ELSEVIERJournal of Experimental Marine Biology and Ecology,

212 (1997) 95-110

JOURNAL OFEXPERIMENTALMARINE BIOLOGYAND ECOLOGY

Larval growth and survival of two catarina scallop(Argopecten circularis, Sowerby, 1835) populations and their

reciprocal crosses

Pedro Cruz, Ana M. Ibarra*Centro de Investigaciones Biologicas del Noroeste (CIBNOR), Division de Bi%gia Marina. Programa de

Cultivos Marinos, Km. I Carr. San Juan de la Costa. E/ Comitan. A.P. 128, La Paz B.C.S., Mexico23 ()()()

Received 8 March 1996; revised 12 August 1996; accepted 17 September 1996

Abstract

Populations of catarina scallop are distributed along both coasts of the Baja CaliforniaPeninsula, Mexico. Those populations represent potentially different genetic resources foraquaculture, and the evaluation of their genetic and production characteristics is important. Todetermine those characteristics, intra- and intercrosses of two populations were produced and theirphenotypic response to growth and survival at the hatchery were compared, determining therelative magnitude of maternal effects and heterosis. There was a clear maternal effect forsurvival, evidenced by a difference between the reciprocal crosses. Larvae from the Magdalena(M) population and the reciprocal cross produced with those eggs had a higher survival (45.8%and 47.5%) than larvae from the Concepcion (C) population and its maternal reciprocal cross(32.5% and 28.9%). Average growth during the larval period indicated larvae derived from BahiaMagdalena spawners had a larger size (:!:half width confidence intervals) (166.8:!:7.9 /-lm) thanthose derived from Bahia Concepcion spawners (140.4:!:6.7 /-lm). Both reciprocal crosses(FI-paternal-maternal) larvae grew (160.1 :!:7.7 and 153.3:!:7.3 /-lm, FI-CM and FI-MC) as wellas the Magdalena larvae. When length was analyzed at age to determine the effects of egg originand mating strategy on growth, a significant maternal effect was revealed on the reciprocalcrosses' growth up to day II, which decreased by day 15, and disappeared by day 17. Thedissipation of maternal effects was coincident with the first appearance of a heterosis value by day15 (3.5%), increasing to day 17 (6.8%). The presence of maternal effects is explained because eggenergy reserves are different between the two populations despite the simultaneous conditioningfor 15 days for both groups of spawners prior to spawning induction. The importance of stockselection is emphasized not only for juvenile or adult phenotypic traits of artificially-producedprogeny, but also on the maternal quality of the spawners producing that progeny. © 1997Elsevier Science B.Y.

*Corresponding author. Fax: (+ 52-112)5-3625; e-mail: aibarra@cibnor.mx

0022-0981/97/$17.00 © 1997 Elsevier Science BV All rights reservedPll 50022-0981 (96)02742-6

96 P. Cru~, A.M. Ibarra / J. Exp. Mar. Bioi. Ecol. 212 (1997) 95-110

Keywords: Argopecten circa/aris; Heterosis; Larvae; Maternal; Populatiuns; Crosses

1. Introduction

Scallop culture worldwide is a recent activity, with technology developments forhatchery production dating from the 1970s (Castagna and Duggan, 1971; Gruffydd andBeaumont, 1972). In Baja California Sur, Mexico, there are two important areas forscallop production, using fisheries and aquaculture, Bahia Magdalena on the Pacific, andBahIa Concepcion on the Gulf of California (Fig. I). The most important species is the"catarina" scallop, Argopecten circularis (Sowerby, 1835), found in bays along bothcoasts. Since different populations are available, each might represent potentiallydifferent genetic resources. An early evaluation of their production characteristics in anaquaculture setting is important, especially when the technology to commerciallyproduce this scallop has been recently developed (Maeda and Ormart, 1995; Maeda etaI., 1995).

32°N~=====================~

Pacific Ocean

1N

220

1':-1-=-=7=0;--------------------::.;1..0,...9-;;;°W~

Fig. 1. Location of the two catarina scallop populations along the Baja California Peninsula, Mexico.

P. Cruz. A.M. Ibarra / J. Exp. Mar. Bioi. Ecol. 2/2 (/997) 95-//0 97

When different populations are available for artificial production of a species, theymust be evaluated to determine whether there are sufficient differences among themfavoring particular ones for production (Newkirk, 1980). Studies on mollusc specieshave already demonstrated that population differences for several phenotypic traits doexist (Dickie et aI., 1984; Kraeuter et aI., 1984; Hawes et al., 1990; Martinez andDiMichele, 1992; Mackie and Ansell, 1993). When genetic improvement programs arebeing planned to increase growth in stocks subject to artificial production, thoseprograms should be based not only on the distinction of available stocks, but also on thegenetic characteristics of important production traits at different life stages during bothhatchery and field growth.

Larval growth traits generally provide minimum information on performance duringgrow-out stages (Newkirk, 1980; Heffernan et aI., 1992; Hilbish et aI., 1993). However,larval growth and survival are the most important traits during hatchery production anddefine the success of this early production stage. Several studies have demonstratedgenetic differences in larval growth and survival among populations of the Americanoyster Crassostrea virginica (Newkirk et aI., 1977; Newkirk, 1978; Mallet and Haley,1983, 1984), and the sea scallop Pecten maximus (Paulet et aI., 1988; Cochard andDevauchelle, 1993).

