Reproduction in puyen, Galaxias maculatus (Pisces: Galaxiidae), in the southernmost extreme of distribution

Reproductive aspects of a peripheral population of Galaxias maculatus are described and the relationship with the physiology and handling of energetic reserves under marginal environmental conditions is investigated. The G. maculatus population of Tierra del Fuego has an extended reproductive season, with differences in timing and duration compared to other populations of continental Patagonia, New Zealand and Australia. Elevated gonadosomatic indexes (I_G) were observed during this period in both sexes (maximum I_G = 33.49% males; 35.94% females). The high abundance of mature males (with high I_G values) on the spawning grounds during the reproductive season suggests that they were waiting for the return of the mature females. Larger females reached total maturation at the beginning of the reproductive season, whereas the size of maturing females diminished toward the end (mean TL = 96 mm, October; 70 mm, February). Both sexes showed an extremely high investment in reproduction, reaching a maximum I_G of about 35% for both sexes. At the beginning of the reproductive season females reached the maximum median I_H (3.37%) and males the minimum (0.96%), suggesting differences in the role of the liver in the management of energetic reserves during sexual maturation. The variation in the fat index (I_F) suggests that fat reserves were used to survive winter (maximum median I_F > 1%, autumn; minimum about 0.2%, spring).     

Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome

White-nose syndrome (WNS) is a new disease of bats that has devastated populations in eastern North America. Infection with the fungus, Geomyces destructans, is thought to increase the time bats spend out of torpor during hibernation, leading to starvation. Little is known about hibernation in healthy, free-ranging bats and more data are needed to help predict consequences of WNS. Trade-offs presumably exist between the energetic benefits and physiological/ecological costs of torpor, leading to the prediction that the relative importance of spring energy reserves should affect an individual''s use of torpor and depletion of energy reserves during winter. Myotis lucifugus mate during fall and winter but females do not become pregnant until after spring emergence. Thus, female reproductive success depends on spring fat reserves while male reproductive success does not. Consequently, females should be “thrifty” in their use of fat compared to males. We measured body condition index (BCI; mass/forearm length) of 432 M. lucifugus in Manitoba, Canada during the winter of 2009/2010. Bats were captured during the fall mating period (n = 200), early hibernation (n = 125), and late hibernation (n = 128). Adult females entered hibernation with greater fat reserves and consumed those reserves more slowly than adult males and young of the year. Consequently, adult females may be more likely than males or young of the year to survive the disruption of energy balance associated with WNS, although surviving females may not have sufficient reserves to support reproduction.     

Seasonal variation in body composition and morphology of adult muskrats in central Saskatchewan, Canada

We quantified seasonal variation in body composition and morphology of adult muskrats ( Ondatra zibethicus ) inhabiting freshwater marsh environments in central Saskatchewan, Canada. The study areas were characterized by long and cold winters extending over six months during which muskrats were restricted to foraging under ice. A total of 162 adult muskrats were collected during nine sampling periods across the year. The large accumulation of fat reserves (16% of body mass) during winter and the concurrent decline in protein mass suggested a reduced maintenance requirement associated with the presence of energy-rich food resources. Dietary fibre content increased significantly during mid-summer and was manifested by changes in gut morphology. Mobilization of fat reserves during summer months by both sexes reflected high energetic demands for reproduction. Males depleted fat reserves soon after spring break-up, while near-exhaustion of fat reserves in females occurred 4–6 weeks later, during lactation. Pregnant females contained significantly greater fat and protein reserves compared to non-pregnant and lactating females. The dynamics of body reserves in muskrats should be viewed as an integral part of the sex-specific life-history traits of this important herbivore species of marsh environments.     

