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Fertilization efficiency and gamete viability of asessile, free-spawning bivalve, Cerastoderma eduleCarl André a & Mats Lindegarth aa Department of Zoology, Stockholm University, 5-10691, Stockholm, Swedenb Tjärnö Marine Biological Laboratory, 5-452 96, Strömstad, SwedenPublished online: 20 Feb 2012.

To cite this article: Carl André & Mats Lindegarth (1995): Fertilization efficiency and gamete viability of a sessile, free-spawning bivalve, Cerastoderma edule , Ophelia, 43:3, 215-227

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OPHELlA43 (3): 215-227 (December 1995)

FERTILIZATION EFFICIENCYAND GAMETEVIABILITY OF A SESSILE, FREE-SPAWNING

BIVALVE, CERASTODERMA EDULE

Carl A ndre! & Mats Lindegarth2

IDepartment of Zoology, Stockholm University, 5-10691 Stockholm. Sweden

2Tjärnö Marine Biological Laboratory, 5-452 96 Strömstad. 5weden

ABSTRACT

The fertilization biology of the free-spawning bivalve Cerastoderma edule was studied in the labora­tory. Fertilization success dedined drastically with decreasing sperm concentration. Viability ofboth eggs and sperm decreased with age so that no fertilization took place after 4-8 hours. A dilu­tion model suggests that in the field sperm is rapidly diluted to concentrations that would resultin very low fertilization efficiencies. The dilution process thus operates on a much smaller timescale than gamete ageing, indicating that most eggs are fertilized close to spawning males. How­ever, it is also shown that under certain circumstances high concentrations of sperm may accu­mulate over dense populations of bivalves.

INTRODUCTION

Free spawning and external fertilization are typical characteristics of numer­ous marine organisms, induding many bivalves (Giese & Kanatani 1987,Strathmann 1990). Species with this type of reproduction face the problems ofboth temporal and spatial co-ordination, which may influence reproductivesuccess. Spatial co-ordination between reproducing individuals in mobileorganisms is sometimes manifested in aggregative mating behaviour (Thorson1950, Giese & Kanatani 1987), whereas in sessile organisms the possibility ofadult aggregative behaviour is limited. Here future reproductive success mightbe partly fixed already at the recruitment stage, and it has been suggested thatgregarious settlement behaviour may serve to promote subsequent reproduc­tive success (Knightjones & Stevenson 1950, Pawlik 1992).

Although fertilization was early recognized as a potentially important pro­cess, regulating recruitment and population size of marine organisms in gen­eral and of free-spawning benthic invertebrates in particular (Thorson 1950),the demographie importance of variation in fertilization success in the fieldstill remains largely unknown. This is due to the difficulties of observing and

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216 CARL ANDRE & MATS LINDEGARTH

quantifying fertilization in the marine environment, as weIl as the unfeasibilityto track larval cohorts of most marine species (Willis & Oliver 1990). Tradi­tionally, fertilization kinetics has been studied in the laboratory (Lillie 1915,Vogel et al. 1982, Levitan et al. 1991, Benzie & Dixon 1994). Fertilization esti­mates can then be combined with information about water flow to constructmodels on fertilization success in the field (Denny & Shibata 1989). In a fewcases fertilization has been examined in the field, either by artificially inducedspawning (Pennington 1985, Levitan 1991, Levitan et al. 1992, Benzie et al.1994) or by studying natural spawning events (Petersen et al. 1992, Sewell &Levitan 1992). Most studies indicate that sperm is rapidly diluted in the fieldand that fertilization success decreases quickly with increasing distancebetween spawning individuals (Pennington 1985, Yund 1990, Levitan 1991,Levitan et al. 1992), and that a large fraction of the eggs is never fertilized(Levitan et al. 1992). Field studies on the Crown-of Thorns Starfish (Acanthast­er planci) show, however, that successful fertilization may be accomplished byindividuals separated by as much as several tens of meters; this has been sug­gested to be due to the high fecundity of A. planci (Babcock & Mundy 1992,Babcock et al. 1994).

In this study we describe different aspects of the fertilization biology in thesessile suspension-feeding bivalve Cerastoderma edule: fertilization success inrelation to sperm concentration and gamete age, and egg sinking velocity andgamete release rates. The sperm release rate was then used in a model describ­ing sperm dilution due to turbulent mixing.

