuary. Despite its ecological importance, little is known about its population dynamics in the Seine. We studied the effects of temperature (10 °C and 15 °C) and salinity (5, 15 and 25) on reproduction under non-limiting food conditions. We used experiments to determine multiple reproductive parameters for E. affinis. In all experiments, we fed E. affinis a mixture of Rhodomonas marina and Isochrysis galbana. Couples of pre-adult females (C5) and adult males were mated until the female extruded a clutch of eggs and then individual females were observed every 6-12 hours until death to determine (a) embryonic development time, (b) inter clutch time and (c) clutch size throughout their adult lifespan. All reproductive parameters were negatively affected by low temperature (10 °C) and by high salinity (25). At 10 °C and a salinity of 25, mortality during the post-embryonic period was extremely high (85%). Differences in all reproductive parameters between salinities 5 and 15 were minimal. From 15 °C to 10 °C mean latency time (time between hatching of eggs and extrusion of new ones) increased from 0.8 to 2.25 days, the mean embryonic development time from 2.2 to 3.2 days and the mean clutch size decreased from 38 to 22 eggs female^- 1. The mean clutch size decreased when females reached a critical age. The hatching success was high (near 95%) under all conditions except at high salinity. Egg production rates showed no significant differences between salinities 5 and 15 and were significantly higher at 15 °C (13 eggs female^- 1 day^- 1 at salinity 5 and 15) than at 10 °C (4 eggs female^- 1 day^- 1). These values at 15 °C were higher compared to those from other populations of E. affinis in estuaries or lakes. The high reproductive potential of E. affinis from the Seine estuary at 15 °C and low salinities explain its high densities in the low salinity zone during spring and early summer.     

Temporal variability of abundance and reproductive traits of Centropages kroyeri (Calanoida; Copepoda) in Bizerte Channel (SW Mediterranean Sea, Tunisia)

Abundance and reproductive traits (spawning female, egg production, egg hatching success) and naupliar survival of the dominant calanoid copepod Centropages kroyeri were investigated in relation to biotic (chlorophyll a, phytoplankton and microplankton) and abiotic (temperature and salinity) parameters at a monitoring station located in Bizerte Channel, northern Tunisia. The monitoring was carried out between July 2004 and December 2004, according to two temporal sampling strategies. First, during July, the supposed maximum abundance period of C. kroyeri, daily sampling was conducted. Thereafter, sampling was carried out weekly until the end of the sampling period.The temporal variability of the environmental factors in relation to the reproductive traits of C. kroyeri revealed, first, that temperature is important in controlling the reproduction and dynamics of this species, and second, that the quantity and quality of food available in the field also strongly influence its reproduction. On several sampling dates, the output of certain reproductive traits such as hatching success after 24 h was very weak. It is possible that C. kroyeri produced resting eggs during the study period. Nerveless, the analysis of the phytoplankton during these periods showed that low reproductive activity may have been caused by low phytoplankton quantity and/or by the dominant presence of certain diatom species that are supposed to have an inhibitory effect on the reproductive traits of C. kroyeri, especially on egg hatching success.Among the considered external parameters, temperature and food quality and availability seem to be the most important factors for the reproduction and dynamics of C. kroyeri. Under these biotic and abiotic field conditions, this copepod seems able to modulate the abundance of its population while controlling its reproduction.     

