Empirical evidence of a trade-off between reproductive effort and expectation of future reproduction in female three-spined sticklebacks

Optimal life-history models generally predict that the reproductive effort of iteroparous organisms may increase with age, as their expectation of future reproduction decreases. The population of three-spined sticklebacks (Gasterosteus aculeatus) in the Camargue (Rhone River Delta, France) is annual, all adults dying after their first breeding season. As the three-spined stickleback is a multiple spawner, we tested the hypothesis that reproductive effort may increase during the breeding season on field data. From 1987 to 1998, 653 female sticklebacks were collected in the field during the breeding seasons. The body size, body weight and weights of the liver, gonads and carcass were measured for these individuals. Only gravid females with mature eggs (176 fish) were included in the analysis. Considering the female three-spined stickleback as a capital breeder, the energetic resources available for allocation between soma and gonads were estimated by its body weight. Somatic condition decreased during the breeding season and reproductive effort (gonad weight relative to body weight) increased. These patterns did not vary significantly between years. These observed variations in reproductive effort during the breeding season can be interpreted as empirical evidence of a trade-off between reproductive effort and expectation of future reproduction.     

Condition factor and hepatosomatic index as estimates of energy status in male three-spined stickleback

Seasonal variation in direct and indirect measures of energy status was examined using estimates of glycogen, lipid and protein levels in a single cohort of male three-spined sticklebacks from an annual population collected each month over one complete year. Condition factor, somatic condition factor and hepatosomatic index (HSI) were calculated as indirect indices of energy status and the accuracy of these indirect measures as predictors of energy status was investigated. Results indicate that both condition factors were significant predictors of energy reserves (lipid, protein, glycogen and total energy), but that the proportion of variance accounted for was small. Both condition factors perform better as predictors of energy content per unit body weight. The HSI was a significant, but a weak predictor of total glycogen levels over the whole year. On a seasonal basis the relationship between HSI and energy reserves was highly variable. These indices are therefore poor predictors of energy reserves in male three-spined sticklebacks.     

Body condition changes of sand martins (Riparia riparia) during breeding, and a comparison with fledgling condition

The body condition of adult sand martins during the breeding season and a sample of fledglings was investigated by carcass analysis and by examination of live birds in the field. Fat scoring of live individuals was a reliable predictor of an individual's lipid content in most instances. Body mass changes during breeding were related to changes in the size of birds' lipid reserves, pectoral muscle mass, body water, and to development of the reproductive system. In both males and females, reserve lipid declined between the onset of breeding and nestling rearing. Pre-breeding males had significantly greater pectoral muscle masses than did nestling rearing females. The potential significance of protein in pectoral muscles as an energy reserve during breeding was small compared with lipid reserves. By comparing potential energy reserves in body lipid and protein with daily energy expenditure, it was calculated that neither incubating nor nestling rearing adults could survive a day of normal activity without feeding. The selective premium on adults optimizing their use of time and energy for self-maintenance behaviour during breeding is therefore likely to be great.     

Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection

This paper describes the results of a study of the effects of Schistocephalus solidus on one of its intermediate hosts, the stickleback Gasterosteus aculeatus , in an annual population in which infection is known to occur in one major wave in autumn. Weight, as a function of length, was lower in infected sticklebacks compared with uninfected fish during autumn and spring; in winter and summer, both categories of fish were in equally poor condition. In early autumn, the hepatosomatic indices of newly infected fish were higher than those of uninfected fish, perhaps due to a pathological response. Thereafter, relative liver size of uninfected and infected sticklebacks was comparable until spring, when it increased sharply in uninfected sticklebacks but remained stable at a low level in infected sticklebacks. Few infected fish reached maturity. The only males to attain maturity whilst sustaining an infection of S. solidus were in particularly good condition. Nuptial coloration, kidney hypertrophy and testes size were unimpaired in these mature infected males, but whether they were capable of successful reproduction remains debatable.     

Effect of sex and season on the production and deposition of lipid and glycid reserves in the intermittently starving golden hamster.

