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Biochemical changes during the reproductive cycle of Haliotis fulgens (Philippi, 1845) (gastropoda: archaeogastropoda) on the Baja California Sur West Coast.

ABSTRACT This article describes the changes in the concentration of lipids, proteins, and carbohydrates in the gonad, digestive gland, foot and mantle of Haliotis fulgens over a reproductive cycle. An average of 30 specimens was collected each month between September 2011 and August 2013 from La Bocana, Baja California Sur, Mexico. The biometrics of each specimen were recorded, and gonads were processed using a standard histological method. Additionally, from February 2012 to February 2013, portions of nonfixed organs were frozen at -54[degrees]C for use in proximal analyses. This species showed gonadal development and spawning throughout the study period, with a peak in spawning from September through February, coinciding with sea surface temperatures near 20[degrees]C and the beginning of the decline in daylight. This study demonstrates that this species utilizes proteins, lipids, and carbohydrates stored in the foot during gonadal development and that lipid levels decrease in both the digestive gland and the gonad during spawning.

KEY WORDS: reproduction, histology, nutrient storage, Haliotis fulgens

INTRODUCTION

The genus Haliotis is distributed in tropical and temperate waters (Geiger & Owen 2012), mainly in the Pacific coasts of Australia, Japan, Canada, South Africa, California, and the northern and central Baja California peninsula (Dybas 1994). This abalone species inhabits the intertidal and subtidal zones in rocky shores covered by macroalgae and the associated benthic community (Dayton & Tegner 1984).

Seven species of Haliotis have been recorded in Mexico: Haliotis fulgens, Haliotis corrugata (Wood, 1828), Haliotis cracherodii (Leach, 1817), Haliotis rufescens (Swainson, 1822), Haliotis sorenseni (Bartsch, 1940), Haliotis assimilis (Linnaeus, 1758), and Haliotis walallensis (Stearns, 1899); the former two are the subject of a major fishery. The Mexican fishery authorities use the knowledge on reproductive cycles to establish fishing closed seasons as a measure to make the fishery sustainable (Guzman del Proo 1992).

Studies on abalone from other regions [Haliotis asinina (Linnaeus, 1758), Haliotis rufescens, Haliotis varia (Linnaeus, 1758)] have reported a great variability in the spawning periodicity between species, as well as between years and sites for the same species (Young & De Martini 1970; Capinpin et al. 1998, Sobhon et al. 1999, Najmudeen & Victor 2004, Coates & Hovel 2014).

The earliest studies on the reproduction of Haliotis fulgens were carried out in Isla Cedros, Baja California (Sevilla 1971) and Bahia Tortugas, Baja California Sur (Belmar-Perez & Guzman del Proo 1992). The former, conducted in 1965, reported that reproduction takes place mostly from June through September, with only a few individuals still reproducing in October, and that spawning coincides with increase in seawater temperature (to around 20[degrees]C). The second study used samples collected between November 1985 and November 1988 and reported periods of peak reproductive activity in spring and autumn, with occasional total expulsions in winter and summer.

Other molluscs show a close relationship between the nutrient storage and the reproductive cycles. For example, Brousseau (1987) points out that the digestive gland of the bivalve My a arenaria (Linnaeus, 1758) is responsible for the storage and transfer of food assimilated in body tissues and that the onset of oocyte growth depends on the buildup and transfer of reserve nutrients from the digestive gland to the gonad. In other cases, the nutrient storage and the reproductive cycles are clearly distinct (Barber & Blake 2006). For abalone, it has been observed that the gonad index is inversely correlated with the digestive gland index in Haliotis cracherodii, Haliotis rufescens (Boolootian et al. 1962), Haliotis rubra (Leach, 1814) (Litaay & De Silva 2003), and Haliotis varia (Najmudeen 2007), suggesting that the hepatic gland stores nutrients that are essential for gamete development during the reproductive cycle (Boolootian et al. 1962, Litaay & De Silva 2003, Najmudeen 2007), as evidenced by variations in protein and lipid levels in the gonad and the digestive gland (Najmudeen 2007). Proximal analyses of reserve substances in relation to reproduction in H. cracherodii (Webber 1970), H. rubra (Litaay & De Silva 2003, Litaay 2005), and H. varia (Najmudeen 2007) point to the existence of a metabolic demand for gamete production during reproduction.

