Biol. Bull. 216: 94-102. (February 2009)
© 2009 Marine Biological Laboratory
Gonad Development During the Early Life of Octopus maya (Mollusca: Cephalopoda)
Omar Hernando Avila-Poveda1,*,
Rafael Francisco Colin-Flores2 and
Carlos Rosas3
1 Posgrado en Ciencias del Mar y Limnología (ICMyL), Universidad Nacional Autónoma de México (UNAM), Puerto de abrigo S/N, Sisal, Yucatán, Mexico
2 Departamento de Patología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán (UADY), Mérida, Yucatán, Mexico
3 Unidad Multidisciplinaria de Docencia e Investigación (UMDI) Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), Puerto de abrigo S/N, Sisal, Yucatán, Mexico
* To whom correspondence should be addressed. E-mail: oavila{at}colombia.com
 |
Abstract
|
|---|
Abstract. Gonad development during the early life of Octopus maya is described in terms of histological, morphometric, oocytes growth, and somatic-oocyte relationship data obtained from octopus cultured at the UMDI-UNAM, in Sisal, Yucatan, Mexico. This study is the first publication on gonad development during the early life of Octopus maya. A total of 83 O. maya specimens were used; their sizes ranged from 6.5 to 76 mm of total length (TL), 4 to 28 mm of dorsal mantle length (DML), 2.5 to 20 mm of ventral mantle length (VML), and 0.0180 to 7.2940 g of fixed body weight (fBW). Animals were weighed and measured only after preservation. A loss of 10% of living weight was estimated for juvenile octopuses after formalin preservation. The relation of length to weight (VML, DML, TL/fBW) pooled for both sexes had a strong positive correlation (r), as shown by a potential power function that was quite close to 1. Compound images were produced from numerous microscopic fields. The histological examination revealed that, 4 months after hatching, male octopus (24.5 mm DML and 7.2940 g fBW) were in gonad stages 2 (maturing) to 3 (mature), with spermatogonia and spermatocytes in the tubule wall and abundant spermatids and spermatozoa in the central lumen of the seminiferous tubules, suggesting the occurrence of different phases of gonad development at different maturity stages. In contrast, females (22.5 mm DML and 4.8210 g fBW) at the same time since hatching were immature (stage 1), with many oogonia, few oocytes, and germinal epithelium. This suggests that males reach maturity earlier than females, indicating a probable onset of maturity for males at around 4 months of culture or 8 g of wet body weight. Our results indicate the possibility that the size-at-weight can be recognized early with a degree of certainty that allows the sexes to be separated for culture purposes; but more detailed studies on reproduction in relation to endocrinology and nutrition are needed.
Abbreviations: BW, wet body weight • fBW, fixed body weight • DML, dorsal mantle length • TL, total length • VML, ventral mantle length
|
Introduction
|
|---|
Octopus maya (Voss and Solis-Ramírez) is an endemic species from the Yucatan peninsula (Voss and Solis-Ramírez, 1966). It is one of the most important commercially exploited species in Mexican fisheries and has the largest annual catch—about 16 000 tonnes in 2004 (Salas et al., 2006). During the last several decades, this species has been studied from a variety of perspectives, such as behavioral physiology (Segawa and Hanlon, 1988), biochemistry (Fong et al., 1988; Hanlon et al., 1989; Lee, 1992), bioeconomics (Cabrera and Defeo, 2001), culture (Van Heukelem, 1976, 1977, 1983), ecological modeling (Arreguín-Sanchez, 2000), embryonic development (Cazares-Simental, 2006), feeding and feeding physiology (DeRusha et al., 1989; Caamal-Monsreal, 2006; Aguila, 2007; Aguila et al., 2007; Domingues et al., 2007; Rosas et al., 2007a, 2008), fishery (Castro-Suaste et al., 2000; Salas et al., 2006), growth (Nepita-Villanueva and Defeo, 2001), maturation (Santos-Valencia and del Rio, 2006), pathology (Hanlon et al., 1984; Reimschuessel and Stoskopf, 1990), population dynamics (Arreguín-Sanchez et al., 2000; INP-SAGARPA, 2007), juvenile physiology (Rosas et al., 2007b), systematics (Perez-Losada et al., 2002), tissue morphology (Boletzky, 1975; Fermin et al., 1985; Kier and Smith, 1990, 2002), toxicology (Adams et al., 1988), and disease treatment (Forsythe et al., 1990).
However, these studies have focused predominantly on the subadult and adult stages, which are most available for capture, and some reproductive features have been determined. Until now, the only morphometric and sexual data were for specimens with a wet body weight (BW) greater than 300 g (Caamal-Monsreal, 2006; Santos-Valencia and del Rio, 2006; Romero-Soberanis, 2007). In contrast, the reproductive characteristics have not been described for organisms between the hatchling and subadult stages (i.e., early life history), in essence because early-stage juveniles have not yet been found in nature.
O. maya exhibits onset of sexual maturity at about 400 g BW in females and at 300 g BW in males, that is, when displaying an enlargement of the oviductal gland or of the Needham's sac, respectively (Santos-Valencia and Re-Regis, 2003). Nevertheless, Romero-Soberanis (2007) collected and maintained individually O. maya females of about 250 g BW, which laid fertilized eggs. Likewise, one O. maya wild female of 200 g BW was reared and later laid unfertilized eggs (Avila-Poveda and Caamal-Mosreal, PCMyL-UNAM, unpubl. data). Van Heukelem (1983) defined the probable onset of maturity in males as the time when the presence of a hectocotylus (copulating arm) was observed, at an age of 4 months after hatching, when the smallest octopus weighed 10 g BW and the largest weighed 53 g of BW. Similarly, two O. maya wild males of 30 g BW and 40 g BW were observed with hectocotyli (Avila-Poveda, pers. obs.). These maturation processes in females and males could make it possible to distinguish immature and mature octopuses, as well as to determine the life-history stage. Unfortunately, since these first stages have never been defined for cephalopods in general, uncertainty exists regarding the "true" onset of sexual maturity.
