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International Journal of Morphology

versión On-line ISSN 0717-9502

Int. J. Morphol. vol.35 no.1 Temuco mar. 2017

http://dx.doi.org/10.4067/S0717-95022017000100011 

Int. J. Morphol., 35(1):56-61, 2017.

 

Gonadal Development of Peprilus medius (Peters, 1869) (Perciformes: Stromateidae) from Southeast of the Gulf of California, Mexico

 

Desarrollo Gonádico de Peprilus medius (Peters, 1869) (Perciformes: Stromateidae) del Sureste del Golfo de California, México

 

Maria de los Angeles Maldonado-Amparo1,3;Rebeca Sánchez-Cárdenas2; Luis Antonio Salcido-Guevara3 & Jorge Saúl Ramírez-Pérez1

1 Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa. Paseo Claussen s/n, Col. Los Pinos, C.P. 82000, Mazatlán, Sinaloa, México.

2 CONACyT - FACIMAR, UAS, México.

3 Master student.

Correspondence to:


SUMMARY: The gonadal development assessment is a fundamental work in researching the reproduction of Peprilus medius, on the way to understand its population dynamics and to achieve a sustainable management of its fisheries. The diagnosis based on morphochromatic features is the quicker, more practical and cheaper method, and properly validated, it may be an accurate procedure. This is particularly useful in researches when it is required to provide prompt and accurate information to support decision-making for fisheries management, and during long-term fisheries monitoring to detect changes in reproductive patterns due to environmental anomalies. These are issues of concern in P. medius and other fishery resources. In this context, a scale that describes the gonadal development through morphochromatic and histological features is presented, and plus anatomical observations of the reproductive organs. Ovarian development was characterized through six phases: immature, development (sub-phases: early and late), mature, spawning (sub-phases: partial and partial post-spawning), post-spawning and resting. Testicular development was described through five phases: immature, development, ejaculation, ejaculated and resting. The position and shape of the reproductive organs are apparently defined by the shape of the fish and the visceral cavity. P. medius's gonads show a gonadal lobe at lower position and an upper lobe in the visceral cavity, and both lobes presented a horizontal placement from gonopore toward the back of the fish. In addition, gonadal deformities occurrence due to deformities in the visceral cavity was evidenced. We recommend to use presented descriptions as a guide in gonadal assessment.

KEY WORDS: Ovaries; Testes; Gametogenesis; Reproductive anatomy.


RESUMEN: La evaluación del desarrollo gonádico es una labor fundamental para investigar la reproducción de Peprilus medius, en vías a comprender la dinámica de sus poblaciones y lograr un manejo sustentable de sus pesquerías. El diagnóstico a partir de características morfocromáticas es el método más rápido, práctico y barato, y adecuadamente validado puede ser un procedimiento preciso. Este es particularmente útil en investigaciones cuando se requiere aportar información rápida y precisa que apoye la toma de decisiones de manejo pesquero, y durante los monitoreos pesqueros de largo plazo, que permiten detectar cambios en los patrones reproductivos debido a anomalías ambientales. Estos son temas preocupantes en P. medius y otros recursos pesqueros. En ese contexto se presenta una escala que describe el desarrollo gonádico a través de características morfocromáticas e histológicas, y además se presentan observaciones anatómicas de los órganos reproductores. El desarrollo ovárico fue caracterizado a través de seis fases: inmadura, desarrollo (subfases: inicial y avanzado), maduro, desove (subfases: parcial y postdesove parcial), postdesove y reposo. El desarrollo testicular fue descrito a través de cinco fases: inmadura, desarrollo, eyaculación y reposo. La posición y forma de los órganos reproductores están aparentemente definidos por la forma del pez y su cavidad visceral. Las gónadas de P. medius muestran un lóbulo gonádico en posición inferior y uno superior en la cavidad visceral, y ambos lóbulos presentan una colocación horizontal desde el gonoporo hacia la parte posterior del pez. Además se evidencia la ocurrencia de deformidades en las gónadas debido a deformidades en la cavidad visceral. Recomendamos utilizar las descripciones presentadas como una guía en la evaluación de las gónadas.

PALABRAS CLAVE: Ovarios; Testículos; Gametogénesis; Anatomía reproductiva.


