Maturity is one of the most important biological parameters used in stock assessment programmes. Indeed, the macroscopic stage of gonadal development is an essential feature in estimating the maturity ogive and spawning stock biomass. It is also useful for determining the spawning season of a species and for monitoring long-term changes in the spawning cycle as well as for many other research needs related to the biology of fish. Despite the efforts made during the last few decades to standardize maturity stage data among all the researchers, marine biologists continue without a manageable and unique maturity scale to describe the reproductive development of fish gonads. For these reasons, the objectives of this article are 1) to investigate the biological parameters of five selected key species (
La madurez es uno de los parámetros biológicos más relevantes utilizados en los programas de evaluación de stock. De hecho, la etapa macroscópica del desarrollo gonadal es una característica esencial en la estimación de la madurez de la biomasa de la ojiva y del desove. También es útil para determinar la temporada de desove de una especie y para monitorear los cambios a largo plazo en el ciclo de desove, así como para muchas otras necesidades de investigación relacionadas con la biología de los peces. A pesar de los esfuerzos realizados durante las últimas décadas para estandarizar los datos de las etapas de madurez entre todos los investigadores, los biólogos marinos continúan sin una escala de madurez única y manejable para describir el desarrollo reproductivo de las gónadas de peces. Por estas razones, el objetivo de este artículo es 1) investigar los parámetros biológicos de 5 especies clave seleccionadas (
An accurate assessment of population parameters related to fish reproduction is an essential component for an effective fisheries management (
Indeed, sustainable management and exploitation of fish resources are closely related to the stock reproductive potential concept (
The Data Collection Framework programme (DCF, EU Reg. 1543/2000, 1639/2001, 1581/2004 and 199/2008) covers a long-term monitoring of key species including extensive samplings of maturity stages of stocks within European Union waters. However, the surveys have specific technical limitations that need to be considered prior to an assessment. For example, for some target species, survey data do not always cover the spawning season of populations, the difference in coding schemes used (varying from a 4grade scale to a 10grade scale), and the interpretation of particular stages (in particular immature versus postspawning or skippedspawning) gives rise to misinterpretations that could be reflect on the assessment of the maturity ogive and the SSB. Consequently, although the current DCF establishes a high level of accuracy for determining the maturity stages, the aimed precision has not yet been achieved; thus, several stock assessments based on time-invariant maturity ogives are incomplete in covering the spatial distribution of the stocks.
In the last decade, a series of workshops organized by several international commissions for fisheries studies in the International Council for the Exploration of the Sea (ICES), North Pacific Marine Science Organization (PICES) and General Fisheries Commission for the Mediterranean (GFCM), have been conducted to address the maturity staging of species with the objective of developing common maturity scales within partners, decreasing discrepancies between laboratories and validating maturity staging through microscopic evaluation (
Most commercially targeted teleost species are iteroparous (i.e. have a multiple breading season) and may have different spawning patterns: batch spawners (which release multiple batches of eggs per breeding season) (
A series of reproductive strategies has been developed during the evolutionary history of Chondrichthyes with a progression from oviparity to viviparity. For oviparous species, the general trend is a reproduction throughout the year with one or two egg-laying peaks. Reproductive periods of viviparous species are generally well circumscribed annual cycles, with the entire population undergoing nearly synchronous mating, gestation and parturition.
In summary, reproductive timing is highly variable in marine organisms, and a comprehensive understanding of variability in reproductive timing over species, population and temporal scales is lacking.
Therefore, the objective of this article is 1) to investigate the biological parameters of five selected key species with different reproductive strategies following the macroscopic maturity scales (
Biological samplings were carried out all year round in 2015-2017 both on board commercial vessels during the MEDITS surveys and at landing points, according to the framework lines of the Common Fisheries Policy (Council Regulation EC N°199/2008 and Commission Regulation EC N°665/2008). Therefore, the commercial samplings, from both fish marker and observers on board, were performed throughout the year in order to collect biological data and store gonads of the species whose spawning period does not coincide with the MEDITS survey season (mainly from May to July).
As far as possible, data on maturity stages were collected using fresh gonad samples in order to perform appropriate histological analysis. Images were collected by researchers from different GSAs (GSAs 9, 10, 11, 16, 17, 18, 19) and involved in national and international scientific research programmes (
The macroscopic scales used in the present study are based on the female maturity scales from the MEDITS-Handbook Version n. 8 (
A photo of each gonad was taken according to an established protocol (
For each maturity stage, the following sampling biological metrics were reported: Length of specimen; total weight and sampling time. In particular, for fish (Osteichthyes and Elasmobranchii) the total length (TL) with the tail fully extended was recorded to the lowest 0.5 cm. For Crustacea, the cephalo-thoracic length (CL) at the lowest 0.1 mm was measured, while for Cephalopoda, the dorsal mantle length (ML) to the lowest 0.5 cm was obtained.