Sexual maturity is an imprecise term when used with octopuses (Van Heukelem, 1983). Many cephalopods reach sexual maturity only near the end of their lives (during logarithmic growth) and can be called juveniles from hatchling almost until death (Boyle, 1983, 1987). However, for other cephalopods, such as O. maya, a slower phase of the growth curve (exponential growth) could mark the onset of sexual maturity and the step from juvenile to subadult stages (Van Heukelem, 1976, 1983). Moltschaniwskyj (2004) refers to sexual maturity in cephalopods as that affecting growth processes to produce exponential growth, probably in association with the energetic demand of reproduction. Budelmann et al. (1997) point out that the microscopic anatomy of the reproductive system of cephalopods undergoes a variety of changes during juvenile and subadult development, which result in diverse conditions that show group-specific anatomical features that can be generalized in regard to gonadal development.
The aim of this investigation is to provide, for the first time, information on histological changes of the gonad during the early life history of O. maya. We obtained this information from organisms in culture, from hatching and through the juvenile stages. Studies of the histological changes in the gonad during growth and maturation enabled us to elucidate reproductive aspects in order to (a) understand the life cycles of this commercially exploited species; (b) recognize size-weight relationships in an attempt to separate the sexes at the beginning of the life cycle (Van Heukelem, 1976); (c) put forward a hypothesis to elucidate whether sexual maturity is a process that begins early in this species—that is, at the start of the exponential growth—in relation to previous evidence of maturation obtained in O. maya; and (d) distinguish growth sequences or "life-history stages" based on a consistent terminology: juvenile, subadult, and adult.
|
Materials and Methods
|
|---|
Octopuses were obtained from eggs spawned by one wild female acclimated to the maturation area in a culture system at UMDI-UNAM, in Sisal, Yucatan, Mexico. Eggs were artificially incubated at 25 ± 1 °C in a UV-sterilized seawater flow-through system. Embryonic development took 50 days at this temperature. Approximately 1000 embryos hatched alive, and about 10% of them were used in this study. O. maya hatchlings were maintained in a 500-l rectangular black tank (1.40 x 0.70 x 0.50 m), with controlled temperature at 25 ± 2 °C, practical salinity at 36, dissolved oxygen higher than 5 mg l-1, pH above 8, and photoperiod of 12:12 (light/dark). The octopuses were individually placed in a PVC 2-in T-type unit coupled to mesh caps. Each octopus was provided with a clean gastropod conch (Melongena corona bispinosa) as a shelter. Tanks were connected to a recirculation seawater system, coupled to skimmers and sand filters. Throughout the culture period, octopuses were fed twice a day (0900 and 1700 h) with crabmeat (Callinectes spp.) at between 7% and 10% dry weight of octopus per day (Van Heukelem, 1983; Aguila et al., 2007; Domingues et al., 2007).
Animals were sampled every 3 weeks for 4 months, from hatchlings to juveniles. Whole animals were fixed alive in 10% neutral formalin saline solution in seawater for 12 to 15 days and preserved in 70% ethanol with 0.1% glycerin until histological processing (Roper and Sweeney, 1983). All collected animals were weighed and measured only after preservation.
To estimate the weight lost after preservation, a group of octopuses similar to that used in this study was weighed before and after the preservation procedure. A 10% loss of living weight was estimated for juvenile octopuses after ethanol preservation. Total fixed body weight (fBW ± 0.0001 g), total length (TL ± 0.5 mm), dorsal mantle length (DML ± 0.5 mm), and ventral mantle length (VML ± 0.5 mm) were measured according to Roper and Voss (1983). A total of 100 octopuses were individually maintained to be sampled during the study. The 83 octopuses sampled at the end of the study were always in a healthy condition. These specimens were between 6.5 and 76 mm TL, 4 and 28 mm DML, 2.5 and 20 mm VML, and 0.0180 and 7.2940 g fBW.
Octopuses were cut in half along the total length (TL) in sagittal (dorsoventral orientation) and frontal (lateral orientation) planes (Fig. 1). Each half was washed in 50% alcohol (1-h baths with four changes), dehydrated in 96% alcohol (1-h baths with four changes), cleared in warm xylene at 60 °C (15-min baths with three changes), and impregnated in paraffin Paraplast with a 56 °C melting point (30-min baths with two changes). Serial sections of 5 µm were cut with a manual rotary microtome (LEICA RM 2125) and mounted on glass slides with gelatin. Harris's hematoxylin and eosin, regressive method, was used for staining (Luna, 1968). The photomicrographs were captured with a DS-5M-L1 Digital Sight camera system mounted on a Nikon Eclipse ME-600 microscope, and stored in a computer in graphic format.
View larger version (41K):
[in this window]
[in a new window]
|
Figure 1. Diagram illustrating the location and orientation of the cutting planes. (A) Lateral orientation to permit the cutting of frontal sections. (B) Dorsoventral orientation to permit the cutting of sagittal sections.
|
|
The length-weight relations pooled for both sexes are described. In addition, compound images, mainly in the sagittal plane, were produced with numerous microscopic fields (100x) to show the main features. Adobe Photoshop CS2, ver. 9.0, was used for photographic assembly.
