BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, researchlibraries, and research funders in the common goal of maximizing access to critical research.

Gonadal Cycle of Tegula eiseni (Jordan 1936) (Mollusca: Gastropoda) in BahíaAsunción, Baja California Sur, MexicoAuthor(s): Nurenskaya Vélez-Arellano, Sergio Guzmán Del Próo and Esperanza Ortiz OrdoñezSource: Journal of Shellfish Research, 28(3):577-580. 2009.Published By: National Shellfisheries AssociationDOI: http://dx.doi.org/10.2983/035.028.0321URL: http://www.bioone.org/doi/full/10.2983/035.028.0321

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, andenvironmental sciences. BioOne provides a sustainable online platform for over 170 journals and books publishedby nonprofit societies, associations, museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance ofBioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiriesor rights and permissions requests should be directed to the individual publisher as copyright holder.

GONADAL CYCLE OF TEGULA EISENI (JORDAN 1936) (MOLLUSCA: GASTROPODA) IN

BAHIA ASUNCION, BAJA CALIFORNIA SUR, MEXICO

NURENSKAYA VELEZ-ARELLANO,1SERGIO GUZMAN DEL PROO

2,3AND

ESPERANZA ORTIZ ORDONEZ1,3

Escuela Nacional de Ciencias Biologicas – IPN, Laboratorio de Histologıa1 y Ecologıa2.Becarios COFAA3

ABSTRACT The gonadal cycle ofTegula eiseni (Jordan, 1936) was determined onmonthly samples (25–30 organisms) collected

from a population in Bahıa Asuncion, B.C.S., from January 2006 to December 2006. The results of the histological study indicate

that both males and females show stages of gametogenesis and gonad maturation throughout the year and only two major

spawning events: one in spring and another in fall. The species behaved as a partial spawner, and only at certain times was total

spawning observed in females. Maturation and release or spawning times seem to be closely related to seasonal temperature rises

and abrupt changes in surface sea water temperature, which occur at brief intervals for several days at certain times of year.

KEY WORDS: gonadal cycle, gametogenesis, gastropoda, Trochidae, Tegula eiseni

INTRODUCTION

The gastropod mollusc Tegula eiseni (Jordan, 1936) inhabitsthe rocky subtidal floor from the low tide line to a depth of 18m,

obtaining its food from among pebbles and small cavities (Paine1969, Wilson et al. 1999, Veliz & Vasquez 2000). In the rockyshelves of Baja California, this species stands out within the

benthic invertebrate community because it is a major herbivoreand carries a high importance value index (Guzman del Prooet al. 1991, Guzman del Proo 1994). It occurs in one of themajor

fishing areas of the Pacific coast of Baja California, coexistingwith species of high economic importance such as abalone(Haliotis fulgens), snail (Megastrea undosa), and spiny lobster(Panulirus interruptus) (Guzman del Proo et al. 1991).

Studies on the biology of T. eiseni are scarce. Padilla (2004described the histology of the testicle and ovary of this species.Other studies conducted on other members of the genus

describe larval development in T. funebralis (Hewatt 1934,Moran 1997, Guzman del Proo et al. 2006), and Paine (1969examined changes in the energy content of females of the T.

funebralis at different stages of sexual maturation, suggestingthat a single annual spawning takes place in Mukkaw andNeah bays in Washington state. In the case of T. rustica, from

Vostok Bay, Japan, its reproductive cycle and larval andjuvenile development have been described by Kulikova andOmel’yanenko (2000).

Given its high abundance in shoals where abalone, lobster,

and other economically important invertebrates are caught inBaja California, T. eiseni has been a part of recent ecologicalstudies focusing on the rocky facies community, research that

has sought to identify the animal’s role in resource distributionwithin the benthic community. In the context of these studies,this paper examines gonad development of this species, as part

of a wider project on the reproductive biology and ecology ofmajor gastropods in the central Pacific region of Baja California.

