Effects of early resource limitation and compensatory growth on lifetime fitness in the ladybird beetle (Harmonia axyridis)

Acceleration of growth following a period of diet restriction may result in either complete or partial catch-up in size. The existence of such compensatory growth indicates that organisms commonly grow at rates below their physiological maxima and this implies a cost for accelerated growth. We examined patterns of accelerated growth in response to temporary resource limitation, and assayed both short and long-term costs of this growth in the ladybird beetle Harmonia axyridis. Subsequent to the period of food restriction, accelerated growth resulted in complete compensation for body sizes, although we observed greater larval mortality during the period of compensation. There were no effects on female fecundity or survivorship within 3 months of maturation. Females did not discriminate against males that had undergone compensatory growth, nor did we observe effects on male mating behaviour. However, individuals that underwent compensatory growth died significantly sooner when deprived of food late in adult life, suggesting that longer-term costs of compensatory growth may be quite mild and detectable only under stressful conditions.     

Do females preferentially associate with males given a better start in life?

A poor start in life owing to a restricted diet can have readily detectable detrimental consequences for many adult life-history traits. However, some costs such as smaller adult body size are potentially eliminated when individuals modify their development. For example, male mosquitofish (Gambusia holbrooki) that have reduced early food intake undergo compensatory growth and delay maturation so that they eventually mature at the same size as males that develop normally. But do subtle effects of a poor start persist? Specifically, does a male''s developmental history affect his subsequent attractiveness to females? Females prefer to associate with larger males but, controlling for body length, we show that females spent less time in association with males that underwent compensatory growth than with males that developed normally.     

Stressful Dieting: Nutritional Conditions but Not Compensatory Growth Elevate Corticosterone Levels in Zebra Finch Nestlings and Fledglings

Unfavourable conditions throughout the period of parental care can severely affect growth, reproductive performance, and survival. Yet, individuals may be affected differently, depending on the developmental period during which constraints are experienced. Here we tested whether the nestling phase compared to the fledgling phase is more susceptible to nutritional stress by considering biometry, physiology, sexually selected male ornaments and survival using zebra finches (Taeniopygia guttata) as a model species. As nestlings (day 0–17) or fledglings (day 17–35), subjects were raised either on low or high quality food. A low quality diet resulted in significantly elevated baseline corticosterone titres in both nestlings and fledglings. Subjects showed substantial compensatory growth after they had experienced low quality food as nestlings but catch-up growth did neither lead to elevated baseline corticosterone titres nor did we detect long term effects on biometry, male cheek patch, or survival. The compensation for temporally unfavourable environmental conditions reflects substantial phenotypic plasticity and the results show that costs of catch-up growth were not mediated via corticosterone as a physiological correlate of allostatic load. These findings provide new insights into the mechanisms and plasticity with which animals respond to periods of constraints during development as they may occur in a mistiming of breeding.     

Reproductive biology of <Emphasis Type="Italic">Astyanax lacustris</Emphasis> (Characiformes: Characidae) in the southern Pantanal floodplain,upper Paraguay River basin,Brazil

We studied the reproductive biology of Astyanax lacustris in the southern Pantanal, Brazil. A total of 382 fish were analyzed from February 2009 to January 2011. The sex ratio differed significantly from 1:1, with a larger proportion of females (χ² = 27.24; p < 0.001). Females achieve higher standard length than males (mean 72.30 mm and 56.51 mm, respectively), and possess negative allometric growth while males have positive allometric growth. Size at first maturation did not differ between sexes. The greatest reproductive activity occurred during the rainy season, when temperatures were highest (November to February). Total fecundity was significantly correlated with standard length (r_s = 0.74; p = 0.01), and spawn type was total. Then, the life history traits of A. lacustris are adjusted to seasonal variation in the Southern Pantanal.     