Nelson et al. (2002) showed that lipids are essential for gonadal development and maturation in Haliotis fulgens. Further studies are needed, however, to gain a deeper insight into the reproductive and nutrient storage cycles. This work describes the changes in the biochemical composition (lipids, proteins, and carbohydrates) of the gonad, digestive gland, foot, and mantle during the reproductive cycle of H. fulgens and explores the relationship of the reproductive cycle with environmental factors such as temperature and photoperiod.

MATERIALS AND METHODS

Assisted by fishermen of the Progreso cooperative in La Bocana, Baja California Sur, Mexico (26[degrees] 46.411' N; 113[degrees] 42.639' W), 592 adult specimens of Haliotis fulgens ranging in length from 60 to 200 mm (mean length 136 mm) were collected between September 2011 and August 2013; on average, 30 specimens were collected each month from depths between 8 and 12 m.

The central portion of the digestive gland-gonad complex of each specimen was fixed in 10% formalin-seawater and embedded in paraffin as part of the histological technique; 5-[micro]m-thick sections were obtained and stained with hematoxylin and eosin (Humason 1979). The following gonadal stages were considered to describe the reproductive cycle: developing, mature, spawning, postspawning and undifferentiated (Velez-Arellano et al. 2015).

Additionally, from February 2012 to February 2013, portions of nonfixed gonad, digestive gland, foot, and mantle were frozen at -54[degrees]C to determine the protein, lipid, and carbohydrate contents following the methods proposed by Bradford (1976), Barnes and Blackstock (1973), and Roe (1955), respectively.

Histological slides of the central portion of the digestive gland-gonad complex of specimens collected during this period were digitized, and the area occupied by the gonad, digestive gland, and digestive gland-gonad complex was measured using the software Sigma Scan Pro 5.0. The gonad index was calculated dividing the area occupied by the gonad by the area of the digestive gland-gonad complex; similarly, the digestive gland index was calculated as the area occupied by the digestive gland divided by the area of the digestive gland-gonad complex.

Monthly averages of seawater surface temperature data were obtained from National Oceanic and Atmospheric Administration Aqua MODIS satellite measurements. Such data have the advantage over traditional measurements of being inexpensive, spatially extensive, automatically repeated in time, and validated, that is, well correlated with discrete field measurements (Thomas et al. 2011), similar to other investigations where the reproductive cycle of several mollusc species has been related to temperature data obtained from satellite imagery (Garcia-Cuellar et al. 2004, Calderon-Aguilera et al. 2010, Garcia-Dominguez et al. 2011, Matias et al. 2013).

RESULTS

Reproductive Cycle

The identification of the various gonad development stages and their relative frequency of occurrence on a monthly basis provide a clear picture of the reproductive development cycle of Haliotis fulgens (Fig. 1). This study showed an increasing frequency of undifferentiated specimens from September 2011 and their predominance until August 2012. The development stage was observed throughout the study period, except in October 2011; maturity and spawning began between February and May, increased from June to September, and prevailed until February 2013. The higher spawning frequency from February to August 2013 relative to the same period in 2012 suggests interannual variations in factors that influence the maturation process. Finally, postspawning was observed virtually throughout the study period, except in February, July, and August 2013, reaching its highest frequency in September 2011 (Fig. 1).