In order to confirm the assigned macroscopic maturity stages, a histological analysis was conducted following the description and terminology of oocyte stages proposed by
Protocol of the microscopic material collection
The histological protocol used by all involved laboratories for all analysed species followed
fixation in 5% buffered formaldehyde (0.1 M, pH 7.4) for a maximum period of 48 h and storage in ethanol 70%; dehydration through a progressively higher series of alcohol concentrations (70%-100%), embedding in a synthetic resin (GMA, Technovit 7100, Bio-Optica), cutting at 3.5 μm with a rotative microtome (LKB, Historange) and staining with techniques including Gill or Carazzi’s haematoxylin and alcoholic eosin or toluidine blue (to analyse the histological structure of ovaries, and oviducal glands), All sections were then observed using a Zeiss Primo Star optical microscope equipped with a Canon EOS 1100D at different magnifications (40×, 100×, 400×), edited with Adobe Photoshop CS6.
Biological parameters
All reproductive parameters were estimated for 6 GSAs (GSA 9, 10, 11, 16, 18 and 19) considering the years 2015, 2016 and 2017. The sample size for each GSA is showed in
Species | GSA | Reproductive period | Size at first maturity | ||
---|---|---|---|---|---|
Sample number | Sample size range | Sample number | Sample size range |
||
9 | 4860 | 10.0-27.0 | 4962 | 10.0-26.5 | |
10 | 19770 | 9.5-24.5 | 1149 | 11.0-26.0 | |
11 | 3735 | 10.0-25.0 | 2646 | 10.0-25 | |
16 | 5882 | 10.0-25.0 | 7129 | 9.0-25.0 | |
18 | 45275 | 10.0-27.5 | 3021 | 10.0-26.5 | |
19 | 26503 | 9.5-27.0 | 29885 | 9.5-27.0 | |
9 | 865 | 32.0-56.0 | 3704 | 32.0-56.0 | |
10 | 615 | 41.0-54.5 | 260 | 42.5-54.5 | |
11 | 670 | 39.5-54.5 | 1728 | 38.0-54.5 | |
16 | 621 | 31.0-55.0 | - | - | |
18 | 426 | 37.5-57.0 | 134 | 37.5-57.0 | |
19 | 562 | 42.0-55.5 | 562 | 42.0-55.5 | |
9 | 48 | 28.0-43.0 | 493 | 28.0-43.0 | |
10 | 43 | 33.0-44.0 | 44 | 33.0-44.0 | |
11 | 68 | 35.0-44.5 | 135 | 10.5-44.5 | |
16 | 709 | 24.5-52.5 | - | - | |
18 | 29 | 31.0-39.5 | 29 | 31.0-39.5 | |
19 | 27 | 31.5-40.5 | 32 | 31.5-40.5 | |
9 | 5513 | 19.0-66.0 | 582 | 23.0-66.0 | |
10 | 15003 | 21.0-67.0 | 1135 | 21.0-62.0 | |
11 | 11733 | 18.0-60.0 | 4715 | 18.0-60.0 | |
16 | 3298 | 21.0-59.0 | - | - | |
19 | 70084 | 19.0-65.0 | 73652 | 19.0-65.0 | |
9 | 112 | 10.5-26.0 | 418 | 10.5-21.0 | |
10 | 18 | 14.0-25.0 | - | - | |
11 | 36 | 14.5-26.5 | 516 | 14.5-26.5 | |
16 | 539 | 10.0-40.0 | 1695 | 10.0-40.0 | |
18 | 100 | 11.5-23.5 | 77 | 11.5-23.5 | |
19 | 16 | 12.0-21.5 | 12 | 12.0-21.5 |
The reproductive seasonality of the target species was inferred through an analysis of the seasonal/monthly evolution of the percentage of maturity stages of females.
