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Try out PMC Labs and tell us what you think. Learn More. The relationship between growth and sexual maturation is central to understanding the dynamics of animal populations which exhibit indeterminate growth. In sequential hermaphrodites, which undergo post-maturation sex change, the size and age at which sex change occurs directly affects reproductive output and hence population productivity.
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However, these traits are often labile, and may be strongly influenced by heterogenous growth and mortality rates. We analysed otolith microstructure of a protandrous i. Growth trajectories of individuals with contrasting life histories were examined to elucidate the direction and extent to which growth rate influences the size and age individuals change sex.
Then, the relationships between growth rate, maturation schedules and asymptotic maximum size were explored to identify potential trade-offs between age at female maturity and growth potential.
Rapid growth was strongly associated with decreased age at sex change, but this was not accompanied by a decrease in size at sex change. Individuals that were caught as large females grew faster than those caught as males, suggesting that fast-growing individuals ultimately obtain higher fitness and therefore make a disproportionate contribution to population fecundity.
These indicate that individual-level variation in maturation schedules is not reflective of trade-offs between growth and reproduction. Rather, we suggest that conditions experienced during the juvenile phase are likely to be a key determinant of post-maturation fitness. These findings highlight the vulnerability of sex-changing species to future environmental change and harvest. Sequential hermaphroditism, where organisms undergo ontogenetic sex change, is a striking life history feature of a wide range of marine fishes, invertebrates molluscs and crustaceans and plants.
Sex-changing species may breed initially as males before transitioning into females protandryor vice-versa protogynywith some species also capable of bi-directional sex change 1. Because the sexes are not evenly distributed throughout age and size classes in hermaphroditic species, extrinsic factors e. As such, understanding the extrinsic and intrinsic factors regulating sex change is an essential aspect of managing exploited populations of hermaphroditic species 578. Considerable research effort has been dedicated to examining the evolutionary mechanisms underpinning sequential hermaphroditism 9 — In such systems, large female body size is favoured due to the increased size facilitating higher fecundity, while small males are still able to successfully compete for mating opportunities alongside larger males.
Alternatively, protogyny is favoured when large size enables dominant males to monopolise reproductive access to females.
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Sex allocation theory predicts that individuals should change sex when the reproductive value i. In cases where social hierarchy governs mating opportunities, as with most protogynous fishes, sex change may be initiated in response to changes in hierarchy structure such as the death of the dominant male within a harem 111315 Where near-random mating occurs with respect to male body size as typical of protandrous speciessex change may be triggered once a sufficient size or age is attained hermaphrodite dating Savannah GA Growth in most fishes is indeterminant and the size and age at sexual maturation is thus strongly influenced by growth rate and mortality risk 19 The relationship between growth rate and the timing of sex change within and among species can, however, be flexible 5 In some species, sex change may occur at a relatively consistent size or age, whilst in others considerable overlap is evident in the age and size distributions of males and females 521 Other individuals delay sex change, despite attaining a size and age at which sex change may be expected 17 Such life-history divergences among individuals may be shaped by a wide range of factors, such as differences in individual physiology or morphology, local environmental conditions, and intra-specific social interactions 25 — The cues that affect the timing of sex change must be well understood to predict population-level responses to disturbances, such as fishing harvest and climate change 5.
An inherent property of sequentially hermaphroditic species is that reproductive success is higher in the second sex 1228which makes them susceptible to anthropogenic disturbance via several mechanisms. First, size-selective fishing practices may disproportionally target the larger sex, resulting in increasingly skewed sex ratios and potentially reducing egg and sperm production in protandrous and protogynous species, respectively 5.
Second, subsequent compensatory declines in the length and age at which sex change occurs may have the effect of reducing population fecundity, despite partially offsetting skewed sex ratios 8hermaphrodite dating Savannah GA Third, degradation of aquatic habitats and climate change may impact growth and mortality rates which, in turn, may alter the timing of sex change in sequentially hermaphroditic species. The aim of the current study was to investigate the relationship between individual growth rate and the timing of sex change in the barramundi or Asian sea bass Lates calcarifer.
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Barramundi is a facultatively catadromous, protandrous fish that inhabits coastal and fresh waters throughout the Indo-West Pacific region, where it supports ificant commercial, recreational and subsistence fisheries Barramundi have widely been considered to mature as males at 3—5 years before transitioning to females at 4—8 years, a process reportedly driven by age rather than hermaphrodite dating Savannah GA A small percentage of barramundi are primary females 31and some individuals skip spawning as males and reproduce for the first time as females Spawning coincides with spring tides during the monsoonal wet season in saline estuaries or associated coastal areas Females may spawn several times over the course of a breeding season, and males may fertilise the eggs of multiple females 33 Barramundi typically form large aggregations on the spawning grounds, suggesting that mating occurs randomly throughout the population and is not restricted to social groups Growth rates are highly variable among systems, habitats, cohorts and individuals 323536although the link between growth rates and maturation remains unclear.
We investigated the relationship between age-specific growth rates in barramundi and age-at-sex change and size-at-sex change. Additionally, relationships between juvenile growth rate and size-at-age were analysed to explore potential trade-offs between growth, age-at-sex change and adult body size. Growth rates were compared between groups of individuals with contrasting sex change schedules to examine the influence of growth rate on the timing of protandrous sex change.