In golden hamster adapted to intermittent starvation (with access to food for 3 days a week only), the glycogen and lipid content of the liver, total body fat and RQ values measured in vivo were investigated. These parameters were studied in dependence on the duration of the adaptation period (6 weeks versus 20 weeks), season of the year (winter versus summer) and sex. The liver glycogen content in intermittently starved males and females increases after 6 weeks of adaptation during winter. In summer an increase was found after long-term adaptation, but only in males. Male hamsters also exhibited a higher ability to accumulate liver lipids during both seasons. In spite of their lower weight intermittently starving males have a higher percentage of body fat in comparison with females, a stimulating effect being observed in winter. Increased lipogenesis in golden hamsters adapted to intermittent starvation may be concluded from the increased RQ values when compared with relative data gained in controls fed daily ad libitum. Significant differences between RQ measurements according to season and sex were not found.     

Quantitative seasonal changes in the protein, lipid and energy content of the carcass, ovaries and liver of adult female plaice, Pleuronectes platessa L.

A detailed study was made of the seasonal changes in energy reserves in adult female plaice, Pleuronectes platessa L. The weights of lipid, protein, glycogen and ash in the carcass, liver and ovaries were measured in females approximately 35 cm long on ten occasions during one year. These data were converted to data for a'real'growing female by using a growth curve to take account of increasing length during the year. Growth of the whole body and of the body components was assumed to be isometric.
Plaice show a marked seasonal cycle of body weight and energy content. A six year old female plaice of 330 g, 32.6 cm long and with an energy content of 406 kcal in May, assimilates 560 kcal before December when it ceases to feed. Of this, 234 kcal is used to produce eggs, 159 kcal is used for metabolism during starvation, and the remainder 167 kcal, is used in growth. There is an increase in length to 35.9 cm and in weight to 462 g over the year. From December until March, when plaice do not feed but grow large ovaries, 40% of the protein in the body is utilised, 33% is devoted to egg production and 7% is metabolised to provide energy; 64% of the lipid is used, only 14% being used for egg production but 50% is metabolised for energy. Lipid supplies 75% of the energy for metabolism and so forms the major reserve; 42% of the energy assimilated during the year is devoted to reproduction. The main source of lipid and protein reserves is the carcass.     

Male reproductive strategy and reserve allocation in sand smelt from brackish lagoons of southern France

In male sand smelt Atherina boyeri , from three coastal brackish lagoons of southern France, the duration of the reproductive season differed according to fish size: larger fish exhibited an extended reproductive season from February to August while smaller males reproduced only from April to June-July. Smaller and larger fish showed differences in their seasonal pattern of reserves. Through the cold season, energy content was exhausted for over-winter maintenance and reproductive needs, and was restored just after fish ceased reproducing. In smaller fish, however, reserves were more rapidly restored than in larger fish, and exhibited a decrease in autumn. This result suggested that small fish invested their energy into growth and winter survival rather than reproduction while older fish invested in reproduction. These results are discussed in terms of life history Strategies.     

Seasonal changes in condition indices in adult mature and non-maturing burbot, Lota lota (L.), in the north-eastern Bothnian Bay, northern Finland

The population structure and seasonal changes in condition factors of the burbot in a shallow coastal region of the north-eastern Bothnian Bay are described. The significance of the so-called rest years is examined by comparing condition indices in immature or sterile and mature burbot. The somatic condition index ( K ₂), liver index ( K ₁), intestine index ( K ₁) and gonad index ( K_g ) are determined monthly in terms of organ weight in relation to body length. Approximately 30% of the whole catch of 1052 burbot were non-maturing but were 40 cm or more in length. K ₂, K ₁ and K ₁ were lowest in the autumn, when the first sign of gonad recrudescence was observed in mature burbot. The non-maturing burbot were never in poorer condition than mature ones. As mature and non-maturing burbot dissipated their energy stores during the warmest period of the summer, it is concluded that burbot spending a rest year do not accumulate and store energy reserves over the summer for the next year, and that such rest years, if they exist, do not occur for nutritional reasons.     

Interspecific differences in growth of somatic and reproductive tissues during the breeding season in Menidia menidia and M. beryllina

The annual atherinid fishes, Menidia menidia and M. beryllina , are extremely similar morphologically, but appear to differ in their energetics and life histories. They emerge from winter in relatively emaciated condition. Menidia menidia males and females showed little change in carcass weight but significant increases in gonad weight in March and April prior to spawning in May. Female liver weight increased in March and remained high. Thus, this species had reached its reproductive size in the autumn and allocated its energy to gonadal growth during the spring. Menidia beryllina showed no significant increases in weight until early May, when carcass, liver and gonad all increased simultaneously, a pattern very different from its congener. The later spawning of M. beryllina is probably due both to its need for carcass growth in spring prior to spawning and to its apparent requirement for warmer water for growth. Females of both species invested more into liver and gonad than did males. Maximum gonadosomatic index was about twice as large for M. menidia males as for M. beryllina males, but the index was similar for females of both species.     