MATERIALS AND METHODS

Bahıa Asuncion, in Baja California Sur, was selected as thestudy area (Fig. 1). Samples were obtained monthly over the

course of one year (2006) by skin diving in the rocky subtidal

zone of Asuncion Island (27�06#00$N latitude, 114�18#00$Wlongitude) at a depth of 6–12 m. Samples ranged from 25–30individuals. Surface water temperature was recorded at each

sampling.Specimens were shelled and the gonad was removed. Sex

identification was based on gonad coloration (moss green in

females and cream-colored in males). Gonads were fixed in a10% formalin solution in sea water for processing withhistological techniques. In the laboratory, small pieces of thegonad of each individual were extracted. These were washed,

dehydrated, cleared, and finally embedded in paraffin. Thinsections were 7-mm thick, and the slides, after paraffinremoval, were stained with hematoxylin-eosin and Masson’s

Figure 1. Location of the study area: Bahıa Asuncion, B.C.S.Correspondence. E-mail: nurens@hotmail.com

Journal of Shellfish Research, Vol. 28, No. 3, 577–580, 2009.

577

trichrome. Microphotographs were taken with a Nikon photo-microscope.

The following characteristics of gonadal tissue were usedto describe the reproductive cycle: (1) volume, (2) degree ofgametogenic cell development, and (3) presence and abundanceof gametogenic cells. Using these criteria, the following stages

were defined: gametogenesis, maturation, partial spawning, andtotal spawning.

RESULTS

A total of 248 adult specimens were examined. The sex ratiowas 1:1 females to males; a chi-square test showed no significant

difference (P > 0.05).

Gonadal Cycle Stages: Females

Oogenesis

During this stage, gonadal tissue is small in volume. A large

number of oogonia (diameter 10–30 mm) and oocytes atdifferent developmental stages are attached to the trabeculae.Fully 100% of specimens examined in the months of January

and April were found to be at this stage (Fig. 2A & 3A).

Maturation

Gonadal tissue is almost totally taken up by mature oocytes;oogonia and developing oocytes are also seen. Fully 100% of

specimens examined in August, September, and Novemberwere found to be at this stage (Fig. 2B & 3A).

Figure 2. Thin sections of the gonad of female and maleTegula eiseni. (A) Oogenesis stage: digestive gland (Dg), trabeculae (Tr), oogonia (Og), oocytes

at different developmental stages (Od), mature oocytes (Om), simple cylindrical epithelium (Ep), smooth muscle fibers (Fm), and caliciform glands (Cg);

Masson trichrome technique, Bar$ 15 mm. (B) Maturation stage: Masson trichrome technique, Bar$ 15 mm. (C) Total spawning stage: degenerating

oocytes (Do); Masson trichrome technique, Bar$ 15 mm. (D) Spermatogenesis stage: spermatogonia (sg), spermatocytes (St), spermatozoa (Sz);

hematoxylin-eosin technique, Bar$ 20mm. (E)Maturation stage:Masson trichrome technique, Bar$ 20mm. (F) Partial spawning stage: hematoxylin-

eosin technique, Bar$ 20 mm.

VELEZ-ARELLANO ET AL.578

Total Spawning

The gonad is empty with only a few degenerating oocytespresent. Trabecular organization is lost. The total number ofspecimens found tobeat this stagewas four, collected inFebruary

andMarch.This is equivalent to7%and15%, respectively, of thetotal number of specimens examined (Fig. 2C & 3A).

Gonadal Cycle Stages: Males

Spermatogenesis

During this stage, several layers of immature gametogeniccells formed by spermatogonia (diameter 10-mm), spermatocytes

at different developmental stages (diameter 5–6-mm), and feath-ery bundles of spermatozoa (nucleus diameter, 2.1-mm) are seenatop the trabeculae. Fully 100% of specimens examined in themonth of January corresponded to this stage (Fig. 2D & 3B).

Maturation

Spermatozoa are abundant and arrayed as feathery bundles,

taking up most of the gonad; germinal tissue has decreased.Asmany as 67%of specimens examined in Junewere found to beat this stage; these frequencies were 80% in July, 64% in August,

60% in November, and 58% in December (Fig. 2E & 3B).

Partial Spawning

Empty spaces visible in gonadal tissue give the gonad a slack

appearance. Immature cells are present atop the trabeculae, andspermatozoa seem free or lightly bundled, suggesting thatpartial release has occurred. This developmental stage was

observed in February in 91% of samples examined; in MarchandApril in 75% of specimens examined eachmonth; in 92% inSeptember; and in 78% in October (Fig. 2F & 3B).