 

INTRODUCTION

Peprilus medius (Peters, 1869) is a fish of Stromateidae family that inhabits in the neritic-pelagic zone from the Gulf of California to northern of Chile, and Galapagos Islands (Chirichigno & Velez, 1998; Tobón-López et al., 2008; Palacios-Salgado et al., 2012). Accurate knowledge about morphology and development of reproductive organs of P. medius has not been published, but there is some information about other stromatids. Such as, Peprilus triacanthus's ovaries were described as symmetric and paralleled organs, fused at the posterior portion, having triangular-circular cross-sectional form and localized completely in the visceral cavity (Kobelkowsky, 2012). The ovaries of Pampus argenteus and Stromateus stellatus present an asynchronous development, which is consistent with partial spawning mode (Dadzie et al., 2000; Almatar et al., 2004; Lone et al., 2008; Carocca & Chong, 2010). The development of ovaries of Peprilus burti was briefly described by eight morphochromatic phases: immature, maturing virgin, early developing/resting, late developing I, late developing II, gravid, ripe and spawning/spent (Murphy & Chittenden, 1991). Latter, Pampus argenteus's ovaries development was described by seven morphochromatic phases: virgin, developing, maduring, ripening, spawning or running, partially spawned, spend and resting (Almatar et al.; Lone et al.).

P. medius is socially and economically important in several coastal communities along its geographic distribution, because it is a target species in the coastal fishery for human consumption, to make fish meal and to use it as bait (Inga-Barreto et al., 2008; Prado, 2010). As with many other species, there is a growing concern to study and to monitor systematically its populations to get biological information to make fishery decisions. Particularly, because P. medius could change its reproductive behavior due to strong environmental changes (Kameya et al., 2001; King & McFarlane, 2003 & Tam et al., 2008). In this context, this contribution describes phases of gonadal development of P. medius defined by morphochromatic and histological traits, and some additional anatomical findings, as a guideline for accurate identifying gonad maturation status in an easy, cheap and quick manner. This is particularly useful for extensive fishery monitoring.

MATERIAL AND METHOD

A weekly sampling of ten P. medius specimens was made through artisanal fishery from Mazatlan, Mexico, during September 2014 to November 2015. Fishes were weighed (Wt) and dissected to observe and remove the reproductive organs. Each gonad was photographed and its size, texture, weight (Wg), color, form and position in visceral cavity were registered. Gonadosomatic index (GSI) was calculated as Wg/(Wt ­ Wg) and expressed as a percentage (Devlaming et al., 1982). The RGB color values were defined using color tool of Paint application (Windows 2010 version) from photographs of gonads and making manual adjustments.

Gonads were fixed in 10 % formalin, and then cross-sectional sections were dehydrated, cleared and paraffin-embedded, and 5 mm-thick sections were obtained and stained through hematoxylin-eosin technique, using dewaxing with soap (Humason, 1979; Buesa & Peshkov, 2009).

Gonads phases firstly were described according with their morphochromatic features (including average RGB color values) and GSI, followed by the histological diagnosis. The gonadal phase was determined based on gametes stages (types, organization and more advanced stage of gamete), structure of wall and gonadal stroma, and the presence of elements as post-ovulatory follicles and atresia, following Wallace & Selman (1981), Lone et al., and Núñez & Duponchelle (2008).

RESULTS

The ovaries and testes of P. medius are formed by two elongated lobes, and usually one lobe is wider, being most evident when the organ is mature. The gonad is contained and has to develop in a cavity with a horizontal narrow space and a larger vertical space. The cavity wall is not flexible and the gonopore is approximately under the middle cavity space. The gonadal lobes are horizontally positioned since the gonopore (gonoduct connection) to posterior area of visceral cavity, and the narrower lobe is lying on the ventral side (lower lobe) of the cavity and the wider is up (upper lobe) (Fig. 1). The gonads may present the lower lobe deformed (very small) due to a cavity deformity (Fig. 1).

Six ovarian development phases were described: immature, development, mature, spawning, post-spawning and resting (Table I; Fig. 2). During ovarian development and subsequent phases more than two oocytes stages were observed simultaneously. The oocyte release was in batches following two patterns: frequently it is a continuous release (just released a batch is preparing to release the next, and it was called partial spawning); but a few times (34.8 %) is a release with pauses (post-ovulatory follicles are almost reabsorbed and the next batch is in diapause, and it was called partial post-spawning). These spawning patterns were observed only by histological diagnosis, and also the difference between immature and resting phases.

