Re-evaluation of reproductive cycle and fecundity of finetooth sharks Carcharhinus isodon (Valenciennes 1839) from the Northwest Atlantic Ocean,with new observations on ovarian cycle and reproductive endocrinology of biennially reproducing sharks

To provide updated information on life history for improved fishery management, the reproductive cycle of the finetooth shark Carcharhinus isodon from Northwest Atlantic (NWA) populations was investigated by examining temporal changes in morphology and histology of reproductive organs. Changes in plasma concentrations of gonadal sex hormones in relation to reproductive stage were also examined. Increases in testis width, epididymis head width, plasma testosterone concentrations and occurrence of mature spermatozoa were observed in male sharks between December and April, suggesting a seasonal pattern in reproduction that culminates with copulatory activity in May. Increases in maximum follicular diameter, oviducal gland width, plasma 17β-estradiol concentrations and occurrence of vitellogenic follicles were observed in non-pregnant female sharks during the same time period along with the occurrence of newly pregnant females in May, demonstrating strong synchronicity between male and female reproductive cycles. Pregnant females bearing full-term embryos were also observed in May, indicating that parturition occurs between mid-May and early June and gestation requires 12 months. Only transient temporal changes in follicle size and oviducal gland width were observed in pregnant females, indicating that reproductive periodicity is biennial; nonetheless, a single female exhibiting signs of concurrent vitellogenesis and pregnancy was observed. Mean brood size ± S.D. was 3.9 ± 0.9 offspring/female. Fecundity was not significantly correlated with female size, in part due to an unexpectedly high rate of early embryo mortality, which occurred in 11% of pregnant females, and was more common in larger individuals. Changes in ovarian activity during mid-pregnancy were observed, suggesting possible roles for the ovary in regulating some aspects of early to mid-gestation. This study confirms that earlier characterizations of the reproductive cycle and fecundity in NWA finetooth sharks remain valid for use in fishery management. This study also highlights unusual features of finetooth shark pregnancy (e.g., early embryo death, mid-pregnancy changes in ovarian function) that may have broader relevance to understanding elasmobranch reproduction.     

Sex, seasonal, and stress-related variations in elasmobranch corticosterone concentrations

Serum corticosterone was previously studied in numerous elasmobranch fishes (sharks, skates and rays), but the role of this steroid, widespread throughout many taxa, has yet to be defined. The goal of this study was to test whether corticosterone varied in response to acute and chronic capture stress, and across the reproductive cycle in the bonnethead shark, Sphyrna tiburo, and Atlantic stingray, Dasyatis sabina. Serum corticosterone in S. tiburo increased following capture and again 24 h post-capture, possibly caused by interference with 1α-hydroxycorticosterone, the primary stress hormone in elasmobranchs. Higher serum concentrations in males compared to females were observed in both species. Variations in corticosterone also occurred during the reproductive cycle in both species. Consistent with other taxa, elevations in male bonnethead sharks and stingrays coincided with peak testicular development and mating. Elevations in female bonnethead sharks occurred from the time of mating through sperm storage into early gestation. In contrast, corticosterone levels in female stingrays were low during their protracted mating season, but elevated through late gestation and parturition. These results indicate that corticosterone has a limited role, if any, in acute and chronic stress associated with capture in S. tiburo, but likely has physiological functions associated with its glucocorticoid properties across the reproductive cycle of both species.     

Plasma steroid concentrations of adult male Atlantic sharpnose sharks, <Emphasis Type="Italic">Rhizoprionodon terraenovae,</Emphasis> in the northern Gulf of Mexico,with notes on potential long term shifts in reproductive timing

In previous literature it was proposed that Atlantic sharpnose sharks, Rhizoprionodon terraenovae, from the western Atlantic Ocean (WAO) population exhibited differences in their reproductive timing when compared to the northern Gulf of Mexico (GOM) population. The objective of the current study was to examine the reproductive cycle of mature male sharpnose sharks from the northern GOM population. Plasma testosterone (T) and estradiol (E₂) were measured from 76 mature male sharpnose sharks sampled from 1999 to 2001, and the gonadosomatic index (GSI) was determined for 53 additional mature males sampled from 2007-2008. Plasma T, E₂, and GSI exhibited similar cycles with peak values occurring in late spring (April/May) and lowest values occurring during the summer. These results suggest that male sharpnose sharks in the northern GOM are reproductively active one to two months earlier than previously reported, which now brings them into synchrony with the WAO population. Interestingly, this shift in reproductive timing corresponds with a 3.0°C (13.4%) increase in spring sea surface temperature (SST) from the Mississippi Sound over a 29 year period, which could translate into GOM male sharpnose sharks becoming reproductively active earlier in the year thus explaining the late spring peak in GSI.     

