The role of larval migration in the maintenance of an encrusting sponge population

Netherlands Journal of Sea Research 7:159-170 (1973) 7th European Symposium on Marine Biology

THE ROLE OF LARVAL MIGRATION MAINTENANCE OF AN ENCRUSTING POPULATION

IN THE SPONGE

by W. G. FRY (Department of Science, Luton Collegeof Technology, Bedfordshire, U.K.)

CONTENTS I. II. III. IV. V.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . Isolation of the populations . . . . . . . . . . . . . . . . . . . . Evolutionary fitness of the populations . . . . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . .

159 160 164 169 169

I. I N T R O D U C T I O N The red encrusting sponge Ophlitaspongia seriata (GRANT, 1826) occurs on rocks around the coasts of Anglesey and the North Wales mainland, which are separated by the Menai Strait (Fig. 1). In two previous papers (FRY, 1970, 1971) some aspects of the physiology (see Plate II), of the larval behaviour and of skeletal differences between populations at Bodorgan and Church Island have been discussed. Skeletal and physiological differences (Plate I) were found between samples from the 2 populations. On the other hand, it was found that larvae liberated in the laboratory from specimens from the 2 populations fused readily to give rise to viable sponges (Plate I). The environments of the Menai Strait and Bodorgan populations differ clearly in their temperature means and times of maxima, in their salinities, in the degree of wave force to which they are exposed, and in the silt load and the annual cycle of nutrients in the water (BuCHAN, FLOODGATE ~: CRISP, 1967; EWINS ~: SPENCER, 1967; FRY, 1971, HARVEY • SPENCER,1962). The geological history of the region indicates that the Menai Strait can have been in existence only since the PostGlacial, approximately 12,000 years, and it would appear that the Menai Strait population either has diverged, or is in process of diverging in its genotype from the Bodorgan and other neighbouring populations of the species. However, if the Church Island and Bodorgan populations are in genetic contact by virtue of exchanges of larvae, divergence of the genotypes should be swamped. Furthermore, such a

160

w.G. FRY

swamping of divergence is likely to reduce the long-term evolutionary fitnesses of the populations. Acknowledgements.--The majority of the data discussed in this paper were collected during tenure at Menai Bridge of the Red H a n d Compositions Fellowship. However, it is to Mr Garth Fish of Luton that my especial thanks go for his cogent and sometimes trenchant advice on statistical procedures. I thank also my wife Patricia for her resistance to excesses of abstraction.

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Fig. 1. Map of Angle.seyand the Menai Strait. The Swilliesare a group of islets adjoining Church Island and lying between the road and rail bridges connecting Angleseyand the mainland; a, sampling station on the Holyhead-Kishsteamer route 1955-66; b, and c, samplingstations on the Liverpool-Dublinsteamer route 1966-68. Data for the Holyhead region after 1968 are fragmentary only. II. I S O L A T I O N OF THE POPULATIONS The narrow vertical littoral band inhabited by Ophlitaspongia seriata, the apparent necessity for the sponges to inhabit steep rock faces which are well scoured by water, the apparent absence of such faces in the Menai Strait southwest of the Swillies (Fig. I), and the lack of observations of the species between the tide-marks in the Strait southwest of the Swil-

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Fusion of 35 Ophiltaspongia seriata post-larvae induced to settle in a small area. Above: 48 h after settlement; S, isolated post-larvae; F, fusion masses of 2 post-larvae; Fm, tusion mass of more than 2 post larvae. Below: 2 weeks after settlement; note the complete disappealance of isolated post-larvae, the formation of aquiferous systems a n d skeletal structures in the fusion masses, and indication that morphogenetic vigour of fusion masses is ielated to the n u m b e r of their constituent post-larvae. Scales 5 mm.

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Regenerating capabilities of Bodorgan and Church Island Ophlitaspongia seriata cells in slow-flowing Menai Strait sea water at 18' C as represented by types of morphogenesis achieved in 2 weeks fbllowing maceration. Above: Bodorgan cells represented by a few small diamorphs. Below : Church Island cells showing well-developed aquiferous and skeletal systems. Scale 1 cm.

