Variation in length and age at sexual maturity of Atlantic groundfish: a reply

Synopsis The assertion has been made by Halliday (1987) that trends in size and age at maturity of Atlantic groundfish published by Beacham (1983a, b, c, d, e, f) are artifacts induced by errors in determining the sex of an individual, distinguishing between immature and mature fish, sampling fish outside of the regular spawning season, and by nonrandom sampling of the population. In particular, Halliday asserts that for the Atlantic argentine,Argentina silus analysis, the conclusions of Beacham (1983a) that: (1) median length at sexual maturity declined over time; and (2) males matured at older ages than did females are invalid owing to biases in both sampling and analysis. In fact, if some of the biases indicated by Halliday were significant, then the decline in median length at sexual maturity is enhanced and the conclusions of Beacham (1983a) reinforced. Size and age at sexual maturity are dynamic characters in many vertebrate populations, and the fact that they should change for Atlantic groundfish should not be surprising given variable exploitation patterns in the fisheries since 1960.     

Maturity Ogives for South Pacific Albacore Tuna (Thunnus alalunga) That Account for Spatial and Seasonal Variation in the Distributions of Mature and Immature Fish

Length and age at maturity are important life history parameters for estimating spawning stock biomass and reproductive potential of fish stocks. Bias in estimates of size and age at maturity can arise when disparate distributions of mature and immature fish within a population are not accounted for in the analysis. Here we investigate the spatial and temporal variability in observed size and age at maturity of female albacore tuna, Thunnus alalunga, using samples collected across the South Pacific. Maturity status was identified using consistent histological criteria that were precise enough to allow for mature but regenerating females to be distinguished from immature females during the non-spawning season, permitting year-round sampling for maturity estimation in albacore. Using generalised linear mixed models, we found that the proportion of mature females at length varied significantly with latitude and time of year. Specifically, females at northern latitudes (∼10–20°S, where spawning occurs) were mature at significantly smaller lengths and ages than females at southern latitudes (∼20–40°S), particularly during the spawning season (October–March). This variation was due to different geographic distributions of mature and immature fish during the year. We present a method for estimating an unbiased maturity ogive that takes into account the latitudinal variation in proportion mature at length during a given season (spawning or non-spawning). Applying this method to albacore samples from the western region of the South Pacific gave a predicted length at 50% mature of ∼87 cm fork length (4.5 years).     

Sexual dimorphism of drumming muscles in European hake (<Emphasis Type="Italic">Merluccius merluccius</Emphasis>)

Dissections of mature and non-mature European hake males and females (N = 142) collected in waters off the western coast of Norway and in the Bay of Biscay (France) in 2004–2006 demonstrate for the first time that this gadoid species contains drumming muscles. There were differences in drumming muscles weight with body length, sex and maturity stage. This study shows that the difference between females and males is primarily manifested during the spawning season, seen both in the French and Norwegian samples. For the mature females the drumming muscles dry weight increases only slightly, if at all, with increase in total length. For mature males there is a corresponding rapid increase. There does not seem to be any consistent difference between the average dry weight of the drumming muscles in immature male and immature and mature female hake of the same length, tested on the Norwegian samples. Our results suggest that male hake, like the males of other gadoids studied, may produce sounds in the context of spawning.     

Probabilistic reaction norm reveals family-related variation in the association between size,condition, and sexual maturation onset in Atlantic salmon (Salmo salar)

This study investigated the relationship between the size, condition, year class, family, and sexual maturity of Atlantic salmon (Salmo salar) using data collected in an aquaculture selective breeding programme. Males that were sexually mature at 2 years of age (maiden spawn) have, on average, greater fork length and condition factor (K) at 1 year of age than their immature counterparts. For every 10-mm increase in fork length or 0.1 increase in K at 1 year of age, the odds of sexual maturity at 2 years of age increased by 1.48 or 1.22 times, respectively. Females that were sexually mature at 3 years of age (maiden spawn) have, on average, greater fork length and K at 2 years of age than their immature counterparts. For every 10-mm increase in fork length or 0.1 increase in K at 2 years of age, the odds of sexual maturity at 3 years of age increased by 1.06 or 1.44 times, respectively. The family explained 34.93% of the variation in sexual maturity among 2-year-old males that was not attributable to the average effects of fork length and K at 1 year of age and year class. The proportion of variation in sexual maturity among 3-year-old females explained by the family could not be investigated. These findings suggest that the onset of sexual maturation in Atlantic salmon is conditional on performance (with respect to energy availability) surpassing a threshold, the magnitude of which can vary between families and is determined by a genetic component. This could support the application of genetic selection to promote or inhibit the onset of sexual maturation in farmed stocks.     

