Reproductive biology of Haemulon plumierii in the south‐western Atlantic Ocean's most extensive reefs: implications for fisheries management

The reproductive biology of the white grunt Haemulon plumierii was studied from 360 individuals obtained from artisanal fisheries landings in the Abrolhos Bank, Brazil, between August 2010 and March 2012. The overall sex‐ratio did not differ significantly from 1:1, although males predominated in larger size classes. β‐Binomial modelling of historical sex‐ratio data indicated that the catch rate of females has increased in recent years. Females reached maturity at a smaller total length (L_T; 214 mm) than males (235 mm L_T) and the L_T at which 50% of all individuals are mature (L₅₀) was 220 mm, corresponding to 41·5% of the maximum recorded L_T. Variation in the gonado‐somatic index and in the relative frequency of reproductive stages indicates that reproduction occurs year round, with increased activity during the austral spring and summer. Fecundity was not size dependent. The reproductive parameters provided here can support management measures focussed on seasonal closures during spawning peaks (September to November and February to March) and minimum sizes (>L₅₀) for the capture of this important artisanal fisheries resource in Abrolhos, the region with the largest and most biodiverse coralline reefs in the South Atlantic Ocean.     

Life‐history traits of the long‐nosed skate Dipturus oxyrinchus

This work investigates life‐history traits of the long‐nosed skate Dipturus oxyrinchus, which is a common by‐catch in Sardinian waters. The reproductive variables were analysed from 979 specimens sampled during scientific and commercial hauls. Females (10·4–117·5 cm total length, L_T) attained larger sizes than males (14·5–99·5 cm L_T). To evaluate age and growth, a sub‐sample of 130 individuals (76 females and 54 males) were used. The age was estimated by annuli counts of sectioned vertebral centra. Four models were used for the length‐at‐age data: the von Bertalanffy, the exponential, the Gompertz and the logistic functions. According to the Akaike's information criterion, the Gompertz model seemed to provide the best fitting curve (L_∞ mean ± s.e. : 127·55 ± 4·90 cm, k: 0·14 ± 0·09, IP: 3·97 ± 0·90 years). The oldest female and male were aged 17 (115·5 cm L_T) and 15 years (96·0 cm L_T), respectively. Lengths at maturity were 103·5 cm for females and 91·0 cm for males, corresponding to 90% of the maximum observed length in both sexes. The monthly distribution of maturity stages highlighted an extended reproductive cycle, with spawning females and active males being present almost throughout the year, as confirmed by the gonado‐somatic index. Ovarian fecundity reached a maximum of 26 yolked follicles with a mean ± s.e. size of 19·7 ± 6·5 mm.     

Reproductive biology of the crocodile shark Pseudocarcharias kamoharai

From February 2005 to September 2007, a total of 490 crocodile sharks Pseudocarcharias kamoharai, caught as by‐catch in the swordfish and tuna longline fishery that operates in the tropical western Atlantic Ocean, was studied in regard to their reproductive biology. Maximum observed total lengths (L_T) were 1220 and 1090 mm for females and males respectively, with a high proportion of the catch being composed of mature specimens. Sexual maturity was attained at 760–810 mm L_T for males (L_T50 = 800 mm) and 870–980 mm L_T for females (L_T50 = 916 mm). The size at birth was estimated at 415 mm L_T. Temporal variation in gonad morphology and mass suggests that in this region P. kamoharai, an aplacental viviparous species with oophagy, does not show a well‐defined reproductive seasonality, with mating and parturition occurring possibly over an extended period of the year. Mean ±s.d . fecundity was estimated to be 3·9 (± 0·6) pups per reproductive cycle.     

Reproductive biology of the southern thorny skate Amblyraja doellojuradoi (Chondrichthyes,Rajidae)

The total lengths (L_T) of 193 males (209–556 mm) and 130 females (275–515 mm) of Amblyraja doellojuradoi, a commercial by‐catch species on the Argentinean continental shelf, which are increasingly retained, were analysed. No sexual dimorphism was observed in the L_T at which 50% of individuals were sexually mature; males matured at 448 mm and females at 411 mm, c. 80 and 82% of maximum L_T. The hepato‐somatic index was similar among sexes, but significantly different between maturity stages, being lower in mature than immature specimens. Males had no seasonal difference in the hepato‐somatic index and females had the lowest index in autumn. The gonado‐somatic index was lower in males than in females and significantly higher in mature than immature specimens of both sexes. Males had the highest index in autumn and females had no seasonal difference. Collectively, these results would indicate that A. doellojuradoi breeds in autumn.     