Size at first maturity (SFM50= length at which 50% of the individuals are mature) was estimated by fitting maturity ogives to the proportion of mature individuals in each size class (1 cm for Osteichthyes and Elasmobranchii, 0.5 cm for Cephalopoda and 1 mm for Crustacea). The mature portion included stages 2b-4b for Osteichthyes, stages 3a-4b for Elasmobranchii, stages 2b-3b for Cephalopoda and stages 2b-2e for Crustacea. The SFM50 and the maturity range (length range between SFM75 and SFM25; MR=SFM75 - SFM25 where SFM75 and SFM25 are the length at which 75% and 25% of the individuals are mature respectively) were estimated using the following ogive model: M(L)=e(a+bL)/1+e(a+bL), where M(L) is the proportion of adult individuals (
The maturity stage changes in the gonado-somatic index (GSI) of viviparous elasmobranchs were calculated as follows GSI = (GM/ TW) × 100, where GM was the gonad mass and TW the total weight.
Both macroscopic and microscopic stage description for each chosen target species is reported as follows.
The description of the macroscale of red mullet fits well with what is reported in the MEDITS manual for Osteichthyes (
Stage | Photos | Gonad description |
---|---|---|
1 – Immature = Virgin |
|
Small pinkish and translucent ovary shorter than 1/3 of the body cavity. Eggs not visible to naked eye. |
TL 9.0 cm; TW 10 g; ST: November; GSA11 | ||
2A – Virgin developing | |
Small pinkish/reddish ovary shorter than ½ of body cavity. Eggs not visible to naked eye. |
TL 12.0 cm; TW 18 g; ST: November; GSA10-18 | ||
2B – Recovering | |
Pinkish-reddish/reddish-orange and translucent ovary about ½ length of body cavity. Blood ked eye. |
TL 16.5 cm; TW 49 g; ST: February; GSA11 | ||
2C – Maturing | |
Ovary pinkish/yellow in colour with granular appearance, about 2/3 length of the body cavity. Eggs are visible to naked eye trough the ovaric tunica, which is not yet translucent. Under light pressure eggs are not expelled. |
TL 15.5 cm; TW 43 g; ST: May; GSA10-18 | ||
3 – Mature/Spawner | |
Ovary orange/pink in colour, with conspicuous superficial blood vessels, From 2/3 to full length of the body cavity. Large transparent, ripe eggs are clearly visible and could be expelled under light pressure. In more advanced conditions, eggs escape freely. |
TL 14.4 cm; TW 31 g; ST: June; GSA19 | ||
4A – Spent | |
Reddish ovary shrunken to about ½ length of the body cavity. Flaccid ovaric walls; ovary may contain remnants of disintegrating opaque and/or translucent eggs. |
TL 15.0 cm; TW 41 g; ST: August; GSA10-18 | ||
4B – Resting | s |
Pinkish/reddish and translucent ovary. About 1/3 length of body cavity. Eggs not visible to naked eye. |
TL 17.0 cm; TW 50 g; ST: October; GSA10-18 |
The gonads modify colour with the progression of their maturation development, changing from pinkish/reddish (stages 2a and 2b named respectively virgin developing and recovering) to pinkish orange (stages 2c and 3 named respectively maturing and mature-spawner). Also the dimension switches from being 1/3 - 1/2 of the body cavity in the immature (stage 1) and developing (stage 2a) stages to being from 2/3 to full length of the body cavity in the maturing and mature stages (stages 2c and 3). Post-spawning stages (stages 4a and 4b named respectively spent and resting) are characterized by a reddish progressively shrunken ovary. The eggs are visible to the naked eye in the maturing, mature and spent stages, but they escape freely from the abdomen only in mature condition (
The histological criteria used to distinguish the reproductive stages of
Stage | Photos | Gonad description |
---|---|---|
1 – Immature=Virgin | |
Only oogonia and primary growth (PG) oocytes present. No atresia or muscle bundles. Thin ovarian wall and little space between oocytes. |
GSA11 (H&E) | ||
2A – Virgin developing | |
Cortical alveoli (CA) present. Absence of post-ovulatory follicles (POFs). |
GSA11 (H&E) | ||
2B – Recovering | |
PG and CA oocytes. Some atretic follicles may be present. Absence of POFs. |
GSA11 (H&E) | ||
2C – Maturing | |
Primary (Vtg1) and secondary (Vtg2) vitellogenic oocytes present. No evidence of POFs or tertiary vitellogenic oocytes . |
GSA11 (H&E) | ||
3 – Mature/Spawner | |
Tertiary vitellogenic oocytes (Vtg3) or POFs present. Atresia of vitellogenic and/or hydrated oocytes. GVBD, germinal vesicle breakdown and germinal vesicle migration may be present. Early stage of oocyte maturation (OM) may be present. Only Vtg3, POF and OM can be observed in total spawners. |
GSA11 (H&E) | ||
4A – Spent | |
PG oocytes dominate but some CA and/or Vtg1 and Vtg2 oocytes are present. Mass of atretic oocytes (At) and POFs present. Thick ovarian wall. Hydrated and overripe eggs may also be present. |
GSA11 (H&E) | ||
4B – Resting | |
Presence of space, interstitial tissue and capillaries around PG oocytes. Thick ovarian wall (OW) and muscle bundles. |
GSA11 (H&E) |
The end of the spawning season is indicated by the capture of numerous females in the spent stage (stage 4a). From the histological point of view this stage is characterized by abundant atresia, POFs, and few (if any) healthy Vtg2 or Vtg3 oocytes. Fish remain at this stage for a relatively short time and then move to the resting stage (stage 4b) distinguished by the presence of a lot of PG, similar to the immature stage, but with a thicker ovarian wall, the presence of more space, interstitial tissue, capillaries around PG oocytes and the presence of atretic oocytes. Fish at this stage are sexually mature but reproductively inactive. Sub-stage 2b represents specimens that have finished a reproductive cycle and are preparing to start another one. At this stage the specimens are inactive mature, the gonad has undergone development but it has taken part in the spawning in the current year. The only fish actually spawning and reproducing in the current year are those in (sub)-stages 2b, 2c, 3 and 4 (both sub-stages 4a and 4b).