Comparison of mesenteric and tissue fat content in relation to sexual cycle of the sardine, Sardina pilchardus (Walb., 1792), in the eastern Middle Adriatic fishery grounds (Croatia)

The study objective was to analyse Sardina pilchardus (Walb., 1792) for mesenteric fat, which is easier to evaluate than the muscle lipid, for comparisons thereof with the sexual cycle and condition of the examined specimens. Fat reserves, moisture and the sexual cycle of sardines were studied from monthly random samples of purse seine catches from March 2004 to February 2005. A total of 1209 specimens were collected (668 males; 541 females). Total length and mass ranged from 13.0 to 19.0 cm and from 16.7 to 51.5 g, respectively. Lipid analyses in muscle tissues were done using the Soxhlet method. An inverse relation between fat content and the sexual cycle was established. Greatest fat quantities were observed in August (72%) during the gonadal resting phase; lowest values were noted in winter, and in spring during the spawning period peak. Moisture content and sexual cycle were positively correlated ( r  = 0.7913). Total lipids in sardine tissues were higher in females than in males; however, the moisture content was higher in males than in females.     

Lipid levels in the South Island pied oystercatcher (Haematopus ostralegus finschi)

Wing lengths and some major body components were compared among the sexes and age classes of a sample of 48 South Island pied oystercatchers (Haematopus ostralegus finschi). Immature males were significantly lighter in wet weight and fat‐free weight than either immature females or adults, and were significantly lighter than adults in lean dry weight. No statistical differences were found in wing length, total lipids, or fat measure for birds in this sample. In a larger sample of 182 birds, fat measure varied similarly in the age classes, from a low in autumn to a peak in spring just before vernal migration. Massive pre‐migratory fattening typical of many small passerines does not occur in this species, but even so the average fat reserves in spring adults are sufficient for an approximate flight range of 2140 km, well in excess of need. It is hypothesised that the amount of fat deposited before vernal migration is a compromise between the energy cost of acquiring and transporting extra fat and the advantages of arrival at the breeding grounds with sufficient fat reserves for early achievement of breeding condition.     

Fat is sexy for females but not males: the influence of body reserves on reproduction in snakes (Vipera aspis)

Reproduction is energetically expensive for both sexes, but the magnitude of expenditure and its relationship to reproductive success differ fundamentally between males and females. Males allocate relatively little to gamete production and, thus, can reproduce successfully with only minor energy investment. In contrast, females of many species experience high fecundity-independent costs of reproduction (such as migration to nesting sites), so they need to amass substantial energy reserves before initiating reproductive activity. Thus, we expect that the relationship between energy reserves and the intensity of reproductive behavior involves a threshold effect in females, but a gradual (or no) effect in males. We tested this prediction using captive vipers (Vipera aspis), dividing both males and females into groups of high versus low body condition. Snakes from each group were placed together and observed for reproductive behavior; sex-steroid levels were also measured. As predicted, females in below-average body condition had very low estradiol levels and did not show sexual receptivity, whereas males of all body condition indices had significant testosterone levels and displayed active courtship. Testosterone levels and courtship intensity increased gradually (i.e., no step function) with body condition in males, but high estradiol levels and sexual receptivity were seen only in females with body reserves above a critical threshold.     

Fat cycling in the mosquitofish (Gambusia affinis): fat storage as a reproductive adaptation

Summary We argue, based on reviewed literature covering reptiles, amphibians, birds, and fish, that fat storage may represent a life history adaptation because it enables an organism to shift in time when resources are allocated to reproduction. We applied these arguments to fat and population cycles in three populations of the mosquito fish, Gambusia affinis. For males, there appeared to be a constant size at maturation during the reproductive season. Mature males became scarce late in the summer. At the same time, immature males delayed maturity and attained much larger sizes; they matured in large numbers in the fall. The amount of stored fat tended to be equal for immature and mature males at all times except in the late summer. In the August samples, when mature males were relatively rare, they also had the lowest level of fat reserves. It appears that the older generation of mature males did not store fat and did not overwinter. At the same time, immature males registered a two to three fold increase in fat reserves. These differences in fat content between mature and immature males disappeared by September, probably because of the recruitment of a new generation of mature males. The reserves were gradually utilized during the winter. Females reproduced from the late spring through mid- to late-summer. They stopped reproducing in the late summer, when there was ample time to produce an additional litter of young. There was an inverse relationship between resources devoted to reproduction and fat reserves. As reproductive allotment decreased in the late summer, fat reserves increased. The magnitude of the change in fat reserves was similar to that displayed by males. The reserves were depleted over the winter. Significant reserves remained at the beginning of the reproductive season the following spring. Reproducing females utilized the remaining reserves significantly more rapidly than non-reproducing females. An analysis of resource availability revealed an overall decrease in food availability in the late summer, coincident with the increase in fat reserves. These cycles are therefore not attributable to changes in resource availability. They instead indicate a change in how resources are allocated by the fish. The trends in the data indicate that fat reserves are used to shift investment in reproduction from the late summer to the following spring. In males, deferring maturity, rather than maturing in August, allows them to store the necessary reserves to survive the winter so that they can mate the following spring. In females, a subset of the fat reserves is intended for producing the first clutch of eggs the following spring. The female pattern corresponds to those reported for a diversity of organisms. The possible advantages of shifting reproductive effort from the fall to the following spring include higher fecundity and higher offspring fitness. The limitations of the methodology and potential directions for future research are discussed.     