In addition to the recognition of population differences at these early stages, it isimportant to study growth performance in progenies derived from crossing differentpopulations, looking for the effects of both heterosis, because of the expected increasedheterozygosity of crosses, and maternal effects. There is a positive correlation in naturalpopulations of molluscs between heterozygosity and growth and fitness (Beaumont andZouros, 1991; Koehn, 1991; Gaffney, 1994). While those studies have been on naturalpopulations, the same correlation has not been thoroughly evaluated in hatchery­produced populations using crossbreeding (Gaffney, 1994). Crossbred progeny areexpected to manifest heterosis whenever there are differences in allele frequenciesbetween the two pure populations producing the crosses, provided the genes concernedwith that particular trait present the characteristic of directional dominance (Falconer,1989). Therefore, the presence of heterosis for growth or survival should be an indicatorof the same positive correlation between increased heterozygosity and growth or fitnessseen in natural populations.

Animal breeders have recognized there exists a "maternal effect", where the maternalphenotype influences the progeny phenotypes through both genetic and nongeneticfactors (Pirchner, 1983). For some mollusc species, egg size and reserves can beimportant factors for energy supply and for survival during the earliest stages ofdevelopment (Cragg and Crisp, 1991). The determination of maternal effects is animportant consideration when deciding on the best spawner stock to use in production.Indirect evidence for the existence of maternal effects and heterosis have been reportedfor larval growth and survival of several mollusc species (Mallet et aI., 1986; Stromgrenand Nielsen, 1989; Ludwig and Gaffney, 1991).

Surprisingly, most of the studies testing for the effects of crossbreeding in molluscshave been limited to grow-out stages, with no information provided about larvalperformance and its relationship to maternal effects and heterosis. Given the generalizedconclusion through heritability studies that maternal and dominance effects are important

98 P. era:. A.M. Iharra 11. Exp. Mar. BioI. Ecol. 212 (1997) 95-110

aspects of larval growth and survival, and the impact those effects can have on larvaeproduction in the hatcheries, it is important to determine the magnitude of each, todetermine which, maternal effects or heterosis, is the most important factor affectingearly life stages, and to be able to separate these from the environmental effect ofcommon rearing conditions. In the few studies approaching this problem, results haveindicated not only differences among populations at larval stages, but also from heterosisand maternal effects (Newkirk et aI., 1977; Newkirk, 1978; Mallet and Haley, 1983,1984).

We report here a study where growth and survival were compared for two stocks ofthe catarina scallop, as well as for their reciprocal crosses. The objective was todetermine population differences, maternal effects, and heterosis at larval stages, byproducing intra- and intercrosses of the two populations, and by rearing them under thesame artificial conditions.

2. Material and methods

2.1. Study sites

The two catarina scallop populations evaluated were from different environments,Bahia Concepcion and Bahia Magdalena (Fig. 1). Bahia Concepcion, on the Gulf ofCalifornia, has low productivity (chlorophyll a 0.38 to 1.63 mg m-3) and is a morestressful environment because of a higher average annual temperature (24.9°C) and itswide range (17.7 to 32.1 °C) (Reyes-Salinas, 1994). Bahia Magdalena, on the Pacific, hasan average temperature of noc with a smaller range (20 to 26.6°C) (Hernandez-Rivas etaI., 1993), and a higher chlorophyll a concentration (1.5-5.1 mg m - 3) (Acosta-Ruiz andLara-Lara, 1978). The spawning season at Bahia Concepcion is January to Februarywhen the water temperatures are between 16 to noc (Villalejo-Fuerte and Ochoa-Baez,1993), and March to May at Bahia Magdalena when water temperatures are around 17to 20°C (Felix-Pico, 1993).

2.2. Spawners and conditioning

Sixty scallops selected for their maturity (between stages III and IV in the Ref. Sastry,1963 scale), were collected from each of the two populations and transported to thegenetics laboratory of CIBNOR at La Paz. Conditioning consisted of feeding eachspawner a food ration of 3.5 X 106 cells of a I: I ratio of Isochrysis galbana andChaetoceros muelleri daily. Water temperature and salinity were 21°C (:tIOC) and 38ppt (:t I ppt). Water was exchanged daily and feces removed by siphoning them from thebottom of each 45 I container.

Approximately fifteen days after conditioning began, the breeders of both populationsreached ripeness (stage IV) under the visual scale of Sastry (1963).