Oocytes (female) and spermatogonia (male) were measured at magnifications of 20x, 100x, 400x, and 600x, using the same digital system. The phases and stages of gonadal development were classified using Roman numerals (i.e., Phase I) and Arabic numerals (1: Immature, 2: Maturing, 3: Mature, 4: Spawning) for both sexes. We used the microscopic stages proposed by Khallahi (2001), Rodriguez-Rua et al. (2005), and Idrissi et al. (2006) for Octopus vulgaris and by Laptikhovsky and Arkhipkin (2001) for squid Loligo gahi; and the macroscopic stages proposed by Santos-Valencia and Re-Regis (2003) for Octopus maya.
|
Results
|
|---|
Length-weight relations
The relationship between the lengths (VML, DML, TL) and fixed body weight (fBW), pooled for both sexes during the ontogenetic range studied (0.0180–7.2940 g fBW), showed a strong positive correlation (r = 0.98, 0.99, and 0.98, respectively) as demonstrated by the potential power function (Y = aXb). The slope of the length-weight regressions indicated an isometric growth for VML (b = 3.3361) and DML (b = 3.2722), whereas a smaller power coefficient (b = 2.6791) was revealed for TL, indicating an allometric growth (Fig. 2).
View larger version (25K):
[in this window]
[in a new window]
|
Figure 2. Relationships between lengths (TL, DML, VML) and fixed body weight (fBW) pooled for both sexes of Octopus maya during the periods of early development studied (6.5–76 mm TL or 4–28 mm DML or 2.5–20 mm VML, and 0.0180–7.2940 g fBW). Continuous lines indicate power function trend.
|
|
Gonad development
The octopus ovary is nearly round, but shape and absolute size vary depending on the number and diameter of oocytes enclosed (Figs. 3, 4, 5). Two phases and one stage of ovary development were found in our female samples.
View larger version (67K):
[in this window]
[in a new window]
|
Figure 3. Compound digital image in sagittal plane of an Octopus maya female in culture for 60 days after hatching (27 mm TL, 10 mm DML, 7 mm VML, and 0.4120 g fBW). a, arm; as, anterior salivary gland; b, brain; bm, buccal mass; bh, branchial heart; c, cecum; cr, crop; da, digestive gland appendage; dg, digestive gland; f, funnel; i, intestine; is, ink sac; m, mantle; mc, mantle cavity; oe, esophagus; ov, ovary; ps, posterior salivary gland; ra, renal appendage; st, stomach; su, suckers; sy, statocyst; wb, white body.
|
|
View larger version (151K):
[in this window]
[in a new window]
|
Figure 4. Compound digital image in sagittal plane of the gonad of an Octopus maya female in culture for 45 days after hatching (18 mm TL, 8.5 mm DML, 5.5 mm VML, and 0.1750 g fBW). bh, branchial heart; c, cecum; o, oocyte; og, oogonia; ra, renal appendage.
|
|
View larger version (167K):
[in this window]
[in a new window]
|
Figure 5. Compound digital image in sagittal plane of the gonad of an Octopus maya female in culture for 60 days after hatching (27 mm TL, 10 mm DML, 7 mm VML, and 0.4120 g fBW). bh, branchial heart; c, cecum; ge, germinal epithelium; m, mantle muscle; o, oocyte.
|
|
In general, females about 8.5–22.5 mm DML were immature (stage 1), with oocyte diameter varying from 15 to 90 µm (Fig. 6). The spherical nuclei increased from 10 to 41 µm. The nuclei possessed one or two nucleoli of 2–12 µm. Females of about 8.5-mm DML showed the ovary to be in phase I with a large production of oogonia, indicating a proliferative mitosis of the germinal epithelium or pre-meiosis of oocytes; and they also produced the first oocytes of 23 ± 12 µm in the long axis with a nucleus of 11 ± 1 µm (Fig. 4). From 10 mm up to 22.5 mm DML, the ovary was in phase II (oocytogenesis), characterized by a scarce germinal epithelium, without oogonia, but with a greater production of oocytes (Figs. 5, 7) that varied from 30 to 90 µm in diameter (Fig. 6).
View larger version (173K):
[in this window]
[in a new window]
|
Figure 7. Section in sagittal plane of the gonad of an Octopus maya female in culture for 126 days after hatching (55 mm TL, 22.5 mm DML, 15.5 mm VML, and 4.8210 g fBW). c, cecum; ge, germinal epithelium; mc, mantle cavity; o, oocyte.
|
|
The octopus testis consists of several seminiferous tubules, elongated in the frontal section and semicircular in the sagittal section (Fig. 8). Several phases of gonad development and different maturity stages were observed in males. Early in the life cycle of the cultured octopuses it was possible to observe immature stage (1), maturing stage (2), and mature stage (3). The process of spermatogenesis in its three phases (spermatocytogenesis, spermatidogenesis, and spermiogenesis) was clearly observed as well. Males smaller than 21-mm DML were in phase 0 with a large production of spermatogonia, revealing clearly the immature stage (1)—that is, only spermatogonia of 3.4 ± 0.5 µm in diameter (Fig. 9) located in the seminiferous tubule (Fig. 10). From 24.5 mm DML on, the maturing (2) and mature (3) stages had already begun, characterized by some empty spaces among cells. Also phases I, II, and III of spermatogenesis had begun, characterized by showing all types of cells: spermatogonia of 3.9 ± 0.5 µm in diameter (Fig. 9) were adjacent to the inner tubule wall; spermatocytes were circular in appearance and denser, but smaller than spermatogonia and located among the spermatogonia and central lumen; spermatids were easily identifiable by the elongated shape of their core, which was very dense; spermatozoa were provided with one flagellum and localized in the central lumen (Fig. 11).