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The are discussed with regards to their potential implications on population fecundity and productivity. Barramundi otoliths were collected between and from the Fitzroy river catchment in the wet-dry tropical region of northern Western Australia Figure S1 Discharge is highly seasonal, with flows peaking during the monsoon December—Apriland then progressively decreasing during the dry season May to November.
During the dry season, the river is usually restricted to a series of isolated pools that are sustained by alluvial aquifers 37 Otolith microstructure was analysed to explore barramundi growth throughout ontogeny using annual growth increments as a proxy for somatic growth see A total of barramundi were collected using recreational hook and line and commercial gill nets fishing methods from a range of sites within estuarine and freshwater reaches of the river and associated tributaries, as well as from King Sound see Total length mm and weight g were recorded and the sex of each fish was determined by gonad examination via dissection.
One otolith from each fish was embedded in 2-part epoxy resin, sectioned transversely through the primordium and mounted on glass slides. The age of each fish was estimated by counting the of annuli in each otolith section The second otolith from of these fish was selected for growth analyses. A transect along the proximal axis from the core to the outer edge was used to recreate the growth history of each fish.
Reconstruction of growth histories via otolith increment analysis explicitly assumes that otolith growth is proportional to somatic growth across the life history In our barramundi samples, regression analysis demonstrated the fish length L —otolith radius R relationship was influenced by fish age, with older fish tending to have larger otoliths for their size than younger fish i. Therefore, otolith increments were converted to back-calculated fish growth in mm based on length at capture.
Therefore, a back-calculation model was developed using the Polynomial Scale Proportional Hypothesis, following the methods outlined by Vigliola and Meekan 44 :. Each annual growth estimate was ased a growth year based on back-calculation from known date of capture. A substantial impediment to drawing comparisons between contrasting sex change schedules in our barramundi samples is that the precise ontogenetic timing that an individual transitioned from male to female is unknown.
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Fish harvested as old, large females may have transitioned several years prior, whilst individuals captured as young, small males may have imminently transitioned into females had they not been captured. To address this issue, analyses were focused on three separate comparisons between groups of individuals.
Firstly, to examine individual variation in the age at which fish transitioned, growth trajectories were compared between barramundi that had matured as females prior to their 5th birthday hereafter referred to as young sex-changers versus individuals that remained males beyond age 5 old sex-changers. Secondly, to examine individual variation in size at sex change, growth trajectories were compared between barramundi captured as females smaller than mm small sex changersversus barramundi captured as males larger than mm large sex changers.
These age and size classifications were selected to be close to the population average i. Thirdly, growth rates were compared between large i. These two groups of individuals are assumed to be undertaking the same life-history strategy i.
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Hermaphrodite dating Savannah GA we compared groups of individuals harvested at different stages of ontogeny, we focused our analyses on the first three years of life, as this is the period for which all groups had sufficient overlapping growth data.
This three-year period is also considered most relevant because among-individual variation in growth becomes less pronounced as barramundi grow older 31 Details of barramundi samples used in this study, showing the of individuals classified into the life history types of interest. Table shows the of individuals per group for which age data were available, and the subset of individuals subjected to growth analyses.
The proportions in the GLM were weighted to for heterogeneity in the underlying sample sizes To assess the relative importance of size and age in determining when individuals change sex, models were compared containing age and length fitted to barramundi sex.
Three different subsets of the barramundi growth data set were then explored: i young sex-changers and old sex-changers to investigate the relationship between growth rate and the age that individuals changed sex ; ii large sex-changers and small sex-changers to investigate the relationship between growth rate and the size that individuals changed sex ; and iii large females and small males to test whether growth rate affects the likelihood of becoming a large, highly fecund female.
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A mixed effects modelling framework was developed to investigate the relationship between growth trajectory back-calculated length-at-agemm and Sex-at-capturefor each of the three subsets of growth data reflecting different life history comparisons. A series of models were developed using the lme4 package These models contained different sets of intrinsic individual and extrinsic environmental predictor variables, and their interactions. A fixed Age effect was included to allow for declining growth rates with increasing age. A random intercept for FishID was included to for repeated measures of increment data from individual fish, and to allow each fish to have higher or lower growth than the model intercept.
To for any persistent growth affects among individuals from a common year class, a Cohort random intercept was included.
We also tested whether fitting a quadratic term for age interacting with sex to the optimum model improved model performance. To satisfy model assumptions, Length-at-age and Age were log-transformed, and the predictor variables were mean-centered to facilitate model convergence.
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Random effects structures and fixed effects structures were compared using restricted maximum likelihood estimation REMLand maximum likelihood MLrespectively. There was considerable overlap with respect to the age and size distributions of male and female barramundi Fig. Young female maturation was strongly associated with rapid growth during the juvenile phase Fig.
Individuals that attained female status early had consistently fast growth rates across each of the first 3 years. However, growth rate was not strongly linked to variation in the size that barramundi underwent sexual transition Fig. The largest individuals in the data set i. for the fixed and random effect model selection are provided in Table S2 and Table S3respectively. Linear mixed-effects growth curves illustrating differences in size-at-age between different life history types. Blue lines, males; red lines, females.
Considerable variation was evident in the timing of protandrous sex change in Fitzroy River barramundi.