2.3. Spawning

P. Cruz. A.M. Ibarra / J. Exp. Mar. Bioi. Ecol. 212 (1997) 95-110 99

Thirty-two individuals from each population were selected for spawning. The meanlength, measured with calipers, of the Magdalena spawners was 54.25 mm (:to.76 SE)and those from Concepcion were 54.41 mm (:to.77 SE). To induce spawning, eachorganism was injected with 0.2 ml of 0.5 mM serotonin (5-hydroxytryptamine) into theabductor muscle. To prevent polyspermy caused by the large amount of sperm releasedin a limited volume tank, groups of eight organisms were first placed in 40 I tanks toallow for the partial release of sperm, and then transferred to the spawning tanks (1500 Itanks). Four groups that consisted of the following intra- and intercrosses were formed:the two parental populations Magdalena (M) and Concepcion (C) and their reciprocalcrosses, FI-CM and FI-MC (FI-paternal-maternal). Because this species is a hermap­hrodite, to reduce the probability of self-fertilization each individual was allowed torelease the sperm in one tank and the eggs in another. Therefore, for each mating andreciprocal cross we used two tanks, placing eight individuals per tank (N, = 16individuals/genetic group). For the reciprocal crosses, sixteen breeders from eachpopulation were used, placing the organisms from the Magdalena population in twotanks and the organisms from the Concepcion population in two other tanks. Once eachof those groups had finished releasing sperm, the scallops were reciprocally exchangedbetween tanks, thereby performing reciprocal crosses (FI-CM and FI-MC). Theresulting offspring are related (full- or half-sibs) but with one factor differentiating them;the origin of the egg is from either the Magdalena or the Concepcion populations. Watertemperature and salinity during spawning were 20°C and 38 ppt.

2.4. Larvae rearing

Thirty six hours after fertilization, when the "0" larvae can be handled, each tankwas individually drained through a 30 f.Lm sieve. The larvae collected from each tankwere placed in 15 I buckets with sea water and counted by using the average of triplicatesamples of 0.5 m!. The numbers were then extrapolated to total volume. After this, thelarvae from the two tanks containing the same genetic group were mixed in equalproportions. The experiment was started with approximately 24000 larvae per geneticgroup, divided into three conical 80 I rearing tanks (8000 larvae/tank), at an initialstocking density of 10 larvae ml- 1

• Maintenance during larval culture consisted ofexchanging 100% of the water every other day (preventive methods to avoid the transferof larvae from tank to tank during maintenance are described in Ref. Ibarra et aI., 1995).Water temperature and salinity were noc and 38 ppt. Feeding consisted of adding amixture of lsochrysis galbana and Chaetoceros muelleri (I: I) at an increasing rationaccording to larval development: for days 2 to 6, 7 to 13, and 14 to I7 the rationincreased from 30 000 to 60 000, and then to 100 000 cells ml- I .

2.5. Experimental design and sampling

The experimental units were the 80 I tanks. For each genetic group, we establishedthree replicates randomly distributed among the experimental units following the

100 P. Cruz. A.M. Ibarra I J. Etp. Mar. Bioi. Ecol. 212 (1997) 95-110

procedures of Ref. Neter et al. (1985). For growth evaluations, samples were taken fromeach replicate on days 7, II, 15, and 17 and preserved with 4% formaldehyde solution.For each replicate, length (anteroposterior shell distance) was measured on 30 larvaewith a stage micrometer. Survival at day 17 was estimated by counting the survivinglarvae in each tank, using triplicate aliquots of 1.5 ml and extrapolating to total holdingvolume.

2.6. Statistical analyses

2.6.1. GrowthGrowth differences among the genetic groups for the complete larval period were

evaluated using analysis of variance. Lengths were converted to logarithms to increasenormality and homoscedasticity (Neter et aI., 1985). The following model of crossed­nested effects was used:

where Y;jkm = length of the m larvae in the k replicate within the j genetic group, at age i;u=overall constant; Ai=age effect (fixed) on length (i= 1,2,3,4); Gj=genetic group(fixed) effect on length (j = 1,2,3,4); RGk(j) = replicate (random) effect (k = 1,2,3) withingenetic groups; A,XGJ=interaction term between age and genetic group; A,XRGk(j)=

random age-replicate interaction effects within experimental groups; and emlUk ) =

random observation error (m = 1,... , 30). Fixed effects means were compared with aTukey test, setting Cl' = 0.05.

2.6.2. SurvivalPercent survival values were transformed to angular values to stabilize the variances

of the errors (Rohlf and Sokal, 1981). Differences in survival among the genetic groupswere analyzed with a one factor analysis of variance model. Survival means in angularvalues were compared with a multiple comparison test (Tukey method), definingconfidence intervals for each genetic group mean survival and back-transforming to thepercent value. All statistical analyses were done on a SAS System (Statistical AnalysesSoftware) and significance for all analyses was set to p <0.05.

2.6.3. Maternal effects and heterosisIn addition to possible heterotic effects because of the expected increased hetero­

zygosity in the crosses, a second effect from maternal differences was considered. Todetermine the significance of each of those effects on length and survival at day 17, weexamined the mean values of length (or survival) with a two factor analysis of variancemodel, testing for the effects of "egg origin" (Magdalena vs. Concepcion dams) and"mating strategy" (intra- vs. intercrosses), with the following model:

where Yijk = mean length (or percent survival value) of the k replicate from the i eggorigin and the j mating strategy; u = overall constant; EOi = egg origin effect on length

P. Cruz. A.M. Ibarra /1. Exp. Mar. Bioi. Ecol. 212 (/997) 95-110 IOl

(or survival) (i = 1,2); MSJ

= mating strategy effect on length (or survival) (j = 1,2);(EOXMS);j=interaction effect between egg origin and mating strategy; and eijk =random observation error (k= 1,2,3). Length means at age were compared with amultiple comparison test (Tukey method).