Temporal and latitudinal comparisons of reproductive parameters in a heavily exploited shark,the bonnethead,Sphyrna tiburo (L. 1758), in the southern Gulf of Mexico

In the southern Gulf of Mexico, the bonnethead shark, Sphyrna tiburo, is one of the most frequently captured species in landings of small-scale fisheries. Based on the analysis of two fishery-dependent sampling periods (1993–1994 and 2007–2014), this study aimed to determine reproductive parameters and identify temporal differences between the two time periods. In the first sampling period, 776 males and 352 females with a size range of 28.0–120.0 cm total stretched length (L_T) were analysed, and in the second sampling period, 387 males and 432 females with a size range of 28.0–122.0 cm L_T were analysed. The size at 50% maturity in the second sampling period was significantly different between sexes, 82.6 cm L_T for females and 73.8 cm L_T for males (no estimation was possible for the first sampling period). The size at 50% maternity was not different between sampling periods, 97.3 cm L_T for the first sampling period and 99.0 cm L_T for the second sampling period. Litter size varied from 3 to 19 embryos and the average was not statistically different in both periods, 10.1 (S.D. = 3.8) for the first sampling period and 11.3 (S.D. = 3.5) for the second sampling period. The female reproductive cycle is asynchronous, and it seems to be annual, with a gestation period of 5–6 months, and a consecutive ovarian cycle and gestation period. Temporal (between sampling periods) and latitudinal (southern Gulf versus northern regions) variations occur in the synchronicity of the reproductive cycle, temporal variation in the relationship between maternal length and litter size, and latitudinal variation in average size of mature sharks.     

Reproductive biology of the guitarfish Rhinobatos percellens (Chondrichthyes,Rhinobatidae) from the São Paulo Coast,Brazil, western South Atlantic Ocean

The reproductive biology of the guitarfish Rhinobatos percellens was studied from 751 specimens caught by bottom pair trawlers off the coast of São Paulo, Brazil, between c. 24° 00′ S; 45° 15′ W and c. 25° 10′ S; 47° 52′ W, from September 2007 to August 2009. The total length (L_T) and total mass (M_T) relationship for males and females combined was M_T = 1·29E‐06 L_T^3·15 (r = 0·99, n = 751). The mean L_T of sexually mature specimens was 548 mm for males and 583 mm for females. Clasper growth was allometric and showed three distinct phases. Most claspers were calcified in specimens of c. 550 mm L_T. The mean diameter of the largest oocyte was 29·8 mm, the mean ovarian fecundity was seven oocytes and ovulation occurred between August and November. Uterine fecundity ranged from two to 13 embryos (mean of five embryos). Larger females had higher litter sizes and larger embryos; the size‐at‐birth was c. 200 mm L_T. The hepato‐somatic index oscillated seasonally for males and females; the gonado‐somatic index had little variation in males, but varied seasonally in females. The presence of many non‐pregnant adult females and of encapsulated eggs during two consecutive seasons suggests a resting period between gestations and the possibility of diapause.     

Reproductive aspects of the Atlantic angel shark Squatina dumeril in the southern Caribbean Sea

The maturity and reproduction of the Atlantic angel shark Squatina dumeril were assessed using 77 females (29·2–110·4 cm total length; L_T) and 269 males (58·7–108·2 cm L_T) harvested by artisanal gillnetters off Venezuela. The biased sex ratio implied segregation or sex‐specific gear selectivity. Based on the development of the reproductive tract, 50% L_T at sexual maturity (L_T50, mean ± s.e .) for females and males were estimated at 86·14 ± 0·64 and 81·55 ± 0·12 cm, respectively. Uterine fecundity ranged between one and six and with a maximum embryo size of 25·7 cm L_T. Gravid females were observed from August to December, including those close to parturition and while the gestation period was not confirmed, the size of ovarian follicles among some specimens implied protraction. The low fecundity of the species supports close monitoring of catches.     