AGE,GROWTH, AND REPRODUCTIVE PATTERNS OF DALL'S PORPOISE (PHOCOENOIDES DALLI) IN THE CENTRAL NORTH PACIFIC OCEAN

Life history parameters were estimated for Dall's porpoise, Phocoenoides dalli, from biological specimens collected in the western Aleutian Islands, during 1981–1987. Of 2,033 males and 3,566 females examined, reproductive data were available for 1,941 males and 1,906 females; ages were determined for 813 males and 1,297 females. Female sexual maturity was based on the presence of one or more corpus on either ovary; 845 were sexually immature and 1,061 were sexually mature. Two estimates of female average age at sexual maturity (ASM) were 3.8 and 4.4 yr; average length at sexual maturity (LSM) was 172 cm. Males were considered sexually mature when evidence of spermatogenesis was detected; 1,136 were sexually immature and 805 were sexually mature. Two estimates of male ASM were 4.5 and 5.0 yr; LSM was 179.7 cm. Physical maturity was assessed for 246 males and 446 females by examining the degree of fusion in thoracic vertebral epiphyses. For both sexes, the average age at physical maturity was 7.2 yr. Average length at physical maturity was 202.6 cm for males and 192.7 cm for females. Average lengths of physically mature males (x?= 198.1 cm, SE = 0.8566) and females (x?= 189.7 cm, SE = 0.4002) were significantly different(P < 0.0001). Early postnatal growth was rapid in both sexes. A secondary growth spurt in both mass and length was characteristic for both sexes; the increase in length preceded the mass increase by 1–2 yr. Average length at birth (LOB) was approximately 100 cm; birth mass averaged 11.3 kg (SE = 0.0772). By the time the umbilicus had healed (<2 mo), the average length and mass had increased to 114.1 cm and 23.8 kg, respectively. Gestation period based on projections using LOB was 12 mo, but this was considered an overestimate. Calving was modal, centered in early July; an annual reproductive interval was indicated. Among the sexually mature females, 120 were pregnant, 55 were pregnant and lactating, 321 were pregnant with colostrum, and 33 were “resting.” By 3 July (95% CI =x? 1 d), 50% of births had occurred, during each of the seven years sampled. The ovulation rate was estimated at 0.914 ovulations per average reproductive year. Enlarged follicles and recent ovulations were observed in postpartum females in late July.     

The effect of growth rate,size, and season on oocyte development and maturity of Atlantic cod (Gadus morhua L.)

The effect of growth rate, body weight, age, and season on ovarian development and maturation was investigated for Atlantic cod (Gadus morhua L.) reared in the laboratory over 10 months, for each of two consecutive years, 1978–1980. Cod were also collected from the Gulf of St. Lawrence, the Scotian Shelf, Georges Bank, the Flemish Cap, and the N.E. Newfoundland Shelf.The state of maturity was recognized by oocyte size. Stage I oocytes did not vary in size with growth rate, season, age, or maturity, while the size of stage II oocytes was positively correlated with maturity and negatively correlated with maximum stage of development achieved. Ovarian wall thickness was positively correlated with age and maturity.The frequency distribution of stage I and II oocytes distinguished the state of maturation, with cod that would mature by the next spawning season having a minimum of 20% ($\text{x}\text{?}\text{= 42\%}$) of their oocytes at stage II or greater level of development.Maturing 3-yr-old cod had greater life specific growth rates than immature 3-yr-olds, but growth rates during the third year itself were not significantly different. A hypothesis of a three-part density-dependent mechanism controlling fecundity is postulated. Future reductions in partial recruitment and total fecundity are predicted for the Gulf of St. Lawrence cod stock based on calculated growth rates for Gulf cod in 1979.     