Additionally, maternal effects and heterosis were estimated at each age of sampling(7, 11, 15 and 17 days) for length, and at the end of the rearing period (day 17) forsurvival. The equation to determine heterosis was taken from Ref. Stufflebeam (1989):

Heterosis% = [(FI - P) X lOO]IP

where, P = average of both parental populations; F 1 = average of the reciprocal crosses.An equation to compare maternal performance was taken from Ref. Van Vleck et al.

(1987), where the maternal effect from each population is given by:

ME(X) = FI(-X) - P - (Heterosis X P)

where, ME(X)=maternal effect from population X; F1(-X)=mean length (or survival)for the reciprocal cross produced with the eggs from population X; and P as before.

A maternal performance comparison (MPC) at each age (i=7, II, 15, and 17 days)was then estimated from:

3. Results

3.1. Length

Table la contains the results of the complete larval-growth model. Both main effects(age and genetic group) and their interaction were significant (p < 0.05). There were no

Table 1Analysis of variance for the global model of growth and survival

Source D.F. M.S. P

(a) LengthAge 3 3.9407 0.0001*Genetic group 3 0.3686 0.0011*Replicate (Gen. group)' 8 0.0236 0.0525Age XGenetic group 9 0.0271 0.0267*Age Xreplicate (Gen. group)' 24 0.0102 0.1787Error 1392 0.0081

(bJ SurvivalGenetic group 3 92.4343 0.0020*Error

,8 7.2392

Mean square (M.S.), degree freedom (D.F.) and values of P., Random effects. * Indicates the effect is significant at the established level.

102 P. Cruz, A.M. Ibarra / J. Exp. Mar. Bioi. Ecol. 2i2 (1997) 95-/10

replicate effects within genetic groups nor interaction effects between age and replicatewithin a genetic group. Age had an effect in agreement with the expected increase inmean larval length(::t::half width confidence intervals); 113.23(::t::3.56) /-Lm at day 7,145.56(::t::4.58) /-Lm at day II, l80.99(::t::5.69) /-Lm at day 15 and 192.78(::t::6.06) /-Lm atday 17. Additionally, the significance of the age and genetic group interaction effectindicated a different growth rate was present among genetic groups (Fig. 2). There wereno significant differences in the average during the larval culture among the BahiaMagdalena larvae (I66.79::t::7.99 /-Lm), and the reciprocal crosses (l60.l3::t::7.68 /-Lm and153.32::t::7.35 /-Lm for the Fl-CM and Fl-MC). Larvae from Bahia Concepcion were thesmallest (l40.44::t::6.73 /-Lm) among all groups, being significantly different from BahiaMagdalena larvae and the reciprocal crosses.

3.2. Survival

The analysis of survival at day 17 indicated differences among the genetic groups forthis trait as well (Table Ib). The larvae from the Magdalena population and thereciprocal cross with that maternal complement, Fl-CM, had the higher survival(45.83% and 47.49%), both being significantly different (Table 2a) from the Concepcionpopulation (32.49%) and the reciprocal cross with that maternal complement, FI-MC(28.88%).

-j .- -+ --+--- -r-- -r---,- i

:; :; 0 0 :; :; 0 0 :; :; 0 00 :; 0 :; 0 :;u:: u:: u:: u:: u:: u::

11 d 15 d 17d7d

230

220 ­

210 •

200 ­

190 ­

180

E 170

-=160=~ 150 -~ 140 •

130 ­

120

110 ­

100

90

80 ,

Genetic groups by age

Fig. 2. Growth of the four genetic groups during the larvae culture. M = Magdalena population larvae;C = Concepcion population larvae; Fl-MC = reciprocal cross Magdalena-Concepcion; FI-CM = reciprocalcross Concepcion-Magdalena, where FI-patemal-matemal.

P. Cruz. A.M. Ibarra I J. Exp. Mar. Bioi. Ecol. 212 (/997) 95-1/0 103

Table 2(a) Percent survival means I (%) and their confidence intervals (C\). (b) Heterosis and maternal performance

comparison (MPC) for the genetic groups at age 17 days (FI-maternal-paternall

Genetic group

(a)

MagdalenaFI-CMFI-MCConcepcion

(b)

HeterosisMPC

% Survival (CI)

45.83 (39.65 to 52.08)"47.49 (41.28 to 53.74)"28.88 (23.39 to 34.69)"32.49 (26.78 to 38.46)"

o18.61

I Means with the same letter are not statistically different (p > 0.05).

