Reproductive biology of a large, aggregation-spawning serranid, Epinephelus fuscoguttatus (Forsskål): management implications

The reproductive biology of Great Barrier Reef populations of the long-lived grouper Epinephelus fuscoguttatus (brown-marbled grouper or flowery cod) was investigated using histological analyses. Evidence provided by gonad morphology and age-based demographics suggested monandric protogynous hermaphroditism. Younger age groups contained only immature and mature females, and all males were above the size and age of 100% female maturity, consistent with secondary males derived from mature females by adult sex change. Fishing records confirmed that spawning aggregations of this species and the co-occurring Epinephelus polyphekadion (camouflage grouper) are sometimes targeted on the Great Barrier Reef. Sampling data revealed strong spawning seasonality for E. fuscoguttatus , with a relatively narrow annual spawning period (November to January). The temporal pattern of reproductive activity within the spawning period, based on occurrence of near spawning ovaries (containing hydrated oocytes), indicated spawning events may occur throughout much of the lunar cycle and only partly coincide with seasonal fishing closure periods on the Great Barrier Reef. The results indicate that protection would be enhanced by a longer seasonal closure.     

Females better face senescence in the wandering albatross

Sex differences in lifespan and aging are widespread among animals. Since investment in current reproduction can have consequences on other life-history traits, the sex with the highest cost of breeding is expected to suffer from an earlier and/or stronger senescence. This has been demonstrated in polygynous species that are highly dimorphic. However in monogamous species where parental investment is similar between sexes, sex-specific differences in aging patterns of life-history traits are expected to be attenuated. Here, we examined sex and age influences on demographic traits in a very long-lived and sexually dimorphic monogamous species, the wandering albatross (Diomedea exulans). We modelled within the same model framework sex-dependent variations in aging for an array of five life-history traits: adult survival, probability of returning to the breeding colony, probability of breeding and two measures of breeding success (hatching and fledging). We show that life-history traits presented contrasted aging patterns according to sex whereas traits were all similar at young ages. Both sexes exhibited actuarial and reproductive senescence, but, as the decrease in breeding success remained similar for males and females, the survival and breeding probabilities of males were significantly more affected than females. We discuss our results in the light of the costs associated to reproduction, age-related pairing and a biased operational sex-ratio in the population leading to a pool of non-breeders of potentially lower quality and therefore more subject to death or breeding abstention. For a monogamous species with similar parental roles, the patterns observed were surprising and when placed in a gradient of observed age/sex-related variations in life-history traits, wandering albatrosses were intermediate between highly dimorphic polygynous and most monogamous species.     

Reproduction and feeding habits of the highly seasonal Brachyhypopomus bombilla (Gymnotiformes: Hypopomidae) from southern Brazil with evidence for a dormancy period

The reproductive biology and feeding habits of the hypopomid Brachyhypopomus bombilla were studied. The species has seasonal behavior, with breeding and feeding activity occurring mostly during the Southern Hemisphere spring and summer. We defined fractional spawning for the species and a relative fecundity similar to those previously reported for other gymnotiform species. According to the analysis of the food items, B. bombilla was included in the trophic category invertivorous, feeding mainly on autochthonous insects. The reproductive periods of males and females as well as female feeding activity were significantly related to the photoperiod. During a period of 5?months, when the lowest water temperatures and shortest photoperiod were recorded, all the specimens of B. bombilla were found buried in the muddy bottom of the creek, with lower electric organ discharge activity, empty stomachs, and gonads in early stages of the maturation process. This period, herein defined as a dormancy period, is reported here for the first time for a species of the Gymnotiformes order.     

Permanent and Seasonal Expressions of Sexual Dimorphisms in a Weakly Electric Fish, Mormyrus rume proboscirostris Boulenger 1898 (Mormyridae, Teleostei)

Several sexually dimorphic characters of the anal-fin complex in the mormyrid fish, Mormyrus rume proboscirostris, assist during courtship when the male envelops the female's anal fin with its own to form a common spawning pouch (anal-fin reflex). We found that developmental growth and seasonally cycling gonadal activity selectively affect their expression. The structures defining the anal fin undergo a permanent sexually dimorphic transformation at a time when ripe spermatozoa first appear in the testis of young males. However, the expression of a dorsally directed indentation of the posterior ventral body wall, affecting the dorsal margin of the anal fin, appeared to be more plastic as it correlated with the gonadosomatic index, that is, testis size. We surmised that this indentation is influenced by cyclic anabolic action on muscle involved with the execution of the anal-fin reflex.     

