BULLETIN OF MARINE SCIENCE. 59(3): 490-497. 1996

AGE AND GROWTH OF ASTRAEA UNDOSA WOOD (: ) IN BAJA CALIFORNIA, MEXICO

Fabio German Cupul-Magaiia and Guillermo Torres-Moye

ABSTRACT Although the marine gastropod Astraea undosa is becoming an important fishery resource in Baja California, limited data are available on its growth. We verified formation of the annual opercular growth rings and compared the age-growth relationship for both sexes of a natural population in Todos Santos Bay. The hialine (low growth) ring was formed during spring-summer and the opaque (high growth) ring during autumn-winter. Growth patterns differed among sexes, the males having higher growth.

The marine gastropod Astraea undosa is becoming an important fishery re- source on the Pacific coast of Baja California, Mexico. There is little published literature on individual growth of this gastropod or other related . The work of Schwalm (1973) on Point Lorna, San Diego, California on A. undosa, and Guanes and Torres (1991) in Todos Santos Bay, Baja California, Mexico on A. turbanica, appear to be the only studies on growth of the genus Astraea. The available information for A. undosa is with reference to the habitat in which it is found (McLean, 1962; Bishop and Bishop, 1973), opercular mineralogy and biochemistry (Adegoke, 1973), food preference and stomach content analysis (Leighton, 1966; Aguilar et aI., 1990), predation (Schmitt, 1981) and population dynamics and energetics (Schwalm, 1973). The study of opercular marks has been a useful technique to determine the individual growth rate of gastropods (Kubo and Kondo, 1953; Miranda, 1975; Sire and Bonnet, 1984; Santarelli and Gros, 1985; Kraeuter et aI., 1989; Guanes and Torres, 1991). However, not always do the authors verify the periodical for- mation of the growth rings and such omission can result in serious underestimates of ages, which its important to understand the biology and stock dynamics (Gef- fen, 1987). This present study reports data on growth of A. undosa in Baja California, Mexico. We verify the periodical formation of opercular growth marks and use them to determine and compare the individual growth patterns of males and fe- males.

METHODS AND MATERIALS

The study site was the semiexposed rocky sublittoral flat of Punta Banda, located on the south- western side of Todos Santos Bay (Fig. 1). Monthly sampling was carried out with Scuba gear from May 1987 to June 1988 except for the month of August 1987. On each sampling date, samples were obtained at depths between 2 and 6 m on areas of approximate 12 m2, collecting all the individuals of A. undosa present regardless of their size until a sample of approximately 30 organisms was reached. The were transported alive to the Marine Science Faculty laboratory, in Ensenada, Baja California, Mexico where the shells were measured, sex was determined and operculi were extracted. The longest diameter of the shell's base (Fig. 2) was the size estimated for each individual, consid- ering this a practical measurement that has recently been considered for fishing regulations. All shell and opercular measurements were done with a vernier caliper to the nearest 0.01 mm. Snails were sacrificed to determine their sex, based on the color of the gonads observed under the stereoscopic microscope. Operculi were separated from the foot, and their length were measured with vernier caliper. Func-

490 CUPUL-MAGANA AND TORRES-MOYE: AGE AND GROWTH OF ASTRAEA UNDOSA 491

II !l0'

31°50'

~ TODOS SANTOS TODOS SANTO~ BAY ISLANDS ~

Figure 1. Study area and sampling station a in the Todos Santos Bay, Ensenada, Mexico.

tional regressions (Ricker, 1973) were calculated to relate the opercular length and longest shell di- ameter. Operculi were polished on the internal side with grinding paper discs of 600, 450 and 240 grit (Kennish et aI., 1980), to remove the periostracum and to make growth rings clearer. Operculi were exposed to transmitted optic fiber light and observed with the aid of a stereoscopic microscope. The opercular rings (Fig. 3) corresponded to slow zones (narrow hialine rings) and rapid growth zones (wide opaque rings). To confirm the annual ring formation within the operculum, we made monthly estimations of the Marginal Increment (M.I.) calculated as follows: M.I. = Ro - rn, where M.I. is Marginal Increment in mm, Ro is operculum length in mm and rn is distance to the most recently formed hialine ring in mm. Monthly mean values for the M.I. and their 95% confidence interval were estimated with a "t" distribution (Sokal and Rohlf, 1979), and multiple comparisons were obtained to test the significance 492 BULLETIN OF MARINE SCIENCE. VOL. 59. NO.3. 1996

a) b)

B L.D.S.B

Figure 2. Astraea undosa. a) maximum height and b) longest diameter of the shell base.