3.3. Maternal effects and heterosis

In addition to the population differences observed, the effect each of those populationshad on the reciprocal crosses' performance was highly significant because of the eggeach one contributed to the crosses. This was indicated by the significance of the eggorigin factor for both traits evaluated, growth and survival (Table 3), by the maternal

Table 3

Analyses of variance considering egg origin and mating strategy effects for length at each age and survival atday 17

Source D.F. M.S. P

(a) LengthAge 7 dayEgg origin (EO) 0.003078 0.0434*Mating strategy (MS) 0.000050 0.7674EOXMS 0.000001 0.9598Age II dayEgg origin (EO) 0.008058 0.0021 *Mating strategy (MS) 0.000418 0.3401EOxMS 0.001503 0.0906Age 15 dayEgg origin (EO) 0.009694 0.0012*Mating strategy (MS) 0.000919 0.1712EOXMS 0.004667 0.0095*

Age 17 dayEgg origin (EO) 0.006466 0.0055*Mating strategy (MS) 0.002898 0.0356*EOxMS 0.007229 0.0040*

(b) SurvivalEgg origin (EO) 268.3991 0.0003*Mating strategy (MS) 1.2494 0.6887EoxMS 7.6544 0.3339

* Indicates the effect is significant at the established level.

104 P. Cruz. A.M. Ibarra I J. Exp. Mar. Bioi. £Col. 212 (1997) 95- JlO

Table 4(a) Geometric means I of genetic groups length at age. (b) Heterosis and maternal performance comparison(MPC) at age (FI-maternal-paternal)

Genetic Agegroup 7 day I I day IS day 17 day

(a)Magdalena 117.0J" 160.73' 198.15" 207.63"FI-CM 117.95" 148.56"" 188.41" 199.20"FI-MC 109.75" 138.80" 181.01 ' 200.40'Concepcion 108.54" 135.46" 158.78" 166.65'

(b)Heterosis 0.94 0 3.50 6.77MPC 8.20 9.76 7.40 -1.20

I Within each column, means with the same letter are not statistically different (p>0.05).

performance comparison (MPC) estimated for survival at day 17 (Table 2b), and forlength at each age (Table 4b). However, while egg origin was the only significant effectwhen survival was considered, mating strategy also had an effect on length at older ages.Up to day II, the eggs from Bahia Magdalena individuals produced larger larvae thanthe eggs from Bahia Concepcion individuals, regardless of whether they were crosses orpure populations (Table 4a). However, by day 15, the presence of a significantinteraction between egg origin and mating strategy (Table 3a) indicated length was notdependent on egg origin any longer and mating strategy was becoming a significantfactor affecting larval growth. By day 15 and up to day 17, the reciprocal crosses' meanwas larger than the mean population value (Fig. 3). These results agreed well with boththe estimated heterosis for length and the MPC along the rearing days. Though the MPCindicated a large advantage in length for the reciprocal cross produced with Magdalenaeggs (Fl-CM) up to day 15, heterosis estimates by that same day were the firstpractically different from zero, indicating an advantage of an increased heterozygositydue to mating strategy. By day 17, the MPC indicated maternal effects were no longerpresent, evidenced by the reciprocal crosses having the same mean length, whereasheterosis for length had increased (Table 4b).

4. Discussion

4. J. Populations

Our results on two phenotypic traits, larval growth and survival, clearly indicate agenetic differentiation between the two catarina scallop populations evaluated simul­taneously and under the same environmental conditions. From day 11 and to day 17,there were significant length differences, as well as survival differences at the end of therearing period, between the larvae from Bahia Magdalena and Bahia Concepcion. Thisresults were not unexpected, because these two populations are geographically isolatedby a land barrier, the Baja California Peninsula (Fig. I). Reproductive isolation resulting

P. Cruz. A.M. Ibarra / 1. Exp. Mar. Bioi. £Col. 2/2 (/997) 95- //0

220 -r-------------------,

105

- -0 15 d

____ 017d

210

200

190

180

170-E::::L 160-.c:-C) 150cCI)

...J

140

130

120

110

100

90

o .. .. ..11d

7d

MEgg origin

c

Fig. 3. Interaction effects of egg origin (M and C) and mating strategy on length at age. Populations:continuous line. Reciprocal crosses: dotted line.

from a barrier between populations can result in genetic differentiation as a consequenceof natural selection, adaptation to environmental conditions, and genetic drift (Avise,1980).

4.2. Maternal effects

Additionally, and for both traits, length and survival, each of the reciprocal crossesresembled more the population contributing the egg. In fact, the effect of the egg origin

106 P. Cruz. A.M. Ibarra / J. Exp. Mar. Bioi. Ecof. 2/2 (/997) 95-110

resulted in a significant maternal effect on total survival evaluated at day 17, and onlength up to days II and 15. Newkirk et al. (1977) recognized a significant maternaleffect on larval survival up to day 6 when comparing two populations of the Americanoyster and their reciprocal crosses, although the effect had dissipated when survival wasevaluated between days 6 to 16. Because our sampling design for estimating survivalwas delayed to the end of the rearing period, we can not eliminate the possibility thatmost of the mortalities occurred early in the rearing period as in Ref. Newkirk et al.(1977).