A review of reproductive strategies in cephalopods

Cephalopod reproductive strategies are reviewed in order to clarify their current, confusing status. Based on the type of ovulation, spawning pattern and growth between egg batches or spawning periods, five comprehensive and flexible cephalopod reproductive strategies are defined. Accordingly, with these three factors the following classification is proposed. (a) Spawning once (formerly semelparity) consisting of simultaneous terminal spawning, with synchronous ovulation, monocyclic spawning and absence of growth between egg batches. (b) Spawning more than once (formerly iteroparity) including: (i) polycyclic spawning with egg-laying occurring in separate batches during the spawning season and growth occurring between production of egg batches and spawning seasons; (ii) multiple spawning, with group-synchronous ovulation, monocyclic spawning and growth between egg batches; (iii) intermittent terminal spawning, with group-synchronous ovulation, monocyclic spawning and no growth between egg batches; (iv) continuous spawning, with asynchronous ovulation, monocyclic spawning and growth between egg batches. Examples of species exhibiting each of these reproductive strategies are given. The large amount of inter-species variation in several life-history traits related to reproductive events is discussed.     

Seasonal change in sexual size dimorphism of the major cheliped in the hermit crab <Emphasis Type="Italic">Pagurus minutus</Emphasis>

Sexual size dimorphism is a common phenomenon in the animal kingdom, and its seasonal change has been reported in some species that possess traits dimorphic only in males and specialized for male mating success. However, few studies have examined seasonal change in sexual dimorphism of traits possessed by both sexes. Here, we examined the reproductive biology of the hermit crab Pagurus minutus, at a sandflat in the Waka River estuary, Japan, with special reference to seasonal changes in sexual dimorphism of the large claw (major cheliped) size by conducting population and precopulatory guarding-pair sampling. Previous investigation demonstrated that the major cheliped is used as a weapon, and its size, more than body size, determines the winner in male–male contests of this species. We found ovigerous females from November to April, peaking in January, when 80% of females were ovigerous. Sexual size dimorphism of the major cheliped was observed; the degree of dimorphism increased in the reproductive season, when only males possessed an enlarged major cheliped. In addition, in the reproductive season, precopulatory guarding males had a larger body and larger relative size of the major cheliped than did solitary males, although the major cheliped size in guarding males seemed to reach an upper limit. These results suggest that seasonal change in sexual dimorphism of the major cheliped size in P. minutus strongly reflects sexual selection favoring the development of this natural weaponry, and that the degree of the dimorphism might be limited through natural selection.     

Relationships of hydrology and life-history strategies on the spatio-temporal habitat utilisation of fish in European temperate river floodplains

Floodplain inundation is considered as crucial for the recruitment of fish in lowland rivers, by either providing suitable spawning areas as well as breeding habitats for young-of-the-year fish (YOY), as well as for supporting species that exhibit different life history-strategies in order to be differently adapted to long term discharge patterns. Fish communities in a set of 38 waterbodies on the Lower Rhine floodplain, representing different long-term frequencies of inundation and differently affected by seasonal inundations, were sampled by means of electro fishing (point abundance sampling, total n = 42,701 points) over a four-year period in order to identify species-specific and life-history strategy related patterns of spatio-temporal floodplain habitat utilisation. For 18 species (total catch: n = 107,150), typically occurring in European lowland rivers and representing different ecological guilds, different responses towards seasonal inundations were found. YOY of most species closely associated to the periodic strategy (e.g., Abramis brama, Aspius aspius, Blicca bjoerkna) were highly abundant in frequently inundated waterbodies, provided these were subject to inundations occurring in spring and early summer and coincided with temperatures required for spawning. However, recruitment in these species was impaired or failed when no inundations in this time frame occurred, although adults were present. In contrast, most species associated to the opportunistic strategy (e.g., Gasterosteus aculeatus, Pseudorasbora parva, Leucaspius delineatus) had highest recruitment in waterbodies unaffected by inundations in this time frame, which had detrimental effects on these predominantly small sized species. Spatio-temporal floodplain habitat utilisation of YOY fish (most rheophilic species as well as eurytopics) is suggested to be size-related, since most fast growing periodic strategists left the floodplain at given connectivity at latest in winter and were then absent in the subsequent year. Smaller YOY fishes and all opportunistic species either remained in more isolated waterbodies, or dispersed from there across the floodplain to some degree during extensive winter floods. These findings suggest adaptations to the long-term hydrograph of large river systems, with flood-related recruitment patterns predominantly occurring in periodic strategists and low-flow recruitment strategies in opportunistic strategists and stagnophilic species. The results of this study point to the significance of hydrological transversal floodplain gradients that provide diverse communities and population maintenance of different life-history strategies, evidencing that fish communities within the floodplain act as indicators for the hydrological conditions.     