In the case of
Stage | Photos | Reproductive apparatus description | |
---|---|---|---|
1 – Immature | |
Ovary is barely discernible with small isodiametric eggs. Distal part of oviducts is thick-walled and whitish. The oviducal glands are less evident. | |
TL 21.1 cm; TW 32 g; ST: March; GSA11 | |||
2 – Maturing | |
Whitish and/or few yellow maturing eggs of small-medium size are visible in the ovary (OV). The distal part of oviducts (uterus, UT) is well developed but empty. The oviducal glands (OG) are small. | |
TL 32.8 cm; TW 115 g; ST: June; GSA19 | |||
3A – Mature | |
Ovaries contain yellow eggs (large yolk eggs). The oviducal glands (OG) are enlarged and oviducts are distended. | |
TL 46.3 cm; TW 321 g; ST: March; GSA11 | |||
3B – Mature/Extruding | |
|
Ovary walls transparent. Oocytes of different sizes, white or yellow. Oviducal glands large. Egg-cases (EC) more or less formed in the oviducts (Extruding Stage). |
TL 49.2 cm; TW 402 g; ST: June; GSA19 | |||
4A – Resting | |
Ovary (OV) walls transparent. Oocytes of different sizes, white or yellow. Few large vitellogenic follicles entering atresia. Uteri (UT) appear much enlarged, collapsed and empty. The oviducal glands (OG) diameter are reducing. | |
TL 49.3 cm; TW 336.6 g; ST: August; GSA11 | |||
4B – Regenerating | |
The ovary is full of small follicles similar to stage 2. The oviducal glands and uterus are enlarged. |
|
TL 46.5 cm; TW 242.4 g; ST: July; GSA11 |
As defined in the WKMSEL2 (ICES 2013), the juvenile females can be assigned to an immature stage (stage 1) when a cut is made in the ovary and no follicles are observed inside. Generally, in this stage, a primordium of the oviducal gland, as a thickening of the uterus, can be identified in some skate species but is less distinguishable in sharks.