Sexual conflict and environmental change: trade-offs within and between the sexes during the evolution of desiccation resistance

Intralocus sexual conflict occurs when males and females experience sex-specific selection on a shared genome. With several notable exceptions, intralocus sexual conflict has been investigated in constant environments to which the study organisms have had an opportunity to adapt. However, a change in the environment can result in differential or even opposing selection pressures on males and females, creating sexual conflict. We used experimental evolution to explore the interaction between intralocus sexual conflict, sexual dimorphism and environmental variation in Drosophila melanogaster. Six populations were selected for adult desiccation resistance (D), with six matched control populations maintained in parallel (C). After 46 generations, the D populations had increased in survival time under arid conditions by 68% and in body weight by 20% compared to the C populations. The increase in size was the result of both extended development and faster growth rate of D juveniles. Adaptation to the stress came at a cost in terms of preadult viability and female fecundity. Because males are innately less tolerant of desiccation stress, very few D males survived desiccation-selection; while potentially a windfall for survivors, these conditions mean that most males’ fitness was determined posthumously. We conjectured that selection for early maturation and mating in males was in conflict with selection for survival and later reproduction in females. Consistent with this prediction, the sexes showed different patterns of age-specific desiccation resistance and resource acquisition, and there was a trend towards increasingly female-biased sexual size dimorphism. However, levels of desiccation resistance were unaffected, with D males and females increasing in parallel. Either there is a strong positive genetic correlation between the sexes that limits independent evolution of desiccation resistance, or fitness pay-offs from the strategy of riding out the stress bout are great enough to sustain concordant selection on the two sexes. We discuss the forces that mould fitness in males under a regimen where trade-offs between survival and reproduction may be considerable.     

Flight energetics in relation to sexual differences in the mating behaviour of a mayfly,Siphlonurus aestivalis

Summary Mayflies (Ephemeroptera) are known to have short adult life-spans. Adults are unable to feed, and they utilize reserves stored during their aquatic larval stage. Energy reserves (fat, glycogen, and free sugars) of mature larvae, subimagoes and imagoes of both sexes of Siphlonurus aestivalis Eaton were compared. All the stages of both sexes had low glycogen and free sugar contents, and the only significant change occurred during the transformation of the mature larva to subimago when almost all the reserves of free sugars were used up. Glycogen and free sugars may serve as energy sources permitting individuals to swim and fly out of the water during emergence. Fat made up most of the energy reserves of mature larvae and was the main source of energy used during the final development of both sexes. Young adult males had high fat reserves which they used as a source of energy for their swarming flights. In contrast, females did not seem to use a significant amount of fat for flight. This difference is probably related to the different mating strategies of the sexes in this species. Males perform long flights waiting for females, whereas females perform only brief flights to mate and reproduce.     