Aspects of reproductive biology of curimba Prochilodus lacustris (Pisces,Prochilodontidae) in a tropical lake in Northeastern Brazil

This study evaluated the annual cycle of biological reproductive aspects of Prochilodus lacustris, a neotropical fish species, in Baixada Maranhense Protection Area in northeastern Brazil. Fish were collected monthly between June of 2015 and June of 2016 using gill nets. In the laboratory, 600 individuals were weighed, measured, and eviscerated to obtain biometric data and data for the microscopic and macroscopic analyses of the maturation stages of the gonads. These analyses allowed the determination of the reproductive period using biological indicators such as the gonadosomatic index and hepatosomatic index, condition factor, stomach repletion index, and spawning season. Abiotic variables were measured in situ during the samplig: temperature, pH, dissolved oxygen, and electrical conductivity. In addition, local rainfall data was also obtained. The results showed that the total body length of individuals varied from 151 to 211 mm in males, and from 142 to 239 mm in females. The sex ratio showed a predominance of females over males, and the species showed negative allometric growth. The annual variation of reproductive indicators and the frequency of individuals in advanced stages of gonadal maturation suggest that the reproductive cycle of the species occurs between November and January, with a reproductive peak in January. This reproductive peak coincides with the beginning of the region's rainy season. Although we did not do the fertility analysis, our results suggest that the species presents partitioned spawning. In conclusion, this results demonstrates that the reproduction of the investigated specie is influenced by associations between environmental variables on a seasonal scale and can be contribute to improve the understanding of the dynamics of the physiological reproductive process in lentic environments.     

Annual changes in brain concentration of arginine vasotocin and isotocin correspond with phases of reproductive cycle in round goby,Neogobius melanostomus

Reproductive cycle of seasonally breeding fish is synchronized with changes of photoperiod and temperature in environment. We hypothesize that arginine vasotocin (AVT) and isotocin (IT) are involved in timing and synchronization of seasonal reproductive activity in the round goby (Neogobius melanostomus). To verify this hypothesis, we examined the annual profiles of brain AVT and IT in round goby males and females in relation to their reproductive cycle. Wild round gobies were exposed to annual environmental changes in their natural habitats from where they were sampled monthly over a year. AVT and IT were measured using HPLC with fluorescence detection preceded by solid-phase extraction. This study shows seasonal variations in brain AVT and IT levels. Profiles of changes were similar in males and females: the peak of AVT was observed before spawning in March-April, whereas that of IT during spawning in May–June. Furthermore, the lowest AVT level was noted out of breeding season from November to January, while the level of IT decreased immediately at the end of the spawning. The results show that high AVT levels correlate with pre-spawning period whereas the highest IT levels correspond to spawning. A significant decline in AVT and IT in non-spawning season coincided with the quiescent phase of gametogenesis in both sexes.     