LARVAL

MIGRATION

IN SPONGE

POPULATION

161

lies, indicate that the Bodorgan and Church Island populations are separated physically by approximately 20 km. Thus, if there is any gene flow between the populations it must be by direct gene flow across this distance. Unlike some other sponges, e.g. Halichondria panicea, Haliclona oculata, Adocia cinerea and Hymeniacidon perleve, Ophlitaspongia seriata does not break up into fragments which can re-attach and grow; nor is there any evidence that Ophlitaspongia seriata produces gemmules. So small are the larvae of Ophlitaspongia seriata, and so slow is their swimming, that their ability to move laterally relative to currents of speeds of more than a very few cm/sec must be regarded as nil. The interchange of larvae between Church Island and Bodorgan is likely, therefore, to depend entirely upon the topography of the Strait and the northern part of Caernarvon Bay, and upon the speeds and the durations of tidal currents between the 2 populations. The effect of the tides is to produce pulsating water movements in the Menai Strait and along the southwestern coast of Anglesey (HARVEY, 1967, 1968). Admiralty Hydrographic Office records made in 1962 show that off Llandwyn Island (Fig. 1) there is a predominantly north-south water movement with a residual of 9.27 cm/sec at 267 ° true north. Drift poles indicated both northerly and southerly current speeds in excess of 150 cm/sec. Southerly currents occurred during flood tides; northerly currents during ebb tides. A survey by HARVEY (1968) of tidal currents in the Menai Strait showed that there is residual flow through the Strait in a southwesterly direction during each diurnal tidal cycle. This indicates that there may be larval movement from Church Island to Bodorgan, and that the reverse gene flow may occur less frequently. The residual southwesterly flow through the Strait has been determined as approximately 11 cm/sec during a mean tidal range cycle, and as approximately 18 cm/sec during a mean spring tidal cycle. Therefore, larvae liberated at Church Island and remaining in the tidal stream would travel approximately 9.5 km and 15.5 km respectively southwest of Church Island in 24 h. The distance between Church Island and Belan Point (Fig. 1) is approximately 16 kin. Thus, it is just possible that larvae from Church Island can escape into Caernarvon Bay before having to metamorphose. If the larvae passed Belan Point directly into a northerly tidal stream, then they could be transported the 6 km or so to Bodorgan in approximately 1.5 h. However, laboratory experiments indicate that the larvae must sink to metamorphose after 24 h (FRY, 1971). Sand and mud shores stretch with but one interruption from Belan Point to Bodorgan. The only suitable intervening substratum is the tip of Llanddwyn Island, which