Plasma progesterone concentrations in female little brown bats (Myotis lucifugus) during hibernation

Monthly collections of hibernating little brown bats contained (1) nulliparous females with small uteri and no antral follicles, (2) nulliparous females with swollen uteri and mature follicles, and (3) parous females, which, despite obvious differences in reproductive status, had equivalent plasma progesterone values. During the principal study season, mean monthly progesterone concentrations (measured by radioimmunoassay) showed recurrent increases with an apparent periodicity of about 60 days, but limited data obtained in the subsequent season did not. However, comparison of activity patterns in the two seasons with monthly progesterone concentrations suggests that ovarian activity during hibernation is affected by variations in metabolic level. We saw no evidence that nulliparous bats with small uteri developed antral follicles during hibernation. Despite their apparent immaturity, however, they had cornified vaginae and most were demonstrably inseminated. These indications of oestrus and the lack of differences between their plasma progesterone concentrations and those of patently mature females suggest that they were physiologically post-pubertal but failed to complete folliculogenesis before entering hibernation.     

Reproductive cycle of the blacknose shark Carcharhinus acronotus in the Gulf of Mexico

The reproductive periodicity of blacknose sharks Carcharhinus acronotus in the northern Gulf of Mexico was determined by examining reproductive tissues from specimens collected monthly from 2002 to 2005. Monthly changes in shell gland mass, right ovary mass and ovarian follicle diameter were assessed for 74 mature females. Temporal changes in testes mass, testes width and proportion of mature spermatocysts were examined for 64 mature males. Trends in female reproductive tissues suggested an annual peak in reproductive activity during June and July, while trends in male variables suggested an annual reproductive peak during May and June. Although male and female reproductive activity peaked in different months, a strong synchronicity existed between the proportion of mature spermatocysts and the diameter of the largest ovarian follicle. Based on these results, the mating season of blacknose sharks lasts from mid-May to July in the Gulf of Mexico. Maximum embryo sizes were observed in May, which suggested that partition occurs during late May or early June. Results indicate that blacknose sharks have a clearly defined annual cycle in the Gulf of Mexico. This conclusion is further supported by the complete absence of gravid females without vitellogenic ovarian follicles among all mature females examined.     

Reproductive biology of Carcharhinus acronotus in the coastal waters of South Carolina

The reproductive biology of blacknose sharks Carcharhinus acronotus in the western North Atlantic Ocean was studied by examining specimens collected in the coastal waters of South Carolina. Males begin the maturation process between 875 and 910 mm fork length ( L _F), as indicated by the presence of functional claspers and siphon sacs. The presence of vitellogenic oocytes and developing oviducal glands and uteri indicated that females begin to mature at c . 870 mm L _F. Length at which 50% of the population reached maturity was 896 and 964 mm L _F, equivalent to 4·3 and 4·5 years, for males and females, respectively. Gonado‐somatic indices suggested that spermatogenesis and vitellogenesis began after December. Mating took place during the end of May and the beginning of June. Fertilization occurred during late June and early July, suggesting that female blacknose sharks were capable of sperm storage. Based on the timing of fertilization and occurrence of females carrying near‐term pups in late May and early June, the gestation period for blacknose sharks was c . 11 months. Female blacknose sharks reproduced biennially based on the absence of vitellogenic oocytes in near‐term females and there being no indication of vitellogenesis in postpartum females. Male blacknose sharks were capable of reproducing annually as indicated by turgid genital ducts, which were observed in all mature males collected during late May and early June.     