Effects of 17α-Methyltestosterone on Sexually Dimorphic Characters in the Weakly Discharging Electric Fish,Brienomyrus niger(Günther, 1866) (Mormyridae): Electric Organ Discharge, Ventral Body Wall Indentation, and Anal-Fin Ray Bone Expansion

Adult males of African weakly discharging electric fish (family: Mormyridae) are distinguished from juveniles and adult females by a dorsally directed indentation of the posterior ventral body wall and by massive bone expansion of the bases of a select number of anal-fin rays. These sexually dimorphic structures seem to facilitate the anal-fin reflex that is displayed during courtship when the male envelopes its anal fin around the female's to form a common spawning pouch. Expanded bone could provide additional surface for muscle attachment and thus assist in part with the courtship sequence. Based on the fact that the expression of the male sexually dimorphic electric organ discharge (EOD) is under androgen control, and that the female EOD can be masculinized through testosterone administration, we hypothesized that androgens should also drive anal-fin ray bone expansion in male mormyrids and equally effect male-like changes in treated juveniles and adult females. Exogenous androgen treatment (17α-methyltestosterone) of adult femaleBrienomyrus nigerresulted in a male-like EOD, and male-typical structural transformations (body wall indentation and anal-fin ray bone expansion). Some of these changes were immediate and receded following hormone withdrawal (EOD), while others developed more slowly and were apparently permanent (indentation and bone formation). 17α-Methyltestosterone administration affected only those targets in females that are normally involved in the male's reproductive behavior, i.e., its courtship signal (EOD) and two morphological features (body-wall indentation and bone expansion). Rays of the dorsal or caudal fins were never affected.     

Reproductive strategy of Psectrogaster rhomboides Eigenmann & Eigenmann, 1889, a freshwater fish from Northeastern Brazil

Several environmental parameters related to the spawning season of the freshwater fish, Psectrogaster rhomboides were identified. The hypothesis predicts synchrony of the spawning season with the rainy period, presenting a seasonal reproductive strategy. This study investigated the total body length and body mass, sex ratio, body size at first sexual maturity, gonadosomatic index, condition factor, fecundity and reproductive period of P. rhomboides in the natural environment. Twelve monthly samplings (mean n = 20) were carried out from March 2009 to February 2010. Fish were captured using 4 cm diameter cast nets and environmental parameters such as rainfall, temperature, dissolved oxygen concentration, pH and electrical conductivity of the water were registered. The sampled population of P. rhomboides (n = 444) showed a sex ratio of 1 : 1. Females attained first sexual maturity at 15 cm total length and males at 15.3 cm total length. Spawning occurred from March to May, with high gonadosomatic index values during the rainy season. This species is a total spawner, with a mean fecundity of 6188 (±367) mature oocytes. P. rhomboides presents a seasonal reproductive strategy, providing a population increase and exploitation of the environmental resources during the rainy period. Rainfall (196.5 ± 4.9 mm) and the concentration of dissolved oxygen (7.82 ± 0.7018 mg L^?1) were influential factors during the spawning season. Gonadosomatic index and the condition factor were negatively correlated during the gonadal development cycle of this species. The monthly gonadosomatic index values show that spawning begins when the rainy season is at its maximum and ends synchronously (females r = 0.9171; males r = 0.889) with the end of the rainy season.     

Age and growth of a colonizing minnow,Barbus anoplus,in a man-made lake in South Africa

Synopsis Aspects of the life history of Barbus anoplus were studied in Lake le Roux, a turbid man-made lake on the Orange River, South Africa. This minnow underwent a population explosion and successfully colonized the shoreline of the newly-formed lake during the early phases of reservoir filling. Male and female B. anoplus reach sexual maturity in one year at about 40 mm fork length. They have a multiple spawning habit with the first spawning in November–January and the second in February–March. The growth of the two resulting cohorts is discussed. It is proposed that the offspring from the second spawning not only acts as a ‘back-up’ but is capable of prolonging the life of that year-class into an additional reproductive season. Most of the minnows die after their second summer, but more offspring from the second spawning, especially females, live into a third summer. Females attain a larger maximum size (73 mm FL) and age (3–4 years) than males (60 mm FL, 2–3 years). B. anoplus is small and short-lived with a high seasonal reproductive potential, which is in contrast to the larger Barbus species in the Orange River system. These life-history traits enable the species to colonize and successfully inhabit unstable environments and probably account for its widespread distribution.     