of the monthly mean differences using a Bonferroni method with 0: = 0.05 and k = 78 (0: = level of significance, k = number of comparisons) (Martin-Andres and Luna del Castillo, 1992) after normality and variance homogenity of data were verified. Once the annual ring formation was confirmed, the back calculation method (Chugunova, 1963; Bagenal, 1978) was used to estimate each year's opercular length by measuring the width of each hialine growth ring. Considering the mean opercular length for each year class and using the functional regression equations, we estimated the year class of each mean shell diameter size. Finally, following Kimura (1980) we estimated the parameters of the von Bertalanffy's growth model to describe and compare the growth patterns of both sexes.

RESULTS The total sample size of gastropods was 384, of which 201 were males and 183 females. The functional regressions and R2 values for opercular length and shell size are given on Table 1. The regression equation parameters were the same for both sexes, and hight R2 values suggest an evident proportionality among the measured variables. The M.l. monthly mean values are presented in Figure 4. Lower values were obtained from May to September 1987 and from April to June 1988, and higher

rn rn-l rn-2

rn-3

rn-4

rn-5

rn-6

Figure 3. Astraea undosa. Diagramatic representation of opercular growth rings: hialine (slow growth) and opaque (rapid growth) rings. CUPUL-MAGANA AND TORRES-MOYE: AGE AND GROWTH OF ASTRAEA UNDOSA 493

Table I. Functional regression equation and R2 values for the operculum length and the longest diameter of the shell's base from male, female and both sexes

R' Sex Equation Determination coefficient

Male Y = log-J(0.526 + 0.904 logX) 0.936 Female Y = log-J(0.526 + 0.905 logX) 0.927 Both Y = log-J(0.555 + 0.833 logX) 0.934 values appeared from October 1987 to March 1988. Significant (95% confidence) differences were found between low and high growth months (Table 2). Table 3 shows the opercular mean lengths for each year class of both sexes with the corresponding 95% confidence interval (C.r.). The general non-overlap- ping c.r. values between successive year classes for males and females, indicate their clear differentiation and the low c.r. values suggest a low variation in in- dividual growth. Growth curves of males and females and their von Bertalanffy's equations are shown on Figure 5. Patterns differed with consistently higher growth by the males. The age structure of the total sampled population (Fig. 6) was dominated by snails 4 to 10 years of age. Those outside this age spectrum were rare, presenting less than 10% frequency values. A clear domination by males existed for age classes 3 to 6, followed by a female domination on ages 7 to 10. The global sex proportion (male: female) was 1.0:0.91.

DISCUSSION A. undosa presented two different growing periods during our one year study. A slow growth period (low M.r. values) and hialine formation, ocurred mainly during the spring and summer months. The high growth period in which the opaque ring was formed, ocurred during the autumn and winter months. Such growth differences appear to be caused by gastropod's its reproductive cycle. During our study period, A. undosa presented three different reproductive phases;

82.5e -.•.. ~ 2 e f Col 1.5 .5 '; c '6iJ l. C':l ~ 0.5

o MAY .u.I JUL AUG SEP OCT NOV DEC JAN FEB MAR APR MAY JUN 87 88 Months Figure 4. Marginal increments, monthly mean values. 494 BULLETIN OF MARINE SCIENCE, VOL. 59. NO.3. 1996

0; =o 00 tl: .••..00 '2 •....• .~ o'" c:: II Z ..c =o 8 00 B ~ I zz ..c:: o =8 00 8 00 ClClCl o S; {/H/HIl ..= •..•~ ~

r- ~lzzzSlSlz

r- ~lzzzzSl~z

r- ~IZZZZZ~~~

r-

{f.)~ I ~zzzSl~zzz

r- ~ I I I I I I I I I I I

r- ~ I zz I ZZZZZZ~ZZZ CUPUL-MAGANA AND TORRES-MOYE: AGE AND GROWTH OF ASTRAEA UNDOSA 495

Table 3. Average opercular length at various ages of male and female of Astraea undosa; SD: standard deviation; C.I.: 95% confidence interval