Flexible response to short‐term weather in a cold‐adapted songbird

To improve survival during winter, temperate species use a variety of behavioural and physiological adaptations. Among songbirds, the maintenance of lipid reserves is a widely‐used strategy to cope with the severity of winter; however, little is known regarding how multiple synchronously acting environmental mechanisms work together to drive these effects. In a context where temperate winter conditions are becoming more variable, it is important to widen our understanding regarding the flexible adaptations that may allow wintering species to adjust to projected climate change. Using a long‐term dataset collected across multiple wintering populations (7 years; 8 locations), we analyzed the effects of daily variation in weather (e.g. temperature, snowfall) on the variation in energy reserves (i.e. fat stores) of wintering snow buntings Plectrophenax nivalis. Our results support the prediction that birds carry more reserves to increase the safety margin against starvation when conditions are energy‐demanding and access to food is unpredictable (i.e. colder, snowier conditions). Birds responded to daily changes in weather by increasing their reserves as conditions deteriorated, with maximal temperatures and snow depth being the most important predictors of fattening decisions. We also found that females consistently exhibited higher fat reserves than males relative to their body size, suggesting that differential physiological adaptations among sexes or social dominance may play an additional role in explaining variation in energy reserves across individuals in this species. Overall, our findings increase knowledge on phenotypic adjustments used by species wintering in temperate zones to match variation in their environment.     

Growth, maturation and reproductive investment in Arctic charr

Size and rates of growth in a cohort of 1 + Arctic charr housed in standard conditions were tracked over 12 months (December to December) and mature and immature males and females compared retrospectively. In both sexes, maturing fish were larger than non-maturing ones. In males, this size differential was the result of differences in growth in winter and early spring, but not in the remainder of the study period. In females, size differentials resulted mainly from growth rate differences immediately prior to breeding. In females but not in males, gonadosomatic index was predicted by growth rates in the months leading up to maturation, and among the females that matured, faster growing fish produced more eggs. Lipid reserves in July were correlated negatively with growth during the previous 7 months and, in females only, lipid reserves were significantly lower in maturing fish than in non-maturing fish, indicating that mobilization of lipid energy reserves in maturing fish had commenced by this time. Variation in investment in gonadal tissue, measured as gonadosomatic index, was not explained by variation in July lipid reserves for either males or females. However, July lipid reserves were negatively correlated with egg number, so females investing more in ova exhibited greater depletion of lipid reserves. These results are discussed in the context of the relationship between body condition and the onset of maturation in salmonids, relative investment in reproduction and sexual differences in the cost of reproduction.     

The energetic costs of tail autotomy to reproduction in the lizard Coleonyx brevis (Sauria: Gekkonidae)

Summary Energy reserve utilization and energy budgets were compared in tailed and tailless adult female Coleonyx brevis. Carcass, fat body and caudal energy reserves were used for vitellogenesis; mass and energy content (cal/mg and/or cal/reserve) of each were significantly lower at oviposition than at the initiation of vitellogenesis. Total energy reserves accounted for 53% of the reproductive energy investment in tailed females compared to 29% in tailless females. Tailed females had over twice as many reserve calories for egg production than tailless females. Caudal energy reserves represented 60% of the total reserves of tailed females and were one-third greater than the total energy reserves of tailless females. To produce a clutch of eggs both tailed and tailless females supplemented energy reserves with net metabolizable energy that was available after metabolic costs were paid. Tailless females had a significantly greater rate of food ingestion and more net metabolizable energy available for reproduction than tailed females, yet allocated significantly fewer calories/day to reproduction than tailed females, primarily because of the loss of caudal reserves. Reproductive efforts of tailed and tailless females were equivalent. However, the loss of caudal reserves resulted in the production of eggs that were significantly lower in mass and energy content (cal/mg and cal/egg) than when caudal reserves were used. Results empirically support the hypothesis that reproduction has energetic priority over tail regeneration in short-lived, iteroparous species with a low probability of future reproductive success.     