We thank Per Jonsson and Peter Lundberg for comments on an earlier draft. The study was sup­ported by The Swedish Natural Science Research Council (contract B-AA/BU 06737-306), TheSwedish Royal Academy of Science and the Helge Ax:son Johnsson Foundation.

MATERIAL AND METHODS

The edible cockle, Cerastoderma edule (Linnaeus, 1758), is common and abun­dant on shallow soft-sediment bottoms in northern Europe. On the west coastof Sweden, C. edule has a peak spawning period in late May - early June (Möl­ler & Rosenberg 1983, pers. obs. 1987-1995). Adult C. edulewere collected inearly June 1992, at a subtidal cockle bed dose to the laboratory at Tjärnö onthe west coast of Sweden. Previous attempts to induce or delay spawning tofacilitate handling have not been successful (pers. obs.), and all experimentswere thus based on spontaneous spawning in the laboratory. The cockles wereplaced individually in 200-ml plastic beakers containing filtered (40 prn) sur­face seawater (25%0 S, 20°C). After a few minutes some of the cocklesspawned spontaneously; individuals that had not spawned within 2 hours werediscarded. When an individual started to spawn it was immediately transferredto a new beaker where it continued to release gametes.

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FERTILIZATION IN C.E.'RASTODER1'vIA 217

Sperm concentration

A first series of experiments investigated the effect of sperm concentration onfertilization success. In the first experiment different sperm concentrations,originating from one male, were obtained by diluting 10 ml of "dry" sperm in20 ml of seawater, and then diluting this concentration 10-fold 3 times, giving4 different sperm concentrations. In the two succeeding experiments, differ­ent sperm concentrations were obtained by running dry sperm, originatingfrom two different males, through aseries of 5, 10-fold dilutions, yielding 6concentrations. The actuaI concentrations of sperm were determined bycounting cells in a hemocytometer.

For each experiment 1-5 x 102 freshly spawned eggs from one single femalewere transferred to each of 24 small dishes. Each dish contained either 0.5 ml(first experiment) or 1 ml filtered seawater. Five hundred pl (first experiment)or 10 pl sperm dilution was then added to the dishes. There were thus 4 differ­ent sperm concentrations, each replicated 6 times in the first experiment, and6 different sperm concentrations, each replicated 4 times in the two subse­quent experiments.

The egg/sperm mixture was incuhated at 20°C for 12 h (cf. Kingston 1974).Wi thin that period of time C. edule develops a ciliated trochophore larva whichmoves around inside the egg envelope. To estimate fertilization success wecounted the number of ciliated, moving larvae among the 50 first encoun­tered eggs under an inverted microscope at 100 X magnification.

Gamete longevity

In a second series of experiments we studied the effect of gamete age afterspawning on fertilization success. In the experiments on egg Iongevity, a largeamount of freshly spawned eggs from 1 female was collected, and 1-5 x 102

eggs added to each out of 8 dishes containing 1 ml filtered seawater. Freshsperm originating from 2 different males was added to 4 dishes each; the finalsperm concentration in the dishes was « 250 pP. After approximately 0, 1, 2, 4,8 and 20 hours this procedure was repeated with eggs from the same batch butwith fresh sperm from new males. The entire experiment was repeated 4times.

The experiments on sperm longevity followed approximately the same pro­tocol: Sperm from 1 male was collectecl and transferred to a beaker. After 0, 1,2 and 4 h (male 1 and 2) or 0, 1, 2, 4, 8 and 24 hours (male 3 and 4) spermwas mixed with freshly spawnecl eggs in each of 4 dishes. At each time a newfemale was used. The experiment was thus repeated 4 times. In addition, weused a ten-fold diluted sperm concentration (25 pP) in two of the experi­ments. All dishes were incubated for 12 hand the assessment of fertilizationsuccess was carried out as above.

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218 CARL ANDRE & MATS LINDEGARTH

Dilution and dispersion ofgametes

To be able to predict dilution and dispersion characteristics of the gametes ofC. edule we measured egg sinking velocity and gamete release rates. For meas­urements of egg sinking velocities, we used an aquarium with filtered seawaterwhich was placed in a larger tank with cool circulating water, ensuring a con­stant temperature in the aquarium (10.5°C), and thus minimizing convection.A few eggs at a time were added 1 cm below the water surface. Falling eggswere then observed and recorded using a horizontally mounted dissectingmicroscope equipped with a video camera (Panasonie CCD-F10) at 12 X mag­nification. Measurements were made on 10 individual eggs from each of 3females.