Biochemical Composition

Carbohydrates

Carbohydrate levels in the gonad ranged from 19 to 82 mg/g, with high levels in April, May, and September 2012. Concentrations in the digestive gland ranged from 14 to 86 mg/g, with a peak in February. The foot showed higher carbohydrate concentrations than other tissues: 54 mg/g in January to 200 mg/g in May. Carbohydrate concentration in the mantle ranged from 0.2 to 0.5 mg/g (Fig. 2B).

In the undifferentiated stage, carbohydrate levels were higher in the gonad, decreasing during development and maturity, rising again during spawning, and declining again during postspawning. In the digestive gland, the development stage was associated with higher carbohydrate levels. In the foot, peak concentrations occurred in the undifferentiated stage and the lowest during gonadal development, rising progressively as maturity and spawning progressed, to decrease again during postspawning. In the mantle, the highest carbohydrate concentration was associated with the undifferentiated stage (Fig. 3).

Lipids

In the gonad, lipid concentrations varied throughout the year between 72 and 136 mg/g. The digestive gland showed wide variations in lipid levels throughout the study period, with peak concentrations in February 2012 (471 mg/g) and the lowest levels in February 2013 (72 mg/g); percent spawning showed an opposite behavior during these months. In the foot, lipid concentrations decreased from 47 mg/g in February 2012 to 13 mg/g in November 2012. The mantle displayed the lowest lipid levels, which varied from 0.18 mg/g in February 2012 to 0.6 mg/g in June 2012 (Fig. 2A).

The highest lipid concentration in the gonad occurred in the maturity and postspawning stages and the lowest in spawning. In the digestive gland, the lowest levels were recorded in the undifferentiated and spawning stages. In the foot, the highest lipid concentrations occurred in the undifferentiated stage and the lowest during development. In the mantle, lipid concentrations remained virtually unchanged throughout the reproductive cycle (Fig. 4).

Proteins

Protein concentration in the gonad remained at around 470 mg/g, with the highest value recorded in June (677 mg/g) and the lowest in February 2013 (389 mg/g). In the digestive gland, low protein concentrations were observed from February to June, with the minimum in May (440 mg/g); the peak concentration was 686 mg/g in August. In the foot, peak protein concentrations occurred in February (199 mg/g) and the lowest in November (48 mg/g). The mantle showed the lowest protein concentration of all organs analyzed, with the peak in April (7.8 mg/g) and the lowest in February 2012 (2.8 mg/g) (Fig. 2C).

Both the gonad and the digestive gland displayed parallel variations in protein concentration throughout the reproductive cycle, with low values during maturity. In the foot, high concentrations occurred in the undifferentiated stage, decreasing during gonadal development and then increasing steadily during maturity and spawning. In the mantle, the undifferentiated stage showed the highest protein concentrations, which subsequently decreased gradually until the post-spawning stage (Fig. 5).

Gonad and Digestive Gland Indices

The gonad index increased gradually from February to December 2012, then decreased in January 2013; the highest figures were observed from September to December 2012, matching the reproduction season. Figures calculated for February 2012 (0.1) were lower than those for February 2013 (0.35); the higher values are consistent with the higher frequency of spawning. The digestive gland index rose from 0.91 in March 2012 to 0.27 in December 2012, followed by a decline until January 2013 and a subsequent rise to 0.64 in February 2013 lower than that in the previous year (0.8) (Fig. 6).

Environmental Factors

Sea surface temperature in the study area ranged from 27[degrees]C in September 2012 to 15[degrees]C in April 2013. In general, when temperatures were low (March-July 2012 and February-May 2013), Haliotis fulgens specimens were in the development stage. High temperatures were recorded from September 2011 to December 2012 and from August 2012 to December 2012, coinciding with a higher frequency of spawning (Fig. 7).

With regard to photoperiod, USNO (2015) records indicate that daylength was shorter from October to February and longer from March to September. A higher frequency of spawning was observed during shorter days (Fig. 7). In the study area, a lower sea surface temperature is associated with a longer daylength as a result of the displacement of cold water of the California Current at this time of the year (Lluch-Belda et al. 2000).

