Reproductive traits and relative gonad expenditure of the sexes of the free spawning Chiton articulatus (Mollusca: Polyplacophora)

ABSTRACT

Reproductive studies of an intertidal free-spawning population of Chiton articulatus (Mollusca: Polyplacophora) from Puerto Angel, Oaxaca, Mexico were undertaken during 2011. We used gonad histology and gonadal indices to assess the relative gonad expenditure of the sexes (RGES) and other reproductive traits, accounting for individual and seasonal variation within this population. At this location, C. articulatus is gonochoric, without sexual dimorphism, except internally by gonad colour (testis is ‘salmon’ coloured and ovary olive green). Annual and monthly sex ratios (m/f) do not differ significantly from 1:1. Highest population-level gonadosomatic index (GSI) corresponded to maximum (peak) ripe stage (i.e. maximum gonad investment), with a first peak in May with a high value (8.4 ± 0.5) and a second peak during August-September with a lower value (4.7 ± 0.3). GSI fluctuated throughout year implying that gonad expenditure may be seasonally constrained, but with overall synchrony between sexes of ripe and spawning stages. July to December was the main reproductive season with some facultative spawning occurring off-season. Ripe and spawning RGES did not differ between sexes, suggesting that either sperm competition is intense and/or that sperm limitation is high. Early spawning individuals may quickly replenish their gametes for a second phase of gamete release later.

Abbreviations: RGES: relative gonad expenditure of the sexes; GSI: gonadosomatic index; GDS: gonad developmental stages; MiMI: microscopic maturity index; SST: sea-surface temperature.     

Gametogenesis and reproductive dynamics of Rhinella schneideri (Anura: Bufonidae): Influence of environmental and anthropogenic factors

This is the characterisation of the reproductive dynamics of Rhinella schneideri in an urban area during two non‐consecutive periods. Germ cells are similar to those of other anuran species, but some characteristics were more marked for R. schneideri, such as the morphological similarity of spermatogonia and oogonia, which may be related to their potential for development into both stem cell types. The presence of lampbrush chromosomes, the extensive variation in number and organisation of the nucleoli and the organisation of the nuclear cortex are also characteristic of this species. All of these features appear to work together, participating in the dynamic growth of the oocyte. In some specimens, previtellogenic oocytes were also observed in the seminiferous tubules, which may be related to anthropogenic changes induced in the study area. In the first study period, reproductive dynamics revealed synchrony between the sexes, with the preparation of the gonads from October to December and the reproductive season from October to January, coinciding with the rainy season. In the second period, reproductive synchrony was also observed, but gonad preparation occurred from February to June and the reproductive season was from August to November, before the rainy season. These changes in the reproductive cycle suggest that urbanisation affects the reproduction of this species.     

Hermaphroditism in two populations of Chiton articulatus (Mollusca: Polyplacophora) from the eastern tropical coast of México

Through histological analyses, this study reveals an unusually high incidence of hermaphroditism in Chiton articulatus. Specimens were sampled every 30?days between September 2010 and September 2011 at two locations (Las Brisas and Jaramillo beaches, Acapulco) on the tropical eastern Pacific coast of Mexico. At both sites, hermaphroditism was found throughout the year, although in varying proportions. Higher percentages of hermaphroditism were found during the pre-spawning summer months (Las Brisas Beach 63%, Jaramillo Beach 68%). Two different kinds of hermaphroditic gonads were found, showing a preponderance of either male or female tissues but, commonly, female tissues occupied the greatest part of the gonad cross sections. Similar to other species of polyplacophorans, there was a predominance of males, although M:F sex ratios ranged from 0.7 to 4.5: 1 at Las Brisas Beach and 0.3–8: 1 at Jaramillo Beach.     

Oviducal glands throughout the gonad development stages: a case study of Octopus mimus (Cephalopoda)

The oviducal glands (ODG) play a crucial role in octopus reproduction. Herein, structural changes of each section of the ODG of Octopus mimus are described histologically throughout the gonad development stages (GDS). To do this, the epithelial height, stereociliated or non-stereociliated epithelium, nucleus type (pycnotic or non-pycnotic), epithelial secretions and the value range of the macroscopic maturity index (MaMI), which directly involves ODG status, were measured. The ODG are internally constituted of two glandular units (central and peripheral glands) and one set of receptacles (the spermathecae). High epithelia (40 to 80?μm) were observed in both gland units during periods with low MaMI values (< 0.1) corresponding to III-mature and IV-pre-spawning. The stereociliated epithelium was only apparent in II-maturing and III-mature in both gland units. The nuclei were noticeably pycnotic in the central gland during III-mature, IV-pre-spawning and V-spawning, but pycnotic in the peripheral gland only during VI-depletion. The epithelium was disorganised during VI-depletion, while sulphated acid mucin was only present during III-mature in the central gland. The epithelium transformations during the GDS are related to the functions of the gland units and to their multiple secretions. The ODG histology complements the GDS and provides better reproductive status assessment.     