DISCUSSION

The annual sex ratio of Tegula eiseni was 1:1. This ratio is

similar to that reported for Tegula funebralis (Paine 1969) as wellas other organisms in the Trochidae family, such as Haliotisrufescens (Young&DeMartini 1970),H. cracherodi (Gonzalez&

Ortiz 1986), Astraea undosa (Belmar-Perez 1988), Trochus nilo-ticus (Gimin&Lee 1997), andH. rubra (Litaay &De Silva 2003).

Throughout the year, the female population of Tegula eiseni

included specimens in the stages of gametogenesis and matura-tion; only in February and March were specimens in the total

spawning stage found. Although no sections showed partial

spawning in this sex, the constant presence of females in thematuration and subsequent gametogenesis stages, along with thepresence of males with evidence of partial spawning, suggests

that this population has a continuous gonadal cycle in whichpartial spawnings predominate most of the year. This reproduc-tive behavior is similar to that reported in Chorus giganteus

(Jaramillo&Garrido 1990),A. undosa (Belmar-Perez et al. 1991),Thais chocolata (Avendano et al. 1997), Trochus niloticus (Gimin& Lee 1997), and Collisella subrugosa (Rocha-Barreira 2002).

The highest frequency of these partial spawnings and releases

occurred in spring and fall. This seasonality is coincident withthat reported in other gastropods such as H. fulgens (Sevilla1971), Crassostrea glomerata (Dinamani 1974), A. undosa

(Belmar et al. 1991), Thais chocolata (Avendano et al. 1997),Melongena corona (Zetina et al. 2000), Melarhaphe neritoides(Cronin et al. 2000), Zidona dufresnei (Gimenez & Penchasza-

deh 2002), H. rubra (Litaay & De Silva 2003), Patella depressa(Brazao et al. 2003), and Strombus pugilis (Baqueiro et al. 2005).

On the other hand, the simultaneous occurrence of males

with evidence of partial spawning and females in thematurationand subsequent gametogenesis stages leads us to suppose thatgamete release is synchronous among sexes, thus ensuringfertilization, as is also the case in other gastropod species such

as H. fulgens, where female spawning occurs only after spermare released by the male (Sevilla 1971).

Gamete release is undoubtedly influenced by temperature, a

determining physical factor in the release times and developmentof the gonadal cycle in gastropods (Fretter & Graham 1962,Dinamani 1974: C. glomerata; Sevilla 1971:H. fulgens; Baqueiro

et al. 1983:Hexaplex erythrostomus; Gimin & Lee 1997: Trochusniloticus; Gimenez & Penchaszadeh 2002: Zidona dufresnei; Lee2001: Omphalius rusticus; and Naegel & Garcıa-Dominguez2006: Plicopura pansa). Figures 3A and 3B show the relationship

between the temperature recorded in Bahıa Asuncion and gonaddevelopment in Tegula eiseni. Clearly, the periods of maximummaturation and spawning in Tegula coincide with the seasonal

temperature rise from July to November. However, records ofthe evolution of surface water temperature taken at hourlyintervals in the area of Bahıa Asuncion, as reported by Ponce

(2004, show abrupt 1�C–3�C changes lasting from several days toaweek.Quite probably, these abrupt temperature shifts stimulatethe partial release of gametes over brief periods of time. Thismay

explain why we found no evidence of the partial spawning of

Figure 3. Relationship between mean surface sea water temperature and frequency of the different stages of the Tegula eiseni gonadal cycle. (A)

Females. (B) Males. Gametogenesis, Maturation, Partial spawning, Total spawning, Temperature (�C)

GONADAL CYCLE OF TEGULA EISENI (BAHIA ASUNCION) 579

females or of total release by males because sampling took placeat one-month intervals, and these events had already occurred or

were about to occur.

ACKNOWLEDGMENTS

The authors thank Fernando Lopez Salas from ‘‘Coopera-tiva de Produccion Pesquera Leyes de Reforma,’’ who

collected the samples. The project was financed by theCoordinacion General de Posgrado e Investigacion of the

Instituto Politecnico Nacional (CGPI-20060101 ‘‘Ecologıa despecies bentonicas de arrecifes rocosos de Baja California:Reclutamiento’’) and CIBNOR-NSF (‘‘Linking human andbiophysical processes in coastal marine ecosystems of Baja

California’’).