Five testicular development phases were described: immature, development, ejaculation, ejaculated and resting (Table II; Fig. 3). The testes presented continuous spermatogenesis and simultaneous spermatozoa release during ejaculation phase, and near the end of spawning, the spermatogenesis was gradually reduced.

Fig. 1. Gonads position in Peprilus medius and a deformed ovary.
AA, anterior area; WL, wider lobe; NL, narrower lobe; PA, posterior area.

Table I. Scale of ovarian developmental phases of
Peprilus medius from southeast of Gulf of California.

Fig. 2. Ovarian developmental phases and sub-phases of Peprilus medius: A, immature; B, early developing (sub-phase); C, late developing (sub-phase); D, mature; E, spawning (E1, partial spawning sub-phase; E2, partial post-spawning sub-phase); G, post-spawning; H, resting. Tissular and cellular structures in ovaries: NC, nuclear chromatin; P, perinucleolar; CA, cortical alveolus; Vt1, early vitellogenesis; Vt2, late vitellogenesis; MN, migrating-nucleus; POF, Post-ovulatory follicle; POF-L, late post-ovulatory follicle; AT, atresia; TR, tissue in reabsorption. The bars's scale is 100 µm (-) and 1 cm ( ). Hematoxylin-eosin technique.

Tabla II. Scale of testicular developmental phases of
Peprilus medius from southeast of Gulf of California.

Fig. 3. Testicular developmental phases of Peprilus medius: A, immature;
B, development; C, ejaculation; D, ejaculated; E, resting. Tissular and cellular
structures in testes: SG, spermatogonia; SPC, spermatocyte; SPD, spermatid;
SPZ, spermatozoa; TL, spermatogenic tubule lumen; CT, connective tissue.

DISCUSSION

The form and position of gonads are related with body form of P. medius, as in other fishes (McMillan, 2007). P. medius's laterally-compressed body and its narrow and in flexible visceral cavity propitiate the position of gonadal lobes (one down and one up) and define the wider shape of the upper lobe, and if the cavity is deformed, the organ takes the form. The gonads deformities can affect fishes fecundity (Wootton & Smith, 2015), thus is very important that deformities do not occur in high proportion. The orientation of gonadal lobes from gonopore to posterior area of visceral cavity, is an adaptation that could be advantageous to minimize water pressure on gonads during swimming. This could permit that P. medius maintains displacement during spawning season taking care the gonads and let it spawn at different places.

P. medius's ovaries present asynchronous development, characterized by simultaneous presence of more than two oocyte stages during oogenesis according to Marza (1938). Females can spawn at least three times during spawning days period, evidencing that P. medius is batch partial spawner. This spawning pattern have been described for Pampus argenteus and Stromateus stellatus (Dadzie et al.; Almatar et al.; Lone et al.; Carocca & Chong), also members of Stromateidae.

The external morphochromatic features of gonads are related with cellular and tissular changes in organs due to gametogenesis, similar to general gonadal development described to other fishes by authors like Lowerre-Barbieri et al. (2011), Brown-Peterson et al. (2011) and Wallace & Selman. Thus, the gonadal development phases can be identified by morphochromatic features, except spawning's sub-phases and the difference between ovarian immature and resting phases, that can be only note by histological diagnosis. Therefore, the presented gonadal development scales gives possibility to define most developmental phases only with morphochromatic features, this being a desirable attribute of scales because phases definition is quick and cheap (Lowerre-Barbieri et al.). This also makes it feasible to use the scales in extensive works, like fishery monitoring.

P. medius's gonadal developmental scales incorporate additional traits, for example, vascularization, turgor, IGS values and RGB color values, for easier phase definition. Other stromatids's scales do not include these features, as Pampus argenteus's scale (Lone et al.).

ACKNOWLEDGEMENTS

The authors thank the support from projects: PROFAPI-2014/165, PROFAPI-2014/199,231525-Infraestructura-CONACYT-2014 and 2137-Cátedras CONACYT.Maldonado-Amparo is grateful the support from CONACyT fellowship programme (scholarship 634525). Sánchez-Cárdenas thanks the support from Cátedras CONACyT programme. Also we thank to anonymous reviewers, because their suggestions to this manuscript and to Mel Rudeen for English language revision.

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Corresponding author:

Rebeca Sánchez-Cárdenas

CONACyT - FACIMAR, UAS
MEXICO

Email: rsanchez@uas.edu.mx

Received: 17-10-2016
Accepted: 23-12-2016

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