Reproductive biology of the greeneye spurdog Squalus chloroculus (Squaliformes,Squalidae)

The reproduction of the greeneye spurdog Squalus chloroculus was studied based on animals caught in the multispecies and multi‐gear southern and eastern scalefish and shark fishery on the upper continental slope off southern Australia. One hundred and ninety‐nine females (502–990 mm, total length, L_T) and 189 males (515–810 mm L_T) were examined. The female reproductive cycle, based on 41 breeding animals, is continuous and triennial, with the pregnancy period estimated to be 31–34 months, seasonal and synchronous with the ovarian cycle; a third of the breeding female population is estimated to give birth between September and December each year. The estimated L_T at which 50% of females are mature is 799 mm (95% c.i. : 794, 804), whereas the L_T at which 50% are maternal is 825 mm (95% c.i. : 817–833), but these estimates are probably biased by the phenomenon of apparent change of L_T at maternity and L_T at maturity following severe length‐selective fishing mortality. Litters ranged from four to 15 embryos with a 1:1 sex ratio, and litter size increased with maternal length. The breeding cycle of males is neither seasonal nor synchronous with the female cycle. The estimated L_T of males where 50% are mature was 629 mm (95% c.i. : 603, 645).     

Reproductive and population parameters of spiny dogfish Squalus acanthias in the south‐western Atlantic Ocean

The objective of this study was to estimate reproductive and population parameters of the spiny dogfish Squalus acanthias for the south‐western Atlantic Ocean. In total, 2714 specimens (1616 males and 1098 females) were collected from surveys carried out using research vessels. Males ranged from 225 to 861 mm total length (L_T) and females from 235 to 925 mm L_T. The size at maturity of females (651 mm) was significantly greater than that of males (565 mm). The maximum proportion of mature individuals (P_max) of the gestation ogive was <1, which indicates that a proportion of mature females was not in gestation. This inactivity may be explained by the occurrence of resting periods between cycles or by the asynchrony of the reproductive cycle. The estimated P_max for the maternity ogive suggested that about one third of mature females were in the maternity stage (i.e. with embryos >156 mm). The temporal and spatial co‐occurrence of non‐gravid adult females at different stages of ovarian development, as well as gravid females at all embryonic development stages would indicate that the female reproductive cycle in the south‐western Atlantic Ocean is asynchronous. The results indicate that S. acanthias is susceptible to fishing pressure on account of its length at maturity, extended reproductive cycles and low fecundity.     

Zygoparity and sex steroid hormone profiles in bluemouth Helicolenus dactylopterus

Two hundred and seven individuals (103 females and 104 males) of bluemouth Helicolenus dactylopterus (Scorpaeniformes, Sebastidae), a commercially important deep‐water species with an unusual reproductive strategy, from the eastern Atlantic Ocean ranging from 13·9 to 37·5 cm total length (L_T) were analysed from September 2011 to October 2012. The analysis included gonad maturity phases and blood‐plasma levels of oestradiol‐17β (E₂), 11‐ketotestosterone (11‐KT) and 17,20β‐dihydroxypregn‐4‐en‐3‐one (17,20β‐P). Results confirmed the existence of an annual reproductive cycle with asynchrony between females and males and a spawning season from January to May. A pronounced peak in 17,20β‐P in October for both sexes was associated with possible mating behaviour and recent copula. Levels of E₂ increased preceding the elevation of the gonado‐somatic index during ovarian growth and were lower during regression and regeneration. The frequency distribution of oocyte–embryonic stages and variation of hormone levels suggest the existence of daily rhythms. Fertilization was detected between 2000–0000 and 0800–1200 h and spawning took place throughout the day peaking between 2000 and 0000 h. The cyclic pattern of sex steroids and ovarian recruitment provides a new insight into the reproductive strategy of this species.     