The chiton gill: Ultrastructure in Chiton olivaceus (Mollusca,Polyplacophora)

Gills of Chiton olivaceus, a primitive mollusc, are relatively simple in their structure and ultrastructure but are well adapted to a life in the intertidal zone. In contrast to some other molluscs, there is no differentiation of the gill epithelium into functional regions other than respiratory ones. Ciliation of the epithelium in certain areas may optimize water flow from the outer to the inner part of the mantle cavity. The hemolymph sinuses are oriented so that hemolymph flows in the opposite direction. Interstitial cells link epithelial cells with nerve endings. Muscle cells as well as the collagenous matrix in the connective tissue differ within the main gill axis and the lateral lamellae. The life cycle of immunoactive cells within the connective tissue and the hemolymph is described.     

Gonad development and size‐at‐maturity of silver therapon Leiopotherapon plumbeus (Kner 1864; Teleostei:Terapontidae) in tropical volcanic lakes in south Luzon,Philippines

Gonad development of the silver therapon Leiopotherapon plumbeus in two volcanic crater  lake  habitats (Sampaloc Lake, Taal Lake) in south Luzon, Philippines was examined during the annual reproductive cycle. The minimum body size‐at‐maturity of fish in these two lake habitats was also compared. Four gonad development stages were characterized as basis for the classification of ovarian (immature, maturing, mature, spawned) and testicular maturation (immature, maturing, mature) phases. The occurrence of all development stages in individual gonads suggest an asynchronous development whereby advanced stages are recruited continuously from a pool of younger stage germ cells to result in elevated female and male GSI throughout the annual cycle due to active gonadogenesis. Together with the increasing occurrence of advanced stage oocytes and spermatozoa from March until October, the elevated GSI of fish may indicate peak gonadal growth during the onset of the dry season (December–January) for eventual spawning from the beginning (May–June) until the end of the wet season (October–November). In both lake habitats, male fish were smaller than females but, regardless of sex, the minimum size‐at‐maturity of fish in Sampaloc Lake was significantly smaller than fish in Taal Lake. Overall, asynchronous development during oogenesis and spermatogenesis allows for year‐round reproduction of silver therapon, with elevated gonad growth in the dry season in preparation for spawning during the wet season. Compared with fish in Taal Lake, a smaller size‐at‐maturity of fish in Sampaloc Lake may be a response of the wild fishery stock to long‐term high fishing mortality and degradation of the lake habitat.     

An analysis of the reproductive pattern in the sea star Astropecten irregularis (Pennant) from the Bristol Channel

Summary

The reproductive cycle in Astropecten irregularis is described, making use of a range of statistical techniques detailed previously. Analysis of gonad weights proved more satisfactory than the use of gonad indices, as the latter are not independent of animal size. When examining the course of oogenesis, standardised residuals in an (R × C) contingency table are much easier to interpret than size/frequency polygons.

The species has an annual cycle with spawning in June or July, but the gonads are small even when the animals are gravid, and the annual cycle in gonad weights is more marked in males. Proliferation of oogonia may apparently occur at any time of year, and the ripe ovary contains many small, previtellogenic oocytes. There is an annual cycle of small magnitude in the size of the pyloric caecum, with a peak in December.     

