Reproductive cycle and gonadal development of the Atlantic sea urchin Arbacia punctulata in the Gulf of Mexico: changes in nutritive phagocytes in relation to gametogenesis

ABSTRACT

The annual reproductive cycle comprises steady gametogenic activities that synchronize gonadal maturation and spawning rhythms, which are important for aquatic organisms including marine echinoderms (Echinodermata, Echinoidea). In this study, we report the annual reproductive cycle, gonadal development, and changes in nutritive phagocytes (NPs, which accumulate nutrients in germ cells) in relation to gametogenesis of the Atlantic sea urchin (Arbacia punctulata, an edible echinoid) in the Gulf of Mexico. Monthly changes in gonadal development and maturation were observed morphologically and histologically. We calculated gonadosomatic index (GSI) and compared the stages of gonadal development in order to determine the NPs index, and characteristics of germ cells (eggs and sperm) during the annual reproductive cycle. According to GSI and histological analyses, gametogenic activities were classified into four stages of both sexes: mature (June–August), spent (September–November), recovery (December–March), and growing (April–May). The GSI values in both sexes were high during summer months. In males, testicular lobules were densely packed with sperm from June to August. In females, however, mature eggs first appeared in some ovaries in May, numerically increased from June to July, and decreased in August. During gametogenesis, on the other hand, NPs in both testes and ovaries were depleted from June to August. Collectively, our results suggest that the Atlantic sea urchin spawns during summer months in the Gulf of Mexico. This is the first report, to the best of our knowledge, on gonadal development and changes in NPs during the annual reproductive cycle of any Arbacia species in the Gulf of Mexico.     

Length‐weight relationships of four sharks caught in the Northern Persian Gulf and Oman Sea

The length–weight relationships (LWRs) for four little‐known shark species collected in the Persian Gulf and Oman Sea from March 2014 to September 2015 are presented, namely: Carcharhinus dussumieri, Carcharhinus macloti, Chiloscyllium arabicum, and Chaenogaleus macrostoma.     

Coral reproduction in the world��s warmest reefs: southern Persian Gulf (Dubai, United Arab Emirates)

Despite extensive research on coral reproduction from numerous geographic locations, there remains limited knowledge within the Persian Gulf. Given that corals in the Persian Gulf exist in one of the most stressful environments for reef corals, with annual variations in sea surface temperature (SST) of 12°C and maximum summer mean SSTs of 36°C, understanding coral reproductive biology in the Gulf may provide clues as to how corals may cope with global warming. In this study, we examined six locally common coral species on two shallow reef sites in Dubai, United Arab Emirates (UAE), in 2008 and 2009 to investigate the patterns of reproduction, in particular the timing and synchrony of spawning. In total, 71% colonies in April 2008 and 63% colonies in April 2009 contained mature oocytes. However, the presence of mature gametes in May indicated that spawning was potentially split between April and May in all species. These results demonstrate that coral reproduction patterns within this region are highly seasonal and that multi-species spawning synchrony is highly probable. Acropora downingi, Cyphastrea microphthalma and Platygyra daedalea were all hermaphroditic broadcast spawners with a single annual gametogenic cycle. Furthermore, fecundity and mature oocyte sizes were comparable to those in other regions. We conclude that the reproductive biology of corals in the southern Persian Gulf is similar to other regions, indicating that these species have adapted to the extreme environmental conditions in the southern Persian Gulf.     

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.     

The reproductive cycle of Norway lobster

The reproductive biology of female Norway lobster Nephrops norvegicus was studied throughout an annual cycle from January to December 2007 in Pagasitikos Gulf, a large semi-enclosed Gulf in the central west Aegean Sea, in Greece. Six ovarian maturation stages were described to follow gonadal development, based on the combined external observation and histological examination of the ovary. Reproduction showed clear seasonality both in terms of ovarian maturation and brooding period. The proportion of fully mature females in the catch increased from January to the summer months with a peak in June. The species has a protracted brooding period that peaks in November and December, while the release of eggs from females' pleopods occurs from January to March. The size at which 50% of females reached sexual maturity was estimated, using a logistic model, to be 28.1 mm of carapace length. The undiscovered reproductive dynamics will be valuable for optimizing population models and management strategies for this important fishery resource.     