Proximate causes of sexual size dimorphism in Colorado pikeminnow, a long‐lived cyprinid

Evidence for sexual size dimorphism (SSD) and its possible causes were examined in the endangered Colorado pikeminnow Ptychocheilus lucius, a large, piscivorous, cyprinid endemic to the Colorado River system of North America. Individuals representing 18–24% of the upper Colorado River population were captured, measured, sexed and released in 1999 and 2000. Differing male and female total length‐(L_T) frequency distributions revealed SSD with females having greater mean and maximum sizes than males. Although both sexes exhibit indeterminate post‐maturity growth, growth trajectories differed. The point of trajectory divergence was not established, but slowed male growth might coincide with the onset of maturation. Differing growth rate was the dominant proximate cause of SSD, accounting for an estimated 61% of the observed difference in mean adult L_T. The degree of SSD in adults, however, was also related to two other factors. Evidence suggests males become sexually active at a smaller size and earlier age than females; a 2 year difference, suggested here, accounted for an estimated 12% of the between‐sex difference in mean adult L_T. Temporal shifts in gender‐specific survival accounted for an additional 27% of the observed between‐sex difference in mean adult L_T. Estimated age distributions indicated a higher number of older females than older males and more younger males than younger females in the population during the period of sampling. Dissimilarity of age distributions was an unexpected result because the male : female population sex ratio was 1 : 1 and estimates of long‐term annual survival for adult males and females were equal (88%). Future assessments of SSD in this population are apt to vary depending on the prior history of short‐term gender‐specific survival. Without recognizing SSD, non‐gender‐specific growth curves overestimate mean age of adult females and underestimate mean age of adult males of given L_T. Assuming age 8 years for first reproduction in males and age 10 years for females, the adult male : female ratio was estimated as 1·1 : 1 and mean adult age, or generation time, was estimated as 16·4 years for males and 18·4 years for females.     

Reproductive life history of the introduced peacock grouper Cephalopholis argus in Hawaii

This research investigated the reproductive biology (sex ratio, hermaphroditic pattern, size and age at maturity) of Cephalopholis argus, known locally in Hawaii by its Tahitian name roi. The results suggest that C. argus exhibits monandric protogyny (female gonad differentiation with female to male sex change) with females reaching sexual maturity at 1.2 years (95% c.i .: 0.6, 1.6) and 20.0 cm total length (L_T; 95% c.i .: 19.6, 21.2). The female to male sex ratio was 3.9:1. The average age and L_T at sex change was 11.5 years (95% c.i .: 11.1, 12.9) and 39.9 cm (95% c.i .: 39.5, 41.2), respectively. Current information on spawning seasonality of this species is incomplete, but based on the occurrence of spawning capable and actively spawning females, spawning probably takes place from May to October. Evidence of lunar spawning periodicity was found, with an increased proportion of spawning capable and actively spawning females, and an increased female gonado‐somatic index during first quarter and full‐moon phases. This information fills a valuable information gap in Hawaii and across the species' native range.     

Biological observations on the bristly catshark Bythaelurus hispidus from deep waters off the south‐west coast of India

Biological data are presented for the poorly known bristly catshark Bythaelurus hispidus based on specimens collected from the by‐catch of the commercial deep‐sea shrimp trawl fishery operating in the Arabian Sea at depths of 200–500 m off the south‐west coast of India. One hundred and sixty‐two individuals, which ranged from 120 to 366 mm total length (L_T), were collected for this study. Size‐at‐maturity (L₅₀) for females and males was estimated at 252 and 235 mm L_T, respectively. The reproductive mode of B. hispidus was aplacental viviparity, which is the rarest reproductive mode within the Scyliorhinidae and is considered to be the most advanced of the three reproductive modes occurring within this family. Dietary analysis of stomach contents revealed B. hispidus feeds on a variety of prey, primarily fishes.     