The maturing stage (stage 2) is characterized by the presence of ovarian follicles of small-medium size, but no large ones are present. Large yolked follicles, ready to be ovulated, can be observed only in the mature specimens (stage 3a – mature), which will be considered as mature “extruding” only when egg capsules are present (stage 3b mature-extruding). Indeed, the characteristics of the ovary in stage 3a and 3b are the same; the only difference can be found in the presence of egg capsules in 3b (
The resting stage (stage 4a) is characterized by the presence of uteri that have collapsed and reduced in size (compared with the previous stages 3a and 3b). Also, the oviducal gland appears reduced in dimension. The presence of few but large atresic follicles is the key to the assignment of this stage; in the micro sections post-ovulatory follicles (POFs) may also be visible (
Stage | Photos | Reproductive apparatus description |
---|---|---|
1 – Immature | |
Ovaries: primordial and primary follicles (PO), connected to the germinal epithelium and tunica albuginea. Uteri: composed mainly of connective tissue, covered by simple columnar epithelium with some invaginations. |
GSA11 (H&E) | ||
2 – Maturing | |
Ovaries: late-form of pre-vitellogenic follicles (PVO) of various sizes with visible lipidic drops. Oviducal glands: gland tubules beginning to form (early stage) or completely formed with secreting zones differentiated (late stage). Uteri: epithelium more invaginated and vascularized than in immatures females with some secretory cells. |
GSA11 (H&E) | ||
3A – Mature | GSA11 (H&E) |
Ovaries: follicles in all stages of development, vitellogenic follicles (VObeing) the most abundant. Post-ovulatory follicles may be present. Oviducal glands: gland tubules filled with secretions. Uteri: invaginated, longitudinal folds with secretions into the lumen. |
3B – Mature/Extruding | ||
4A – Resting | |
Ovaries: follicles in all stages. Some post-ovulatory and atretic follicles (AO), with collapsed basal lamina. |
GSA11 (H&E) | ||
4B – Regenerating | |
Ovaries: pre-vitellogenic follicles (PVO) of different sizes are present. Oviducal glands: no secretory material detected. No observations of uteri are detected. |
GSA11 (H&E) |
In the immature specimens (stage 1) the ovarian tissue consists of follicles in early pre-vitellogenesis (50-100 μm), connected to the germinal epithelium and to the tunica albuginea. The follicular epithelium surrounding the follicle is single and consists mainly of squamous cells, and lipid inclusions are visible in the cytoplasm (
In general, the macroscopic scale of the viviparous species fitted well with what is reported in the MEDITS manual, only few integrations are reported in bold in
Stage | Photos | Reproductive apparatus description | |
---|---|---|---|
1 – Immature | |
Ovaries (OV) barely visible or small, whitish; undistinguishable ovarian follicles. Oviducal gland (OG) often not visible. In some species, a thickening of the uteri where the gland will develop may be present. Uterus (UT) is thread-like and narrow. | |
TL 28.3 cm; TW 95 g; ST: January; GSA11 | |||
2 – Developing | |
Ovaries (OV) enlarged with small follicles (oocytes) of different sizes. Some larger yellow follicles may be present. Ovaries lack atretic follicles. Developing oviducal gland and uterus. (UT). | |
TL 36.0 cm; TW 227 g; ST: November; GSA11 | |||
3A – Capable to reproduce | |
Large ovaries (OV) with enlarged yolk follicles all of about the same size so that they can be easily distinguished. Oviducal gland (OG) and uterus (UT) are developed. Uterus is not dilated and does not contain yolky matter and embryos. | |
TL 36.5 cm; TW 292 g; ST: January; GSA9 | |||
3B – Early pregnancy | |
Uteri (UT) well filled and rounded with yolk content (usually candle shape). In general, segments cannot be distinguished and embryos cannot be observed. | |
TL 38.0 cm; TW 252 g; ST: November; GSA11 | |||
3C – Mid-pregnancy | |
|
Uteri (UT) well filled and rounded, often with visible segments. Embryos (E) are always visible, small and with a relatively large yolk sac (YS). |
TL 36.0 cm; TW 232 g; ST: June; GSA19 | |||
3D – Late pregnancy | |
|
Embryos (E) fully formed, yolk sacs reduced or absent. Embryos can be easily measured and sexed. |
TL 38.0 cm; TW 272 g; ST: January; GSA9 | |||
4A – Regressing | |
Ovaries (OV) shrunken without follicle development and with atretic (degenerating) follicles. The oviducal gland diameter may be decreasing. Uterus (UT) appears much enlarged, collapsed, empty and reddish. | |
TL 41.1 cm; TW 280 g; ST: November; GSA11 | |||
4B – Regenerating | |
Ovary (OV) with small follicles in different stages of development with the presence of atretic ones. Uterus (UT) enlarged with flaccid walls. Oviducal gland (OG) distinguishable but reduced in size. | |
TL 38.5 cm; TW 253 g; ST: November; GSA11 |
In
The vitellogenesis process consists in the formation of yolk drops, in the pseudo-stratification of the follicular epithelium and in an increase in the peripheral vascularization between the technical layers and the follicular epithelium (
In general, subjectivity in the macroscopic distinction between maternal stages 3c (mid pregnancy) and 3d (late pregnancy) can influence the attribution of the stage. The capability for noticing this differentiation is only acquired with species-specific experience regarding the state of the yolk sac. In case of difficulties to distinguish between these stages, taking measurements of the embryos is recommended.