Differences in growth performance between Arcto-Norwegian and Norwegian coastal cod reared under identical conditions

Offspring from seven family groups of Arcto-Norwegian cod (AN) and a genetically marked Norwegian coastal cod (NC) broodstock, were mixed at metamorphosis and raised in the same rearing unit. The fish were transferred subsequently to a net-pen and held under standard farming conditions. In December 1992, 466 cod juveniles were measured, weighed, and tagged individually. Length and weight changes were monitored until the fish matured (January 1994). Genotyping of each individual was performed using enzyme electrophoresis to identify the fish to strain. Prespawning females were examined for organ weights and stage of maturity. There were population specific Differences in growth performance. NC displayed significantly higher specific growth rate (SGR) and daily length increment (DLI) during spring/summer season. The AN had significantly lower hepatosomatic and gonadosomatic indices, and were thinner than the NC, indicating Differences in body form and energy allocation pattern between the two strains. All NC (both sexes) became sexually mature at the age of 2 years while 2% of fish in the AN group were still immature at the end of the experiment.     

Sexual size dimorphism, growth and maturity of the Japanese fluvial sculpin,Cottus pollux (large egg type), in the Inabe River, Mie prefecture, central Japan

The population structure of the Japanese fluvial sculpin,Cottus pollux (large egg type), in the upper reaches of the Inabe River, Mie Prefecture, central Japan, was investigated by a mark-and-recapture method from July 1989 to January 1991. Breeding of the species occurred from mid February to early May, peaking from mid February to late March. The mean size of mature males observed in March 1990 was significantly larger than that of females, showing apparent sexual size dimorphism. Data analysis of the growth of 1658 marked individuals revealed that the species matured at 2 years of age in both sexes. Whereas 1 year old males reached ca. 50–70 mm SL, females were less than 50 mm SL at the same age, size dimorphism already being apparent. Immature males exhibited higher growth rates than females during their first and second years, some of the former outstripping mature males of the preceding year class in total length. After attaining sexual maturity, both males and females grew mainly from July to December, with no significant differences in mean growth rate between them. Sexual size dimorphism of the species seems to be attributable to different growth rates between the sexes during their immature stage.     

Ovarian development of Agrilus planipennis: effects of age and mating status and influence on attraction to host volatiles

Emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), is a major pest of ash trees, Fraxinus spp. (Oleaceae), in North America. This study investigated the timing of reproductive development in female beetles and the influence of female reproductive maturity on attraction to host volatiles. Based on dissections of females of increasing age, females with access to males for mating, and thus presumed mated, developed mature eggs only after 18–24 days. In contrast, female beetles reared without access to males, and thus unmated, did not develop mature eggs at any age. Chemical analysis of cuticular hydrocarbons detected the contact sex pheromone, 9‐methyl‐pentacosane, in cohorts of females which were 8–9 days old and older, supporting previous research that this compound signals sexual maturity to males. Results from field‐trapping bioassays demonstrated that stage of female reproductive maturity influenced their attraction to host volatiles: females caught on traps baited with foliar volatiles contained eggs and ovarioles that were significantly less developed than those on traps baited with bark sesquiterpenes. However, our results revealed that females with immature stages of ovarioles and undeveloped eggs, such as those observed in unmated females, were rarely ever caught on traps baited with either of the host volatile lures. Further research on host compounds attractive to immature females is critical for early detection and possible control of A. planipennis populations during the extended pre‐oviposition period.     

Aspects of reproductive biology of the Mediterranean amberjack (Seriola dumerilii Risso) during the spawning period

Wild Seriola dumerilii were collected in the South Mediterranean Sea during the 1990, 1991 and 1992 spawning seasons. Macroscopic and cytological characteristics of ovary and testis were analysed. Depending on the presence and the number of oocytes at different stages, a five point maturity scale was proposed for ovarian maturity. Nine maturity stages of the oocytes are described. Oocyte size-frequency distribution has shown a group synchronous ovarian development type. The testes have a typical lobular-type structure. Depending on lobules and sperm duct development and on the abundance of germ cells, testis maturity was classified in four stages. Maturity rate according to age and size was also determined. 100% of 1-year-old fish show immature gonads. The proportion of females with mature ovaries was 0, 12.5, 84.6 and 100% at the age of 2, 3, 4 and 5 years respectively. The proportion of males with mature testes was 14.3, 40, 80 and 100 at the same age. The median standard length at which 50% of the fish attained maturity is 109 and 113 cm SL in males and females respectively.     