Endocrine and morphological correlates of reproduction in the draughtboard shark Cephaloscyllium laticeps (Elasmobranchii: Scyliorhinidae)

This study examined the endocrine and reproductive correlates of reproduction in 636 female and 468 male draughtboard sharks (Cephaloscyllium laticeps) captured from southeastern Australia. Females were oviparous and displayed a single external-type ovary with a maximum follicle diameter of 35 mm. Vitellogenesis commenced at a follicle diameter of 10 mm. Females showed a constant overlap between follicular recruitment, ovarian growth, and egg laying. The male reproductive tract consisted of paired testes with spermatocysts undergoing diametric development. Plasma levels of the presumptive gonadal steroids, testosterone (T), 17beta-estradiol (E2), progesterone (P4), and 11-ketotestosterone (11-KT; males only) were correlated with morphological developmental stages of the gonads. In females, E2 increased as the follicle developed before declining as the follicle reached maturity. T remained low during the first stages of ovarian growth and increased as the follicle reached maturity. P4 showed a peak just before ovulation. In males, T was the only hormone that varied with maturity, increasing in adults; E2 and P4 were present at low plasma concentrations in males and did not change with stage of gonadal development. 11-KT was undetectable at all times. Endocrine changes in draughtboard sharks were consistent with hormonal correlates reported for other species and suggest roles for E2( in females) and T (in both sexes) in gametogenesis and P4 in maturational events in females.     

Observations on the female reproductive cycles of captive Asian yellow pond turtles (Mauremys mutica) with radiography and ultrasonography

The annual reproductive cycle of 27 female Mauremys mutica was observed by radiography and ultrasonography from April 2006 to August 2007. Radiography was used to monitor clutch size and ultrasonography was used to monitor changes in the ovarian follicles. The follicles started to enlarge in September and became preovulatory in January. The mean maximum follicle diameter of ovulation was 18.30±1.44 mm, and ovulation occurred from March through August. Eggs were laid between April and August. Turtles entered latent period in early August and the maximum follicular size was at a low of 13.22±2.36 mm in late September. The vitellogenesis of the next reproductive cycle began in October. The 24 adult females laid 56 clutches containing a total of 227 eggs. Average clutch size was 4.05 eggs (range 1–8) and there were 2.33 clutches (range 1–4) per female. Egg shell images were first observed on the sixth or seventh day after ovulation. The oviductal period averaged 6.9 weeks (range 2–16 weeks) on the first clutch, 3.4 weeks (range 2–8 weeks) on the second, and 2.75 weeks (range 2–6 weeks) for the third. Radiography and ultrasonography are non‐invasive and convenient methods to evaluate the reproductive cycle of female M. mutica. They should be applicable to other turtles and should greatly enhance knowledge of reproductive physiology. Zoo Biol 29:50–58, 2010. © 2009 Wiley‐Liss, Inc.     

Reproductive cycle and maternal–embryonic nutritional relationship of shovelnose guitarfish Pseudobatos productus in the Gulf of California

Samples of the shovelnose guitarfish Pseudobatos productus were collected on board a vessel and at landings of artisanal commercial fisheries in the Gulf of California from May 2004 to June 2007. Samples of 650 females, 2047 embryos and 484 uterine eggs were examined. The reproductive cycle is annual, ovulation and parturition occur in July, the uterine eggs are in diapause for 9 months (July–March) before an accelerated growth of embryos of 3 months. Histological analyses of the uterine wall of pregnant females suggested that no secretions were used for embryo nourishment. The standard percentage of water content was 48·6% in fertilized eggs and 80·75% in full‐term embryos. Dry mass loss during embryonic development was 16·3% and the chemical balance of development was 0·84. This indicates that P. productus is a strictly lecithotrophic, viviparous species, that makes no maternal contribution of nutrients during embryonic development.     

Reproductive pattern of the freshwater prawn Pseudopalaemon bouvieri (Crustacea,Palaemonidae) from hypo-osmotic shallow lakes of Corrientes (Argentina)

Pseudopalaemon bouvieri undergoes complete abbreviated development. The reproductive cycle (proportion and size of the sexually mature population and juvenile recruitment), fecundity and egg size of this prawn were examined in three subtropical shallow lakes. The reproductive cycle was seasonal; gonadal maturation occurred during the winter, ovigerous females were abundant in the spring and breeding occurred at the end of spring. Females produced small numbers of eggs (9–55) of relatively large sizes (1.0–2.1 mm). The proportion of ovigerous females with respect to the total number of females, the fecundity and egg size differed among the lakes according to the trophic state of the environments. Pseudopalaemon bouvieri has a reproductive strategy similar to other Palaemonidae species that inhabit nutrient-poor inland waters.     