View larger version (136K):
[in this window]
[in a new window]
|
Figure 8. Compound digital image in sagittal plane of the gonad of an Octopus maya male in culture for 126 days after hatching (52 mm TL, 21 mm DML, 15 mm VML, and 3.5660 g fBW). bh, branchial heart; c, cecum; m, mantle; mc, mantle cavity; ra, renal appendage.
|
|
View larger version (152K):
[in this window]
[in a new window]
|
Figure 10. Section in frontal plane of the immature-stage gonad of an Octopus maya male in culture for 126 days after hatching (52 mm TL, 21 mm DML, 15 mm VML, and 3.5660 g fBW) showing seminiferous tubules filled with spermatogonia.
|
|
View larger version (164K):
[in this window]
[in a new window]
|
Figure 11. Section in sagittal plane of the mature-stage gonad of an Octopus maya male in culture for 126 days after hatching (76 mm TL, 24.5 mm DML, 18 mm VML, and 7.2940 g fBW) showing seminiferous tubules with all types of cells. s, spermatozoa; sc, spermatocytes; sd, spermatids, sg, spermatogonia; tw, seminiferous tubule wall.
|
|
Previous histological examinations indicated that males reach the mature stage earlier than females, and that the change from immature to maturing stages in the male occurs over a narrow range of 21–24.5 mm DML (52–76 mm TL). Thus, it would be possible to designate a probable onset of maturity for males in culture at around 4 months after hatching, at a DML between 21 and 24.5 mm or a fBW of 7 g.
|
Discussion
|
|---|
The present study reports for the first time a length-weight relationship in the early life history of Octopus maya (4–28 mm DML). Length-weight relationship obtained for TL had a slope lower than 3, while the slopes for DML and VML were markedly higher than 3. These results demonstrate that, in this species, during the first days after hatching, the increment in total length (TL) is mainly due to growth of the arms rather than of the mantle, suggesting that hatchlings change morphologically at the beginning of the life cycle. Similar growths for both sexes have been reported in other octopuses, such as Octopus vulgaris (BW = 0.0007 x VML3.0960, Hernandez-Garcia et al., 2002) and Octopus bimaculoides (BW = 0.00046 x DML2.94, Forsythe and Hanlon, 1988). Positive allometric arm growth is a characteristic of octopuses with direct egg development that live 12 months or less (Okutani, 1990), and of the paralarval and juvenile stages of small-egg octopus species with planktonic hatchings (Villanueva and Norman, 2008).
Early change in the relative allometric growth of the arms is an adaptation common to benthic-hatching octopuses, especially in early life, and evolved in response to the need to make a shift in prey selection (Boyle and Rodhouse, 2005). However, the values of the power equation coefficient (3.3361 for VML and 3.2722 for DML) indicate that the mantle of Octopus maya grows in a direct relationsip with development and physiological adjustment of the internal organs (Rosas et al., 2007b).
A newly hatched individual of O. maya externally resembles the adult in many aspects. Internally, the organ systems are present (Fig. 3), and morphological differentiation—including that of the gonad (Peterson, 1959; Fioroni and Sundermann, 1983)—is quite well advanced (Budelmann et al., 1997). In the early life history of O. maya the internal and gross structural anatomy of the male and female gonads resemble those of the subadult and adult stages of several cephalopods (Peterson, 1959; Budelmann et al., 1997). However, the proportions of several organs and structures differ from those of the adult.
The beginning of sexual maturity is a critical event because it triggers physiological processes. It has been said that maturation in octopus is a long process of development and gonadal growth—at least in females, due to yolk accumulation (Buckley, 1977; Gnap, 1987; Boyle and Chevis, 1992; Young, 1992). In the present study, females of O. maya showed an early meiotic maturity, beginning at about 8.5-mm DML, just when an intense proliferation of germinal cells and the first morphological differentiation from oogonia to oocytes were observed in the ovary. This agrees with the process of oocyte growth and gonadal maturation in Eledone cirrhosa (Gnap, 1987; Boyle and Chevis, 1992; Young, 1992) and in Octopus vulgaris (Buckley, 1977). From this point, the oocytes grow until vitellogenesis is reached (Gnap, 1987; Young, 1992); but this process appears to be associated with somatic growth (Boyle and Rodhouse, 2005); for this reason, ovulation, followed by only one spawning period, generally coincides with the moment at which females have reached their maximum size.
In contrast with the females, the males of O. maya showed a precocious maturity, suggesting that they remain in reproductive condition for a prolonged time; consequently, they have the potential to transfer their gametes more than once during their lifetime. This agrees in general with observations made in other cephalopods (Voight, 2001, 2002), such as Eledone cirrhosa, Octopus vulgaris (Gimenez-Bonafe et al., 2002), Octopus dofleini martini (current name Enteroctopus dofleini, Mann et al., 1970), Octopus mimus (Olivares et al., 2003), and Sepia officinalis (Hanlon et al., 1999). Unfortunately, the testicular function and spermatic viability of precocious octopuses of different sizes have not been studied (Olivares et al., 1996).