Gamete release rates were measured by transferring spawning individuals(ca 35 mrn in length) to separate glass beakers containing 100 ml of seawater,where they continued to spawn. After 4-5 minutes of incessant spawning, thecockles were removed and the concentration of gametes estimated. Gameterelease rates were investigated for 6 males and 5 females.

Rates of sperm release were transformed into patterns of sperm concentra­tion around spawning individuals using the diffusion model suggested by Den­ny (1988: eq. 10.34). The model assurnes unidirectional, rough turbulent flow,which is probably simplistic compared to shallow soft sediment areas which isthe predominant habitat for cockles. However, this model serves to illustratethe range of sperm concentrations on small spatial scales. The highest concen­trations of sperm will be found downstream of and level with the point ofrelease and for simplicity the concentrations were only evaluated at y=O andz=O. The model predicts that the concentration downstream of a spawningmale varies as:

c(x)= Qü2n<xpzu *2x2

(1)

where Q is the rate of gamete release, ü is the mean flow velocity, a; and <Xz aredispersion coefficients, and u, is the friction velocity. The range of flow veloc­ities modelIed was from 1 to 0.01 m s·l; u, was set to 0.1 ü, and Uy and <Xz to 2.2and 1.25 respectively (Denny 1988).

RESULTS

Sperm concentration

Fertilization success declined drastically with decreasing sperm concentration(Fig. 1). In suspensions with 1000 sperm pP more than 70 % of the eggs werefertilized on average, whereas virtually no eggs were fertilized in treatmentswith sperrn concentrations below 10 pP. Unfortunately, for male 2 and 3 the

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FERTILIZATION IN CERASTODERMA 219

____ Male 1

----.- Male 2

---Ar- Male 3

0.9

0.8Uls 0.70Oll;>..

0.6N

Ollt:

~ 0.5t:0 0.4'E0c, 0.30....

Il<0.2

0.1

00.001 0.01 0.1 10 100 1000 10000 100000

Sperm concentration Olr 1)

Fig. 1. Fertilization as a function of sperm concentration for 3 different males. Errorbars (± SE) indicate variation among 6 (male 1) or 4 (male 2 and 3 ) independent

incubations for each male and sperm concentration.

higher part of the appropriate range of sperm concentrations was not covered,and maximum fertilization efficiencies may not have been reached.

Gamete longevity

Viability of both eggs and sperm declined with age so that the fertilization wasreduced to 50% after ';'2 hours, and no fertilizations were observed after 4-8 h(Figs. 2 and 3). There was considerable variation among and within individu­als, especially in the experiments on egg viability. Here sperm from two differ­ent males were used at each occasion. Variation within these females may thusreflect differential compatibility between certain sperm:egg combinationsrather than egg longevity per se.

In the experiment with lower sperm concentration (25 llI-l), fertilization wasgenerally lower, and declined with age similar to the treatment with highersperm concentration (Fig. 4).

Dispersion and dilution 01gametes

The sinking velocity of individual eggs was about 0.1 mm S-l (0.077±0.021,mean±S.D.). With this sinking velocity the eggs will remain in suspensionunder most flow conditions and will be evenly distributed in the water column.However, if the current velocity is low ('" 10-2 m sl) eggs released "" 0.1 m abovethe bottom will stay on average 103 s in the water column and travel 10 mbefore settlement.

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220 CARL ANDRE & MATS LINDEGARTH

I

0.9 l1J11 Female I

0.8~

• Female 2

'" , o Female 35 0.7Oll o Female4>.N 0.6Ollc:

f +~ 05~c:0.40.€ •0 0.30..

0....p...

~~i ~ f +)~Q'I I I I U I ltiI CJ I I L:lI

0 I 2 3 4 5 6 7 8 9 10

Egg age (h)

Fig. 2. Fertilization as a function of egg age. At each time, each of 4 females wascrossed with 2 rnales. Fertilization is presented as the mean (± SE) of 4 independentincubations for each combination of female, male and egg age. After 20 h 110 fertil-

ization took place and these data points are omitted in the graph.