It is worth noting that, in the maternal stages the uterus description is not taken into account. However, a distinction among viviparous species between those with synchronicity and those with asynchronicity of uterine and ovarian phases, respectively, should be made. In species such as
In the post-natal phase (stage 4a and 4b), the ovarian tissue appeared flaccid and contained only primary and pre-vitellogenic follicles (
Stage | Photos | Reproductive apparatus description |
---|---|---|
1 – Immature | |
Ovaries: primordial (PrO) and primary follicles, connected to the germinal epithelium and tunica albuginea. Uteri: composed mainly of connective tissue, covered by simple columnar epithelium with some invaginations. |
GSA11 (H&E) | ||
2 – Developing | |
Ovaries: primordial, primary (PO) and pre-vitellogenic (PVO) follicles of various sizes. Vitellogenic follicles may be present. Oviducal glands: gland tubules beginning to form (early stage) or completely formed with secreting zones differentiated (late stage). Secretions may be observed inside the gland tubules. Uteri: no observations available. |
GSA11 (H&E) | ||
3A – Capable of reproducing | |
Ovaries: follicles in all stages of development, vitellogenic (VO) follicles being the most abundant. Post-ovulatory follicles may be present. Oviducal glands: fully differentiated in four zones. They are filled with secretions in the tubules. Uteri: no available information. |
GSA11 (H&E) | ||
3B – Early pregnancy | |
Ovaries: primary (PO), pre-vitellogenic (PVO), some vitellogenic follicles and atretic follicles (AT) were present (early stages of pregnancy). Ovarian tissue with only primary and pre-vitellogenic follicles observed (final stage of pregnancy). Oviducal glands: secretory material decreased with the progress of pregnancy. Uteri: no available information. |
GSA11 (H&E) |
The macroscale of
Stage | Photos | Reproductive apparatus description |
---|---|---|
1 – Immature | |
Whitish or translucid ovary hardly visible in transparency. After dissection of the tegument ovary is small and lobes are flaccid, stringy and poorly developed. No spermatophores on thelycum visible. |
CL 20.3 mm; TW 4 g; ST: March; GSA11 | ||
2A – Virgin developing | |
Ivory coloured with orange pink violet dotting ovary in development. Cephalic and lateral lobes are small but distinguishable by naked eye. Abdominal extensions are thin and just visible. |
CL 24.0 mm; TW 8 g; ST: June; GSA10 | ||
2B – Recovering | |
Ivory-coloured with orange pink violet dotting ovary in re-development. Cephalic and lateral lobes are small but distinguishable by naked eye. Abdominal extensions are thin and just visible. Occasionally presence of spermatophores. |
CL 53.6 mm; TW 52 g; ST: May; GSA11 | ||
2C – Maturing or almost mature | |
Lilla-coloured ovary developed and occupies almost entirely the dorsal portion. The cephalic and lateral lobes are much developed and have a turgid consistence. |
CL 39.2 mm; TW 21 g; ST: June; GSA11 | ||
2D – Mature | |
Turgid violet ovary extends to the whole dorsal portion covering the organs below. Lobes and extensions well developed; in particular, the abdominal extensions are very evident. Oocytes well developed. |
CL 29.8 mm; TW 11 g; ST: June; GSA11 | ||
2E – Resting adult | |
Uncoloured resting ovary. Presence of spermatophores. |
CL 45.7 mm; TW 30 g; ST: September; GSA11 |
Stage | Photos | Reproductive apparatus description | |
---|---|---|---|
1 – Immature | |
Presence of oogonia and of both early and primary oocytes and occasionally late primary oocytes, scattered around the stroma with no special organization. | |
GSA19 (H&E) | |||
2A – Virgin developing | |
|
The ovarian parenchyma is now structured into a germinative zone containing oogonia and early primary oocytes (EPO). The maturative zones are organized into lobuli containing late primary oocytes (LPO). |
GSA11 (H&E) | GSA19 (H&E) | ||
2B – Recovering | |
|
The ovarian parenchyma is now structured into a germinative zone containing oogonia and early and primary oocytes. The maturative zones are organized into lobuli containing late primary oocytes (LPO). |
GSA11 (H&E) | GSA19 (TB) | ||
2C – Maturing or almost mature | |
|
Besides all the previous cell types, early (EVO) and late (LVO) vitellogenic oocytes are visible in the maturative zone. Quadrangular EVO oocytes form packet with a mosaic pattern, as they became late vitellogenic oocytes. |
GSA11 (H&E) | GSA19 (H&E) | ||
2D – Mature | |
In addition to all the previous cell types, advanced LVO may occur. In these cells, the nucleus migrates to the periphery and cortical granules appear. | |
GSA11 (H&E) | |||