162

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FRY

is so sand scoured as to support no specimens of O. seriata. On the other hand it must not be overlooked that field temperatures lower than experimental temperatures might delay obligatory settlement. In order to escape into Caernarvon Bay well before obligatory settlement, the larvae must traverse the 16 km to Belan Point in a single southwesterly tidal flow. Taking a maximum rate of water movement between Church Island and Belan Point as the mean of all recorded values (see HARVEY, 1968), 170 cm/sec, it would require a little over 2.5 h for larvae to be transported into Caernarvon Bay. This is probably a low estimate, for the maximum southwesterly flow is maintained only for an hour or so. Nonetheless, it is clear that larvae can be transported from Church Island past Belan Point to Bodorgan within a single southwesterly tidal stream and well before obligatory settlement. Experiments have shown (FRY, 1971) that the larvae attempt to move out of turbulent water. But larvae appear to be liberated at slack high water, which is succeeded immediately by the southwesterly flow. Larvae escaping into the open Strait after liberation would not have the mobility to escape from the fast southwesterly tidal stream. So it must be concluded that some larvae from Church Island parents will be transported to Bodorgan, and even further north, each year. It appears less likely that larvae originating from Bodorgan regularly reach Church Island. An average north-easterly velocity of 80 cm/sec represents the published data. At this speed it would require slightly more than 5.5 h for larvae from Bodorgan passing Belan Point to reach Church Island. The north-easterly tidal stream persists southwest of the Swillies for approximately this length of time in any tide cycle. Therefore, although larvae from Bodorgan may be transported to Belan Point in less than 2 h, they must pass Belan Point at the very beginning of the flood tide if they are not to be swept back into Caernarvon Bay by the ensuing southwesterly tidal stream. The Bodorgan population is one of many populations of Ophlitaspongia seriata occurring along the west coast of Anglesey and spreading north and east as far as the western end of Red Wharf Bay (Fig. 1), which interrupts the distribution by several kilometres of sandy shore. Other populations of O. seriata occur on the coast of Puffin Island and the neighbouring Anglesey coast. The possibility must be considered, therefore, that the Bodorgan and Church Island populations are in genetic contact via the populations around the northern and eastern coasts of Anglesey. Immediately northeast of Menai Bridge pier some specimens of the sponge occur on isolated rocks scattered over approximately 1 km on the Anglesey shore. These sponges can be regarded as being in genetic

LARVAL MIGRATION IN SPONGE POPULATION

163

contact with the Church Island population. Beyond this point the shores on both sides of the Strait give way to mud and stone substrata unsuitable for the species. Continuing northeast into the mouth of the Strait, no other specimens have been found on either shore until the Anglesey coast opposite Puffin Island is reached. Thus the Church Island population is separated from other specimens to the northeast by approximately 10 km. Mean maximum northeasterly tidal flows have been reported as 80 cm/sec near Church Island and as approximately 30 cm/sec off Bangor. Assuming an average northeasterly flow of 30 cm/sec, and assuming that they avoided southwesterly transport by the tidal stream immediately following liberation, the larvae would require to travel for approximately 9.3 h to the northeast in order to reach settling grounds suitable for growth to maturity. However, the northeasterly current persists for less than 7 h in a single tidal cycle, and the larvae would therefore have to travel northeast for this period and then remain out of the succeeding southwesterly current before proceeding northeast again. It is probable, therefore, that larval transport from the Menai Bridge population to the vicinity of Puffin Island is of very low freq u e n c y _ i f it ever occurs at all. SIMPSON,FORS~S & GOULD (1971) have shown that infrequently, when neap tide periods coincide with prolonged southwesterly wind speeds of more than 20 m/sec, the residual flow through the Strait may be reversed. Such events will increase the chances of Bodorgan larvae reaching Church Island, and of Church Island larvae reaching the Puffin Island area, but the coincidence of such physical events with larval liberation must be very rare. On the other hand, larval movement from the Puffin Island region to Church Island appears eminently possible. The mean maximum southwesterly tidal flow off Bangor has been recorded as approximately 40 cm/sec. If larvae from the Puffin Island specimens are liberated at slack high water, then they will be transported the 10 km to Church Island in slightly less than 7 h at this speed. Occasionally, therefore, Puffin Island larvae can reach Menai Bridge in a single southwesterly tidal flow, and at mean spring tides the residual flow would ensure their reaching Church Island in considerably less than 24 h. It can be concluded, therefore, that the Church Island population is not genetically isolated from other populations of the species. However, while contributing larvae to populations to its south and west, the Church Island population probably receives migrant larvae solely from populations to its northeast. The latter populations probably undergo larval exchange with those populations, such as Bodorgan and Rhosneigr, which receive genetic material from Church Island.