Nest-building activity and laying date influence female reproductive investment in magpies: an experimental study

Nest size or nest-building activity has recently been hypothesized to be a postmating sexually selected signal in monogamous birds: females may assess a male's parental quality and willingness to invest in reproduction by his participation in nest building. Females may thus adjust their reproductive effort (i.e. clutch size) not only to their own abilities but also to those of their mates. We investigated whether female magpies, Pica pica, use nest-building activity rather than nest size to adjust their reproductive effort during replacement breeding attempts. After we removed their first clutch, high-quality pairs that built a large nest for the first clutch were more capable of building a replacement nest and females adjusted their clutch size in relation to the time it took to build the nest rather than nest size. We also found support for the hypothesized trade-off between clutch size and egg size in magpies. In replacement clutches females decreased clutch size and increased egg volume, thereby probably improving the survival probability of their offspring in less favourable conditions.Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

Thermal dependence of reproductive allocation in a tropical lizard

In ectotherms, environmental temperature is the most prominent abiotic factor that modulates life-history traits. We explored the influence of environmental temperature on reproduction in the Madagascar ground gecko (Paroedura picta) by measuring reproductive traits of females at constant temperatures (24, 27, 30 °C). Females of this species lay clutches of one or two eggs within short intervals. For each female, we measured egg mass for the first five clutches. For one clutch, we also measured the energetic content of eggs via bomb calorimetry. Temperature positively influenced the rate of egg production, but females at 30 °C laid smaller eggs than did females at either 24 or 27 °C. Dry mass of eggs scaled allometrically with wet mass, but this relationship was similar among thermal treatments. Females at all temperatures produced eggs with similar energy densities. Females at 24 °C allocated less energy per time unit (≈8 mW) to reproduction than did females from higher temperatures (≈12 mW). However, females at either 24 or 27 °C allocated significantly more energy per egg than did females at 30 °C. Our results demonstrate that a complex thermal sensitivity of reproductive rate can emerge from distinct thermal sensitivities of egg size, egg composition and clutch frequency.     

The mating and reproductive biology of the freshwater planktonic calanoid copepod Eudiaptomus gracilis

1. Quantitative aspects of the mating and reproductive biology of the freshwater planktonic calanoid copepod Eudiaptomus gracilis, including duration and frequency of mating, duration of various phases of the oviducal cycle, egg production rate and adult longevity were studied under laboratory conditions. One set of copepods was fed the alga Chlamydomonas reinhardtii whose density was adjusted to 2 × 10⁵ cells mL^?1 (about 10 mg C L^?1), another set was fed a mixed diet consisting of natural plankton (copepod nauplii, small rotifers and large algae) in the size range of 50–150 μm (dry mass approximately 90 mg L^?1). 2. The entire mating process, from the grasping of the female by the male’s right geniculate antennule to the separation of the pair, lasted about 2 min. Spermatophore placement started at about 30 s to 1 min after mating began and took approximately 1 min. Immediately after the spermatophore had been fixed in the female’s genital segment, the pair separated. 3. The total oviducal cycle, including the gravid phase where the female carried ripe oocytes and the non‐gravid phase where the female did not carry ripe oocytes, lasted about 5–6 days. The non‐gravid phase was particularly long; it was longer than the gravid phase and constituted 62–72% of the total cycle. 4. Mating and spermatophore placement usually occurred with gravid females although occasionally (in 30 of 200 observations) spermatophores were attached in the genital segment of non‐gravid females. Generally two to four, but up to seven, spermatophores were observed at a female’s genital segment at the same time. 5. Clutch size, rate of egg production and adult longevity depended on food. When fed on C. reinhardtii, females carried 7–8 eggs clutch^?1, produced a mean of 1.3 clutches and lived 14 days on average. When fed natural mixed food, females carried 10 eggs clutch^?1, produced 5.6 clutches and lived 37 days on average. 6. Removal of males after the first clutch resulted in no further egg production. Re‐mating is necessary in E. gracilis for continuous clutch production and the production of fertile eggs. 7. Mating duration is comparatively short and the non‐gravid phase comparatively long in E. gracilis. This could be an adaption to the life in the pelagic zone of the lake, where fish predators are present. Fish select ovigerous females, pairs in copula and, probably, females with ripe oocytes which make them conspicuous. Thus, a short mating duration and a prolonged period without conspicuous oocytes, can be advantageous.     