REPRODUCTION IN MALE ATLANTIC WALRUSES (ODOBENUS ROSMARUS ROSMARUS) FROM THE NORTH WATER (N BAFFIN BAY)

Age at sexual maturity and timing of the mating season were determined in male Atlantic walruses ( Odobenus rosmarus rosmarus , L.) from the "North Water" subpopulation in northern Baffin Bay. Testes and epididymides of 174 male walruses (between 0 and 30 yr old) from NW Greenland (1987–1990) were studied macroscopically and a subset of 57 specimens was analyzed microscopically. In physically mature bulls ( i.e. , ≥12 yr old), sperm or apparently ripe spermatids were found between 9 November and 12 July. In younger walruses these signs of fertility were found in a few specimens (7–11 yr old) collected between 9 January and 28 May. The mating season seems to peak in January—April. The youngest sexually mature individual was 7 yr old and the oldest apparently immature individual was 13 yr old. Average age of sexual maturity was 10.9 yr (95% C.I.: 9–6–12.2 yr) and all were sexually mature by the time they were 14 yr old. The non-spermiogenetic testes and epididymides showed accelerated growth between about the 5–6th and about the 12–15th year of life, indicating that sexual maturation occurs during these years. The length of the baculum increased gradually until about 12–15 yr of age, when physical maturity was reached.     

Gonad development and reproductive cycle of the white‐spotted rabbitfish Siganus canaliculatus (Park, 1797) in Palompon,Leyte, Eastern Visayas,Philippines

The siganid production in the Philippines is continuously declining from 2007 up to present. In Palompon, Leyte, annual yield of siganids, particularly Siganus canaliculatus (Park, 1797) also showed a decreasing trend of total production. This is consistent that this stock is under heavy pressure, and when left unmanaged, this could lead to further overexploitation and the collapse of the stock in the long run. Regardless of this, detailed reproductive biology and potential of this species are very few in the Philippines. Therefore, this study was conducted to provide information on the reproductive biology and breeding cycle of S. canaliculatus in Palompon, Leyte where fishing pressure is high and sound management formulation is necessary. S. canaliculatus is a group‐synchronous, multiple spawners with skewed sex ratio where males predominates over females. Maturity stages based on macroscopic examinations identified four maturity stages (immature, developing, mature and spent) while six maturity stages (immature, developing, mature, spawning, spent and re‐developing) were identified through histological analysis. A single ovo‐testis was identified among the 669 specimens examined. Based on histological sections, the smallest size of mature male was 5.5 cm standard length, and the smallest mature female was 7.1 cm standard length. On the other hand, length at first maturity for mature fish were 8.1 cm standard length for males and 9.7 cm standard length for females. Two defined peaks of gonadosomatic index were identified in both sexes: a major peak from February to May and a minor protracted one from July to December. Mature and older ovaries and testes occurred throughout the year, an indication of your round breeding season of S. canaliculatus in Palompon. Implementing a fishing ban during the major and the minor breeding spawning peaks would allow the mature and older individuals to contribute first to the population; allowing the continuity of the stock.     

Sexual maturity cycle and spawning of Greenland halibut Reinhardtius hippoglossoides in the Davis Strait

Female sexual maturation cycle and the main spawning time of Greenland halibut Reinhardtius hippoglossoides in the Davis Strait were studied through regularly collected samples during 1 year starting in spring 2003. Samples were collected from the southern slope of the Davis Strait Ridge between Canada and Greenland in the depth range 1000–1500 m. Female sexual maturation was described using different approaches: gonado‐somatic index, visual macroscopic maturity stage index, histological microscopic maturity index and oocyte diameter measurements. A significant increase in the gonado‐somatic index was seen from September onwards until February with a maximum estimated value of 18%. The proportion of mature fish increased from December until March. At the same time, the proportion of females with a low gonado‐somatic index also increased from February, indicating that spawning had occurred and females were recovering. Oocyte diameter distribution revealed a leading cohort development during autumn through to December to February. A coupling between sexual maturity and fish condition was seen for females in maturing condition indicating a steady build up of stored energy in the liver from June to November.     