2E – Resting adult | |
The ovary tissue appears empty. Residuals of fully mature oocytes can still be seen. Atretic oocytes (AO) are also present. | |
GSA11 (H&E) |
Considerable differences in the colour and shape of the ovaries are observed in
The reproductive apparatus changes from its immature condition characterized by small dimension, translucid appearance and absence of oocytes, to a full maturity status (stage 3a) through two distinct phases of developing (stage 2a) and maturing (stage2b) (
Stage | Photos | Reproductive apparatus description |
---|---|---|
1 – Immature (virgin) | |
Ovary semi-transparent, stringy and lacking granular structure (oocytes not visible to the naked eye). Small and translucent nidamental glands (NG) and oviducal gland (OG). Oviduct meander and accessory nidamental glands not visible. |
ML: 14.5 cm; TW: 90 g; ST: July; GSA11 | ||
2A – Developing | |
Whitish ovary with visible granular structure (very small oocytes), not reaching the posterior half of the mantle cavity. NG enlarged, covering some internal organs; OG and ovidicut (OVD) meander clearly visible. Accessory nidamental glands not visible. |
ML 15 cm; TW 103 g; ST: July; GSA11 | ||
2B – Maturing | |
Ovary occupies the whole posterior half of the mantle cavity, containing tightly packed oocytes (small isodiametric oocytes). Large NG covering the viscera below. OVD fully developed but empty. OG developed with a lateral brownish strip. Small accessory nidamental glands (AG) visible and lightly red pigmented. |
ML 14.6 cm; TW 83 g; ST: July; GSA11 | ||
3A – Mature | |
Ovary containing a higher percentage of large oocytes. Enlarged and turgid NG and OG (marked brownish strip). OVD full of amber-coloured oocytes (Ø >= 2 mm). Bright orange-red AG bigger than that of stage 2b. |
ML 26.2 cm; TW 442 g; ST: July GSA11 | ||
|
Appearance of the organs as above but ovary with a lower number of large oocytes and OVD just emptied or with remains of ripe oocytes. | |
ML 20.5 cm; TW 255 g; ST: July; GSA 11 | ||
3B – Spent | |
Flaccid ovary with strikingly loose disorderly aspect. Few oocytes may be attached to the central tissue. Flaccid NG, OG and AG (light pigmented). |
ML 21.1 cm; TW 251 g; ST: September; GSA11 |
As shown in
From a histological point of view (
Stage | Photos | Reproductive apparatus description |
---|---|---|
1 – Immature (virgin) | |
Oogonia and early primary oocytes (EPO) oval in shape located on the connective tissue. |
GSA11 (H&E) | ||
2A – Developing | |
EPO and late primary oocytes (LPO) surrounded by a layer of flat follicle cells. Pre-vitellogenic oocytes (PVO) with a double layer of follicular cells and in some cases the follicle forms a syncytium. |
GSA11 (H&E) | ||
2B – Maturing | |
Abundant vitellogenic oocytes (VO). The follicular epithelium active in vitellogenesis and in the formation of a chorion. PVO and LPO also present. |
GSA11 (H&E) | ||
3A – Mature | |
Abundant advanced vitellogenic oocytes (AVO) surrounded by a well-developed chorion. Follicular folds are being displaced towards to the oocyte periphery. Thick oviduct with smooth ripe oocytes (RO), ready for ovulation, inside. |
GSA11 (H&E) | ||
|
||
GSA11 (H&E) |
In general, a similar reproductive period of the species is observed between the geographic areas studied (Figs 4-8). Red mullet females showed a reproductive period from April to July with a code in early autumn in all GSAs considered. The peak of the spawning period seems to be concentrated in May-July in GSAs 9-11-18-19, whereas it appears just more extended from April to July in GSA 10 and from April to August in GSA 16 (
The reproductive season of the viviparous
The SFM50 of
Species | GSA | SFM50 | SE_SFM50 | MR | SE_MR |
---|---|---|---|---|---|
9 | 13.00 | 1.00 | 1.53 | 0.14 | |
10 | 11.59 | 0.01 | 0.63 | 0.01 | |
11 | 10.77 | 0.08 | 1.10 | 0.10 | |
16 | 12.15 | 0.29 | 1.24 | 0.02 | |
18 | 11.81 | 0.01 | 0.63 | 0.01 | |
19 | 11.17 | 0.01 | 1.19 | 0.02 | |
9 | 32.95 | 0.99 | 2.73 | 0.95 | |
10 | 34.74 | 1.07 | 1.69 | 1.29 | |
11 | 36.39 | 0.47 | 3.13 | 0.62 | |
18 | 32.29 | 0.79 | 1.14 | 0.92 | |
19 | 36.59 | 0.59 | 3.38 | 0.71 | |
9 | 41.80 | 0.99 | 1.92 | 1.26 | |
10 | 45.16 | 0.41 | 2.42 | 0.56 | |
11 | 45.31 | 0.40 | 4.93 | 0.56 | |
18 | 46.59 | 0.71 | 2.45 | 0.89 | |
19 | 45.70 | 0.19 | 2.89 | 0.25 | |
9 | 23.10 | 1.40 | 2.03 | 0.07 | |
10 | 24.15 | 0.10 | 0.33 | 0.10 | |
11 | 21.88 | 0.35 | 0.57 | 0.37 | |
18 | 24.02 | 0.16 | 0.56 | 0.19 | |
19 | 25.67 | 0.01 | 0.14 | 0.01 | |
9 | 14.87 | 1.00 | 1.06 | 0.30 | |
11 | 17.92 | 0.27 | 2.16 | 0.30 | |
16 | 15.43 | 0.29 | 0.93 | 0.02 | |
18 | 14.44 | 0.19 | 1.70 | 0.18 | |
19 | 16.27 | 0.20 | 0.62 | 0.19 |