164

w.G. FRY III. E V O L U T I O N A R Y FITNESS OF THE POPULATIONS

In a series of papers L~wNs (1962, 1964, 1968) has constructed a theoretical model with which to describe the effect upon a population's evolutionary fitness of gene flow under different environmental stresses. He has expressed this relationship as: E(Wi)~l--(S--P)S--var(S)--var(Pi)--E(vAPHE)÷2cov(S,

Pi)

(1)

where E(Wt) is the population's evolutionary fitness, S is the optimum phenotype under pertaining environmental conditions, P is the mean actual phenotype, var(S) is the variance of the optimum phenotype, var(Pi) is the variance of the mean actual phenotype, E(VAPHE) is the phenotypic variance within the population, and cov(S,Pi) is the covariance in each generation between environment and mean actual phenotype. It can be shown that, if2 populations share an environment which is constant in time but variable in space, and if there is gene flow between the 2 populations, then the mean actual phenotypes will be displaced from the optimal phenotypes by amounts which increase with the difference between the 2 environments and by the amount ofgene flow, but which decrease with additive genetic variance. This may be expressed as: P1 = St -- m(S1 -- $2)/(2m fi- V)

and

(2) P2 = $2 -- m(S2 -- $1)/(2m ~c- V)

where m is gene flow, which we can translate as larval exchange, and V is the additive genetic variance of the genotypes. Referring to equation (1), it can be seen that for any population receiving genetic material from another under these conditions E(VAPHE) also will be increased by m, since each population becomes a mixture of 2 populations with different mean genotypes. LEVINS has examined the working of his model under different conditions. His third set of conditions, in which the 2 environments vary constantly in space and synchronously, appears to fit the case under discussion. Fig. 2 shows the variations in recent years in temperature and salinity of the water in the Bodorgan and Church Island vicinities. It can be seen that these 2 factors have varied synchronously. They have also varied to very similar degrees, although there is some indication that salinity in the Menai Strait is more variable than in Irish Sea coastal waters.

LARVAL MIGRATION IN SPONGE POPULATION

165

Under these conditions P varies inversely with V and directly with ($1 -- $2), but is almost completely independent of the value of m. I.O -

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Fig.2. Average monthly salinity anomaliesin ~o S (a) and average monthly temperature anomalies in °C (b) from 5-year moving means. Solid line, data from Menai Bridge pier; broken line, data from stations a, b, and c, off Holyhead (Fig. 1). With the proviso that it would not be expected that either E or E (WBodorgan) equal unity, i.e. no population is evolutionarily perfectly fit--an expression of "HALDANE'S dilemma" (HALDANE,1957, 1960; VAN VALEN, 1965), relative values of some variables in LEVIN'S model can be obtained for the Church Island (CI) and Bodorgan (B) populations. By inserting these values into Equations (1) and (2) an idea can be obtained of the evolutionary fitnesses of the 2 populatons. LEVIN'S equation (2) can now be applied as:

(Wchurch Island)

PcI = S c I -- m(Sei - - SB)/(2m ÷ V) and PB = SB - - m(SB - - S c i ) / ( 2 m -k V).

From what has been written above it can be seen that ScI ~ SB and, therefore, that ( S e x - SB) and ( S B - Sci) must have large values tending to displace S from P and induce large values of (S -- P) ~ in equation (1) which will cause E(Wa) to depart from unity. It has been shown, however, that the 2 populations have different mean phenotypes in regard to skeletal and some other characteristics (Pci ~ PB). Unless one or both genotypes have remarkably skew frequency distributions of alleles, then the additive genetic variance (V) of the popu-

166

w . o . FRY TABLE

I

Ophlitaspongia seriata. Normality of spicule size data computcd from moments about

the means and their standard errors. For each sponge 3 spicule types were measured in 2 samples from oscular regions (Osc.) and 2 samples from interoscular regions (Int.o.). Numbers of samples tested sponges with 2 normal samples sponges with 1 normal samples sponges with 0 normal samples samples that are normal

Subtylostyles Osc. Int.o.

Tylostyles Osc. Int.o.

Osc.

Toxa Int.o.