Gamete release rates (mean±S.D.) were 1.5 x 107±0.88 x 107 s-1 for males and1.9 x 102±1.5 x 102 s-I for females. Applying the dilution model to measurerates of sperm release (Fig. 5) shows that the concentration of sperm decreas­es rapidly downstream of the source (the decrease is even more rapid in theother directions), and that the dilution effect is highly dependent on the flowregime. For all flow velocities, the model predicts a decrease in sperm concen­tration by at least 3 orders of magnitude at a point situated D.5 m downstreamofthe source. At low current velocities (0.01 m s-I), the maximum concentra­tion is on the order of 105 pI-I, while high flow velocities (1 m s-I) produce max­imum concentrations of 103 pP (Fig. 5).

DISCUSSION

In this study we intend to quantify and discuss various parameters affecting thefertilization biology of a free-spawning sessile species, represented by thebivalve Cerastederma edule. Since artificially controlled spawning was not suc­cessful, some aspects of the fertilization biology of C. edule, such as the interac­tion between sperm concentration and gamete age, could not be assessed andthus a detailed statistical analysis was not possible. However, the results showthat (1) sperm concentration had a profound effect on the fertilization ofeggs, with complete fertilization at sperm concentrations of 103-104 pP andpractically no fertilization at sperm concentrations less than 10pI-!; (2) both

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FERTILIZATION IN CERASTODERMA 221

0.9111 Male 1

• Male 2

fJ

o Male 3

o Male 4

~ t+

~

t•

'"<UoOllc-,N

Oll.,:;:

~l::o.~

8'0..

0.8

0.7

0.6

0.5

0.4

0.3

0.2

0.1

oo 2 3 4 5 6 7 8 9 10

Spenn age (h)

Fig. 3. Fertilization as a function of sperm age in 4 different males. Fertilization ispresented as the mean (± SE) of 4 independent incubations for each combinationof male and sperm age. After 24 h no fertilization took place and these data points

are omitted in the graph.

eggs and sperm became infertile after 4-8 hours; (3) males have the capacity torelease « 107 sperm s-I while females may release » 102 eggs s'. Further, the dilu­tion model predicts that in the field the sperm is rapidly diluted to concentra­tions, which according to our laboratory experiments would result in very lowfertilization efficiencies.

The fertilization biology of marine free-spawning invertebrates has hithertomainly been studied in epibenthic mobile echinoderms, especially sea urchins.Cockles live buried in the bottom sediment, thus representing both a differenthabitat and a more limited motility. A few other studies have, however,focussed on bivalves. In comparison with these, our results indicate a relativelylow fertilization efficiency in C. edule. The concentration experiments showedthat 50% of the eggs were fertilized when exposed to sperm concentrations ofabout 5 102 111-1 (a sperm:egg ratio of 1-5 103) . In Mytilus edulis, Sprung &Bayne (1984; fig 1) observed 50% fertilization at concentrations of only 10°­101 sperm 111-1, at similar egg concentrations as in our experiments, and for Pec­ten maximus 50% fertilization occurred at concentrations in the order of 10sperm egg-I (Cruffydd & Beaumont 1970; fig 9). On the other hand some ofour experiments on gamete viability resulted in fertilization of 90% of the eggsat sperm concentrations of 2.5 102111-1 (Figs. 2 and 3), which indicates that the

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CARL ANDRE & MATS LINDEGARTH

__ 250/-lr 1

___ 25/-lr 1

222

1

0.9'"o 0.8äco 0.7e-,Neo 0.6<=

~ 0.5<=

O€ 0.40 0.3Po.0.... 0.2Po.

0.1

00 2 3 4 5

Male 1

Fig. 4. Fertilization as a functionof sperm age in 2 different malesat 2 concentrations of sperm. Fer­tilization is presented as the mean(± SE) of 4 independent incuba­tions for each combination ofmale and sperm age. (Measure­ments at 250 Ilj-l are also included

in Fig. 3).

Male 2

-- 250/-lrl

--- 25/-lr1

~ 3 4Time (h)

1 1 I 1

0.9

0.8

0.7

0.6

0.5

0.4

0.3

0.2

0.1

o I I

o 1

'""äec~co<:

~<=ooBo

I

results from the experiments on gamete concentration may be slightly under­estimated.

One limitation common to most laboratory studies on fertilization rates isthe lack of realistic water movements in the experimental containers. In stillwater experiments contacts between sperm and eggs are mainly due to spermmotility, whereas in the field encounter rate also depends on the hydrodynam­ic conditions. For example, in shallow areas with high turbulence intensities,encounter rates between sperm and eggs due to turbulence-induced shear areprobably of, at least, the same magnitude as encounters due to sperm motility(SeeJumars 1993).