The SFM50 of
The SFM50 of
Knowledge on sexual maturation process of a species is vital in understanding its life cycle and can play a key role in its assessment. With this information, fishery assessment scientists can provide estimates for a given species (e.g. onset of maturity by length and age), characterize the life cycle identify recruits, juveniles, adults, pregnant, etc., determine the duration of egg-laying/pregnancy/gestation periods and monitor long-term changes in the reproductive strategy (estimating fecundity, energy budget allocation and maturity-survival-longevity tradeoffs. etc.) (
Basically, the creation of a maturity scale is not easy and it is often complicated to decide how many steps should be included; this obviously depends on the use of the scale and of the aims of the research (
The standardization of maturity stage classification is fundamental when stock assessment is based on several institutes’ data. In order to estimate new maturity ogives, all institutes involved in stock assessment should use the same criteria to distinguish immature and mature specimens.
In this paper, thanks to the opportunity of having maturity gonad data collected from different countries taking part to the MEDITS programme, we tried to made an analysis of the maturity scales used inside the project for the determination of gonad maturity stages of teleostean, elasmobranch, crustacean and cephalopod females. The analysis was done taking into consideration the correspondence between key histological processes of development and corresponding modifications observed at the macroscopic level. In general, the macroscopic stage description in the different scales fitted well with what discriminated at histological level. Only a few specifics are added in the existing tables. However, as for elasmobranch species, the analysis of the ovary aspect alone is not sufficient to determine the correct maturity stage. As reported in the last ICES report (
For cephalopod species, various more or less detailed scales have been developed in relationship to the three types of female reproductive systems characteristic of octopods, squids and cuttlefish (e.g.
Generally, when maturity data are used for maturity ogive estimation, one important issue should be taken into consideration: the possible macroscopic misclassification of resting females as immature (
For the red mullet, the immature specimens are rare/lacking during the spawning period because they reach the first maturity in the first years of life (
During the regenerating phase within the reproductive cycle, only histology can be helpful for producing reliable results and not without difficulties (
On the other hand, a reduction in SFM50 may be indicative of overexploitation of stock and/or a decrease in stock reproductive potential (
The reproductive periods of key selected species, estimated through the monthly evolution of macroscopic maturity stages, are in general in agreement with those already reported in literature for the Mediterranean Sea (e.g.
The SFM50 calculated in this work, thanks to the same maturity scales per species and same procedure, show similar trends, highlighting that no difference exists among GSAs. Indeed, survey data, differently from commercial ones considered important to obtain maturity ogives of species with a protracted spawning season, have advantages because they are collected under more controlled conditions from a known design. Moreover, considering that in stock assessment models maturity ogives have no effect on the estimates of stock numbers but directly on the assessment process through the calculation of SSB, care must be taken in their calculation. Indeed, once the SSB has been calculated, assessments use it to make forecasts, set biological reference points through the stock-recruitment relationship and judge where the stock is in relation to these reference points.
In conclusion, it appears fundamental to define standardized maturity scales suitable for different systematic classes in order to highlight some specifics that are useful for calculating reproductive parameters. In fact, the accuracy of the correct maturity stage attribution could be particularly suitable in the calculation of the ogives and in the definition of any other reproductive items.
The MEDITS surveys have been carried out within the Data Collection Framework. The European Commission and Member States of the Mediterranean countries are thankfully acknowledged. We are also grateful to all the colleagues who have spent effort and time in collecting and classifying the gonads during the MEDITS surveys.