30 1

30 1

30 12

30 12

30 6

30 7

6 8

5 9

2 1

3 0

8 1

7 1

8

7

26

27

19

21

lations will be large. This will have the effect of reducing values of (S -- P)2 a n d so of restoring E(WcI) a n d E(WB) towards unity. Before it can be concluded unequivocally t h a t VcI,• is large, it must be r e m e m b e r e d t h a t skeletal characteristics are known to be phenotypically variable (J6RGENSEN, 1944, 1947; STONE 1970a, 1970b, 1970c). However, spicule growth is rapid and is affected by short term variations, while the d a t a were derived from specimens all collected in the same month. Therefore, unless the environment of C h u r c h Island is far more heterogeneous t h a n is suspected, the observed variances of the skeletons of the C h u r c h Island a n d Bodorgan populations must reflect genotypic variance. It has been seen t h a t salinity and temperature (Fig. 2) have varied in the past few years. I f those variations have been of sufficient magnitude to exert selection pressure, then var(Sei) and var(SB) must have high values causing E(WcI) and E(WB) to depart from unity. As mentioned above, there is some slight indication that salinity has been TABLE

II

Ophlitaspongia seriata. Results of program CDAM. Ranks (r') of variability in size of

3 spicule types in oscular (Osc.) and interoscular (Int.o.) regions among B populations; high values of r' indicate high similarity of variability; high values of Zr'/Zr × 100 indicate high variability. Population

Church Isl. Bodorgan Roscoff

Subtylostyles Tylostyles Osc. Int.o. Osc. Int.o.

2 I 2

2 1 2

2 1 3

1 1 2

Toxa Osc. Int.o.

3 2 2

2 2 2

Sum of ranks (Zr')

Index of variability Er'/ Y~r x 100

12 8 11

85.71 57.14 78.57

L A R V A L M I G R A T I O N IN SPONGE P O P U L A T I O N TABLE

167

III

Ophlitaspongia seriata. Concordance ofF-test and program CDAM probabilities from second-order Kolmogorov-Smirnov tests on intrapopulation and interpopulation comparisons for populations of Church Island (CI), Bodorgan (B) and Roscoff (R). Populations

CI × CI : B × B CI × B : CI × R CI × B : B × R CI x R : B × R CI × CI : R × R B × CI : R x R

Oscular r e g i o n F-tests CDAM

Interoscular region F-tests CDAM

< > > > < <

> < > < > >

0.05 0.05 0.05 0.05 0.05 0.05

0.021 0.367 0.699 0.999 0.091 0.001

0.05 0.05 0.05 0.05 0.05 0.05

0.944 0.004 0.994 0.005 0.648 0.216

more variable in the Strait than off Bodorgan. If this is significant, then and hence E(WcI) < E(WB). As has been described elsewhere (FRY, 1970) much of the spicule data from the 2 populations is not normally distributed (Table I). The skeletal phenotypic variances of the 2 populations were compared therefore, by a non-parametric analogue of variance analysis (Program CDAM), which required the medianisation of spicule size frequency data and the subsequent two-order comparison of the transformed frequency distributions by means of the Kolmogorov-Smirnov test similar to that used for comparing the populations (FRY, 1970). This appears to be as satisfactory a method as any of obtaining comparisons of variance under such conditions (FRASER, 1966; TATE & McLELLAND, 1957) Table II shows the results of these comparisons, demonstrating that in regard to spicule size frequencies the Church Island population is more variable than the Bodorgan population. Some of the spicule size frequency distributions were normal and their variances were compared by a standard F-test. The results of these F-tests are compared in Table I I I with their counterparts obtained by the non-parametric analogue (Program CDAM). The similarity of the results vindicates, in general terms, the use of the non-parametric analogue. It can, therefore, be stated that, in regard to some spicule characteristics, E(VAPHE)cI > E(VAPHE)B. Consequently, E(Wci) must be regarded as further from unity than E(WB). Insufficient data have been collected to ascribe directly any relative values to var(Pei) and var(PB); this will require study of the populations over m a n y more years. Similarly, insufficient data have been collected for any direct measurement of cov(S,Pei) and Cov(S,PB). However, if the recorded environmental variations have been exerting selection pressure on the spon-