The ontogeny of Pseudis platensis (Anura,Hylidae): Heterochrony and the effects of larval development on postmetamorphic life

Recent studies have described the giant tadpole, delayed metamorphic transformations, and absence of postmetamorphic growth of the skeleton of Pseudis Platensis. These features address questions about derived patterns of life cycles and the role of the heterochrony during the metamorphosis in anurans. Using anatomical methods, we provide new data on the development of reproductive, digestive and integument systems, and age inference obtained from ontogenetic series of Pseudis platensis. Our results indicate that at the end of metamorphosis, the adult skin is completely differentiated, including the calcified dermal layer; the testis has seminiferous tubules with spermatogonia, spermatocytes, and spermatids; ovarian sacs present previtellogenic ova; and the adult digestive tract is fully formed. The froglets differ from adults only in being unable to reproduce. The entire life cycle of P. platensis can occur in 4 years. In the first year, larval development, growth to adult size, and gonad differentiation are completed. Long larval development rather than size of the tadpoles seems to be involved in the absence of juvenile stages. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Reproductive strategy of the Patagonian catfish Hatcheria macraei

This study describes the reproductive strategy of the stream‐dwelling catfish Hatcheria macraei in the Pichileufu River, Argentina. Gonad maturity phases, classified on the basis of histological analysis, stages of gamete development and the frequency distribution of oocyte size, were correlated with macroscopic features of the gonads. Hatcheria macraei has a cystovarian ovary, asynchronous oocyte development and lobular testes. Five oocyte and four spermatogenic stages were identified and related to macroscopic gonad characteristics, making it possible to divide gonad development into five phases for females and males. Mature oocyte diameter ranged from 922 to 1935 µm. Absolute fecundity in mature females varied from 115 to 480 oocytes. Hatcheria macraei has multiple spawning during a protracted reproductive season that extends from December to April. This, together with its small size, is characteristic of an opportunistic reproductive strategy, commonly found in species that inhabit adverse and unpredictable environments, such as the low‐order rivers of Patagonia.     

Asexual and puzzling sexual reproduction of the Mediterranean sponge Haliclona fulva (Demospongiae): life cycle and cytological structures

Despite the common assumption that most Haplosclerida are viviparous sponges, this study of the reproductive cycle of Haliclona fulva demonstrates that this species is actually oviparous and gonochoric. Intriguingly, not a single male was recorded in 15 months of sampling. Oogenesis is synchronous, starting in late April and terminating in September. Asexual reproduction is represented by cyclic budding, which occurs from late November to early March. During the season of asexual reproduction, the reproductive effort represents from 0.21% to 1.49% of the parental tissue, with the highest values being recorded in winter. During the season of sexual reproduction, the female reproductive effort ranges 0.05–1.15%, with the highest effort appearing in early summer. However, no significant correlation between reproductive efforts and seawater temperature fluctuations could be detected. We describe the ultrastructural morphogenesis of the buds for the first time in this species. This process is asynchronous, with buds of variable size being attached to the maternal apical surface via a short stalk. Young buds lack any particular anatomical organization, whereas bud maturity is characterized by the development of mesohyl and by the appearance of an increasing number and volume of lacunae in the central part of each bud. At this stage, buds harbor numerous small choanocyte chambers scattered throughout the inner region, and all cell types known from the mesohyl of parental sponges: microgranular cells, granular cells, archaeocytes, endopinacocytes and exopinacocytes, central cells, and sclerocytes.     

Reproductive characteristics of pike‐characids Boulengerella cuvieri (Ctenoluciidae) in the middle Xingu River,Eastern Amazon

This study evaluated the reproductive characteristics of pike‐characids, Boulengerella cuvieri, during the hydrological cycle in the Xingu River, eastern Amazon. The sex ratio was 1:1 and the gonado‐somatic index and relative frequency of maturation stages indicate a short breeding season of single phase spawning that coincides with a filling and flood period. Mean standard length at first sexual maturity for female B. cuvieri was estimated to be 22·9 cm.     

Structure of the reproductive system of the squid Thysanoteuthis rhombus (Cephalopoda: Oegopsida)

The structure of the reproductive systems of mature males and females of the nektonic, oceanic squid Thysanoteuthis rhombus are described. The main peculiarities of the female system are relatively low capacity oviducts, set in a tight spiral, and hypertrophically developed oviducal glands with a very large second section. The male reproductive system is characterized by a long, narrow Needham's sac containing 10–15 large spermatophores 80–100 mm in length. The mesentery supporting the gonad, and protruding into it dorsally, is a characteristic feature in both sexes. The hectocotylus structure differs markedly from that in other squids and resembles that of sepiids. The reproductive system of T. rhombus possesses primitive features (pattern of gonad attachment and hectocotylus) but mostly secondary characters (small oviducts, very large oviducal glands and ovary). The complex morpho-ecological adaptations of T. rhombus are reflected in the distinctive features of the reproductive system.     