Both egg and sperm viabilities were on the same order of magnitude asfound for some other free-spawning invertebrates (e.g. Yund 1990, Benzie &Dixon 1994), although other authors (eg. Havenhand 1991) have reportedegg and sperm viabilities at time scales an order of magnitude larger thanhere. The results from the dispersal model around individual cockles (Fig. 5)show rapid dilution of sperm which suggests that significant fertilization will

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FERTILIZATION IN CERASTODE-BMA 223

-- 0.01 m/s

- - - 0.1 m/s

- - - I m/s

-----

106

105

\

104 ~ \, \, \

10 3 -J \ \, "--,

102 ~, <,\

<, ..... .....

<=:.~

'"b<=:lI.lu<=:oo

E~ 10 1

c,CI)

6-

10°

1.41.21.00.40.2o I I I I I I I0.0 0.6 0.8

Distance (m)

Fig. 5. Concentration gradients of sperm downstream of a spawning male at 3 differ­ent arnbient flow velocities, 0.01, 0.1 and 1 m/s.

only be accomplished very elose to spawning male cockles. This implies thatthe time scale for sperm dilution is much shorter than the longevity of thegametes (10 vs, 104 s) and thus gamete longevity will have little impact on thefertilization efficiency (cf. Pennington 1985, Levitan et al. 1991). This conclu­sion, however, rests on the assumption that there is a continuous dilution ofsperm and that released eggs only encounter sperm from one individual male.As shown by Denny et al. (1992) reduced dilution may have great impact onfertilization efficiency. Furthermore, C. edule lives on shallow soft bottoms andis often found in dense patches, of varying size (Möller & Rosenberg 1983,Lindegarth et al. 1995). To that end, a simple heuristic model was constructedto investigate under what conditions there is a potential for a long-term accu­mulation of sperm over a bed of cockles, up to concentrations which will resultin a significan t degree of fertilization.

In the model, a number, N, of cockles are aggregated in a patch with area L2m", The water depth is d m giving the volume ofwater over the bed of cocklesas L2d m 3. The average current velocity over the bed is ü. Assuming instanta­neous mixing of sperm through the entire water column and substituting DL2for N where D is the density of cockles, the rate of change in concentration is:

dC(t)= DL2Q-mC(t)-C(t)üLddt

(2)

where Q is the number of sperm released per second and individual (Q =1.5107 s·l) and m is the constant mortality rate of sperm (m =1.4 10-4 s·l; the mor-

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224 CARL ANDRE & MATS LINDEGARTH

tality constant, rn, was calculated by fitting a negative exponential regressionequation to the data in Fig. 3). Solving equation (3) yields:

DVQ DVQC(t) ""-( -Ld)exp-«m+üLd)t) +(~Lm--u m+u d) (3)

The model predicts that, as time goes towards infinity, the concentrationapproaches an equilibrium concentration, Ceq ""DVQI (m +üLd), where theproduction of sperm is balanced by advective loss and mortality. The expectedequilibrium concentrations under different combinations of parameter inter­vals, relevant to C. edule, are shown in Fig. 6. The magnitude of the predictedequilibrium concentrations indicate that, if they are realized, these concentra­tions may be sufficient to cause fertilization rates comparable to fertilizationrates elose to individual cockles «1 m apart, cf. Fig. 5 ), even at low adult den­sities. According to the model, the time needed to reach half the equilibriumconcentration is In 0.5/-(m+üLd). Using the same parameter interval as inFig. 6, this means that high concentrations of sperm may build up after lessthan aminute of simultaneous spawning. Although the assumption of instanta­neous mixing is a simplification that affects this prediction, it is suggested thatthe time needed to load the water volume with sperm is relatively short, espe­cially since individuals of C. edule have been observed to spawn continuouslyfor about 1 hour (pers. obs.).