var(Sci) > var(SB),

168

w.G. FRY

ges, then there should have been extensive death in the field of established sponges as well as of newly metamorphosed larvae. Neither at Church Island nor at Bodorgan was any die-back of sponges observed in any season of the 4 years of field work. On this evidence, either cov(S,Pei) and cov(S,PB) have been very small, or else environmental fluctuations have not been sufficiently large to produce high values of var(S). In the first case, the evolutionary fitness of both populations must be further diminished, whereas in the second case the evolutionary fitnesses must be higher because of low values of var (S). Despite these uncertainties, there remains the fact that E(VAPHE)cI is larger than E(VAPHE)Band, therefore, E(WcI) will tend to depart further from unity than E(Ws). On this basis the future of the population in the Strait appears perilous. However, an alternative situation may exist in which the relationship between var(Sci) and var(Pei) is more subtle and permits of both a high value of cov(S, P ei) and a high value of E(VAPHE)CI without frequent vast mortalities. It has been deduced from studies on larval behaviour (FRY, 1971; and see Plate I) that in the field there is not necessarily a one-to-one relationship between settled larvae and adult specimens of O. seriata. The larvae may settle in swarms and subsequently fuse. If it be assumed, in the simplest case, that the larvae of a fusion mass consist of cells of 2 genotypes A and B, of which the A-type are unfavoured but the B-type favoured in the subsequent year of growth, then the B-type cells will be dominantly responsible for skeletal construction and general maintenance. The A-type cells need not necessarily die, but may play a minor and dependent role within the sponge. Under steady environmental conditions a majority of gametes would arise from B-type cells. This would lead to a local preponderance of B-type homozygous larvae and therefore to a low larval mortality. If environmental conditions then changed to favour the A-type cells over the B-type cells, then the basic skeletal architecture would not change, although new skeletal material might be different, and homozygous A-type larvae would predominate with, once again, reduced local larval mortality. On the basis of this hypothesis the high recorded value ofE(vAPHE)CI is delusive, since it is based on skeletal characteristics which could be a reflection of more than one year's growth in a varying environment. The low evolutionary fitness of the Church Island population may be apparent rather than real, and a mechanism such as this would allow for a high, but hidden value ofcov(S,Pci) without enormous wastage of gametes and larvae during years of marked environmental anomalies. Some species of sponge have enormously wide geographical distributions, e.g. Halichondria panicea, Hymeniacidon perleve. While taxono-

LARVAL MIGRATION IN SPONGE POPULATION

169

mists disagree about the exact status of far flung populations of such species it seems profitable to test this hypothesis and to determine whether or not such a mechanism enables sponges to invade, and to maintain themselves within, new habitats without either vast larval mortalities or a surrender of evolutionary fitness. In the present case we must examine the possibility that the 2 populations' additive genetic variance (V) is not large. We have seen that Sci ~ SB and, therefore, that (S -- P)2 is large for both populations if V is not large. It has also been shown that differences between the populations' environments are mirrored by differences in their phenotypes. If V is not large, then we can interpret this phenomenon without postulating extreme evolutionary unfitness for both populations (and for the Church Island population especially) only by assuming that no successful larval exchange takes place. In these circumstances we must accord to the Church Island population the rank of a separate species with a suspect future because of its high value of E(VAPHE). IV. SUMMARY Two populations of Ophlitaspongia seriata on the north Welsh coasts occupy different environments which vary synchronously. The 2 populations have different phenotypes and different phenotypic variances. The local hydrography indicates that they can exchange larvae. Using these data within a model of mechanisms for varying evolutionary fitness it may be concluded that one population, within the Menai Strait, is evolutionarily more unfit than the other, open coast, population. It is suggested that the phenomenon of larval coalescence, by reducing post-larval mortalities during environmental fluctuations, makes peripheral sponge populations evolutionarily more fit than is at first apparent. Such a mechanism may permit individual sponge species to colonise and persist in widely varied and varying environments. If the hypothesis is rejected, the data can be interpreted by ascribing to the Menai Strait population the status of a genetically isolated species in grave danger of extinction. V. REFERENCES BUCHAN,S., G. D. FLOODGATE& D.J. Cruse, 1967. Studies on the seasonal variation of the suspended matter in the Menai Straits. I. The inorganic fraction.-Limnol. Oceanogr. 12 (3): 419-431. Ewms, P. & C. P. SPENCER, 1967. The annual cycle of nutrients in the Menai Straits.--J. mar. biol. Ass U.K. 47; 533-542. FRASER, D. A. S., 1966. Nonparametric methods in statistics. Wiley, New York, London and Sydney: 1-299.