Nutrition,sex and season contribute to variation in fat and glycerol levels in the long‐lived moth Caloptilia fraxinella

The ash leaf cone roller Caloptilia fraxinella Ely (Lepidoptera: Gracillariidae) is an invasive leaf‐mining moth pest of horticultural ash Fraxinus spp. in the Canadian Prairie Provinces. Caloptilia fraxinella overwinter as adults in reproductive diapause and mating occurs after overwintering in the spring. The effect of a carbohydrate food source on fat and glycerol reserves throughout the long adult life stage of this moth is investigated. Insects collected as pupae are given access to either water or sugar water upon adult eclosion. Moths held under the different feeding regimes are sampled before (summer and autumn) and after overwintering in the spring. Analysis of either glycerol or lipid content is conducted for male and female moths from each collection period. Both moth weight and glycerol concentration are affected by moth sex, food regime and season of collection. Although female moths are heavier than males, a higher glycerol concentration occurs in males. Moths fed sugar are heavier and have a higher glycerol concentration than water‐fed moths late in reproductive diapause and after overwintering. Moths collected in the spring after overwintering are lighter and have a lower glycerol content than moths collected before winter. There is a significant influence of feeding regime and season on moth body lipid content, with sugar‐fed moths having more fat than water‐fed moths; however, this difference is smaller in the summer than the autumn or spring. An initial understanding of the overwintering biology and diapause of this pest is provided in the present study.     

The seasonal partitioning of energy in an estuarine fish, the common goby, Pomatoschistus microps Krøyer

The common goby, Pomatoschistus microps , is an abundant brackish water species which has an appreciable role, both as predator and prey, in the ecosystems of British estuaries. The partitioning of energy within each sex is described and discussed, and energy values are provided for the gonad, liver and carcass throughout almost the entire life of one year class. Partitioning of resources within the body at different times of the year shows considerable variation, not only with time but also between the sexes. In particular, the energy content of the male gonad during the spawning season is never more than 3.7% of that of the female. Important aspects of the biology of the species which relate to energy partitioning are maturation at an early age, high reproductive investment, high stochastic mortality, and death usually after a single breeding season.     

Seasonal changes in condition, nutrition, gonad maturation and energy content in barbel, Barbus sclateri, inhabiting a fluctuating river

The objective of this study was to investigate the seasonal cycle of condition, nutrition and gonad development, as well as the magnitude of seasonal variations in energy content of somatic and gonad tissues in juveniles, males and females of Sclater's barbel, Barbus sclateri, from the upper Guadalete River (south Spain). The influence of reproductive cycle on somatic changes was also investigated and discussed. Measurements of condition factor (K), somatic index (SI), gonadosomatic index (GSI) and somatic and gonad energy content (J g^-1 dw) were made in individual specimens taken from the Guadalete River monthly for 12 months. This freshwater ecosystem is characterised by strong seasonal fluctuations in water and flow level, temperature and food supply. It was found that in general juveniles, males and females of barbel exhibited a similar condition, nutrition and somatic energy cycle throughout the year, with the highest values in spring and the lowest in summer. Depletion of K, SI and somatic energy storage from spring until mid-summer seems to be associated with high metabolic demands during this period, and in adult fish also with spawning-related activity. The gonad index and energy content of the gonad were the highest in April and the lowest in summer for both sexes. Spawning took place during late spring – early summer, with fish quiescent by mid summer. The energy required for ovarian development (3970 J g^-1 dw) was greater than the one for testes development (2763 J g^-1 dw). Data on gonad energy content indicated a period (March to April) of intense energy accumulation (64% males and 37% females) which was related to the decline in the average somatic energy content in males and females. The somatic energy content was linearly related to K and SI. In the same way, GSI correlated positively with gonad energy. Linear trends were found between somatic parameters (K, SI and energy content) and gonad parameters (GSI and energy content). This revised version was published online in July 2006 with corrections to the Cover Date.     