Reproductive biology of deep-sea catsharks (Chondrichthyes: Scyliorhinidae) in the eastern North Pacific

Apristurus brunneus, A. kampae, and Parmaturus xaniurus were caught by trawl and longline between Washington and southern California (48°N to 32°N latitude) from June 2001 through October 2004. In females, oviducal gland width increased with TL in all three species but remained within 4 to 6% of TL. Oocyte diameter increased with TL during reproductive development in all species, and continued to increase with size after reproductive maturity was reached. The weight-length relationships differed significantly among species but not between sexes of any species from the eastern North Pacific combined. Using logistic regression, it was determined that total length at 50% maturity (TL₅₀) of A. brunneus males was 514 mm TL and all A. brunneus males were mature at 547 mm TL. Female A. brunneus reached TL₅₀ at 501 mm TL and all female A. brunneus were mature at 581 mm TL. Apristurus kampae males and females reached TL₅₀ at approximately 485 mm TL and 490 mm TL, respectively. Parmaturus xaniurus males reached TL₅₀ at 444 mm TL and females at 501 mm TL. Gravid female A. brunneus were found in all months of the year, but gravid P. xaniurus were found primarily June through September. Adult A. kampae females were found only in July through November and there were gravid females in all these months. Based upon gonadosomatic indices, I _G, these species may mate within a defined period of time (April through June); however, A. brunneus appear to reproduce throughout the year and P. xaniurus reproduce within a defined season (approximately July through September).     

Correlated responses to selection on female egg size in male reproductive traits in a butterfly

Genetic correlations between male and female traits can act as evolutionary constraints and, if involving reproductive traits, potentially influence sexual selection. Artificial selection on egg size in the tropical butterfly Bicyclus anynana has yielded highly divergent lines. Here we report evidence for correlated evolution in male traits. Males from the large-egg selected lines produced significantly heavier spermatophores independent of body size and tended to have more fertile sperm stored in their reproductive tracts than those from the small-egg selected lines. This may be due to an underlying genetic correlation in reproductive effort between the sexes. However, non-fertile sperm number and testis size remained unaffected by selection on egg size. Phenotypic correlations within an unselected population revealed that spermatophore mass and fertile sperm number, but not testis size and non-fertile sperm number, were positively related to male body size, and that larger spermatophores contained more fertile, but not non-fertile sperm. In addition, males provided larger females with bigger spermatophores and more fertile sperm, indicating males may be exercising mate choice during copulation.     

Reproductive biology of the Brazilian guitarfish,Pseudobatos horkelii (Müller & Henle, 1841) from southeastern Brazil,western South Atlantic

This study provides information on the seasonal occurrence, length‐width relationship, sexual development and size at first maturity of the critically endangered Brazilian guitarfish Pseudobatos horkelii in southeastern Brazil. Samples were obtained from September 2007 to August 2009 from commercial fisheries off São Paulo State coast at depths of 10–50 m, with net mesh sizes of 150 mm in the main net and 100 mm in the cod end. A total of 143 specimens (71 males, 72 females) were analyzed. Total length (TL), disc width (DW), sex and reproductive variables were recorded for each individual. Pseudobatos horkelii presents sexual dimorphism in length‐width relationships, with females attaining larger TL and DW. Females also mature at a larger TL, at 81.1% of the maximum TL, while males mature at 67.8% of the maximum TL. No specimens were captured in winter, and only a small sample size was observed in autumn. Males captured in spring and summer presented semen in the seminal vesicle, indicating that this species may reproduce in the warmer months, as already observed for other Rhinobatidae as well as for P. horkelii in southern Brazil.     

Reproductive biology of the milk shark Rhizoprionodon acutus and the bigeye houndshark Iago omanensis in the coastal waters of Oman

Female Rhizoprionodon acutus were found to mature between 62 and 74 cm total length ( L _T) whereas males matured between 63 and 71 cm L _T. The L _T at 50% maturity was 64·3 cm for females and 64·7 cm for males. Litter size varied from one to six embryos, and was positively correlated with maternal L _T. Female embryos outnumbered males by a ratio of 2·3:1. The size at birth was c . 37 cm L _T. Full‐term embryos and post‐partum females were observed during all seasons although their occurrence was highest in spring. Spermatozoa were rarely recorded in the oviducal gland, indicating that this species does not store sperm. It was not possible to generate maturity curves for Iago omanensis but it was evident that females matured by the time they reached 35 cm and males were mature by 31 cm L _T. This species displayed a clearly defined reproductive cycle with parturition occurring primarily in spring, after a gestation period of c . 1 year. Maximal embryo size was 19 cm L _T while maximal litter size was 24 embryos. The oviducal gland appeared to act as a seminal receptacle and it appeared that females may utilize these stores by not mating every year.     