Seasonal changes of progesterone and testosterone concentrations throughout gonad maturation stages of the Mexican octopus,Octopus maya (Octopodidae: Octopus)

Variations in progesterone (P₄) and testosterone (T) levels in the gonad of Octopus maya from Sisal in Yucatan State, Mexico, were investigated by radioimmunoassays and in relation to four gonad maturation stages (GMS) and to the reproductive cycle, as represented by two maturity indices (microscopic ‘MiMI’ and macroscopic ‘MaMI’). According to the GMS and the maturity indices, the reproductive season of O. maya from Yucatan occurred from February to June. In females, P₄ and T displayed the same pattern, with a tendency to increase at the same time, although on average, P₄ had seven-fold higher concentrations than T. In contrast, P₄ and T in male gonads displayed a different pattern, where T concentrations were relatively stable throughout all of the study months. In the female gonad P₄ was lowest (close to 0 pg?g^–1) during both developing (GMS-I) and maturing (GMS-II) stages, and increased (189?±?53?pg?g^–1) approaching the mature stage (GMS-III) to a maximum value of 611?pg?g^–1. Concentrations of T in the male gonad were lowest (106?±?9?pg?g^–1) during the maturing stage (GMS-II) and increased up to the mature stage (GMS-III), reaching a maximum of 440?pg?g^–1. Pearson's correlation (r) between hormones and maturity indices showed strong relationships for females (around 0.4 and ?0.7; p?<?0.05), but there were negligible or weak relationships for males (0.2 and ?0.1; p?>?0.05). Hormone correlations in females were inverse with MaMI and direct with MiMI. Our major findings showed that gonadal P₄ levels were elevated during GMS-III and GMS-IV (i.e. periods of vitellogenic oocytes), where the characteristic aspect is an ovary with very high oocyte diameters, with the primary follicle cells deeply infolded in the ooplasm for yolk synthesis. These results suggested a synchrony between P₄ and the process of folliculogenesis, and in turn, vitellogenesis.     

Variability in egg-to-adult development time in the bee Ptilothrix plumata and its parasitoids

1. Ptilothrix plumata (Hymenoptera) is a neotropical solitary bee that nests in bare, sandy soils. Data on the biology and behaviour of this species are provided. Egg‐to‐adult development time of a neotropical solitary bee and its parasitoids is quantified for the first time. 2. The bee showed huge variability in egg‐to‐adult development time. There are two categories of eggs relative to adult emergence. The same season eggs are those from which adults emerge in the same reproductive season in which the eggs were laid. Adults from next season eggs emerge in the next dry reproductive season. This variability in egg‐to‐adult development time is reached through prepupal diapause. The bee larval parasitoids Leucospis genalis (Hymenoptera) and Anthrax sp. (Diptera) showed similar range in their development times. The data show that diapause is controlled by season. 3. By synchronising adult emergence, this variability in egg‐to‐adult development time facilitates mate finding, and population recruitment is a consequence of the bees avoiding the unfavourable reproductive season.     

Annual reproductive activity of Caiman crocodilus fuscus in captivity

We describe the gonadal and abdominal fat storage cycles for a population of Caiman crocodilus fuscus kept in captivity at a breeding farm. The reproductive cycles of males and females are clearly seasonal. Vitellogenic follicles were observed in females year‐round; however, the follicular growth that produces the preovulatory follicles for the breeding season occurs in November–May (most of the dry season to the beginning of the rainy season). These months correspond with the presence of physiologically reproductive males. Oviposition takes place during the wet season (April–August) and the births occur at the end of this season (September–November). Fat storage was not related to reproductive activity, and did not vary by month or between sexes. Although environmental and hormonal conditions have been improved for these captive animals, they maintain a strongly seasonal reproductive cycle, historically fixed to oviposit in the most favorable period for nest construction and hatching during the rainy season. Zoo Biol 22:121–133, 2003. © 2003 Wiley‐Liss, Inc.     