Energetic composition,reproductive output,and resource allocation of Antarctic asteroids

Summary Thirteen species of antarctic asteroids were collected in McMurdo Sound during the austral spring and summer of 1984–1985 and 1985–1986. Variability in the energetic composition of the body wall, pyloric cecum, and gonad was directly related to differences in levels of protein, carbohydrate, lipid and ash in these tissue types. Reproductive output was generally similar between males and females when expressed in gravimetric units. When considered in energy units, females generally had greater reproductive output than males. Reproductive output values of antarctic asteroids were similar to published values for temperate, tropical, and subpolar species. In a given year, the majority of antarctic asteroids have the greatest energy resources in the body wall, a tissue representing a long-term energy investment. Lesser amounts of energy are devoted to annual nutrient storage (pyloric ceca) and reproduction (gonads).     

Seasonal variations in biochemical composition during the reproductive cycle of the veined rapa whelk Rapana venosa (Valenciennes, 1846) from the northern coast of China

Seasonal variations in the biochemical composition of Rapana venosa in relation to reproductive cycle and environment on the northern coast of China were investigated from March 2012 to February 2013. The results indicated that R. venosa has an annual reproductive cycle with synchronized gonad development in both females and males. Gametogenesis was initiated in September and gametes developed slowly during the winter, followed by rapid gonad development during spring and summer. Most individuals from this study were sexually mature between May and June, and gamete release occurred mainly between May and August. The peak of spawning was found in July and the recovery of the gonad was observed between August and November. The key biochemical components including glycogen, protein and lipid were analysed in four tissues, specifically the gonad, digestive gland, mantle and foot. The declining glycogen content in the gonad, digestive gland and mantle during maturation suggested that glycogen was consumed during the development of the gonad. Lipids and protein can be stored in the digestive gland and used during the winter in a period of food shortage. The protein and lipid contents in the ovaries increased during gonad development, which suggested that the protein and lipid had been accumulated as vitellin in oocytes.     

Estradiol-17β effects on lipid and carbohydrate metabolism and on the induction of a yolk precursor in goldfish,

The effects of estradiol-17β treatment on plasma lipid levels, liver lipid and glycogen reserves were examined during different phases of the reproductive cycle in goldfish, . Estrogen therapy resulted in increased plasma and hepatic lipid levels except during the spawning season. Hepatic glycogen deposits were depleted by estradiol injections during all seasons. Treatment of fish with the estrogen antagonist, CI-628, during the spawning season caused a reduction in plasma and liver lipid levels. Electrophoretic studies conducted during the post-spawning season showed that estrogen induces the appearance of a specific lipoprotein, probably a yolk precursor, in the serum and liver of goldfish.     

Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (west coast of France)

We describe seasonal changes in the biochemical composition of digestive gland, adductor muscle and gonad and surrounding mantle area in Crassostrea gigas from the Western Atlantic coast of France. Seasonality in histology of storage tissues and glycogen storage capacity in isolated vesicular cells were also studied. Proteins, the main muscle components did not contribute to the gametogenetic effort. Glycogen and lipids were stored in the digestive gland, gonad and surrounding mantle area during the wintering period and the gonad and surrounding mantle area represented the main storage compartment supplying the reproductive effort. Gametogenesis in spring and summer was associated with an increase in lipid and protein contents and took place at the expense of glycogen reserves. Histological study of storage tissue in the gonad led us to define four seasonal stages of storage tissue development. In vitro, glycogen storage capacity in isolated vesicular cells was high from November to March and markedly reduced during gametogenesis, decreasing below detectable levels after spawning. This physiological state should be taken into account with relation to summer mortalities occurring in commercial growing areas.     

Growth energy partitioning by juvenile bluegill sunfish, Lepomis macrochirus Rafinesque

Growth energy build-up and partitioning by immature bluegill sunfish were studied over the summer months from May to September 1984. Fish sampled in May showed low condition and low lipid reserves. Condition was restored to summer levels within the following month. Fat reserves were built up from 7% to 14% of body weight over the entire summer. Most (80%) of the annual length increase occurred from 1 June to 15 August. Over the winter period (October-April) condition dropped and lipids were depleted. Calculations showed that energy liberated through lipid depletion over this period could supply the energy requirements of inactive wintering fish. It is concluded that the sequencing of growth energy diversion into changes in body length, condition, and lipid build-up enhances mid-summer growth and overwinter survival.     