Population and reproductive biology of the fiddler crab Uca thayeri Rathbun, 1900 (Crustacea: Ocypodidae) in a tropical mangrove from Northeast Brazil

Population and reproductive biology of Uca thayeri Rathbun, 1900 were studied for the first time in a tropical mangrove. Absolute density, sex ratio, population structure, handedness, breeding season and fecundity were investigated. Seven transects were delimited in a mangrove area of the Pacoti River, Northeast of Brazil (3° 43′ 02″ S/38° 32′ 35″ W). On each transect, ten 0.25 m² squares were sampled on a monthly basis during low tide periods from September 2003 to August 2004. A total of 483 crabs were obtained, of which 250 were males, 219 non-ovigerous females, and 14 ovigerous females. The U. thayeri population presented bi-modal size frequency distribution, with males and non-ovigerous females not differing significantly size-wise. Ovigerous females were larger than males and non-ovigerous females. The overall sex ratio (1:1.07) did not differ significantly from the expected 1:1 proportion. The major cheliped was the right one in 50% of the males. The observed density was of 8.5 individuals/m², with the specimens being found mostly in shaded areas. Ovigerous females were found in 5 months of the year, coinciding with the rainy season, suggesting that the population of U. thayeri presents seasonal reproductive events. Juvenile crabs were more abundant during the dry period, while larger crabs were found mainly during the rainy period. The fecundity of the studied population was much smaller than that of subtropical populations of this species. The regression analysis shows that the number of eggs increases linearly with the increase of carapace width.     

Age and growth of the round stingray Urobatis halleri at Seal Beach, California

The age and growth of the round stingray Urobatis halleri was determined using vertebral sections from animals collected at Seal Beach, California from 2002 to 2005. Annual periodicity was validated from U. halleri injected with oxytetracycline and maintained in captivity over a 2 year period ( n = 7). The coefficients estimated by the von Bertalanffy growth model were the disc width asymptote ( W _D∞) (286 mm for males and 224 mm for females) and K (0·09 year⁻¹ for males and 0·15 year⁻¹ for females). The age structure of the population consisted of mostly older, mature males and females. Age at maturity was estimated at 3·80 years for females and 3·75 years for males, and the maximum assessed age was 14 years old. Males were more numerous than females throughout the year; however, from May to September, females outnumbered males. The U. halleri age and growth coefficients were comparable to other species in the family Urolophidae. Based on the seasonality and age structure of this population, Seal Beach offers warm-water refuge for U. halleri of reproductive maturity, and the U. halleri at Seal Beach may garner some behavioural thermoregulation benefit.     

Reproductive biology of Rioraja agassizi from the coastal southwestern Atlantic ecosystem between northern Uruguay (34°S) and northern Argentina (42°S)

A total of 552 individuals of Rioraja agassizi (257 females and 295 males) were collected by bottom-trawl during research cruises. Sexual dimorphism was observed with females are heavier than males for a given total length (TL). Using logistic regression, it was determined that TL at 50% maturity of males was 475 mm TL and of females 520 mm TL. This estimation agrees with the morphological parameters measured. Although not statistically significant, a peak in reproductive activity was observed in males during late spring and summer. The monthly variation in the gonadosomatic index and oviducal gland width, together with the largest diameter of ovarian follicles, suggests that R. agassizi females have a partially defined annual reproductive cycle with two peaks, one from November (spring) to February (summer) and another in July (winter).     

Reproductive biology of the Panama graysby Cephalopholis panamensis (Teleostei: Epinephelidae)

The reproductive biology of the Panama graysby Cephalopholis panamensis was studied from collections and behavioural observations made in the Gulf of California from 2001 to 2006. Histological examinations, particularly the identification of gonads undergoing sexual transition, confirmed a protogynous hermaphroditic sexual pattern. The population structure and mating behaviour provided further support for protogyny. Size and age distributions by sex were bimodal, with males larger and older than females and sex ratios biased towards females. Mating groups consisted of a large male and several smaller females, and courtship occurred in pairs during the evening. Results on spawning periodicity and seasonality were incomplete, but histological data, monthly gonado‐somatic indices (I_G) and behavioural observations suggest that adults spawned around the full moon from May to September. Certain aspects of their reproductive biology (e.g. protogyny and low egg production) indicate that C. panamensis is particularly vulnerable to fishing and would benefit from a management policy in Mexico.     