DISCUSSION

This study revealed that gamete development in Haliotis fulgens took place throughout the study period; spawning specimens were observed virtually all year round, with a higher frequency from September to February. Previous studies on H. fulgens reported that in Isla Cedros, more than 200 km north of La Bocana, most specimens examined spawned from June to September and a few did so in October (Sevilla 1971); in Bahia Tortugas, a locality 150 km north of La Bocana, spawning specimens were collected in all seasons of the year (Belmar-Perez & Guzman del Proo 1992). These reports suggest that H. fulgens is able to reproduce throughout the year, with interannual variations in the intensity of spawning.

On the other hand, unlike Haliotis fulgens, it has been observed that spawning occurs in different days in populations of Haliotis asinina living 1.5 km apart from each other (Counihan et al. 2001). Furthermore, females of Haliotis madaka (Habe, 1977) show alternating patterns of synchronous and asynchronous oocyte development according to the geographic area (Horiguchi et al. 2005), and the spawning season in Haliotis varia displayed slight variations between sampling sites (Najmudeen & Victor 2004). These findings suggest that the abalone gonad development cycle may vary according to the geographic area and local environmental conditions.

Webber and Giese (1969) and Wilson and Schiel (1995) mentioned that in Haliotis species living in temperate and subtropical areas, gonad maturation and spawning show a marked seasonality related to sudden changes in temperature. In this study, Haliotis fulgens did not exhibit a marked spawning seasonality; however, spawning was more intense when temperatures rose above 20[degrees]C, which is consistent with the findings reported by Sevilla (1971).

Another factor related to the reproductive cycle of Haliotis fulgens is photoperiod. This study showed that spawning becomes more frequent when daylength is shorter. According to Beck (1968), photoperiod is a key factor influencing the geographical distribution, seasonal biology, shape, growth, metabolic rate, and behavior of organisms; therefore, photoperiod is a potential exogenous factor that is likely to affect the timing of spawning (Hahn 1989). Its effect of on the reproductive capacity of haliotids has been little studied, with inconclusive results. This is the case of Haliotis eracherodii, a species for which gonad size of mature specimens is not correlated with daylength, although daylight periods longer than 12 h did stimulate gametogenesis (Webber & Giese 1969). In contrast, Setyono (2006) found that Haliotis asinina shows a relationship between the gonad maturation and the increase in daylength; nonetheless, maturation seems to be more closely associated with higher air temperature and tides. On the other hand, studying Haliotis discus (Reeve, 1846) under laboratory conditions, Pena (1986) observed that gonad maturation is negatively affected by an extremely long photoperiod (24 h light) and concluded that maturation requires cyclic variations in photoperiod and temperature.

As for the relationship between biochemical content in tissues and the reproductive cycle, Webber (1970). Brousseau (1987), Rodriguez-Astudillo et al. (2005), Barber and Blake (2006), and Ramesh and Ravichandran (2008) point out that in molluscs, the digestive gland or the foot store and subsequently transfer the assimilated nutrients to other body organs. In Haliotis eracherodii, the foot is considered a reservoir organ, because its size decreases as the gonad volume increases (Webber 1970). This study found that, as gonadal development progresses, protein, lipid, and carbohydrate contents in the foot decrease, whereas these contents increase in the gonad and the digestive gland; this suggests that the foot is the organ that stores and supplies nutrients for gamete production, as the energy in the gonad and digestive gland is consumed.

The inverse relationship between the gonad and digestive gland indices observed in Haliotis fulgens indicates that the digestive gland transfers nutrients to the gonad. This has been reported for other haliotids (Boolootian et al. 1962, Litaay & De Silva 2003, Najmudeen 2007). Besides, Litaay and De Silva (2003) and Litaay (2005) have reported that in Haliotis rubra, the digestive gland is the main supplier of reserve nutrients, mostly lipids, during maturation. In this regard, the results showed a decrease in the levels of protein, lipid, and carbohydrate in the digestive gland during gonad maturation, suggesting that this organ supplies energy for gamete production.