Biology of the electric eel, <Emphasis Type="Italic">Electrophorus electricus</Emphasis>, Linnaeus, 1766 (Gymnotiformes: Gymnotidae) on the floodplain of the Curiaú River,eastern Amazonia

The evaluation of the growth patterns and reproductive strategies of fish species are vitally important for the understanding of their biology and the management of stocks. The present study focused on the Amazonian electric eel (Electrophorus electricus), which is capable of producing an electrical discharge of up to 800 V. Specimens were collected on a monthly schedule from a floodplain in the eastern Amazon basin. The gonads of these specimens were examined, and the sex ratio, growth parameters, population structure, body size at first gonadal maturation, and the gonadosomatic index were determined. A balanced sex ratio was found. Males were larger than females, and both sexes presented isometric growth, which is unusual in species with an elongated anatomy. This isometry may be related to the reduction of the coelomic cavity, and its position near the head. The spawning period coincided with the start of the rainy season, and continued until high water, with the variation in gonadal development following the fluctuations in precipitation and river water levels. The asymptotic body length in both sexes was relatively large, and was inversely related to the growth coefficient (k), with a slower growth rate being recorded in the males. Mortality rates were relatively low in comparison with most species of tropical fish. The larger size of the male may be related to their role in parental care, and sexual selection on the part of the females. These findings may be important for the management of wild stocks, as well as captive rearing.     

Social status, access to food, and compensatory growth in juvenile Atlantic salmon

Juvenile Atlantic salmon Salmo salar subjected to three weeks of cooler temperatures were 8·5% smaller than controls at the end of the temperature manipulation, but had caught up in size 20 weeks later. The behavioural means is examined by which this catch-up or compensatory growth is achieved. While on average compensating fish did not spend more time feeding, dominant fish within each group gained more exclusive access to the feeding area during periods of catch-up growth. Therefore the extent to which compensatory growth could be achieved was dependent on both the social status of the individual and the dominants' ability to monopolize the food patch.     

Influence of reproductive status,sex hormones and temperature on plasma IGF-I concentrations in sunshine bass (Morone chrysops × Morone saxatilis)

Insulin-like growth factor-I (IGF-I) concentrations in male and female sunshine bass (Morone chrysops × Morone saxatilis) were determined in March, early April, and late April in outdoor ponds at a commercial farm. Female fish were always larger than male fish; however, plasma IGF-I concentrations tended to be higher in male fish and increased as pond temperature and feeding increased in both sexes. Gonadal development was greatest in both sexes in March and declined to a regressed state by the end of April and the same pattern of change occurred with plasma estrogen and testosterone. Growth and IGF-I concentrations in sunshine bass fed estrogen, methyl testosterone, or a control diet were also determined. Growth was reduced in fish fed both sex hormones. Fish fed the control diet had the highest IGF-I levels, androgen-fed fish had intermediate levels, and estrogen-fed fish had the lowest IGF-I concentrations after 4 weeks on the diet. Plasma IGF-I concentrations appeared to respond to increasing temperature in the ponds, and were inversely related to gonadal development and sex hormones. Exogenous sex hormones resulted in a decrease in plasma IGF-I, feeding activity and growth.     

Lazy males? Bioenergetic differences in energy acquisition and metabolism help to explain sexual size dimorphism in percids

1. Differences in energy use between genders is a probable mechanism underlying sexual size dimorphism (SSD), but testing this hypothesis in the field has proven difficult. We evaluated this mechanism as an explanation for SSD in two North American percid species--walleye Sander vitreus and yellow perch Perca flavescens. 2. Data from 47 walleye and 67 yellow perch populations indicated that SSD is associated with the onset of maturation: typically, males of both species matured smaller and earlier and attained a smaller asymptotic size than females. Males also demonstrated equal (perch) or longer (walleye) reproductive life spans compared with females. 3. To examine whether reduced post-maturation growth in males was due to lower energy acquisition or higher reproductive costs we applied a contaminant mass-balance model combined with a bioenergetics model to estimate metabolic costs and food consumption of each sex. Mature males exhibited lower food consumption, metabolic costs and food conversion efficiencies compared with females. 4. We propose that slower growth in males at the onset of maturity is a result of decreased feeding activity to reduce predation risk. Our finding that SSD in percids is associated with the onset of maturity is supported by laboratory-based observations reported elsewhere, showing that changes in growth rate, consumption and food conversion efficiency were elicited by oestrogen (positive effects) or androgen (negative effects) exposure in P. flavescens and P. fluviatilis. 5. Researchers applying bioenergetic models for comparative studies across populations should use caution in applying bioenergetic models in the absence of information on population sex ratio and potential differences between the sexes in energetic parameters.     