Morphology of the female reproductive system and reproductive cycle of the mangrove land crab Ucides cordatus (L.) in the Baía de Antonina,Paraná, Brazil

Ucides cordatus is a species of considerable ecological and socioeconomic importance. The goal of this study is to contribute to the understanding of the reproduction biology of this species by describing the macroscopic anatomy, the histology of the female reproductive system and the reproductive cycle of U. cordatus. A total of 367 females were obtained from October of 2002 to March of 2005 during monthly collections in the Baía de Antonina, Paraná, Brazil. Specimens were submitted to necropsy and their reproductive systems (ovary and spermathecae) were analysed histologically. Permanent slides were stained with Harris' hematoxylin and eosin, Mallory's trichromic and the periodic acid‐Schiff reaction. Ovarian analysis allowed for the determination of five developmental stages based on the prevalence of oocytes in different phases of vitellogenesis. During stage V, when ovaries recover from spawning, the presence of oocytes in advanced stages of vitellogenesis was detected, suggesting that there could be more than one spawning in a single reproductive period. Females in stage IV were most common in the spring (November through February), whereas females with their egg mass exposed were most frequent from November through March. The reproductive period of U. cordatus in mangroves of the study region occurred from October to March. The reproductive events observed in the present study suggest that spermatophores acquired during copulation, which takes place during the ‘andada’, are only used in the reproductive period of the following year.     

Reproductive biology of Galaxias maculatus (Jenyns 1842) in the Río Ovando,a high‐latitude environment in southernmost Patagonia,Argentina

This study establishes the reproductive cycle, batch fecundity and oocyte diameter of a diadromic population of the puyen, Galaxias maculatus, in the Río Ovando, Tierra del Fuego, (54°S), at the southernmost limit of its distribution. Given the short ‘favourable season’ in relation to other populations of the species (in terms of temperature, photoperiod and food availability), the study also explores the trade‐offs between feeding and oocyte production and between phases of growth and reproduction. The reproductive cycle was analyzed by the monthly evolution of the proportion of gonadal maturity stages (determined from microscopic examination of the gonads). Oocytes were measured using a micrometric ocular scale and classified by diameter and morphological characteristics; absolute fecundity was established as the total number of hydrated oocytes per ovary. The studied population exhibits a repetitive spawning strategy, given the coexistence of post‐ovullatory follicles and hydrated oocytes in histological sections and the presence in ripe ovaries of an intermediate cohort of yolked oocytes ready for hydration. Individual fecundity is lower (1422 ± 422 oocytes/ovary) than in other puyen populations, but the egg production increases through individual repetitive spawnings during the protracted spawning period (from October to February). Females attain larger sizes than those of other South American populations (the largest female reaching 115 mm total length), maximizing its potential fecundity. The present paper contributes to the knowledge of the variability of reproductive traits of G. maculatus in relation to diadromic populations, given that the bulk of information in South America refers to landlocked populations.     

Nutrient allocation in the gonads of the sea urchin Arbacia dufresnii in different stages of gonadal development

This study reports nutrient allocation in different stages of gonadal development for two populations of the sea urchin Arbacia dufresnii off the Patagonian coast of Argentina (Nuevo Gulf and San Jorge Gulf). The biochemical composition of gonads was used to assess nutrient allocation by measuring ash, soluble protein, lipid and trichloroacetic acid-soluble carbohydrate concentrations, and absolute contents over a 24-month period. Reproductive output in terms of energy was calculated for females. Results were correlated with histological stage of the gonads. Soluble proteins were the main component for the Nuevo Gulf population while unmeasured organic material (i.e. insoluble proteins and nucleic acids, especially in testes) was prevalent in gonads from San Jorge Gulf. Soluble protein and lipid concentrations followed the gonadal cycle, while carbohydrate concentration was almost negligible, especially in the Nuevo Gulf population. The different patterns in the gonadal cycle in the two populations were reflected in the biochemical composition of gonads. Concentrations and contents of the biochemical components and reproductive output were higher in the population from San Jorge Gulf owing to the larger size of gonads and gametes. These findings contribute to the better understanding of the plasticity of the reproductive biology of A. dufresnii in different environments.     

Reproductive biology of Philodryas patagoniensis (Snakes: Dipsadidae) in south Brazil: male reproductive cycle

The male reproductive cycle of Philodryas patagoniensis in south Brazil was described through morpho‐anatomical and histological analysis of individuals deposited in zoological collections. Spermatogenesis occurred during late autumn–winter (June–September) and spermiogenesis occurred in spring–summer (October–March). The volume of the testes was smaller (quiescent) in winter, while the tubular diameter and the epithelial height of the seminiferous tubule were larger in summer (January–March). The ductus deferens presented spermatozoa all over the year and had no seasonal variation in diameter. The length of the kidney was larger in winter–spring (July–December), although the tubular diameter and epithelium height of the sexual segment of the kidney (SSK) were larger only in winter (July–September). Total testicular regression was observed in late autumn (May), simultaneously with the peak in SSK. Therefore, at the individual level, males exhibit a discontinuous cyclical reproduction. Considering the population level, the reproductive cycle is seasonal semisynchronous, with most of the individuals showing a reproductive peak in spring–summer (October–March). Here, we present evidence to support the importance of the microscopic approach to reproductive cycle studies. Finally, we discuss the intrinsic and extrinsic factors influencing P. patagoniensis reproductive patterns.     