Male Female

Age Mean length SD C.I. Mean length SD C.l. (years) (mm) (mm) (mm) (mm) (mm) (mm) 0+ 3.51 0.41 3.44-3.63 3.13 0.10 3.08-3.17 1+ 6.17 0.31 6.10-6.23 5.22 0.20 5.16-5.27 2+ 9.21 0.31 9.15-9.26 8.45 0.56 8.37-8.52 3+ 13.01 0.41 12.94-13.07 11.49 0.15 11.45-11.52 4+ 17.95 0.41 17.88-18.01 14.15 0.31 14.10-14.19 5+ 21.36 0.10 21.35-21.38 17.38 0.15 17.34-17.41 6+ 23.65 0.20 23.60-23.69 19.09 0.15 19.05-19.12 7+ 25.93 0.15 25.87-25.98 20.99 0.20 20.95-21.02 8+ 27.45 0.15 27.37-27.52 23.46 0.15 23.42-23.49 9+ 28.97 0.10 28.92-29.01 26.69 0.41 26.61-26.76 10+ 30.68 0.15 30.60-30.75 30.87 0.36 30.71-31.02 11+ 33.15 0.10 33.06-33.26 33.63 0.10 33.36-33.69 12+ 35.43 0.10 34.51-36.34 35.81 0.25 33.51-38.10 a maturing period (May-July 1987) which ended with a spawning in September and followed by sexually inmature condition (October-March 1988) and another maturation period from April to June 1988 (Almanza and Almanza, 1988). Other studies on opercular or shell ring formation report that most growth occurs during the warmer months of the year (Wefer and Killingley, 1980; Wil- liamson and Kendall, 1981; Santarelli and Gros, 1985; Kraeuter et aI., 1989). This was not the case for A. undosa, in which it appears that once having reproduced, their metabolic energy is directed principall to somatic growth during the colder months (October-March), and the rest of the time to gonad development and

Lt (en = 103.43 (l_e

!ll

80 :S"

30 • Male :: Female 20

10 6 10 11 12 Age (years)

Figure 5. Astraea undosa. Comparison of growth curves (Longest diameter of the shell versus age) for males and females in Todos Santos Bay, Ensenada, Mexico. 496 BULLETIN OF MARINE SCIENCE, VOL. 59. NO.3, 1996

40

N ~ 384 35l

30 Females 183 ,-., • Males 201 ~ 25 '-"" ~ <.l 20 =

o 0+ J+ 2+ 4+ 5+ 6+ 7+ lO+- 11+ 12+

Age (years)

Figure 6. Astraea undosa. Population age structure by sexes. reproduction. A similar relationship between reproductive and somatic growth processes has been reported for Mya arenaria (Brousseau and Baglivo, 1987). Schwalm (1973) proposed an energetic model for A. undosa and suggested a lower growth for females based on a higher energy requirement for gonadal de- velopment. Our results agree with his prediction. Sexual differences in growth rate should be considered for fisheries administration purposes in order to avoid the over or underestimation the age. The size-selective fishery, in which divers prefer to capture the biggest indi- viduals, may have produced the global sex proportion differences (Fig. 6), reduc- ing the proportion of males in older individuals. A. undosa is one of the largest comercial gastropods found in Todos Santos Bay. Its relatively high growth rate could be an ecological advantage by increasing fecundity and reducing predation (Schwalm, 1973). His condition also promotes interest in fishing purposes and requires the implementation of fishing regulations based on biological information such as the growth data obtained in this study.

ACKNOWLEDGMENTS

The authors would like to thank all the individuals of the Group of Basic Studies Applied to Fisheries of the Facultad de Ciencias Marinas that have contributed to this effort over the past years, and to two annonymous reviewers for their valuable suggestions. This contribution was supported by the Secretarfa de Educaci6n PUblica (Projects C87-01-0l36 and C88-01-0077).

LITERATURE CITED

Adegoke, O. S. 1973. Mineralogy and biogeochemistry of calcareous operculi and shells of some gastropods. Malacologia, 14: 39-46. Aguilar, R. R., G. Torres and A. Almanza. 1990, Qualitative analysis of the macroalgal diet of the snail Astraea undosa Wood 1828, in Punta Banda, Baja California, Mexico. Cien. Mar., 16(4): Ill-l20. Almanza, E. and A. Almanza. 1988. Perfodo reproductivo del caracol Astraea undosa en la Bahia de Todos Santos, B.C. Abstracts VII Simposium Internacional de Biologia Marina. 1-5 July 1988. La Paz, B.C.S., Mexico. 45 p. CUPUL-MAGANAANDTORRES-MOYE:AGEANDGROWTHOFASTRAEA UNDOSA 497