Enhancing knowledge on low-value fishing species: the distinct reproductive strategy of two gurnard species

The depletion and overexploitation of several fish stock demands for a valorisation of non-target and discarded species. Nonetheless, such species are often poorly studied, and information on their biological parameters must be gathered for effective population management. For 1 year, the reproductive strategy of the piper gurnard Trigla lyra and the red gurnard Chelidonichthys cuculus was studied by monthly samples obtained from commercial boats operating on western Portuguese coast. Both species showed a biased sex ratio towards females, especially for larger length classes. Length at first maturity could be estimated only for red gurnard (22.1 and 19.9 cm for females and males, respectively) because all piper gurnard individuals caught were mature. Piper gurnard showed determinate fecundity and a short spawning season, from November to February with a peak in January, whereas red gurnard showed indeterminate fecundity and a wide spawning season, from late December to May. The relative annual fecundity estimated for red gurnard (1893 ± 728 oocytes × g⁻¹ eviscerated weight [EW]) was higher than the one estimated for piper gurnard (1018 ± 250 oocytes×g⁻¹ EW). Although important information for understanding the species dynamics is presented in this study, additional information on other life-history parameters and of species landings is required.     

Reproductive characteristics of the ocean leatherjacket, Nelusetta ayraudi

The ocean leatherjacket (Nelusetta ayraudi) is one of the largest members of the family Monacanthidae. Distributed throughout inshore waters around the southern half of Australia, this schooling species supports substantial commercial and recreational fisheries. N. ayraudi do not conform to either of the general reproductive modes reported within the family, but exhibit characteristics of both strong social reproductive behaviour and of being promiscuous and polygynous. Sexual dimorphism, with males and females exhibiting differing colouration and body shapes, and ripe ovaries being an order of magnitude larger than ripe testes, are characteristic of social reproductive behaviour and pair spawning. In contrast, high batch fecundity (mean of 320 oocytes per gram of body weight), similar sizes and ages at sexual maturity (350 mm and 2.5 years respectively) and the formation of large spawning aggregations in offshore waters are characteristic of being promiscuous and polygynous. Similar to many other coastal marine species off the east and west coasts of Australia, N. ayraudi are partial spawners during the austral winter months with spawning restricted to the part of their distribution that is towards the upper area of the prevailing currents. It is hypothesized that N. ayraudi off eastern Australia have evolved a life-history strategy whereby fish move northwards through time, spawning occurs in these more northern waters and the southerly flowing Eastern Australian Current facilitates dispersal of eggs and larvae southwards. The reproductive characteristics described provide various options to fishery managers who wish to enhance the sustainability of the fishery through increased egg production. These include spatial and temporal fishing closures to protect breeding fish during the spawning period, the protection of juveniles through either inshore area closures, improving the selectivity of fishing gears and/or regulated minimum legal lengths.     

Reproductive activity in the commercially exploited mediterranean muricid <Emphasis Type="Italic">Hexaplex trunculus</Emphasis> collected from Boughrara lagoon (Southern Tunisia)

The banded murex Hexaplex trunculus (Linnaeus, 1758) is a commercially exploited gastropod in the Mediterranean region including Tunisia where it has become an important fishery resource these last years. In the present investigation, some reproductive aspects of this species were described in the population of Boughrara lagoon based on macroscopic examination of the gonads (gonadic conditional indices) together with observation of the seasonal hypertrophy of the penis in males and capsule gland in females. This procedure of assessing reproductive activity was validated by field observations of copulation and spawning. Mature females were found during 10 months and mature males during 8 months being both frequent in January and February. Reproductive activity was slightly asynchronous between sexes with males reaching maturity before females. Gonadic release occurred earlier in males between January and March against February to April in females. These findings were in agreement with field observations of copulation in January and February and egg-capsule laying in late February and March. Hatching juveniles were observed in the field in April and May.     