Sex steroids, growth and condition of Arctic charr broodstock during an annual cycle

Changes in plasma concentrations of sex steroids, growth rate and condition of repeat spawning (3+) male and female Arctic charr were studied throughout an annual reproductive cycle. Individually marked fish (mean weight approx. 500 g) were held under conditions of liberal food supply, constant temperature (4° C) and simulated natural photoperiod (Tromsø, 70° N). Once each month fish were weighed, measured and blood samples taken for steroid analysis. Plasma concentrations of testosterone (T), 11-ketotestosterone (11-KT) and oestradiol-17β (E₂) were determined using radioimmunoassay (RIA). Both male and female fish displayed distinct seasonal changes in plasma concentrations of sex steroids, growth rate and condition. From February (minimal concentrations) to March all sex steroids increased slightly and these elevated concentrations were maintained until May. Thereafter, there was a second, and far more pronounced, increase in plasma steroid concentrations which culminated in peak steroid concentrations in September–October. There was then a rapid decline during the spawning period. In winter, growth rate and condition were generally low, then increased during the spring, reached a peak during the summer, and then declined with the onset of autumn. During spring (March–May), the frequency distributions of plasma testosterone concentrations in both male and female fish were bimodal. The fish of the upper modal group of the distribution had significantly higher growth rates and condition than those in the lower modal group. In summer and early autumn (June–September) the association between T and growth rate changed. Significant negative correlations between T and growth rates were observed in females. There was an increase in endocrine activity, indicated by elevated plasma sex steroid concentrations in March, 7–8 months prior to maturation. It is suggested that this may be one factor influencing the onset of spring growth and energy deposition among maturing charr.     

Sex-specific life history patterns in bluegill (Lepomis macrochirus): interacting mechanisms influence individual body size

The ultimate body size that an individual fish achieves can be a function both of direct effects of growth or indirect effects associated with the timing of sexual maturation (and associated energetic tradeoffs). These alternatives are often invoked to explain variation in body size within and among fish populations, but have rarely been considered simultaneously. We assessed how resource availability and timing of maturation interact to influence individual body size of bluegill (Lepomis macrochirus). Resource availability (high and low food) and the social structure of the population (presence or absence of large, mature males) were varied in experimental ponds. Food ration affected growth (larger fish in the high food treatments) and the social structure of the population affected timing of maturation (early maturation of males in the absence of large males). Treatment effects, however, were sex-specific; males responded to the social structure of the population and females were more responsive to resource availability. We also found individuals that became sexually mature were smaller than those that remained immature, although results were sex-specific and resource dependent. For males, individuals that matured were smaller when resources were limited; mature and immature females showed no difference in body size regardless of food ration. We show that both resource availability and the processes that control timing of maturation interact in sex-specific ways to influence body size of bluegill. These results suggest that a more robust explanation for variable body size requires consideration of sex-specific interactions between ecological (food and growth) and evolutionary (timing of maturation) mechanisms.     