Validated age,growth and maturity of the bonnethead Sphyrna tiburo in the western North Atlantic Ocean

The age, growth and maturity of bonnetheads Sphyrna tiburo inhabiting the estuarine and coastal waters of the western North Atlantic Ocean (WNA) from Onslow Bay, North Carolina, south to West Palm Beach, Florida, were examined. Vertebrae were collected and aged from 329 females and 217 males ranging in size from 262 to 1043 mm and 245 to 825 mm fork length, L_F, respectively. Sex‐specific von Bertalanffy growth curves were fitted to length‐at‐age data. Female von Bertalanffy parameters were L_∞ = 1036 mm L_F, k = 0·18, t₀ = ?1·64 and L₀ = 272 mm L_F. Males reached a smaller theoretical asymptotic length and had a higher growth coefficient (L_∞ = 782 mm L_F, k = 0·29, t₀ = ?1·43 and L₀ = 266 mm L_F). Maximum observed age was 17·9 years for females and 16·0 years for males. Annual deposition of growth increments was verified by marginal increment analysis and validated for age classes 2·5+ to 10·5+ years through recapture of 13 oxytetracycline‐injected specimens at liberty in the wild for 1–4 years. Length (L_F50) and age (A₅₀) at 50% maturity were 819 mm and 6·7 years for females, and 618 mm and 3·9 years for males. Both female and male S. tiburo in the WNA had a significantly higher maximum observed age, L_F50, A₅₀ and L_∞, and a significantly lower k and estimated L₀ than evident in the Gulf of Mexico (GOM). These significant differences in life‐history parameters, as well as evidence from tagging and genetic studies, suggest that S. tiburo in the WNA and GOM should be considered separate stocks.     

Reproductive periodicity of the sparid,Acanthopagrus pacificus,on a hierarchy of temporal scales

The reproductive periodicity of the sparid, Acanthopagrus pacificus, over four temporal scales is described. Acanthopagrus pacificus had a short spawning season between June and September, and within this, a peak reproductive period from July to early September. During the peak period there were several spawning peaks corresponding to a lunar periodicity, with intense reproductive activity on new and full moons that peaked during the period of the full moon when the tidal range was greatest. At the smallest temporal scale, spawning occurred at night on ebb tides. Because this study draws on data collected in 1991 and 1995, it provides a useful baseline against which to judge future changes in reproductive periodicity.     

Reproductive system of females of the Magdalena river endemic stingray Potamotrygon magdalenae: Anatomical and functional aspects

We studied anatomical and functional aspects of the reproductive system of females of the Magdalena river stingray Potamotrygon magdalenae using microscopic and macroscopic analysis of each organ. Although the reproductive tract was fully functional on both side, the left organs possibly have a greater contribution to reproductive success, because left ovary and uterus were more developed and had higher number of oocytes and embryos, respectively, than the right ones. This species has histotrophic viviparity given by the presence of uterine trophonemata and by glandular character in pregnant and postpartum females. We suggest that the epigonal organ is involved in the degradation of components of atretic follicles and the embryos begin to develop surrounded by a gelatinous tertiary envelope produced by the oviducal gland. This latter organ is composed by three zones in mature females, club, papillary, and baffle zone, as described for other elasmobranchs. From the anatomical observations, a maturity scale comprising six sexual maturity stages (Immature I, Immature II, early mature, pregnant, post‐partum, and regenerating) was established for female P. magdalenae, and it can be useful as basis for reproductive studies of other potamotrygonid species. Finally, we propose a continuous reproductive cycle for P. magdalenae. J. Morphol. 277:680–697, 2016. © 2016 Wiley Periodicals, Inc.     

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.     

Reproductive cycle of <Emphasis Type="Italic">Antedon mediterranea</Emphasis> (Crinoidea,Echinodermata): correlation between morphology and physiology

Gonads of the mediterranean crinoid Antedon mediterranea were analyzed in order to reconstruct their histological organization. The tissue arrangement resembled that previously described in other crinoids. Five reproductive stages were identified in both males and females: recovery, growing, premature, mature, spent. Sexually dimorphic characters were observed at the gonopore level. Hermaphroditic individuals were never detected. There were novel findings concerning somatic accessory cells of the gonads. The reproductive cycle periodicity was indicated by analysis of reproductive stage frequencies in the period 2003–2005: spring and winter were the seasons with highest and lowest maturity levels, respectively. A role in the regulation of reproduction was hypothesized for testosterone and 17β-estradiol, which were found to be present in A. mediterranea tissues and to vary during the reproductive cycle, thus suggesting a correlation between steroid levels and morphologically recognizable reproductive stages.