Reproductive characteristics of Spondyliosoma cantharus (Linnaeus, 1758) in the Gulf of Tunis

The reproductive features of Spondyliosoma cantharus were studied in the Gulf of Tunis to contribute to better fisheries management on a regional scale and to broaden knowledge on whether there are actual performance differences compared to others areas. A total of 369 fish were caught by trammel and gill nets in the Gulf of Tunis from January 2005 to June 2006. Sex‐ratio, gonad maturation, size and age at maturity, sexual cycle, condition and reproductive strategy were determined. The male : female ratio was initially skewed in favour of females, with males predominating in larger sizes. Length of females at first maturity was 17.8 cm TL (n = 141), which corresponds to 4 years of age. A recommendation is made to increase the length at capture. Spawning season extends from January to May, with a peak in March–April correlated to the lowest sea surface temperatures (14.8–15.6°C); during this period, a dichromatism arises between males and females. The hepatosomatic index and the condition factor present significant monthly changes in relation to the breeding activity. The bimodal size frequency distribution, the biased sex ratio, and the presence of bisexual gonads outline a protogynous hermaphroditism; diandry should be confirmed.     

Reproductive cycle of the commercially harvested sea urchin (Paracentrotus lividus) along the western coast of Portugal

Harvested populations of the sea urchin (Paracentrotus lividus) from the northwestern (Carreço) and southwestern (Aljezur) coasts of Portugal were surveyed to describe the species reproductive cycle and assess possible relationships with geographical location and seawater temperature. Individuals were sampled monthly to analyze gonad histology, mean gonadal index (GI), and gonadosomatic index (GSI) during 2 consecutive years (November 2010–November 2012). Both populations presented an annual reproductive cycle, with synchronous gonad maturation and gamete release between sexes. Gonad maturation occurred throughout autumn–winter, followed by a single but prolonged spawning season during spring–summer. The duration of the spawning season displayed a latitudinal gradient likely related to the north–south increasing trend in seawater temperature, with the northwestern population (Carreço) exhibiting a shorter spawning period compared to the southwestern population (Aljezur). The timing and duration of the spawning season was compared with several populations throughout the distributional range of P. lividus in the Atlantic Ocean and Mediterranean Sea. In the population from Carreço, the size at first sexual maturity (test diameter = 35.9 mm) was considerably smaller than the minimum conservation reference size (MCRS) of 50 mm test diameter legally established for P. lividus. This study confirms that sustainable exploitation depends on harvesters’ awareness of and compliance with the MCRS and provides useful information for the eventual establishment of a closed season in the harvesting of P. lividus.     

Reproductive Stage of the Life Cycle in the Rhizocephalan Barnacle Polyascus polygenea (Crustacea: Cirripedia)

The specific features of the reproductive stage of the life cycle have been studied in the rhizocephalan barnacle Polyascus polygenea, a parasite of the coastal crab Hemigrapsus sanguineus. It is shown that a single crab can bear 1 to 8 externae of P. polygenea. The fecundity of the parasite depends on the size of the externae and their number on the host and may reach as much as 50000 eggs for one externa. In Peter the Great Bay, Sea of Japan, this species repeatedly reproduces during the entire spring–autumn period; externae with developing embryos in the mantle cavity occur from May to September, and planktonic larvae occur from June to October. One externa produces during the season of reproduction no less than three generations of larvae. Thus, the reproductive strategy in P. polygenea comprises a three-stage cascade of reproduction: asexual reproduction via budding of the interna; the development of several generations of one or several externae; and several reproduction cycles of each externa. This allows the parasite to produce a very great number of larvae and ensures the parasitization of a significant proportion of the host crab population. The structure of the ovaries and oogenesis in rhizocephalans and free-living cirripede barnacles have many common features, which provides evidence for integration of these two groups within one monophyletic taxon.     

Various methods to determine the gonadal development and spawning season of the purplish Washington clam, Saxidomus purpuratus (Sowerby)

The monthly variation in reproductive cycle, condition factor (fatness), gonad index (GI), ovarian egg diameter and biochemical composition [RNA, DNA content and their ratio RNA/DNA (R/D)] were compared to determine the spawning season of the purplish Washington clam, Saxidomus purpuratus, collected from the west sea of Taean, Korea. All these factors were correlated to the spawning season from May to October. Monthly variation and concentration of the R/D ratio especially represented indicative information about the processes of gonad development and spawning patterns. The increases in R/D ratio in the ovaries corresponded with increases in ovarian egg diameters and the GI during the spawning season. The peak of R/D and RNA content in females was a good indicator of sexual maturation and the DNA content in males. During winter between November and January, the value of fatness, GI, egg size, RNA and DNA content were lower than in other seasons, indicating depletion of energy reserves and lower metabolic demands because of colder temperatures.