The results showed that in Haliotis fulgens, the digestive gland and the gonad lose lipids during spawning. This could be due to the transfer of lipids from the digestive gland to the gonad for gamete production, followed by the release of gametes during spawning. Moreover, the digestive gland showed the highest percentage of protein relative to the other organs analyzed. This was also observed in Babylonia spirata (Linnaeus, 1758) (Shanmugam et al. 2006), a gastropod in which the lowest levels occurred after the reproductive season, indicating that proteins stored in the digestive gland are used for synthesizing carbohydrates or lipids in the gonad (Ramesh & Ravichandran 2008).

The mantle is an organ that cannot be considered as a nutrient reservoir; its nutrient content never exceeded 1% of any of the nutrients analyzed.

In conclusion, gamete development in Haliotis fulgens takes place throughout the year; spawning occurs primarily between September and February, associated with temperatures near 20[degrees]C and when daylength starts to decrease. Similar to the gonad, the digestive gland shows a steady loss of lipids during spawning, indicating a constant transfer of nutrients to the gonad as it develops. The foot is another nutrient reservoir: lipid, protein, and carbohydrate levels in this organ were observed to decrease during gonadal development.

ACKNOWLEDGMENTS

We gratefully acknowledge the support received from SAGARPA-CONACYT, through grant 01-163322 coordinated by the CRIP-La Paz and CRIP-La Paz for POA-Bentonicos grants in 2012, 2013, and 2014. We also thank the Fisheries Cooperative Society "Progreso" for sample collection, researchers from CRIP-La Paz (Carlos Monroy, Eduardo Quiroz, Mauro Guadarrama, and Veronica Fernandez) for processing biological material, and Rosa Linda Salgado and Teresa Sicard for support in ecophysiology laboratory of CIBNOR. We also acknowledge the Department of Research and Postgraduate Studies of the National Polytechnic Institute (IPN) for funding this project and the Commission for the Operation and Promotion of Academic Activities, IPN for grants awarded to N. Velez-Arellano, F. A. Garcia-Dominguez, O. E. Holguin-Quinones, and M. Ramirez-Rodriguez. Maria Elena Sanchez Salazar contributed to the preparation of the English manuscript.

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NURENSKAYA VELEZ-ARELLANO, (1,5) * FEDERICO ANDRES GARCIA-DOMINGUEZ, (1,4) DANIEL B. LLUCH-COTA, (2) JOSE LUIS GUTIERREZ-GONZALEZ, (3) OSCAR EFRAIN HOLGUIN-QUINONES (1,4) AND MAURICIO RAMIREZ-RODRIGUEZ (1,4)

(1) Instituto Politecnico National, Centro Interdisciplinario de Ciencias Marinas, Av. Instituto Politecnico National s/n Col. Playa Palo de Santa Rita Apdo, Postal 592, La Paz, Mexico; (2) Centro de Investigaciones Biologicas del Noroeste, Av. Instituto Politecnico National 195 Col. Playa Palo de Santa Rita Sur, La Paz, Mexico; (3) Centro Regional de Investigation Pesquera, Carretera a Pichilingue Km 1 s/n Col, El Esterito, La Paz, Mexico; (4) Becario Comision de Fomento y Actividades Academicas del IPN, Mexico D.F., Mexico; (5) Becario de Estinnilo Institutional de Formation de Investigadores (BEIFI), Mexico D.F.

* Corresponding author. E-mail: nurens@hotmail.com

DOI: 10.2983/035.035.0121
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Author:Velez-Arellano, Nurenskaya; Garcia-Dominguez, Federico Andres; Lluch-Cota, Daniel B.; Gutierrez-Gonz
Publication:Journal of Shellfish Research
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Geographic Code:1MEX
Date:Apr 1, 2016
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