Daily profiles of serum and gastrointestinal melatonin in response to daytime or night-time supply of tryptophan-rich diet in carp (Catla catla)

Influences of daytime (~10:00 h) or night-time (~22:00 h) supply of L-tryptophan (Trp)-rich diet on daily rhythm features of melatonin and arylalkylamine-N-acetyltransferase (AANAT) protein (key regulator of melatonin biosynthesis) in gastrointestinal (gut) tissue extracts, and melatonin in serum were studied in carp (Catla catla). Analysis of obtained data revealed that the mesor and amplitude values of both melatonin and AANAT in gut tissue-extracts were higher in daytime-fed fish than those supplied with food at night, and their acrophase varied from ~2 h in the daytime-fed carp to ~10 h in night-time-fed fish. Notably, initiation of stimulatory response of melatonin and AANAT in gut to Trp-rich diet varied from ~2 h (following food supply in day) to ~6 h (after food supply during night). However, in either case, their elevated levels were maintained for ~12 h. Trp-rich diet also caused increase in serum melatonin levels, and the duration of such response varied with the time of food supply. Collectively, present study not only demonstrates the role of Trp-rich diet as a potential inducer of gut melatoninergic system and modulator of daily serum melatonin profiles, but underlines the importance of the time of food supply as a determining factor of its influence as well.     

Calcium metabolism and osmoregulation during sexual maturation of river running Atlantic salmon

As Atlantic salmon return from the ocean to undertake the anadromous spawning migration up the river of origin, profound changes in calcium metabolism and osmoregulation take place. Using tartrate resistant acid phosphatase as a marker, scale osteoclast activity was found to increase throughout sexual maturation and spawning migration. Thus, the participation of osteoclasts in the elevated scale resorption observed during this phase is established. As calcium was simultaneously accumulated in the female gonads, it is proposed that the scales are resorbed in order to provide calcium for the growing ovaries. Plasma oestradiol-17 β levels were elevated in females during sexual maturation, and had decreased at the time of spawning. Plasma testosterone levels were similar in males and females during the first part of the upriver migration, but had increased in males and decreased in females at spawning. In addition to the role of these sex steroids in the gonadal growth, their possible involvement in the increased scale resorption during this phase is discussed. Plasma growth hormone and thyroxine levels were elevated in both sexes at spawning, with the triiodothyronine/thyroxine (T₃/T₄) ratio declining sharply, indicating possible roles for these hormones in the maturational process. The relatively low gill Na⁺, K⁺-ATPase activity of salmon caught in the estuary implies that the fish had already adapted to a hypoosmotic environment. During the upriver migration, the gill Na⁺, K⁺-ATPase activity decreased further, indicating that the hypoosmoregulatory ability was suppressed further during sexual maturation and spawning migration.     

Seasonal sex ratios and the evolution of temperature-dependent sex determination in oviparous lizards

Although the adaptive significance of temperature-dependent sex determination (TSD) remains a puzzle, recent models implicate a seasonal bias in offspring sex production that translates into sex-specific fitness benefits later in life. Sex-specific emergence has been linked to fitness gains in some fish, birds and reptiles, but field data supporting the occurrence of a seasonal pattern of sex ratios in oviparous lizards are lacking. We tested the hypothesis that patterns of nest site selection and seasonal temperature changes combine to inhibit the materialization of sex-biased hatching times in a population of water dragons (Intellagama lesueurii). As predicted, a seasonal increase in air and nest temperatures resulted in a sex bias by nesting date; male-producing clutches were laid 17.8 days sooner than female-producing clutches, on average. However, the seasonal ramping of nest temperatures also caused shorter relative incubation periods in the later, all-female clutches. As a consequence of this developmental ‘catch-up’, the mean hatching date for male-producing nests preceded the mean hatching date for female-producing nests by only 7.2 days. We suggest that a contracted distribution of hatching dates compared to the distribution of oviposition dates represents a general pattern for oviparous reptiles in seasonal climates, which in TSD species may largely offset the temporal disparity in nesting dates between the sexes. Although data are needed for other TSD species, such minor age differences between male and female hatchlings may not translate into fitness differences later in life, an assumption of some models for the evolution and maintenance of TSD.     