Morphologically, Van Heukelem (1983) designated the probable onset of maturity for the male of O. maya when he noticed the presence of a hectocotylus (copulating arm) in animals at an age of 4 months after hatching, when the smallest octopus weighed 10 g BW and the largest weighed 53 g of BW. Similarly, we observed males of around 8.0 g of wet weight (24.5 mm DML) that had hectocotyli and were sexually mature (Fig. 11). Similarly, two O. maya wild males of 30 g BW and 40 g BW were observed with hectocotyli (Avila-Poveda, pers. obs.).
On the basis of our results, it was evident that males passed from immature to sexual maturity very fast, suggesting that O. maya males have a very short subadult stage, which could explain the precociousness of this species.
The onset of sexual maturity in Octopus is determined by a secretion released into the bloodstream by the optic glands (Wells, 1959, 1960; Wells and Wells, 1972). Recently, vertebrate-type steroids have been identified in several species of molluscs (Lafont and Mathieu, 2007), and especially testosterone, progesterone, and estradiol-17b are considered to function in the control of Octopus reproduction (D'Aniello et al., 1996; Di Cosmo et al., 2001, 2002).
Several researchers have pointed out the relationship between age, reproduction, maturity, somatic tissue, and resource availability (Pollero and Iribarne, 1988; Gabr et al., 1999a, b; Moltschaniwskyj and Semmens, 2000; Rosa et al., 2004, 2005). It seems that for sexual maturation and egg production, octopus, cuttlefish, and squid use energy directly from food, rather than from stored products (Gabr et al., 1999a, b; Moltschaniwskyj and Semmens, 2000; Rosa et al., 2005; Otero et al., 2007). In this context, Boyle and Knobloch (1984a, b) suggested that culture conditions could increase gonad growth in small-sized animals exposed to high temperatures, low food supply, or conditions where growth rates are low, because animals in such conditions are forced into maturity when they reach the "reproductive age," regardless of size. Although we do not know whether the culture conditions we used for O. maya hatchlings forced the octopuses to reduce their reproductive age, we think that animals fed twice a day with crab can express their maximum growth rate (6% per day) and, in consequence, show their "normal" reproductive characteristics. Our results thus indicate the possibility of determining the sex of octopuses early (at 8 g of wet body weight), allowing the sexes to be separated for culture purposes.
|
Acknowledgments
|
|---|
This work is part of the Ph.D. thesis of O.H. Avila-Poveda. Thanks are given to CONACYT for doctoral scholarship No. 207833/207137 to O.H. Avila-Poveda. The present study was partially financed by DGAPA-UNAM project No. IN216006-3 and SAGARPA-CONACYT 2005-11720. Thanks are due to the Pathology Department, Veterinary Medicine and Zootecnics School, Yucatan University (UADY-FMVZ) for the use of their histopathology laboratory for histological processing of samples. We appreciate the technical assistance of Raquel Miranda Soberanis (UADY-FMVZ) during the histological processes, and the technical assistance of Claudia Caamal-Monsreal (UMDI-SISAL) and Richard Mena-Loria (UMDI-SISAL) during maintenance of octopuses.
|
Footnotes
|
|---|
Received 19 June 2008; accepted 1 October 2008.
|
Literature Cited
|
|---|
Adams, P. M., R. T. Hanlon, and J. W. Forsythe. 1988. Toxic exposure to ethylene dibromide and mercuric chloride: effects on laboratory-reared octopuses. Neurotoxicol. Teratol. 10:519–523.[Web of Science][Medline]
Aguila, J. 2007. Bases nutricionales para el cultivo del pulpo Octopus maya (Mollusca: Cephalopoda, Voss y Solis, 1966). M.Sc. thesis. Instituto de Ciencias del Mar y Limnologia, UNAM. Distrito Federal, Mexico.
Aguila, J., G. Cuzon, C. Pascual, P. M. Domingues, G. Gaxiola, A. Sánchez, T. Maldonado, and C. Rosas. 2007. The effects of fish hydrolysate (CPSP) level on Octopus maya (Voss and Solis) diet: digestive enzyme activity, blood metabolites, and energy balance. Aquaculture 273:641–655.[Web of Science]
Arreguín-Sánchez, F. 2000. Octopus-red grouper interaction in the exploited ecosystem of the northern continental shelf of Yucatan, Mexico. Ecol. Model. 129:119–129.[Web of Science]
Arreguín-Sánchez, F., M. J. Solís, and M. E. González De La Rosa. 2000. Population dynamics and stock assessment for Octopus maya (Cephalopoda: Octopodidae) fishery in the Campeche Bank, Gulf of Mexico. Rev. Biol. Trop. 48:323–331.[Web of Science][Medline]
Boletzky, S. v. 1975. A contribution to the study of yolk absorption in the cephalopoda. Z. Morphol. Tiere 80:229–246.
Boyle, P. R. 1983. Cephalopod Life Cycles. Vol. 1. Species Account. Academic Press, London.
Boyle, P. R. 1987. Cephalopod Life Cycles. Vol. 2. Comparative Review. Academic Press, London.
Boyle, P. R., and D. Chevis. 1992. Egg development in the octopus Eledone cirrhosa. J. Zool. 227: 623–628.[Web of Science]
Boyle, P. R., and D. Knobloch. 1984a. Male reproductive maturity in the octopus Eledone cirrhosa (Cephalopoda: Octopoda). J. Mar. Biol. Assoc. UK 64:573–579.