Reproductive biology of the fanray, <Emphasis Type="Italic">Platyrhina sinensis</Emphasis> (Batoidea: Platyrhinidae) in Ariake Bay,Japan

The reproductive biology of the fanray, Platyrhina sinensis, was examined in Ariake Bay, Japan, from May 2002 until December 2006. Females reached sexual maturity at a larger size than males [total length (TL) at 50% sexual maturity: male, 393 mm; female, 421 mm]. The present data support a distinct annual reproductive cycle for P. sinensis. The gonadosomatic index (GSI) for mature males showed a clear seasonal trend, declining from August to November. Histological observations showed that mature sperm in the testes occurred from August to November when monthly GSI declined. Concomitantly, pre-ovulatory ova were observed in females collected from August to November. These data indicate that mating, ovulation and fertilization occurred from August to November. Near-term embryos, neonates and recent post-partum females also occurred from August to November. Additionally, all post-partum females possessed large pre-ovulatory ova. Parturition occurred from August to November followed immediately by mating, ovulation and fertilization. Mature females become pregnant every year, and the gestation period is almost 1 year. Fertilized uterine eggs without macroscopic embryonic development were present throughout the annual reproductive cycle, indicating that P. sinensis utilizes embryonic diapause as its reproductive strategy. Both reproductive tracts of females were functional, and fecundity ranged from 1 to 12 with a mean of 6.0, increasing with TL.     

Role of brain hormone in oogenesis of the Indian freshwater leech,Poecilobdella viridis (Blanchard) during the annual reproductive cycle

The possible role of a brain hormone in oogenesis of Poecilobdella viridis has been investigated by brain extirpation and brain extract injections during non-reproductive (November to January) and reproductive (March to May) periods. Brain extirpation during the non-reproductive period ceased maturation of the ovary. It is inferred that brain secretion bears possibly a gonadotropic principle which governs and regulates the oogenesis during the annual reproductive cycle.     

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.     

Bilateral enucleation and captivity influence the reproductive cycle of male Viscacha (Lagostomus maximus maximus)

The viscacha (Lagostomus maximus maximus) is a seasonal rodent living in the Southern Hemisphere. The adult males exhibit an annual reproductive cycle characterized by a gonadal regression period during winter. In this study, we investigated the effects of bilateral enucleation and captivity on their annual reproductive cycle. Testicular volume relative to body weight was recorded monthly in intact and bilaterally enucleated animals placed under natural photoperiod, water, and food ad lib. and constant temperature. Testes and accessory organs were evaluated by qualitative and quantitative light microscopic studies. The intact animals showed an annual reproductive cycle with complete gonadal atrophy in the first year. In the second year, testicular regression was observed but attenuated in regard to that recorded in the first winter period, indicating that adaptive changes might be involved. Bilateral enucleation in the viscacha dampened and extended the period of its annual reproductive cycle. The results suggest that both conditions, constant captivity and enucleation, produced stimulatory effects on the reproductive system of this rodent. Furthermore, local control mechanisms might be responsible for the morphological differences observed in testes, epididymis, and seminal vesicles from both groups, which exhibited similar levels of serum testosterone. Finally, an intact retinohypothalamic-pineal axis and/or photoperiodic input would be necessary to maintain the reproductive cycle amplitude and timing in viscacha.     

Reproductive cycle by histological characterization of the ovary in the butterfly goodeid Ameca splendens from the upper Río Ameca Basin, Mexico

The ovarian cycle was studied in Ameca splendens, a viviparous fish native to western Mexico. Two wild populations living in environments with differential conditions (a small pond adjacent to a reservoir and a spring) were examined to determine whether the conditions these populations are exposed to can elicit differences in the reproductive cycle. The two sites differ from each other with respect to several environmental factors: the spring has clear, oxygen‐rich water while the pond has higher levels of conductivity, hardness and inorganic nitrogen. Six stages of gonadal maturation were identified in A. splendens, based on histological and macroscopic characteristics of the gonad. The relative frequency of gonadic stages at both sites showed two reproductive peaks during the year: from March to May and from September to November. Histologically, ovaries exhibit an asynchronous development in both populations, revealing the existence of a multiple reproductive cycle. Relative mean condition shows organisms are in peak condition (K > 1) at age class 1+ as they recruit to reproduction; K was <1 following the onset of multiple reproduction. The Fulton condition factor shows that the mean condition is slightly higher in the spring population. The relative frequency of gonadal maturation differed between the study sites and is indicative of the plasticity of A. splendens in facing different conditions within the environments it inhabits.