Sexual reproduction of the brooding sponge <Emphasis Type="Italic">Rhopaloeides odorabile</Emphasis>

Sexual reproduction of Rhopaloeides odorabile, a common Great Barrier Reef sponge, was quantified using histological sections from samples collected over two reproductive seasons. Rhopaloeides odorabile is viviparous and gonochoristic with a male biased sex ratio (2.5:1). Commencement and cessation of gametogenesis coincides with rising and falling sea surface temperatures (≈24–29°C). Spermatogenesis occurs from October until January. Females initiate oogenesis in September with the asynchronous development of oocytes, embryos and larvae occurring within the brood chambers. A larval release period of 5–6 weeks occurs during January and February. The minimum size of reproductive individuals was 176 cm³ for females and 192 cm³ for males. The total reproductive output for both sexes shows a positive correlation with size. A relative reproductive output index quantified the maximum reproductive investment at approximately 1 and 3% of the total choanoderm for females and males, respectively, which represents a lower range of reproduction in comparison to other viviparous sponges. Low reproductive output in R. odorabile may be offset by an extended spawning period, alleviating the risk of releasing larvae in potentially adverse conditions via one synchronised spawning event and increasing overall larval survival.     

Life history traits of two dwarf cichlids species in the white waters of the Amazonian floodplain

The reproductive parameters are among the most important life history aspects of fishes influenced by environmental variation. During recent years, the main life history strategies of Amazonian fish species were defined mostly by a set of reproductive parameters. In the present work, we sought to describe important life history parameters, in particular on reproductive characteristics of Apistogramma agassizii and Apistogramma bitaeniata, found in floodplain lakes of the Brazilian Amazonia. The species presented a positive sexual dimorphism, and males were significantly bigger than females. For both sexes, four developmental phase of gonad maturation were detected, and based on those it was possible to identify mature, reproductive specimens throughout the entire period of the study. From the ovaries of mature females, fecundity and spawning type were determined. Low fecundity, short spawning periods, possibly separated only by few months, and total spawning are all good indications that A. agassizii and A. bitaeniata evolved an opportunistic strategy in their life history.     

Reproductive patterns of blacktail comber (Serranus atricauda,Serranidae) from south-west Portugal seamounts

The knowledge of the reproductive strategy is essential for the comprehensive understanding of the population dynamics of any fish species. This study intends to define the spawning season, verify the type of fecundity regulation and estimate relative annual fecundity for Serranus atricauda inhabiting the south-west of Portugal seamounts (Gorringe, Ampère and Lion). Monthly samples, between September 2010 and December 2011, were obtained from commercial vessels. This species is synchronously hermaphroditic, and mature individuals were found all year round, with gonadosomatic index peak from February to September. No clear relation between hepatosomatic index and Fulton’s condition factor and gonadal development was found, and therefore, it is probable that reproductive success depends more on environmental conditions and food availability during the spawning season than on body energy reserves. No gap exists between pre-vitellogenic and vitellogenic oocytes and the oocyte size-frequency distribution during the main spawning season show no dominant cohort progressing through time. The number of standing stock of advanced vitellogenic oocytes showed an increase trend along the spawning season decreasing only at its end and the relative intensity of α-atresia was always low throughout this period with an increase towards the end. All these criteria corroborate the indeterminate fecundity type assigned to S. atricauda in previous studies. Mean relative annual fecundity estimated was 5,655 ± 4,321 oocytes per gram of gutted weight.     

Social Behaviour of Individual Oval Squids (Cephalopoda,Teuthoidea, Loliginidae,Sepioteuthis lessoniana) within a Captive School

The social behaviour of individually identified squids was observed over a period of 4 mo. Squids were reared in captivity and maintained in a shoal of up to 18 animals. Distances between animals averaged 1.6 body lengths, similar to the 1.2 body lengths of wild teleost fish schools. Smaller animals schooled less frequently and were found at the periphery, and familiar and unfamiliar animals shoaled together. Eighty-six apparent reproductive events were observed. This species of squid, Sepioteuthis lessoniana, is not sexually dimorphic to the human eye and male squids copulated with both males and females but they directed their attention disproportionately towards females. Most copulations occurred more than a month before spawning, lasted only a few seconds and, unlike field observations on spawning grounds, were not followed by mate-guarding. Two body patterns are described that were used consistently in social interactions by both males and females; these patterns were both associated with reproductive behaviour but their exact function was unclear. A sister species, Sepioteuthis sepioidea, has been described as showing complex social behaviour; in S. lessoniana, no evidence for such behaviour was seen.