Lipid dynamics and plasma level changes of 17beta-estradiol and testosterone during the spawning season of gilthead seabream (Sparus aurata) females of different ages

The present study was undertaken to evaluate whether the age of brood stock females of Sparus aurata affects the mobilization of lipids from muscle and liver towards the gonads to aid in oocyte development. Taking into account the role some hormones play in lipid mobilization the production of 17beta-estradiol (E2) and testosterone (T) was also measured throughout the spawning season. Four groups of fish were established consisting of 3-, 4-, 5- and 6-year-old females (1.3, 1.5, 2.3 and 2.8 kg average weight, respectively), maintained in separate tanks together with a number of two-year-old males. The results for all four groups showed no variations in fish total length between the beginning and end of the experimental period. However, losses were recorded both of body weight and condition factor. In general terms, there were no significant differences in the plasma levels of E2, T and the gonadosomatic (GSI) and hepatosomatic (HSI) index among the four groups throughout the spawning season. In all groups, the plasma levels of E2, T, GSI and HSI were at their lowest at the end of spawning. Between December (pre-spawning) and March (mid-spawning), all groups suffered depletion of the lipid content of liver and muscle, while gonad lipid content remained constant. The mobilization of lipids from liver and muscle to contribute to the upkeep of the gonadal lipid involved the mobilization of all the fatty acid groups, saturates, monoenes, n-6, n-3, and n-3 HUFA. A good correlation existed between the percentage of the various fatty acid groups transferred from muscle and the age of the reproductive females. However, the greater lipid mobilization from muscle matching the greater age of the reproductive females did not result in greater lipid gonadal reserves or greater body size, suggesting that reproduction on the part of older females requires greater effort. Despite this, the results as a whole indicated that lipogenic capacity, considered as the mobilization of lipids from muscle and liver towards the gonad for the development of oocytes, is unaffected by age in reproductive 3- to 6-year-old gilthead seabream females.     

Mate guarding in relation to seasonal changes in the energy reserves of two freshwater amphipods (Gammarus fossarum and G. pulex)

1. We assessed sex‐specific seasonal changes in major energy storage compounds (triglycerides, glycogen) in Gammarus fossarum and Gammarus pulex collected from the field, with respect to their reproductive activity. 2. The dynamics of stored energy followed a seasonal pattern in both species and sexes. Moreover, over a 4‐year period, these changes were independent of the year in which they were investigated. Stored energy reached a peak in late winter, but was depleted in late summer and early autumn, coinciding with the reproductive periods. 3. Triglyceride (annual mean ± SD) accounted for 79.7 ± 11.9% of the total stored energy and was responsible for the seasonal pattern. In contrast, glycogen contributed a lesser percentage (20.3 ± 11.9%). Over the study period, the amount of stored energy ranged between 0.39 and 4.08 kJ g^?1 dry mass (triglyceride: 0.19–3.69 kJ g^?1 dry mass; glycogen: 0.14–0.80 kJ g^?1 dry mass). 4. In both species, the energy reserves of males were drastically depleted shortly before the cessation of precopulatory mate guarding in the field, thus offering a bioenergetic explanation for the reproductive period in these two widespread species.     

The annual pyloric cycle of Asterias rubens L. (echinodermata: Asteroidea)

Observations of biochemical changes in the pyloric caeca of Asterias rubens L. in different nutritional states and at different stages of the reproductive cycle show the existence of an annual cycle in the pyloric caeca. This pyloric cycle is closely related to that of the gonads. During the gonadal rest (May to September, when the gonads are barely visible) the pyloric caeca grow and store glycogen. During gonadal activity (October to April), they progressively autolyse and first accumulate, then liberate, lipid reserves. This winter pyloric autolysis provides the gonads with the structural material necessary for their annual growth. The summer pyloric growth must be interpreted as the accumulation of the structural material. Under normal conditions, during gonadal rest, the pyloric glycogen reserves ensure the survival of the animal. Pyloric lipid reserves appear only at the beginning of gonadal activity. Their synthesis is intimately related to the start of the gonadal activity of which they are the principal energy source. We believe that the pyloric cycle is under control of hormones that could be transported through the haemal system.The pyloric caeca are the only reserve organs of starfish. Neither the other digestive organs nor the body wall accumulate energy reserves. During starvation of medium duration (2 to 4 weeks) the pyloric caeca suffice to ensure the survival of the animal by liberating their reserve material and simultaneously starting to autolyse. During prolonged starvation, general autolysis occurs and the size of the starfish diminishes.