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.     

Maturation of female common snook Centropomus undecimalis: implications for managing protandrous fishes

The assumption for hermaphroditic fish species that mature individuals of the terminal sex arise directly from mature individuals of the primary sex has led to the use of sex ratios as a proxy for age at maturity (A₅₀). The timing of transition and deficient energy reserves, however, can result in a delay between transition and spawning. To test the assumption of female maturity and investigate the relationship between maturation and energy reserves, common snook, Centropomus undecimalis, a protandrous hermaphrodite, were collected from rivers, estuaries, inlets and offshore habitats on the east coast of Florida during 2010–2015. Immature females were observed every month, with lowest proportions during the peak spawning months of July and August. When calculated based on sex ratio, A₅₀ (8.1 years) overestimated the age at which 50% of the female population was, in fact, mature (4.1–4.9 years). Best-fit models indicate that mesenteric fat index (I_F) and hepato-somatic index (I_H) were significantly affected by gonad phase, month and size and weakly by habitat. In post hoc analysis, immature female I_F did not differ significantly from developing and regenerating females, but immature female I_H was significantly lower than that for all mature phases except animals in the regressing phase. Although immature females may have sufficient energy in terms of fat, it appears that energy is not allocated to reproductive processes, as evidenced by lower I_H. Nonetheless, approximately 95% of females were spawning-capable during peak spawning months, suggesting that the energy threshold at which immature females reach maturity is met by most females each spawning cycle.     

Age at sexual maturity of male and female banana weevils,Cosmopolites sordidus Germar (Coleoptera: Curculionidae)

This study was to determine the age at sexual maturity and the relationships between age and internal reproductive organs of Cosmopolites sordidus. Male banana weevils become sexually mature 18 days after emergence (DAE), that is after 2 weeks of adult eclosion, in spite of the fact that spermatogenesis is completed at emergence. A positive correlation exists between age and male internal organs, for example for mean testis diameter (r = .849, p ≤ .001), mean seminal vesicle diameter (r = .679, p ≤ .001), mean accessory gland length (r = .561, p ≤ .01) and mean accessory gland diameter (r = .498, p ≤ .05), respectively. Significant differences were recorded between sexually mature and immature weevils with respect to mean testis diameter (T = 4.471, p ≤ .001) and mean seminal vesicle diameter (T = 3.939, p ≤ .001), but not with mean accessory gland length and mean accessory gland diameter (T = 1.899 and 1.661). Male internal organs were visibly underdeveloped at emergence but became significantly enlarged and developed on attainment of sexual maturity. Female C. sordidus, on the other hand, are sexually mature at 5 DAE. There was also a strong, positive correlation between age of females and mean ovariole length (r = .656, p ≤ .001), and significant differences existed between mean ovariole lengths of sexually mature and immature females (T = 4.306, p ≤ .001). Increasing age of females witnessed progressive increases in ovariole lengths and developmental changes within female ovarioles and calyces. The findings made here may be helpful in Musa germplasm screening works, as weevils bred on susceptible cultivars may reveal similar results, while those bred on resistant ones may experience possible delays in their reproductive developments.     

Reproductive biology of two sympatric skates in the south‐west Atlantic: Psammobatis rudis and Psammobatis normani

The total lengths ( L _T) at which 50% were mature of Psammobatis rudis and Psammobatis normani , in the south‐west Atlantic were: P. rudis , 428 mm for males and 414 mm for females and P. normani , 443 mm for males and 403 mm for females. Clasper length in mature males was greater in P. normani than in P. rudis , whereas oviducal gland width was not different between species. Females of P. normani with egg cases were found in every month sampled, and in January, March, April and July in P. rudis , although insufficient samples were available to identify peak oviposition times. Geographic variation in size frequency and maturity were found. The effects of oceanographic conditions and fishing pressure are discussed. Size at 50% maturity in both species was >74% of the maximum L _T, indicating late sexual maturity and low potential stock recovery rate.     