Spawning frequency, fecundity, egg weight and spawning type of silver pomfret, Pampus argenteus (Euphrasen) (Stromateidae), in Kuwait waters

Silver pomfret, Pampus argenteus, were collected by fishing with drift gillnets on one spawning ground in Kuwait waters during 1998–2000. Fish size frequency, sex ratio, maturation cycle, spawning frequency, fecundity and egg weight were assessed. The length–weight relationship differed between sexes whereby females were significantly bigger than males. Spawning started in mid‐May and continued until early October. During this time the water temperature ranged from 26.0 to 32.8°C, salinity was ? 39.0‰ and water depth ranged between 5 and 12 m. Large females spawned earlier than young spawners and the overall percentage of males during the spawning period was 70.3%. Spawning occurred after 13.00 h, with peak spawning between 15.00 and 18.00 hours during outgoing tide. Mean daily spawning frequency amounted to 63.2%. Spawning activity was found to be associated with the lunar cycle and spawnings were concentrated during the first and third quarters of the moon period, indicating a semilunar reproduction cycle. It was concluded that a female would spawn at least six times during the season. No change was observed in relative fecundity during the peak spawning season (June–August). Average relative batch fecundity was 176.3 eggs g^?1 somatic weight (SW), corresponding to a relative total fecundity of 1058 eggs g^?1 SW, which is 1.5 times higher than estimates obtained from counting the standing stock of oocytes. Bigger fish produced heavier eggs and the egg weight decreased as the spawning season progressed. Based on gonadal cycles, oocyte size frequency distribution and total fecundity, we concluded that silver pomfret is a multiple batch spawner with indeterminate fecundity.     

On gonadic maturation and reproductive strategy in deep-sea benthic octopus Graneledone macrotyla

The new information reported in this paper is based on five maturing and mature females of the large-tuberculate octopus Graneledone macrotyla. These specimens were caught in bottom trawl surveys ATLANTIS 2009 (February 24 to April 1, 2009) and ATLANTIS 2010 (March 9 to April 5, 2010) carried out off the Argentinean Economic Exclusive Zone. Capture depth ranged from 475 to 921 m and sea bottom temperature between 2.8 and 3.1 °C. Development of the complex ovary, oviducts, and oviducal glands during gonadic maturation is described. The absence of spermathecae in the oviducal glands and the presence of fertilized eggs inside the ovary suggested that fertilization took place within the ovary. Histological techniques showed the presence of four types of oocytes. Maturing oocyte size–frequency distribution was polymodal. Fluorescence reaction showed that atresia occurred in both early and later oocyte maturation stages. Atresia affected 48–55 % of the initial number of oocytes. The maximum observed potential fecundity was estimated at 250–300 eggs. G. macrotyla showed a group-synchronous ovulation pattern, regulative atresia, and a batching spawning pattern with a few egg batches spawned intermittently over an extended period of spawning.     

Enhanced immune function does not depress reproductive output

Costs of reproduction might be mediated by a physiological (resource allocation) trade-off between immune function and reproductive effort, and several recent studies have shown that an experimental increase in reproductive effort is associated with decreased immune function. Here we test the complementary prediction of this hypothesis: that increased immune function (specific antibody production) depresses reproductive output. Female European starlings (Sturnus vulgaris) were injected with a non-pathogenic antigen (sheep red blood cells) following completion of laying of their first clutch, to stimulate an in vivo humoral immune response (primary antibody production). We induced laying of a second clutch by removing the first clutch, and assessed changes in reproductive performance in individual females pre- and post-treatment. Injection of sheep red blood cells produced a significant antibody response in 96% (n=29) of treated females, with titres comparable to previous studies (range 1 to 7). However, increased antibody production did not decrease primary or secondary female reproductive effort (re-laying interval, egg size, clutch size, chick growth or fledging success), compared with control, saline-injected birds (n=22). These data do not support a simple resource allocation model for the cost of reproduction, based on a reciprocal, negative relationship between resources allocated to immune function and reproduction.