Age,growth and maturity of the pelagic thresher Alopias pelagicus and the scalloped hammerhead Sphyrna lewini

Indonesia has the greatest reported chondrichthyan catches worldwide, with c.110,000 t caught annually. The pelagic thresher (Alopias pelagicus) and scalloped hammerhead (Sphryna lewini) together comprise about 25% of the total catches of sharks landed in Indonesia. Age and growth parameters were estimated for A. pelagicus and S. lewini from growth‐band counts of thin‐cut vertebral sections. Alopias pelagicus (n = 158) and S. lewini (n = 157) vertebrae were collected from three Indonesian fish markets over a 5 year period. A multi‐model analysis was used to estimate growth parameters for both species. The models of best fit for males and females for A. pelagicus was the three‐parameter logistic (L_∞ = 3169 mm L_T, k = 0·2) and the two‐parameter von Bertalanffy models (L_∞ = 3281 mm L_T, k = 0·12). Age at maturity was calculated to be 10·4 and 13·2 years for males and females, respectively, and these are the oldest estimated for this species. The samples of S. lewini were heavily biased towards females, and the model of best fit for males and females was the three‐parameter Gompertz (L_∞ = 2598 mm L_T, k = 0·15) and the two‐parameter Gompertz (L_∞ = 2896 mm L_T, k= 0·16). Age at maturity was calculated to be 8·9 and 13·2 years for males and females, respectively. Although numerous age and growth studies have previously been undertaken on S. lewini, few studies have been able to obtain adequate samples from all components of the population because adult females, adult males and juveniles often reside in different areas. For the first time, sex bias in this study was towards sexually mature females, which are commonly lacking in previous biological studies on S. lewini. Additionally, some of the oldest aged specimens and highest age at maturity for both species were observed in this study. Both species exhibit slow rates of growth and late age at maturity, highlighting the need for a re‐assessment of the relative resilience of these two globally threatened sharks at current high levels of fishing mortality throughout the eastern Indian Ocean.     

Catch composition and reproductive biology of Sphyrna lewini (Griffith & Smith) (Carcharhiniformes, Sphyrnidae) in Indonesian waters

Data on the length compositions and reproductive biology have been collected for Sphyrna lewini in Indonesian waters, in which this species makes an important contribution to the biomass of its artisanal and small‐scale fisheries. These data were obtained by recording relevant body measurements and counts for this species while visiting Indonesian fish landing sites. The fish, which had been caught by gillnetting and longlining, covered a wide length range and included substantial numbers of immature, maturing and mature individuals. The vast majority of S. lewini <1100 mm total length (L_T) had been caught by gillnetting, whereas most of those above this length had been obtained through longlining. The number of embryos in pregnant females, which ranged from 14 to 41, with a mean of 25, was positively correlated with the L_T of those females. Birth occurred at c. 400 mm L_T and predominantly in October and November. The number of females was similar to that of males among smaller fish, but far greater than that of males among larger fish. This presumably reflects a faster growth and greater longevity of females, selectivity of longlining for females and a tendency for males to move outside the area fished. For males, the relationships between clasper length and the extent of its calcification, and also with sexual maturation and L_T have been determined. Females attained maturity (L_T50) at a far larger size (2285 mm) than males (1756 mm). The L_T of virtually all females and all males taken by gillnetting were less than their respective L_T50 at maturity, and c. 67 and 51% of the longline catches of females and males, respectively, were likewise immature. This feature, together with the substantial catches of S. lewini and the life cycle traits of elasmobranchs, suggest that this species is likely to be prone to overfishing in Indonesian waters. Furthermore, the removal of large numbers of this apex predator will presumably be affecting the trophic structure in the waters in which it is fished.     

Age, growth, and sexual maturity of the yellownose skate Dipturus chilensis in the south‐eastern Pacific

The age and growth parameters of Dipturus chilensis were estimated by counting growth rings from thin sections of vertebral centra from 400 fish (246 females and 154 males), ranging from 23 to 124 cm total length (L_T), and backcalculating fish lengths at previous ages. Marginal increment analysis lent support to the hypothesis of annual deposition of band‐pairs, which formed during the winter months. The oldest female D. chilensis aged in this study was 21 years and 117 cm L_T, whereas the oldest male was 18 years and 93 cm L_T. A 4·7% index of average per cent error (I_APE) suggested that this is a precise method for calculating the age of D. chilensis. Observed L_T were lower than backcalculated L_T, which implies the influence of Lee's phenomenon. The von Bertalanffy growth equations, based on mean length‐at‐age data, were estimated as L_t = 128·3 (1 ? e^{?0·112 (t + 0·514)}) for females and L_t = 107·8 (1 ? e^{?0·134 (t + 0·862)}) for males where t is age (years). Growth was significantly different between sexes: females reached a larger adult size. Ages and lengths at 50% maturity were estimated at 14 years of age and 106 cm L_T for females and 11 years of age and 86 cm L_T for males. At c. 14 years, there was a decline in growth rates in females. The factor most likely responsible for this was sexual maturity, which caused a discontinuity in growth of female fish. These results show that this species is slow‐growing, long‐lived, relatively large and of delayed maturity, characteristics that make it vulnerable to exploitation.     