Boyle, P. R., and D. Knobloch. 1984b. Reproductive maturity in fresh and aquarium-held Eledone cirrhosa (Cephalopoda: Octopoda). J. Mar. Biol. Assoc. UK 64:581–585.
Boyle, P. R., and P. Rodhouse. 2005. Cephalopods: Ecology and Fisheries. Blackwell Publishing, Oxford.
Buckley, S. K. L. 1977. Oogenesis and its hormonal control in Octopus vulgaris. Ph.D. dissertation, University of Cambridge, Cambridge.
Budelmann, B. U., R. Schipp, and S. v. Boletzky. 1997. Cephalopoda. Pp.119–413 in Microscopic Anatomy of Invertebrates, Vol. 6A, Mollusca II, F. W. Harrison and A. J. Kohn, eds. Wiley-Liss, New York.
Caamal-Monsreal, C. P. 2006. Efecto del tipo de alimento sobre el desove y eclosión del pulpo (Octopus maya), en condiciones controladas. B.Sc. thesis, Technological Institute of Conkal, Yucatán, Mexico.
Cabrera, J. L., and O. Defeo. 2001. Daily bioeconomic analysis in a multispecific artisanal fishery in Yucatan, Mexico. Aquat. Living Resour. 14:19–28.
Castro-Suaste, T., G. Mexicano-Cintora, and O. Defeo. 2000. Las pesquerías del estado de Yucatán (México): evolución y manejo durante el periodo 1976–1997. Oceanides 15:47–61.
Cazares-Simental, R. J. 2006. Caracterización fisiológica y morfológica del desarrollo embrionario y los primeros días de vida de Octopus maya (Voss y Solis1966). B.Sc. thesis, University of Guadalajara, Jalisco, Mexico.
D'Aniello, A., A. Di Cosmo, C. Di Cristo, L. Assisi, V. Botte, and M. M. Di Fiori. 1996. Occurrence of sex steroid hormones and their binding proteins in Octopus vulgaris Lam. Biochem. Biophys. Res. Commun. 227:782–788.[Web of Science][Medline]
DeRusha, R. H., J. W. Forsythe, F. P. DiMarco, and R. T. Hanlon. 1989. Alternative diets for maintaining and rearing cephalopods in captivity. Lab. Anim. Sci. 39:306–312.[Web of Science][Medline]
Di Cosmo, A., C. Di Cristo, and M. Paolucci. 2001. Sex steroid hormone fluctuations and morphological changes of the reproductive system of the female of Octopus vulgaris throughout the annual cycle. J. Exp. Zool. 289:33–47.[Web of Science][Medline]
Di Cosmo, A., C. Di Cristo, and M. Paolucci. 2002. A Estradiol-17β receptor in the reproductive system of the female of Octopus vulgaris: characterization and inmunolocalization. Mol. Reprod. Dev. 61:367–375.[Web of Science][Medline]
Domingues, P. M., N. Lopez, J. A. Muñoz, T. Maldonado, G. Gaxiola, and C. Rosas. 2007. Effects of a dry pelleted diet on growth and survival of the Yucatan octopus, Octopus maya. Aquac. Nutr. 13:273–280.
Fermin, C. D., W. F. Colmers, and M. Igarashi. 1985. Electron-microscopic observations of the gravity receptor epithelia of normal and spinner juvenile Octopus maya. Cell Tissue Res. 240:701–704.
Fioroni, P., and G. Sundermann. 1983. Zur embryonalen Differenzierung der Gonadenanlage bei Coleoiden Cephalopoden. Zool. Jahrb. Anat. 109:153–165.
Fong, S.-L., P. G. Lee, K. Ozaki, R. Hara, T. Hara, and C. D. B. Bridges. 1988. IRBP-like proteins in the eyes of six cephalopod species—immunochemical relationship to vertebrate interstitial retinol-binding protein (IRBP) and cephalopod retinal-binding protein. Vision Res. 28:563–573.[Web of Science][Medline]
Forsythe, J. W., and R. T. Hanlon, 1988. Effect of temperature on laboratory growth, reproduction and life span of Octopus bimaculoides. Mar. Biol. 98:369–379.
Forsythe, J. W., R. T. Hanlon, and P. G. Lee. 1990. A formulary for treating cephalopod mollusc diseases. Pp. 51–63 in Pathology in Marine Science, F. O. Perkins and T. C. Cheng, eds. Academic Press, San Diego.
Gabr, H. R., R. T. Hanlon, M. H. Hanafy, and S. G. El-Etreby. 1999a. Reproductive versus somatic tissue allocation in the cuttlefish Sepia dollfusi Adam (1941). Bull. Mar. Sci. 65:159–173.
Gabr, H. R., R. T. Hanlon, S. G. El-Etreby, and M. H. Hanafy. 1999b. Reproductive versus somatic tissue growth during the life cycle of the cuttlefish Sepia pharaonis Ehrenberg, 1831. Fish Res. 97:802–811.
Gimenez-Bonafe, P., E. Ribes, M. J. Zamora, H. E. Kasinsky, and M. Chiva. 2002. Evolution of octopod sperm. I. Comparison of nuclear morphogenesis in Eledone and Octopus. Mol. Reprod. Dev. 62:357–362.[Web of Science][Medline]
Gnap, M. N. 1987. Oocyte growth and gonadial maturation in the octopus Eledone cirrhosa. Ph.D. thesis, Aberdeen University, Aberdeen, Scotland.