Not surprisingly, the present and previous studies show that a major deter­minant of fertilization success is the concentration of sperm to which the eggsare exposed. Due to turbulent diffusion sperm is often quickly diluted afterrelease, and consequently, several models and field experiments predict thatsignificant fertilization will occur only when females spawn downstream of andelose to spawning males (Denny 1988, Levitan 1991). However, as the densityof individuals decreases, the distance between individuals increases; assuminga random distribution of cockles (Richardson et al. 1993) and a sex ratio of1:1, the nearest male individual will be located 0.5 (n/D)1/2 m away from aspawning female (Pielou 1977), which results in expected distances 0.1, 0.4,1.3 and 4 m for the densities used in Fig. 6. At a density of 1 cockle m-2 and anaverage flow speed of 0.01 m s-l a female will be exposed to sperm concentra­tions of "" 102, pl-l if she is located directly downstream of the spawning male.On the other hand, if the possibility of a long-term accumulation of sperm isconsidered the average concentration of sperm will be "" 102 and 103, pl-l inpatches where L=10 and 100 m respectively and d=O. 1 m.

Dilution of gametes is not the only conceivable effect of turbulence. It hasalso been shown that high turbulent flow can significantly affect the fertiliza­tion efficiency in sea urchins (Mead & Denny 1995). The extremes of theparameter range in our simulations (ü=O.OI and 1 m S-l) roughly correspondsto energy dissipation rates of 8.5 10-8 and 8.5 104 W m-3. The latter value is

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FERTILIZATION IN CERASTODERMA 225

Average flow velocity, U(m s-l)

10°

a

10°

100

c

b

- __ ~Im~

- - O.lm-2

10 m"---.!-m-2

- - - - - - _ _0J. m~

10-1

10-1

10-1

-

-

-107

105

103

101

10-1L---

r: 10-2I-:::t......., 1071=1.9+-' 105ro.....+-'1=1Q) 103o1=10c» 101

S.2 10-1.....:9-';3 10-2

$107

105

103

101

10-1

10-2

Fig. 6. Equilibrium concentrations ofsperm in a water body as a function ofaverage current velocity, ü, at differ­ent cockle densities. (a) patch dimen­sion, L~lO m, depth, d~O.l m (b)L~lOO m, d~O.l m (c) L~lOO m, d~l

m. Note that the presented densitiesare total densities of males andfemales. The resulting concentrations

are based on a sex ratio of 1:1.

clearly in the range where fertilization is negatively affected. However, at lowor intermediate flow speeds the effect will be small or even positive due toincreased mixing (Mead & Denny 1995). Thus, at high flow speeds the fertil­ization efficiency will be small not only due to a low equilibrium concentrationof sperm (Fig. 6), but probably also due to high shear stress on the gametes.

These calculations, using mean distances and concentrations, are of coursesimplifications (note, however, that the concentration gradients in Fig. 5 arethe maximum concentrations). The purpose is, however, to illustrate that theeffects of an accumulation of sperm may lead to other conclusions ahout theefficiency of fertilization than predicted by models of single individuals. For

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226 CARL ANDRE & MATS LINDEGARTH

example, the importance of an exact co-ordination of spawning in space andtime, may be relaxed, since several males at various distances from a spawningfemale may contribute to sperm concentrations leading to successful fertiliza­tion. Moreover, high sperm concentrations may originate from different malesspawning at different time intervals, indicating that the importance of bothsperm and egg longevity to fertilization rates may increase.

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Babcock, R C; C. N. Mundy & D. Whitehead, 1994. Sperm diffusion rnodels and in situ confir­rnation of long-distance fertilization in the free-spawning asteroid Acanthaster planci. - Biol.BuH. 186: 17-28.

Benzie, J. A., K P. Black, P.J. Moran & P. Dixon, 1994. Small-scale dispersal of eggs and sperm ofthe Crown-of-thorn starfish (Acanthaster pland.) in a shallow coral reef habitat, - Biol. Bull. 186:153-167.

Benzie, J. A. & P. Dixon, 1994. The effects of sperm concentration, sperm:egg ratio, and gameteage on fertilization success in Crown-of-thorn starfish (Acanthaster planci) in the laboratory. ­Bio!. BuH. 186: 139-152.

Denny, M. W., 1988. Biology and the mechanics of the wave-swept environment. - Princeton Uni­versity Press, New Jersey.

Denny, M., J. Dairiki & S. DiStefano, 1992. Biological consequences of topography on wave-sweptshores: 1. Enhancement of external fertilization. - Bio!. Bull. 183: 220-232.

Denny, M. W. & M. F. Shihata, 1989. Consequences of surf-zone turbulence for settlement andexternal fertilization. - Am. Nat. 134: 859-889.

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