Sex differences in contaminant concentrations of fish: a synthesis

A comparison of whole-fish polychlorinated biphenyl (PCB) and total mercury (Hg) concentrations in mature males with those in mature females may provide insights into sex differences in behavior, metabolism, and other physiological processes. In eight species of fish, we observed that males exceeded females in whole-fish PCB concentration by 17 to 43 %. Based on results from hypothesis testing, we concluded that these sex differences were most likely primarily driven by a higher rate of energy expenditure, stemming from higher resting metabolic rate (or standard metabolic rate (SMR)) and higher swimming activity, in males compared with females. A higher rate of energy expenditure led to a higher rate of food consumption, which, in turn, resulted in a higher rate of PCB accumulation. For two fish species, the growth dilution effect also made a substantial contribution to the sex difference in PCB concentrations, although the higher energy expenditure rate for males was still the primary driver. Hg concentration data were available for five of the eight species. For four of these five species, the ratio of PCB concentration in males to PCB concentration in females was substantially greater than the ratio of Hg concentration in males to Hg concentration in females. In sea lamprey (Petromyzon marinus), a very primitive fish, the two ratios were nearly identical. The most plausible explanation for this pattern was that certain androgens, such as testosterone and 11-ketotestosterone, enhanced Hg-elimination rate in males. In contrast, long-term elimination of PCBs is negligible for both sexes. According to this explanation, males not only ingest Hg at a higher rate than females but also eliminate Hg at a higher rate than females, in fish species other than sea lamprey. Male sea lamprey do not possess either of the above-specified androgens. These apparent sex differences in SMRs, activities, and Hg-elimination rates in teleost fishes may also apply, to some degree, to higher vertebrates including humans. Our synthesis findings will be useful in (1) developing sex-specific bioenergetics models for fish, (2) developing sex-specific risk assessment models for exposure of humans and wildlife to contaminants, and (3) refining Hg mass balance models for fish and higher vertebrates.     

Variation of diet and food consumption of the scaldfish Arnoglossus laterna(Walbaum, 1792)

Although Arnoglossus laterna (Walbaum, 1792) is a common benthic fish in Portugal, several aspects of its feeding ecology remain incomplete. In this study, diet was examined and the food consumption estimated on inshore waters in the central coast of Portugal. The diet of the scaldfish included mainly mysids, amphipods and polychaetes, while the decapod Philocheras bispinosus Hailstone was the most frequent prey. Variation in the diet according to fish size (two size‐classes), sex and spawning/non‐spawning seasons was examined. Significant differences in diet composition were found between seasons, whereby the most frequently consumed prey in the non‐spawning season were crustaceans, while polychaetes and nemerteneans comprised most of its diet in the spawning season. The average value of the vacuity index was very similar between seasons (24.7% non‐spawning season and 25.0% spawning season). Diet overlap between size‐classes and sexes was high, but low between the two seasons. Food consumption of A. laterna was estimated based on diet characterization and evacuation rate. The estimate of the daily food consumption was 1.15 mg dry weight for the non‐spawning season and 1.67 mg dry weight for the spawning season. Significant differences in consumption rates were found between size‐classes and sexes. Larger individuals showed a higher consumption rate than smaller individuals. Females consumed more food than males in the non‐spawning season, while in the spawning season males consumed more than females.     

Quantitative analysis of compensatory and catch-up growth in diverse taxa

1.?'Compensatory growth' and 'catch-up growth' are often used interchangeably to describe the faster than optimal growth that occurs following a period of dietary restriction in the development of many animals. Concerns about the statistical analysis of these studies have drawn attention to the risk of false detection in reports of compensatory and catch-up growth. 2.?This study aims to quantify the degree to which these compensatory responses occur across the animal kingdom. In addition, this study distinguishes the two terms, 'compensatory growth' and 'catch-up growth', to clarify the fitness consequences of rapid growth. Compensatory growth refers to a faster than usual growth rate, while catch-up growth implies attainment of control size. 3.?Eight meta-analyses and meta-regression analyses were conducted on data extracted from 88 papers, including 11 taxonomic classes. The results confirmed that both growth tactics (i.e. compensatory and catch-up growth) occur across a wide range of taxa and result in decreased direct fitness components. 4.?Importantly, the meta-analytic methods used made it possible to identify the specific experimental techniques that most successfully promoted rapid growth after restriction and key differences in the responses of the four major groups (mammals, birds, fish and arthropods) to dietary restriction. Endotherms are more likely to show a compensatory growth response because of their determinate growth; in contrast, the indeterminate and saltatory growth tactics of fish and arthropods reduce the pressure to rapidly achieve a large size. 5.?Among the first meta-analyses to be conducted in this field, this study provides valuable support for the premises of compensatory and catch-up growth and also discusses weaknesses in experimental design, and possible solutions, in compensatory growth research. For example, we recommend conducting the experiment within the most linear phase of an animal's growth to avoid analytical complications arising from size-dependent growth, and our results indicate that dietary dilution more closely resembles quantitative restriction than clutch size and intermittent feeding restriction methods when normal quantitative restriction is not possible.     