Hanlon, R. T., J. W. Forsythe, K. M. Cooper, A. R. Dinuzzo, D. S. Folse, and M. T. Kelly. 1984. Fatal penetrating skin ulcers in laboratory-reared octopuses. J. Invertebr. Pathol. 44:67–83.[Web of Science][Medline]
Hanlon, R. T., J. P. Bidwell, and R. Tait. 1989. Strontium is required for statolith development and thus normal swimming behaviour of hatchling cephalopods. J. Exp. Biol. 141:187–195.[Abstract/Free Full Text]
Hanlon, R. T., S. A. Ament, and H. Gabr. 1999. Behavioral aspects of sperm competition in cuttlefish, Sepia officinalis (Sepioidea: Cephalopoda). Mar. Biol. 134:719–728.
Hernández-García, V., J. L. Hernández-López, and J. J. Castro-Hdez. 2002. On the reproduction of Octopus vulgaris off the coast of the Canary Islands. Fish Res. 57:197–203.
Idrissi, F. H., N. Koueta, M. Idhalla, D. Belghyti, and S. Bencherifi. 2006. Les modalités du cycle sexuel du poulpe Octopus vulgaris du Sud marocain (Tantan, Boujdour). C. R. Biol. 329:902–911.[Web of Science][Medline]
INP-SAGARPA. 2007. Evaluación de la población de pulpo (Octopus maya) en la península de Yucatán 2007. INP-SAGARPA, Dictámenes y Evaluaciones. [Online] http://www.inp.sagarpa.gob.mx/Dictamenes/Dictamenes.htm [2008, November 13].
Khallahi, O. M. F. 2001. Étude de la gametogenese chez le poulpe Octopus vulgaris (Cuvier, 1797). Bulletin Scientifique du Centre National de Recherches Océanographiques et des Pêches 28:44–52.
Kier, W. M., and A. M. Smith. 1990. The morphology and mechanics of octopus suckers. Biol. Bull. 178:126–136.[Abstract]
Kier, W. M., and A. M. Smith. 2002. The structure and adhesive mechanism of octopus suckers. Integr. Comp. Biol. 42:1146–1153.[Abstract/Free Full Text]
Lafont, R., and M. Mathieu. 2007. Steroids in aquatic invertebrates. Ecotoxicology 16:109–130.[Web of Science][Medline]
Laptikhovsky, V. V., and A. I. Arkhipkin. 2001. Oogenesis and gonad development in the cold water loliginid squid Loligo gahi (Cephalopoda: Myopsida) on the Falkland shelf. J. Molluscan Stud. 67:475–482.[Abstract/Free Full Text]
Lee, P. G. 1992. Chemotaxis by Octopus maya Voss et Solis in a Y-maze. J. Exp. Mar. Biol. Ecol. 156:53–67.[Web of Science]
Luna, L. G. 1968. Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology. McGraw-Hill, New York.
Mann, T., A. W. Martin, and J. B. Thiersch. 1970. Male reproductive tract, spermatophores and spermatophoric reaction in the giant octopus of the North Pacific, Octopus dofleini martini. Proc. R. Soc. B Biol. Sci. 175:31–61.[Medline]
Moltschaniwskyj, N. A. 2004. Understanding the process of growth in cephalopods. Mar. Freshw. Res. 55:379–386.
Moltschaniwskyj, N. A., and J. M. Semmens. 2000. Limited use of stored energy reserves for reproduction by the tropical loliginid squid Photololigo sp. J. Zool. 251:307–313.[Web of Science]
Nepita-Villanueva, M. R., and O. Defeo. 2001. Crecimiento del pulpo Octopus maya (Mollusca: Cephalopoda) de la costa de Yucatán, México: un análisis de largo plazo. Rev. Biol. Trop. 49:93–101.[Web of Science][Medline]
Okutani, T. 1990. Squids, cuttlefish and octopuses. Mar. Behav. Physiol. 18:1–17.
Olivares, P. A., R. O. Zúñiga, G. Castro, C. Segura, and J. Sanchez. 1996. Bases biológicas para el manejo de Octopus mimus: reproducción y crecimiento. Estud. Oceanol. 15:61–74.
Olivares, P. A., E. Bustos-Obregón, A. V. Castillo, and R. O. Zúñiga. 2003. Variaciones del funcionamiento testicular en Octopus mimus adultos. Int. J. Morphol. 21:315–323.
Otero, J., A. F. González, M. P. Sieiro, and A. Guerra. 2007. Reproductive cycle and energy allocation of Octopus vulgaris in Galician waters, NE Atlantic. Fish Res. 85:122–129.
Perez-Losada, M., A. Guerra, and A. Sanjuan. 2002. Allozyme divergence supporting the taxonomic separation of Octopus mimus and Octopus maya from Octopus vulgaris (Cephalopoda: Octopoda). Bull. Mar. Sci. 71:653–664.
Peterson, R. P. 1959. The anatomy and histology of the reproductive systems of Octopus bimaculoides. J. Morphol. 104:61–87.
Pollero, R. J., and O. Iribarne. 1988. Biochemical changes during the reproductive cycle of the small patagonian octopus, Octopus tehuelchus, D'Orb. Comp. Biochem. Physiol. B 90:317–320.
Reimschuessel, R., and M. K. Stoskopf. 1990. Octopus automutilation syndrome. J. Invertebr. Pathol. 55:394–400.[Web of Science][Medline]
Rodríguez-Rua, A., I. Pozuelo, M. A. Prado, M. J. Gómez, and M. A. Bruzón. 2005. The gametogenic cycle of Octopus vulgaris (Mollusca: Cephalopoda) as observed on the Atlantic coast of Andalusia (south of Spain). Mar. Biol. 147:927–933.