Bagenal, T. B. 1978. Methods for assessments of fish production in fresh water. IBP Handbook No. 3, Blackwell Scientific Publication, Oxford. 365 p. Bishop, M. J. and S. J. Bishop. 1973. A census of marine prosobranch gastropod at San Diego California. Veliger 16: 143-152. Brousseau, D. J. and J. A. Baglivo. 1987. A comparative study of age and growth in Mya arenaria (soft shell clam) from three populations in Long Island sound. J. Shellf. Res., 6: 17-24. Chugunova, N. 1. 1963. Age and growth studies in fish. National Sciences Foundation, Washington, D.C. 132 p. Geffen, A. J. 1987. Methods of validating daily increment deposition in otoliths of larval fish. Pages 223-240 in Summerfelt, R. and G. E. Hall, eds. Age and growth of fish. Iowa State University Press, Ames, Iowa. 550 p. Guanes, R. J. and G. Torres. 1991. Estudio de crecimiento del caracol Astraea turbanica Dall (Mol- lusca: Gastropoda) en Bahia de Todos Santos, B.C., Mexico. Rev. Inv. Cient. U.A.B.C.S. 2: 73-82. Kennish, M. J., R. A. Lutz and D. C. Rhoads. 1980. Preparation of acetate peels and fractured sections for observation of growth patterns within the bivalve shell. Pages 597-601 in Rhoads, D. C. and R. A. Lutz, eds. Skeletal growth of aquatic organisms. Plenum Press, New York. 750 p. Kimura, D. K. 1980. Likelihood methods for the von Bertalanffy growth curve. U. S. Fish. Bull. U.S. 77: 765-776. Kraeuter, J. N., M. Castagna and R. Bisker. 1989. Growth rate estimates for Busycon carica (Gmelin, 1791) in Virginia. J. Shellf. Res., 8: 219-225. Kubo, I. and K. Kondo. 1953. Age determination of the Babylonia japonica (Reeve) an edible marine gastropod, basing on the operculum. J. Tokyo Univ. Fish. 39: 199-207. Leighton, D. L. 1966. Food preference in algivorous invertebrates of southern California kelp beds. Pacif. Sci. 20: 104-113. Martfn-Andres, A. and J. de D. Luna del Castillo. 1992. Resumenes de Bioestadfstica. Ediciones Norma, S. A. Madrid, Espana. 53 p. McLean, J. H. 1962. Sublittoral ecology of kelp beds of the open coast area near Carmel, California. BioI. Bull. 20: 95-114. Miranda, O. 1975. Crecimiento y estructura poblacional de Thais (Stromanita) chocolata (Duclos, 1832), en la Bahfa de Mejillones del Sur, Chile (Mollusca; Gastropoda: Thaididae). Rev. BioI. Mar. 15: 263-286. Ricker, W. E. 1973. Linnear regressions in fishery research. J. Fish. Res. Board Can. 30: 409-434. Santarelli, L. and P. Gros. 1985. Determination de I'age et de la croissance de Buccinum undatum L. (Gasteropoda: Prosobranchia) a I'aide des isotopes stables de la coquille at de I'ornementation operculaire. Oceanol. Acta 8: 221-229. Schmitt, R. J. 1981. Contrasting anti-predator defences of sympatric marine gastropod (Family Tro- chidae). J. Exp. Mar. BioI. Ecol. 54: 251-263. Schwalm, C. C. 1973. Populations dynamics and energetics of Astraea undosa. Masters Thesis. California State University, San Diego. 113 p. Sire, J. Y. and P. Bonnet. 1984. Croissance et structure de I'opercule calcifie du gasteropode polynesien Turbo setosus (Prosobranchia: ): determination de l'age individuel. Mar. BioI. 79: 75-87. Sokal, R. R. and F. J. Rohlf. 1979. Biometrfa: principios y metodos estadfsticos en la investigaci6n biol6gica. Editorial Blume, Espana. 832 p. Wefer, G. and J. S. Killingley. 1980. Growth histories of strombid snails from bermuda recorded in their 0'8 and e13 profiles. Mar. BioI. 60: 129-135. Williamson, P. and M. A. Kendall. 1981. Population age structure and growth of the trochid Mono- donta lineata determined from shell rings. J. Mar. BioI. Assoc. U.K. 61: 1011-1026.

DATEACCEPTED: March 17, 1995.

ADDRESSES: (F.G.C.M.) Coordinacion de lnvestigacion, Centro Universitario de la Costa, Universi- dad de Guadalajara, Av. Libramiento esq. prolongaci6n Bolivia 1900, Col. Laz.aro Cardenas, c.P. 48330, Puerto Val/arta, Jalisco, Mexico; (G.T.M.) Facultad de Ciencias Marinas, Universidad Au- t6noma de Baja California, P.O. Box #453, Ensenada, Baja California, Mexico.