Longitudinal analysis of adolescent growth in height,fatness, and fat patterning in rural South African black children

Adolescent growth in height, fatness, and fat patterning was investigated in a sample of 79 rural South African black children studied longitudinally from 6–18 years. Data were analyzed relative to peak height velocity (PHV) to identify the phenomenon of “compensatory” growth in height during adolescence and to describe changes in fatness and fat patterning. Compensatory growth following PHV was clearly observed relative to NHANES data for African-Americans in that Z-scores for height at the start of the adolescent growth spurt were greater than those at the end of the spurt. Statistically significant differences in fatness and centralization between males and females did not occur until about 2 years after PHV was attained. Centralization of fat occurred in both sexes but moreso in males. The lack of centralization in females was due to relatively greater triceps skinfold velocities. The rapid gain in post-PHV fatness in females may represent a physiological adaptation to an energetically sub-optimal environment, buffering the energetic costs of reproduction. © 1994 Wiley-Liss, Inc.     

Sexual differences in the diet of king cormorants at Macquarie Island

Sexual differences in the diet of king cormorants,Phalacrocorax albiventer, were investigated during the 1993/1994 austral summer at Macquarie Island. The major food items, identified by otoliths in regurgitations, were demersal fish; fish mass consumed could be estimated using a wet mass-otolith length relationship. Two fish species,Paranotothenia magellanica andHarpagifer georgianus, constituted 98% of the wet mass (male and female cormorants combined). Estimated individual fish mass ofParanotothenia magellanica (19.6±11.6 g) was greater than that ofH. georgianus (2.8±1.3 g). Total wet mass of food and number of fish in regurgitations did not differ statistically between the sexes of cormorants. However, males tended to feed on larger fish than did females.     

Failure to induce over-compensation of growth in maturing yellow perch

Unlike juvenile F1 male bluegill Lepomis macrochrus × female green sunfish L. cyanellus , maximized episodes of compensatory growth (CG) in 2 year yellow perch Perca flavescens did not surpass control masses because internal regulation caused abrupt appetite reduction upon catch-up. Together, the hybrid sunfish study and present work indicate that CG-maximizing feeding schedules and absence of an internal growth limiting mechanism are both required to produce substantial growth overcompensation (GOC). The less vigorous and less resilient CG responses of the yellow perch relative to those of the similarly fed hybrid sunfish appear indicative of the lack of GOC capacity in the former. This contrast, and results of previous studies are interpreted to suggest that GOC capacity may be limited to early life stages of fishes which have a substantial reproductive potential but are at high risk of mortality due to their small size. The possibility that GOC capacity is time-of-year-dependent and species-specific is considered also. Food deprivation periods that produced the strongest CG responses differed for male (2 days) and female (12 days) yellow perch. Among controls fed without restriction, growth rate and growth efficiency of female yellow perch exceeded those of males two-fold, however, males showed a greater capacity to catch-up to same-sex controls when undergoing CG. A feeding schedule using maintenance feeding v. food deprivation to elicit CG yielded the most rapid catch-up to control masses in the yellow perch. Such feeding schedules may produce even greater GOC than was achieved previously in hybrid sunfish, where feeding schedules involving food deprivation were employed.