Romero-Soberanis, M. G. 2007. Efecto del tipo de alimento en el crecimiento y la maduración sexual de hembras tempranas de pulpo O. maya. B.Sc. thesis, Technological Institute of Lerma, Campeche, Mexico.
Roper, C. F. E., and M. J. Sweeney. 1983. Techniques for fixation, preservation, and curation of cephalopods. Mem. Nat. Mus. Vic. 44:29–47.
Roper, C. F. E., and G. L. Voss. 1983. Guidelines for taxonomic descriptions of cephalopods species. Mem. Nat. Mus. Vic. 44:49–63.
Rosa, R., P. R. Costa, and M. L. Nunes. 2004. Effect of sexual maturation on the tissue biochemical composition of Octopus vulgaris and O. defilippi (Mollusca: Cephalopoda). Mar. Biol. 145:563–574.
Rosa, R., P. R. Costa, N. Bandarra, and M. L. Nunes. 2005. Changes in tissue biochemical composition and energy reserves associated with sexual maturation in the ommastrephid squids Illex coindetii and Todaropsis eblanae. Biol. Bull. 208:100–113.
Rosas, C., G. Cuzon, C. Pascual, G. Gaxiola, D. Chay, N López, T. Maldonado, and P. M. Domínguez. 2007a. Energy balance of Octopus maya fed crab or an artificial diet. Mar. Biol. 152:371–381.
Rosas, C., R. J. Cazares-Simental, C. P. Caamal-Monsreal, O. H. Avila-Poveda, C. Moguel, A. Sánchez, A. Sánchez, and C. Pascual. 2007b. Adaptaciones morfológicas y digestivas durante los primeros días de vida de los juveniles del pulpo de costa Octopus maya (Voss y Solis). XIII congreso bienal, AMENA "Asociación Mexicana de Especialistas en Nutrición Animal, A.C." Oct. 23–26. Veracruz, Mexico.
Rosas, C., J. Tut, J. Baeza, A. Sánchez, V. Sosa, C. Pascual, L. Arena, P. M. Domingues, and G. Cuzon. 2008. Effect of type of binder on growth, digestibility, and energetic balance of Octopus maya. Aquaculture 275:291–297.[Web of Science]
Salas, S., G. Mexicano-Cintora, and M. A. Cabrera. 2006. ¿Hacia Donde van las Pesquerías en Yucatán? Tendencias, Retos y Perspectivas. CINVESTAV-IPN, Unidad Mérida, Mérida, Mexico.
Santos-Valencia, M. G. J., and C. Re-Regis. 2003. Biología reproductiva del pulpo de costa Octopus maya (Voss y Solis, 1966) en el suroeste de la Península de Yucatán. Informe técnico, Centro Regional de Investigaciones Pesqueras, Lerma, Campeche, Mexico.
Santos-Valencia, M. G. J., and R. E. del Rio. 2006. First histological description of the ovogenesis in Octopus maya from Campeche bay. World Aquaculture Society Meeting, Florence, Italy. 390 (Abstract) [online] https://www.was.org/Meetings/AbstractData.asp?AbstractId=10688 [2008, November 13].
Segawa, S., and R. T. Hanlon. 1988. Oxygen consumption and ammonia excretion rates in Octopus maya, Loligo forbesi and Lolliguncula brevis (Mollusca: Cephalopoda). Mar. Behav. Physiol. 13:389–400.
Van Heukelem, W. F. 1976. Growth, bioenergetics and life-span of Octopus cyanea and Octopus maya. Ph.D. dissertation, University of Hawaii, Honolulu.
Van Heukelem, W. F. 1977. Laboratory maintenance, breeding, rearing, and biomedical research potential of the Yucatan octopus (Octopus maya). Lab. Anim. Sci. 27:852–859.[Web of Science][Medline]
Van Heukelem, W. F. 1983. Octopus maya. Pp. 311–323 in Cephalopod Life Cycles, Vol. 1, Species Accounts, P. R. Boyle, ed. Academic Press, London.
Villanueva, R., and M. D. Norman. 2008. Biology of the planktonic stages of benthic octopuses. Oceanogr. Mar. Biol. Annu. Rev. 46:105–202.
Voight, J. R. 2001. The relationship between sperm reservoir and spermatophore length in benthic octopus (Cephalopoda: Octopodidae). J. Mar. Biol. Assoc. UK 81:983–986.
Voight, J. R. 2002. Morphometric analysis of male reproductive features of octopodids (Mollusca: Cephalopoda). Biol. Bull. 202:148–155.[Abstract/Free Full Text]
Voss, G. L., and M. J. Solís-Ramírez. 1966. Octopus maya, a new species from the Bay of Campeche. Bull. Mar. Sci. 16:615–625.
Wells, M. J. 1959. Hormonal control of sexual maturity in Octopus. J. Exp. Biol. 36:1–33.[Abstract]
Wells, M. J. 1960. Optic glands and the ovary of Octopus. Symp. Zool. Soc. Lond. 2:87–107.
Wells, M. J., and J. Wells. 1972. Optic glands and the state of the testis in Octopus. Mar. Behav. Physiol. 1:71–83.
Young, L. E. 1992. Vitellogenesis in the Northern octopus, Eledone cirrhosa., Ph.D. thesis, Aberdeen University, Aberdeen, Scotland.
TOP
Abstract
Introduction