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W . o . FRY

FRY, W. G., 1970. The sponge as a population: a biometric approach. In: W. G. FRY. Biology of the Porifera.--Symp. Zool. Soc. Lond. 25: 135-161. , 1971. The biology of larvae ofOphlitaspongia seriata from two north Wales populations. In: D.J. CRISP, IVth European Marine Biology Symposium. Cambridge Univ. Press: 155-178. HALDANE,J. B. S., 1957. The cost of natural selection.--J. Genet. 55:511-524. , 1960. More precise expressions for the cost of natural selection.--J. Genet 57: 351-360 HARVEY,J. G., 1967. The effect of weather on water level in the Menai Straits.-Dt. hydrogr. Z. 20 (2): 54-58. • , 1968. The flow of water through the Menai Straits.--Geophys. J. R. astL Soc. 15: 517-528. HARVEY, J. G. & C. P. SPENCER, 1962. Abnormal hydrographic conditions in the Menai Straits.--Nature, Lond. 195 (4843): 794-795. J6ROENSEN, C. B., 1944. On the spicule-formation of SpongiUa lacustris (L.). I. The dependence of the spicule formation on the content of dissolved and solid silicic acid of the milieu.--Biol. Meddr 19 (7): 1-45. , 1947. On the spicule-formatlon ofSpongilla lacustris (L.) and Ephydatiafluviatilis (L.) II. The rate of growth of the spicule.--Biol. Meddr 20 (10): 1-22. LEvlys, R., 1962. The theoly of fitness in a heterogeneous environment. I. The fitness set and adaptive function.--Am. Nat. 96: 361-373. , 1964. The theory of fitness in a heterogeneous environment. IV. The adaptive significance of gene flow.--Evolution 18 (4) : 635-638. --, 1968. Evolution in changing environments. Princeton Univ. Press, Princeton: 1-120. LEVINS, R. & R. MAcARTHUR, 1966. The maintenance of genetic polymorphism in a spatially heterogeneous envilonment: variations on a theme by Howard Levene.--Am. Nat. 100 (916) : 585-596. SIMPSON,J. H., A. M. G. FORaES& W.J. GOULD, 1971. Electromagnetic observations of water flow in the Menai Straits.--Geophys. J.R. astr. Soc. 94: 245-253. STONE, A. R., 1970a. Growth and reproduction of Hymeniaddon perleve (Montagu) in Langstone Harbour, Hampshire.--J. zool. Res. 161: 443-459. --, 1970b. Seasonal variation of spicule size in Hymeniacidon perleve.--J, mar. biol. Ass. U.K. 50" 343-348. --, 1970c. Seasonal variation in the gross biochemical composition of Hymeniaddon perleve (Montagu).--J. exp. mar. Biol. Ecol. 5: 265-272. TATE, M. W. & R. C. CLELLAND,1959. Nonparametric and shortcut statistics. Interstate, Danville, Illinois: 1-171. VALEN, L. VAN, 1963. Haldane's dilemma, evolutionary rates and heterosis.--Am. Nat. 97: 185-190. , 1965. Selection in natural populations. III. Measurement and e s t i m a t i o n . Evolution 19 (4): 514-528.