The maternal environment is known to cause maternal effects, which for the most partare produced by both genotype and nongenetic factors of female breeders (dams)(Pirchner, 1983). In this particular case, the observed maternal effects may be explainedby considering the potential effect the energy reserves contained in the eggs derivedfrom each of the two populations have over the initial nutrient supply for development.The accumulation of these energy reserves is a function of female genetic background(i.e. metabolic efficiency), nutrition, and other environmental conditions during sexualmaturation in each of their environments (Barber and Blake, 1991). For mollusc species,the amount of energy reserves in the form of lipids has been shown to be a strongdeterminant of success of early stages of larval development (Cragg and Crisp, 1991). InRef. Newkirk et al. (1977), the observed maternal effects might have been "induced"because of unequal treatment of breeders before spawning when the breeders of onepopulation were left to develop gonads under natural conditions and the others held inthe laboratory. In our case, both populations were transported at the same time to thelaboratory and held in the same environment and using an identical food supply duringthe fifteen days of conditioning. Although it is possible longer conditioning for theConcepcion population could have eliminated such differences, that would haveprecluded producing the reciprocal crosses. Therefore, our observed maternal effectscould be the result of either genetic or environmental differences in egg size between thetwo populations, or the result of egg quality effects because of different environmentalconditions at the site where the spawner's sexual maturation began. Although in thisstudy egg size was not determined, we have found when these two populations aregrown in Bahia Magdalena, there are no differences in egg size (per. obs.). Becausethese two populations are subjected to different environmental conditions during thetime of gonadal maturation, we suggest these environmental effects on each of thespawner populations and their final egg quality might be the main determinant for theobserved maternal effects. Supporting our conclusion are different studies, on Pectinidspecies, that have found a larger effect of environmental conditions on egg quality thanon egg size, and studies indicating no direct correlation between egg size and larvallength. For example, MacDonald and Thompson (1986) found that though unfavorableenvironmental conditions resulted in reduced rates of gamete development for Placopec­ten magellanicus, the diameter of the spawned eggs, as well as the timing of spawning,were apparently unaffected by poor conditions in the natural environment. Paulet et al.(1988) found, for two populations of Pecten maximus that had different egg diameters,the population with the larger eggs had the smaller pediveliger larval length atmetamorphosis, although a large egg size appeared to have an effect on reducing thetime required to reach metamorphosis. Also for Pecten maximus, no differences in

P. Cruz. A.M. Ibarra / J. Exp. Mar. Bioi. Ecol. 212 (/997) 95-110 107

oocyte diameter among four populations of Pecten maximus conditioned in thelaboratory were found, nor any differences in larval length up to day 16, althoughsignificant differences in pediveliger size were seen at day 23 (Cochard and De­vauchelle, 1993).

4.3. Heterosis

In addition to the maternal effects, our results indicated an advantage of increasedheterozygosity on the crosses, although this was not evident until late in the rearingperiod (day 15), when heterosis for length was observed and supported by the interactioneffect between egg origin and mating strategy. Heterotic effects for growth and survivalhave been seen in the American oyster by Newkirk (1978), where some of the crossesfrom four populations at the end of the rearing period performed better than the parentalpopulations, although the expression of heterosis depended on salinity, indicating thepresence of a genotype by environment interaction. Those agreed with the previousstudy by Newkirk et al. (1977), where heterosis for survival was observed in crossesfrom two populations, despite the initial maternal effect already discussed. Mallet andHaley (1983) evaluated different crosses from six populations, but their results on larvalperformance of crosses of the American oyster are difficult to explain, because theyreported an inverse tendency of heterosis for length along the culture days, finding therelatively superior performance of the crosses at day 2 was not maintained later.Unfortunately, in that research, the authors were unable to evaluate maternal effectsbecause the crosses were pooled together and there was no indication it was done inequal proportions. In a subsequent study, Mallet and Haley (1984) studied theimportance of each, heterosis and maternal effects, on the American oyster, findingimportant maternal effects for length and viability. When larval performance of crossesis evaluated, an a priori assumption of maternal effects should be considered in theexperimental design to distinguish between maternal effects and heterosis. In our case,we were able to differentiate between maternal effects and heterosis. Our results agreedwell with theoretical expectations of both characteristics, where maternal effects areexpected to have greatest impact on traits during the early stages of development, fadingat older ages, and sometimes balanced by compensatory growth (Pirchner, 1983) in oneof the reciprocal crosses. Concerning heterosis, it is interesting to see there was anagreement between these results and previously published results on inbreedingdepression for the same species (Ibarra et aI., 1995), where significant differencesamong genetic groups with different inbreeding coefficients were evident until theculture was advanced, at day II. Those results were explained because egg reserves arethe principal determinant for early growth and survival, but differences in metabolicefficiency among genetic groups with different degrees of heterozygosity at later larvalages are the main determinant on the expression of progressive differences in lengthamong genetic groups. In the present research, the mean length of the crosses was notdifferent from the populations mean until day 15, when the FI 's mean length was larger,indicating the expected heterozygosity advantage in the crosses was not evident on theirgrowth until late in the rearing period, and as indicated by the heterosis value for lengthat that age. Although the heterosis value calculated at this age (3.5%), and that

108 P. Cru;:. A.M. Iharra 11. Exp. Mar. Bioi. Em/. 2/2 (/997) 95-/10

calculated at the end of the larval rearing culture (6.77%), do not represent a usefulheterosis (Falconer, 1989) because neither of the crosses was superior to the bestpopulation (Magdalena), it indicates there is a growth advantage of the crosses withregard to the parental mean, which might be a reflection of an increased metabolicefficiency because of an expected larger heterozygosity in the crosses' genotype.