Reproductive biology,multiple paternity and polyandry of the bull shark Carcharhinus leucas

To improve understanding of bull shark Carcharhinus leucas reproductive biology, we analysed reproductive traits from 118 bull sharks caught along Reunion Island coasts (Western Indian Ocean), including 16 gravid females. Specific microsatellite loci were used to investigate the frequency of multiple paternity. Males and females reached maturity at c. 234 cm and 257 cm total length (L_T), respectively, and litter sizes ranged from 5 to 14 embryos. Analysis of the 16 litters collected in various months of the year indicated that parturition occurs between October and December, with a size at birth c. 60–80 cm L_T and that the gestation period is probably c. 12 months. Assuming a 1 year resting period and a period of sperm storage (4–5 months) between mating (in June–September) and fertilisation, the reproductive cycle of bull sharks at Reunion Island would be biennial. At least 56.25% of the litters investigated were polyandrous, sired by 2–5 males. Several males that each sired several litters conceived during the same or distinct mating seasons were detected, suggesting both a seasonal aggregation of sharks to mate and some male fidelity to mating site. Altogether, these findings provide valuable information for both shark risk management and conservation of the species in the Western Indian Ocean.     

Maturation and sexual ontogeny in the spangled emperor Lethrinus nebulosus

The reproductive development and sexual ontogeny of spangled emperor Lethrinus nebulosus populations in the Ningaloo Marine Park (NMP) were investigated to obtain an improved understanding of its evolved reproductive strategy and data for fisheries management. Evidence derived from (1) analyses of histological data and sampled sex ratios with size and age, (2) the identification of residual previtellogenic oocytes in immature and mature testes sampled during the spawning season and (3) observed changes in testis internal structure with increasing fish size and age, demonstrated a non‐functional protogynous hermaphroditic strategy (or functional gonochorism). All the smallest and youngest fish sampled were female until they either changed sex to male at a mean 277·5 mm total length (L_T) and 2·3 years old or remained female and matured at a larger mean L_T (392·1 mm) and older age (3·5 years). Gonad masses were similar for males and females over the size range sampled and throughout long reproductive lives (up to a maximum estimated age of c. 31 years), which was another correlate of functional gonochorism. That the mean L_T at sex change and female maturity were below the current minimum legal size (MLS) limit (410 mm) demonstrated that the current MLS limit is effective for preventing recreational fishers in the NMP retaining at least half of the juvenile males and females in their landed catches.     

Reproductive biology and feeding habits of the prickly dogfish Oxynotus bruniensis

The reproductive biology and diet of prickly dogfish Oxynotus bruniensis, a deep‐sea elasmobranch, endemic to the outer continental and insular shelves of southern Australia and New Zealand, and caught as by‐catch in demersal fisheries, are described from specimens caught in New Zealand waters. A total of 53 specimens were obtained from research surveys and commercial fisheries, including juveniles and adults ranging in size from 33·5 to 75·6 cm total length (L_T). Estimated size‐at‐maturity was 54·7 cm L_T in males and 64·0 cm L_T in females. Three gravid females (65·0, 67·5 and 71·2 cm L_T) were observed, all with eight embryos. Size‐at‐birth was estimated to be 25–27 cm L_T. Vitellogenesis was not concurrent with embryo development. Analysis of diet from stomach contents, including DNA identification of prey using the mitochondrial genes cox1 and nadh2, revealed that O. bruniensis preys exclusively on the egg capsules of holocephalans, potentially making it the only known elasmobranch with a diet reliant solely upon other chondrichthyans. Based on spatial overlap with deep‐sea fisheries, a highly specialized diet, and reproductive characteristics representative of a low productivity fish, the commercial fisheries by‐catch of O. bruniensis may put this species at relatively high risk of overfishing.