LITERATURE CITED

Avendano, M., M. Cantillanez, A. Olivares &M. Oliva. 1997. Conducta

reproductiva de Thais chocolata (Duclos, 1832) (Gastropoda: Thai-

didae) en LaRinconada. Antofagasta, Chile: causal de vulnerabilidad

a la pesca. Revista de Biologıa Marina y Oceanografia. 2:177–187.

Baqueiro, C. E., J. A. Masso R. & A. Velez. 1983. Crecimiento y

reproduccion de una poblacion de caracol chino Hexaplex eryth-

rostomus (Swain. 1831) de Bahıa Concepcion, B.C.S. Ciencia

Pesquera. Inst. Nal. Pesca. Sria. Pesca. Mexico. 4:19–31.

Baqueiro, C., A. Aldana &G.Martınez. 2005. Gonad development and

reproductive pattern of the fighting conch Strombus pugilis (Linee,

1758) (Gastropoda, prosobranchia) from Campeche, Mexico. J.

Shellfish Res. 4:1127–1133.

Belmar-Perez, J. 1988. Biologıa Reproductiva y Aspectos Ecologicos de

Astraea undosa. Tesis Licenciatura. Escuela Nacional de Ciencias

Biologicas. Instituto Politecnico Nacional. Mexico.

Belmar-Perez, J., S. A. Guzman del Proo & I. Martınez-Morales. 1991.

Madurez gonadica y ciclo reproductor del caracol panocha (Astrea

undosa Wood, 1828; Gastropoda: Turbinidae) en Bahıa Tortugas,

B.C.S. An. Inst. Cienc. delMar y Limnol.Univ. Nal. Auton.Mexico.

2:169–187.

Brazao, S., D. Boaventura, S. Morais, L. Narciso & P. Re. 2003.

Reproduction of Patella depressa Pennant, 1777 on the central

Portuguese coast. Bol. Inst. Esp. Oceanogr. 19:453–460.

Cronin, M. A., A. A. Myers & R. M. O’Riordan. 2000. The reproduc-

tive cycle of the intertidal Gastropod Melarhaphe neritoides on the

west and south coasts of Ireland. Biology and environment. Proc. R.

Ir. Acad. [B] 2:96–106.

Dinamani, P. 1974. Reproductive cycle and gonadial changes in the

New Zealand rock oyster Crassostrea glomerata. N.Z. J. Mar.

Freshw. Res. 1:39–65.

Fretter, V. & A. Graham. 1962. British prosobranch molluscs. Their

functional anatomy and ecology. London: Ray Society.

Gimin, R. & C. L. Lee. 1997. The reproductive cycle ofTrochus niloticus

in King Sound, Western Australia. In: C. L. Lee & P. W. Lynch,

editors. Trochus: status, hatchery practice, and nutrition. Australian

Centre for International Agricultural Research. ACIAR Proceed-

ings.70. pp. 52–59.

Gimenez, J. & P. E. Penchaszadeh. 2002. Reproductive cycle of Zidona

dufresnei (Caenogastropoda: Volutidae) from the southwestern

Atlantic Ocean. Mar. Biol. 140:755–761.

Gonzalez, J. G. & M. Ortiz. 1986. Estudio sobre madurez, ındice

gonadal y fecundidad en el abulon negro Haliotis cracherodii

(Mollusca: Gasteropoda) a partir de muestras colectadas en la Isla

de Cedros, B.C. en Junio 1982. Inst. Nal. de Pesca. CRIP Ensenada

Doc. Tec. Inf. 1:54–72.

Guzman del Proo, S. A., S. R. Mille-Pagaza, R. Guadarrama-

Granados, S. De la Campa-De Guzman, J. Carrillo-Laguna,

A. Pereira-Corona, J. Belmar-Perez & M. de J. Parra-Alcocer.

1991. La comunidad bentonica de los bancos de abulon

(Haliotis spp. Mollusca: Gastropoda) en Bahıa Tortugas, Baja

California Sur, Mexico. An. Esc. Nac. Cienc. Biol. Mex. 36:27–59.

Guzman del Proo, S. A. 1994. Biologıa, Ecologıa y Dinamica de

Poblaciones del Abulon (Haliotis spp) de Baja California, Mexico.