In conclusion, it was possible to distinguish between two geographically isolatedpopulations of Argopecten circularis based on two phenotypic traits, larvae length andsurvival. Although some length heterosis was evident by the end of the rearing period,the heterosis observed was not substantial and is probably not important in hatcheryproduction. These results stressed the importance of taking into consideration not onlypopulation responses in growth at different life stages, but also the maternal quality ofdams used for hatchery production.

Acknowledgments

The senior author of this research was partially supported by CONACYT andIPN-PIFI Fellowship programs. We thank MAZAVI Aquaculture Enterprise for thedonation of Bahia Concepcion spawners, and the Mexican Fisheries Ministry (SEMAR­NAP) for their scuba diving assistance (M. Romero) during the collection of BahiaMagdalena spawners. We also thank the valuable technical assistance of S. Avila, J.L.Ramirez and G.A. Garcia. In addition, we thank Dr. E. Glazier for editing this text.

References

Acosta-Ruiz. J. and J.R. Lara-Lara. 1978. Resultados !isico-quimicos en un estudio de variacion diurna en elarea central de Bahia Magdalena. B.e.S. Ciencias Marinas. Vol. 5. pp. 37-46.

Avise. le.. 1980. Diferenciacion genetica durante la especiacion. In. Evolucifin molecular. editado por FJ.Ayala. Omega. Barcelona. pp. 110-127.

Barber. BJ. and NJ. Blake. 1991. Reproductive physiology. In. Scallops: Biology. Ecology and Aquaculture,edited by S.E. Shumway, Elsevier Science, Amsterdam. pp. 377-428.

Beaumont. A.R. and E. Zouros. 1991. Genetics of scallops. In, Scallops: Biology. Ecologv alld Aquaculture,edited by S.E. Shumway. Elsevier Science, Amsterdam, pp. 585-623.

Castagna. M. and W. Duggan. 1971. Rearing the Bay scallop. Aequipeuen irralldians. Pmc. Nat. SheW Au.,Vol. 61, pp. 80-85.

Cochard, J.e. and l\". Devauchelle, 1993. Spawning, fecundity and larval survival and growth in relation tocontrolled conditioning in native and transplanted populations of Pectell maximus (L.): evidence for theexistence of separate stocks. 1. Etp. Mar. Bioi. Eml.. Vol. 169, pp. 41-56.

Cragg. S.M. and DJ. Crisp. 1991. The biology of scallop larvae. In, Scallops: Biology. Ecologv amiAquaculllIre. edited by S.E. Shumway. Elsevier Science. Amsterdam. pp. 75-132.

Dickie. L.M., P.R. Boudreau and K.R. Freeman, 1984. Influences of stock and site on growth and mortality inthe blue mussel Mvtilus eduli.\. Call. 1. Fish. Aquat. Sci .. Vol. 41, pp. 134-140.

Falconer, D.S .. 1989. Ill/roductioll to Quall/itarive Gelletics. Longman Scientific and Technical. England, 3rd.edition. 438 pp..

Felix-Pico, E.F.. 1993. Estudio biologico de la almeja catarina. Argopectell circularis (Sowerby, 1835) enBahia Magdalena, B.C.S .. Mexico. Tesis Maestria ell Ciellcias, CICIMAR, La Paz, B.C.S. 89 pp..

P. Cru:. A.M. Ibarra / J. Exp. Mar. Bioi. Ecol. 212 (/997) 95-110 109

Gaffney, P.M., 1994. Heterosis and heterozygote deficiencies in marine bivalves: more lIght? In, Genetics and

evolution of aquatic organisms, edited by A.R. Beaumont, Chapman and Hall, London, pp. 146-153.

Gruffydd, Ll.D. and A.R. Beaumont, 1972. A method for rearing Pecten maximus larvae in the laboratory.Mar. Bioi., Vol. 15, pp. 350-355.

Hawes, R.O., K. Scully and H. Hidu, 1990. Growth rate of two diverse populations of American oysters,

Crassostrea virginieel, and their reciprocal crosses. Aquaculture, Special Issue Genetics in Aquaculture Ill,pp. 327.

Hernandez-Rivas, M., 1. Gomez-Gutierrez. e.A. Sanchez-Ortiz, RJ. Saldierna-Martinez and G.R. Vera­

Alejandre, 1993. Atlas de temperatura superficial en el complejo lagunar de Bahia Magdalena-BahiaAlmejas, Baja California Sur. Mexico 1980-1989. CICIMAR, La Paz. B.e.S., 85 pp..

Heffernan, P.B., R.L. Walker and l.W. Crenshaw Jr.. 1992. Embryonic and larval responses to selection for

increased rate of growth in adult bay scallops, Argopecten irradians concentricus (Say, 1822). 1. ShellfishRes., Vol. II, pp. 21-25.

Hilbish, TJ., E.P. Winn and P.O. Rawson, 1993. Genetic variation and covariation during larval and juvenile

growth in Mercenaria mercenaria. Mar. Bioi., Vol. 115, pp. 97-104.

Ibarra, A.M .. P. Cruz and B.A. Romero, 1995. Effects of inbreeding on growth and survival of self-fertilized

catarina scallop larvae. Argopecten circularis. Aquaculture, Vol. 134. pp. 37-47.