Allocating protein to reproduction in arctic reindeer and caribou

Reindeer (Rangifer tarandus tarandus) and caribou (Rangifer tarandus granti) use body stores (capital) and food intake (income) for survival and reproduction. Intakes of low-nitrogen (N) food declined in winter and increased in spring (51-83 g dry matter kg(-0.75) d(-1)). Reindeer calved before regaining food intake, whereas caribou calved 28 d later. Body N was conserved by minimizing oxidation of amino acid N to urea. Maternal protein stored from early winter was used for 96% of fetal growth in reindeer but only 84% of fetal growth in later-birthing caribou. Both subspecies rely on maternal body protein for 91% of the protein deposited in the neonate via milk over the first 4 wk. All females lost body protein over winter, but lactating females continued to lose protein while nonreproductive females regained protein. Net costs of lactation above maintenance were greater for N (110%-130%) than for energy (40%-59%). Large fat stores in reindeer spare body protein from oxidation in winter, whereas in caribou, less fat with the same body protein favors migration when food is inadequate. The resilience of Rangifer populations to variable patterns of food supply and metabolic demand may be related to their ability to alter the timing and allocation of body protein to reproduction.     

Proximate control and adaptive potential of protandrous migration in birds

Migration determines where, when, and in which order males and females converge for reproduction. Protandry, the earlier arrival of males relative to females at the site of reproduction, is a widespread phenomenon found in many migratory organisms. Detailed knowledge of the determinants of protandry is becoming increasingly important for predicting how migratory species and populations will respond to rapid phenological shifts caused by climatic change. Here, we review and discuss the potential mechanisms underlying protandrous migration in birds, focusing on evidence from passerine species. Latitudinal segregation during the non-breeding period and differences in the initiation of spring migration are probably the key determinants of protandrous arrival at the breeding sites, while sexual differences in speed of migration appear to play a minor role. Experimental evidence suggests that differences between the sexes in the onset of spring migratory activity are caused by differences in circannual rhythmicity or by photoperiodic responsiveness. Both of these mechanisms are hardwired and could prevent individuals from responding plastically to chronic changes in temperature at the breeding grounds. As a consequence, adaptive changes in both the timing of arrival in spring and of reproduction will require evolutionary (genetic) changes of the cue-response systems underlying the initiation and extent of migration in both males and females.     

Control of reproduction and a survival cost to mating in female Bicyclus anynana butterflies

Abstract.  1. Given that sexual conflict is all pervasive, investigating potential costs to mating and the control of female reproduction are important issues.
2. Here, female reproductive output and longevity are investigated in relation to mating status (virgin vs. once-mated females) and host-plant availability in the tropical butterfly Bicyclus anynana .
3. Both factors significantly affected realised fecundity in a manner demonstrating that female reproduction is not entirely under control of the female herself, but is rather subject to additive contributions of the female, her male partner, and intrinsic physiological processes. As evident from the deposition of significant egg numbers by virgin, host-deprived females, B. anynana is effectively unable to completely inhibit oogenesis.
4. Mated females suffered a reduction in adult life span, which cannot be explained as a side-effect of variation in egg size, lifetime, or early fecundity.
5. Such detrimental effects of mating per se are indicative of the cooperation–conflict balance between sexes being shifted towards conflict in B. anynana .     

Age-specific reproductive performance of female polar bears (Ursus maritimus)

Age-specific patterns of maternal weight, litter size, litter weight and reproductive effort were investigated for polar bears ( Ursus maritimus ) from western Hudson Bay. Most relationships were described by quadratic equations. Maternal weight in spring and autumn increased until 17 and 15 years of age, respectively, and then declined. Age-related increases in maternal weight were thought to be associated with improving hunting skills. The relationships between age and litter size, litter weight and reproductive effort, in both the spring and autumn, increased until 14 to 16 years, followed by a decline. We speculate that age-related decreases in reproductive performance are due to undetennined processes associated with ageing that impair the accumulation of fat stores necessary for reproduction. Pregnant females lost an average of 127 kg overwinter which represented an average of 43.5% of their autumn weight. Fat stores remaining after the overwinter fast may be critical for maintaining an energy supply to cubs once they return to the sea ice where the distribution and abundance of their prey is unpredictable. We suggest that maternal condition is an important factor contributing to lifetime reproductive success in polar bears.     