Tesis Doctoral. Escuela Nacional de Ciencias Biologicas-Instituto

Politecnico Nacional. Mexico.

Guzman del Proo, S. A., T. Reynoso-Granados, P. Monsalvo-Spencer

& E. Serviere-Zaragoza. 2006. Larval and early juvenile develop-

ment in Tegula funebralis (Adams, 1855) (Gastropoda: Trochidae)

in Baja California Sur, Mexico. Veliger 2:116–120.

Hewatt, W. G. 1934. Ecological studies on selected marine intertidal

communities of Monterrey Bay. Ph.D. dissertation Stanford Uni-

versity. Stanford, California.

Jaramillo, R. & O. Garrido. 1990. Ciclo reproductivo de Chorus

giganteus (Gastropoda: Muricidae) en la Bahıa de Corral, Valdivia.

Biologıa Pesquera. 19:49–53.

Kulikova, V. A. & V. A. Omel’yanenko. 2000. Reproduction and

larval development of the gastropod mollusk Tegula rustica in Peter

the Great Bay, Sea of Japan. Russian J. Mar.Biol. Rusia 2:128–130.

Litaay, M. & S. S. De Silva. 2003. Spawning season, fecundity and

proximate composition of the gonads of wild-caught blacklip

abalone (Haliotis rubra) from Port Fairy waters, southeastern

Australia. Aquat. Living Resour. 16:353–361.

Lee, J. H. 2001. Gonadal development and reproductive cycle of the top

shell, Omphalius rusticus (Gastropoda: Trochidae). Korean J. Biol.

Sci. 5:37–44.

Moran, A. L. 1997. Spawning and larval development of the black

turban snail Tegula funebralis (Prosobranchia: Trochidae). Mar.

Biol. 128:107–114.

Naegel, L. C. A. & F. A. Garcıa-Dominguez. 2006. Reproductive cycle

of the purple snailPlicopura pansa (Gould, 1853) from two locations

at Baja California Sur, Mexico. J. Shellfish Res. 3:925–933.

Padilla, B. T. 2004. Estudio Histologico de la Gonada de Megathura

crenulata, Tegula eiseni, T. aureotincta y T. regina (Mollusca

gasteropodo) de Bahıa Tortugas B.C.S. Tesis de Licenciatura.

Escuela Nacional de Ciencias Biologicas-Instituto Politecnico

Nacional. Mexico.

Paine, R. T. 1969. The Pisaster-Tegula interaction: prey patches,

predator food preference, and intertidal community structure.

Ecology 6:950–961.

Ponce, D. G. 2004. Efectos de la mortalidad por pesca y la variabilidad

climatica en la pesquerıa del abulon. Tesis doctoral. Centro Inter-

disciplinario de Ciencias Marinas-Instituto Politecnico Nacional.

Mexico.

Rocha-Barreira, C. A. 2002. Gonad characterization and reproductive

cycle ofCollisella subrugosa (Origy, 1864) (Gasteropoda: Acmeidae)

in the Northeastern Brazil. Braz. J. Biol. 62:885–895.

Sevilla, M. 1971. Desarrollo gonadico del abulon azul Haliotis fulgens

Phillippi. Rev. Soc. Mex. Hist. Nat. XXXII:129–139.

Veliz, D. & J. Vasquez. 2000. La familia Trochidae (Mollusca: Gastro-

poda) en el norte de Chile: consideraciones ecologicas y taxono-

micas. Rev. Chil. Hist. Nat. 4:757–769.

Young, J. S. & J.D. De Martini. 1970. The reproductive cycle, gonadal

histology, and gametogenesis of the red abalone Haliotis rufescens

(Swainson). Calif. Fish Game 4:298–309.

Wilson, W. G., C. W. Osenberg, R. J. Schmitt & R. M. Nisbet. 1999.

Complementary foraging behaviors allow coexistence of two con-

sumers. Ecology 7:2358–2372.

Zetina, Z. A, D. Aldana, T. Brule & E. Baqueiro. 2000. Ciclo

reproductor e ındice de condicion usados en Melongena corona

(Mollusca: Gasteropoda). Rev. Biol. Trop. (supl. 48)1:77–86.

VELEZ-ARELLANO ET AL.580