Koehn, R.K.. 1991. The genetics and taxonomy of species in the genus Mvtilus. Aquaculture. Vol. 94, pp.125-145.

Kraeuter, l.N., L. Adamkewicz, M. Castagna, R. Wall and R. Karney. 1984. Rib number and shell color inhybridized subspecies of the Atlantic Bay Scallop. Argopecten circularis. The Nautilus. pp. 17-20.

Ludwig. A.N. and P.M. Gaffney, 1991. Quantitative genetics of growth in the dwarf surfclam Mu/inia lateraiis(Say, 1822). 1. Shellfish Res.. Vol. 10, pp. 451-453.

MacDonald, B.A. and RJ. Thompson, 1986. Influence of temperature and food availability on the ecologicalenergetics of the giant scallop Placopecten magellanicus. III. Physiological ecology, the gametogenic cycleand scope for growth. Mar. Bioi., Vol. 93. pp. 37-48.

Mackie, L.A. and A.D. Ansell, 1993. Differences in reproductive ecology in natural and transplanted

populations of Pecten maximus: evidence for the existence of separate stocks. J. Exp. Mar. Bioi. Eml., Vol.169, pp. 57-75.

Maeda, A. and P. Ormart, 1995. Sistema marino para crecimiento y engorda hasta la fase adulta de almejacatarina. Patente n. 180 21 ]. Instituto Mexicano de la Propiedad Industrial.

Maeda, A .. P. Monsalvo and T. Reynoso. 1995. Sistema para crianza intensiva en su etapa juvenil de almejacatarina. Patente n. 180 212, Instituto Mexicano de la Propiedad Industrial.

Mallet. A.L.. K.R. Freeman and L.M. Dickie, 1986. The genetics of production characters in the blue musselMvtilus edulis. I. A preliminary analysis. Aquaculture, Vol. 57. pp. 133-140.

Mallet, A.L. and L.E. Haley. 1983. Growth rate and survival in pure population matings and crosses of theoyster Crassostrea virginica. Can. J. Fish. Aquat. Sci., Vol. 40. pp. 948-954.

Mallet. A.L. and L.E. Haley. 1984. General and specific combining abilities of larval and juvenile growth andviability estimated from natural oyster populations. Mar. Bioi., Vol. 81, pp. 53-59.

Martinez. M.e. and L. DiMichele, 1992. Possible genetic influences of the growth rate and survival of twopopulations of Crassostrea \·irginica. Triennial meeting of The National Shellfisheries Association. J.Shellfish Res., Vol. 11. p. 202.

Neter. l .. W. Wasserman and M. Kutner. 1985. Applied linear sliitistimimodeis. Richard D. Irwin, 2nd. edition,1127 pp..

Newkirk. G.. 197H. Interaction of genotype and salinity In larvae of the oyster Crassostrea \'irginica. Mar.Bioi., Vol. 48. pp. 227-234.

]\;ewkirk, G.F.. 1980. Review of the genetics and the potential for selective breeding of commerciallyimportant bivalves. Aquaculture. Vol. 19. pp. 209-228.

Newkirk, G.F., D.L. Waugh and L.E. Haley, 1977. Genetics of larval tolerance to reduced salinities in two

populations of oysters, Crassostrea virginica. 1. Fish. Res. Board Can., Vol. 34. pp. 383-387.

Paulet, YM .. A. Lucas and A. Gerard. 1988. Reproduction and larval development in two Pecten maximus (L.)populations from Brittany. J. Exp. Mar. Bioi. Eml., Vol. 119. pp. 145-156.

Pirchner, F., 1983. Population genetics in animal breeding. Plenum Press, New York. 414 pp..

110 P. Cruz. A.M. Ibarra /1. Exp. Mar. Bioi. Eml. 212 (/997) 95-110

Reyes-Salinas, A., 1994. Relacion entre estructura hidrognifica y la abundancia, distribucion y origen dediferentes expresiones de biomasa del seston organico en Bahia Concepcion, Golfo de California. Tesis Lie.en Biologia. UNAM. La Paz, B.C.S., 86 pp..

Rohlf, F.J. and R.R. Sokal, 1981. Statistical tables. W.H. Freeman and Company, New York. 219 pp..Sastry. A.N., 1963. Reproduction of the bay scallop Aequipeeten irradians Lamarck. Influence of temperature

on maturation and spawning. Bio/. Bull., Vol. 125. pp. 146~ 153.Stromgren. T. and M.V. Nielsen, 1989. Heritability of growth in larvae and juveniles of Mytilus edulis.

Aquaculture. Vol. 80, pp. 1-6.Stufflebeam, C.E., 1989. Genetics of domestic animals. Prentice Hall, New Jersey, 295 pp..Van Vleck, L.D., E.J. Pollak and E.A.B. Oltenacu, 1987. Genetics for the animal sciences. W.H. Freeman and

Company. New York, 391 pp..Villalejo-Fuerte, M. and R.1. Ochoa-Baez, 1993. The reproductive cycle of the scallop Argopecten circularis

(Sowerby. 1835) in relation to temperature and photoperiod. in Bahia Concepcion, B.C.S., Mexico.Ciencias marinas. Vol. 19. pp. 181-202.