Sex‐specific reproductive investment of summer spawners of Illex argentinus in the southwest Atlantic

Energy investment in reproduction and somatic growth was investigated for summer spawners of the Argentinean shortfin squid Illex argentinus in the southwest Atlantic Ocean. Sampled squids were examined for morphometry and intensity of feeding behavior associated with reproductive maturation. Residuals generated from length‐weight relationships were analyzed to determine patterns of energy allocation between somatic and reproductive growth. Both females and males showed similar rates of increase for eviscerated body mass and digestive gland mass relative to mantle length, but the rate of increase for total reproductive organ weight relative to mantle length in females was three times that of males. For females, condition of somatic tissues deteriorated until the mature stage, but somatic condition improved after the onset of maturity. In males, there was no correlation between somatic condition and phases of reproductive maturity. Reproductive investment decreased as sexual maturation progressed for both females and males, with the lowest investment occurring at the functionally mature stage. Residual analysis indicated that female reproductive development was at the expense of body muscle growth during the immature and maturing stages, but energy invested in reproduction after onset of maturity was probably met by food intake. However, in males both reproductive maturation and somatic growth proceeded concurrently so that energy allocated to reproduction was related to food intake throughout the process of maturation. For both males and females, there was little evidence of trade‐offs between the digestive gland and reproductive growth, as no significant correlation was found between dorsal mantle length‐digestive gland weight residuals. The role of the digestive gland as an energy reserve for gonadal growth should be reconsidered. Additionally, feeding intensity by both males and females decreased after the onset of sexual maturity, but feeding never stopped completely, even during spawning.     

Spawning and reproductive patterns of six exploited finfish species from the Arabian Sea, Sultanate of Oman

The spawning periods, sex ratio and length at first maturity were determined for six commercially important finfish species collected from Oman's industrial trawl fishery. During 1 year of monthly sampling, biological data were collected on 5586 fish. ancova was used to compare the length–weight relationships between sexes. There were sex‐specific differences in length‐weight relationships for three of the six species examined. One serranid, Epinephelus diacanthus, and a sparid, Pagellus affinis, had sex ratios significantly different from the expected ratio of 1 : 1. Size–frequency data revealed more male fish in the larger size classes for E. diacanthus, P. affinis and Nemipterus japonicus. Data on the development of female gonads and Gonado‐somatic Index (GSI) revealed that the six species spawned at different times of the year. With the exception of female E. diacanthus, all fish had low GSI values during the onset of the summer monsoon period in June. The proportion of immature vs mature fish in the sample differed among species. For two species, Lethrinus nebulosus and Cheimerius nufar, more than 40% of the fish sampled (both sexes) were immature. Approximately 33% female and 41% male P. affinis were also immature. Management options such as temporal and area closures are discussed in light of the large number of immature fish caught by the fishery.     

Adolescents' Psychosocial Maturity,Problem Behavior,and Subjective Age: In Search of the Adultoid

The objectives of this study were to seek empirical confirmation for the existence of a group of adolescents whose maturity status could be labeled as adultoid, and to identify psychosocial correlates of adolescents' maturity status. Cluster analysis of questionnaire data from 209 predominantly White adolescents (10-18 years old) in working- and middle-class 2-parent families identified 3 maturity status groups: adultoids (low psychosocial maturity, high problem behavior, older subjective age); matures (high psychosocial maturity, low problem behavior, slightly older subjective age); and immatures (low psychosocial maturity, low problem behavior, young subjective age). Regressions revealed that several adolescent- and mother-reported variables were linked to maturity status. Relative to their mature and immature counterparts, adultoid adolescents exhibited more advanced physical maturity, earlier expectations for attaining privileges, higher social involvement, and in boys, higher mother-adolescent conflict. Adultoid adolescents do exist, and they differ from mature and immature adolescents in important ways. These results have implications for understanding the diversity in adolescents' levels of maturity.