Reproductive ecology of Vipera latastei, in the Iberian Peninsula: implications for the conservation of a Mediterranean viper

Eurosiberian vipers have been considered model organisms, and studies on their reproductive ecology have afforded much of the current knowledge concerning viviparity in snakes. However, such studies are biased towards northern species and there is little information on Mediterranean species and/or populations. The reproductive ecology of Vipera latastei in the Iberian Peninsula was studied by analysing a large sample of specimens from collections, to better understand the conservation status of this Mediterranean viper. Males and females matured at small and similar body sizes (240 and 265 mm snout-vent length, respectively) and reproductive cycles in both sexes were seasonal. Spermatogenesis peaked in August, vitellogenesis developed in spring and the timing of the mating period was puzzling, with populations mating in autumn, spring, or in both seasons. The most striking finding was that adult females reproduced triennially on average. Lataste's viper is currently in continuous decline in the IP, and most of its populations are isolated in Mediterranean mountains. We hypothesize that prey scarcity and the brevity of the activity period in mountain habitats diminishes the ability of vipers to recover over the short term the energy expended in reproduction. The species needs 2 years for the acquisition and storage of energy ("capital breeder"), and a third year for the expenditure of this energy (in vitellogenesis and embryogenesis), a year during which females feed consistently ("income breeder"). Thus, this viper combines both strategies to supply the reproductive energy cost. Current decline in population and distribution, together with a poor capacity to renew populations, renders Lataste's viper vulnerable to environmental stochasticity.     

Temporal changes in fat and protein levels in the tropical Anabantid Trichogaster pectoralis (Regan)

Samples of a wild population of the Anabantid Trichogaster pectoralis (Regan) were taken during and after one of the two main breeding periods of the year. Carcasses of both sexes and female gonads were analysed for fat, protein and carbohydrate. Carbohydrates were present in insignificant amounts in all tissues. The fat content of the ovary proved to be high (over 30% of wet weight) and, as a result, ovarian energy in a ripe female formed a substantial proportion of the total energy content of the fish. However, it did appear possible for females to develop large ovaries without depleting the carcass fat stores.
Although protein levels in the carcass were significantly higher in 1 month, relative to fat levels, protein levels remained fairly constant during the period of study. Conversely fat levels showed marked fluctuations throughout the breeding period, being high at the start of the breeding period, low towards the end, finally rising again 1 month after most fish had terminated breeding. The range of fat levels appeared to be independent of the gonadal state of the fish at capture and seemed more closely related to month of capture. Two explanations are suggested; (1) changes in food availability over the period in question and/or (2) if repeated spawnings occur this could deplete fat reserves in the carcass.
In this species fat is stored largely in the muscle but some is stored around the coiled intestine. A visual scoring system was used to assess the extent of this fat deposition and it was found that the fat score was correlated with the level of fat in the carcass. Thus the level of fat around the intestine, although insignificant relative to carcass fat, could be used as a method of assessing the fatness of a fish.     

Both sexes suffer increased parasitism and reduced energy storage as costs of reproduction in the brown anole,Anolis sagrei

Sexual selection theory proposes that males suffer reduced immune function and increased parasitism as costs of expressing sexual signals. Life‐history theory proposes that females suffer the same costs because of inherent trade‐offs between reproduction and self‐maintenance. Mechanistically, each theory invokes an energetic trade‐off, although few experiments have directly compared these costs of reproduction between the sexes as a result of fundamental sex differences in the nature of reproductive investment and a tendency for each theory to focus on a single sex. To test whether males and females experience comparable costs of reproduction in terms of energetics, immune function, and parasitism, we used gonadectomy to eliminate most aspects of reproductive investment in wild brown anole lizards (Anolis sagrei) of both sexes. We compared these nonreproductive males and females with intact, reproductive controls with respect to stored energy (fat bodies), immune function (swelling response to phytohemagglutinin), and the prevalence and intensity of infection by four types of parasite (gastric nematodes, intestinal nematodes, faecal coccidia, and ectoparasitic mites). Gonadectomized anoles experienced dramatic increases in fat storage that were accompanied by decreases in the prevalence of intestinal nematodes and in the intensity of coccidia infection. These costs of reproduction were comparable between males and females, although neither sex exhibited the predicted increase in immune function after gonadectomy. Our results suggest that, despite fundamental sex differences in the nature of reproductive investment, both male and female anoles experience similar costs of reproduction with respect to energy storage and some aspects of parasitism.