The apparent rôle of temperature in breeding initiation and winter population structure in Hyale nilssoni Rathke (Amphipoda): Field observations 1972–1983

J. Exp. Mar. Bioi. Ecol., 1983, Vol.II, pp. 237-248 Elsevier

THE APPARENT

237

ROLE OF TEMPERATURE

AND WINTER POPULATION (AMPHIPODA):

STRUCTURE

IN BREEDING INITIATION IN HYALE NILSSONZ Rathke

FIELD OBSERVATIONS

1972-83

P.G. MOORE University Marine Bialo~‘ca~Station Miilpom Isle of Cumbraoe. Seotiand Abstract: Data are presented on the population structure of Hya/e nilssoni Rathke (an amphipod inhabitant

of high littoral seaweeds) over the period of breeding initiation (late February) of 11 yr. By sampling, as near as possible, the same date annually, photoperiodic effects are controlled. The percentage of ovigerous females on this date was significantly correlated with post-winter solstice mean sea temperature. February sex ratios (M : F) did not correlate with either preceding August or September mean sea temperature such as would have been expected was sex determination temperature sensitive. Sex ratio, however, was significantly positively related to mean winter sea temperatures, with warmer winters having maledominated Hvale populations in late February. Behavioural hypotheses involving amphipod migration and/or size specific elimination of larger males (c.f. females) during harsher winters are offered in explanation. Population size-frequency distributions over 11yr were remarkably consistent. Male size was more heterogeneous between years than female size. Mean male size (late February) proved to be significantly negatively correlated with mean winter sea temperatures. Mean femaie size showed no significant relationship. Given that large males are necessary for precopulatory carrying behaviour it is important that. as shown, they are available to initiate spring breeding, even after harsh winters.

Details of the breeding cycles of remarkably few common British Amphipoda have been elucidated to date (Watkin, 1941; Hynes, 1955; Fish & Preece, 1970; Barnett, 197 1; Sheader, 1978; Fish & Mills, 1979; Moore, 198 1). In 1972, the author commenced work on the life history and ecology of Hyale ndssoni Rathke, the most common amphipod inhabiting high littoral attached seaweeds (Moore, 1977). Detailed observations on the species’ life history, made during the years 1972-76, established gross aspects of seasonal variation (Moore, in prep.). In addition, however, a long-term series of observations on breeding initiation has continued to date to investigate the “fine tuning” of life history characteristics and causative factors. Two factors are widely implicated in the literature as affecting the onset of breeding in amphipods, viz. temperature (Kinne, 1961; Fish & Preece, 1970; Bamett, 1971) and photoperiod (SegerstrNe, 1970, 1971; Bulnheim, 1978; Williams, 1978; Steele et al., 1977; Steele, 1981; de March, 1982). These factors may have interactive effects (de March, 1977) and other factors, e.g. food availability (Fish & Preece, 1970; de March, 1977) may also be important. Disentanglement of the individual importance of photoperiodic and temperature effects, purely from field data, is usually diEcult since their fluctuations may be nearly OO22-0981/83/SO3.~ C 1983 Elsevier Science Publishers B.V.

238

P.G.MOORE

in-phase. Two approaches are feasible, (1) synchronized sampling of the species over a wide latitudinal range or (2) successive sampling of the same population on the same day of the year over many years. In alternative (1), it is unlikely that photoperiodic effects will be completely separable from temperature effects (see Lewis et al., 1982); in (2), however, photoperiodic effects are controlled and any year-to-year variability remaining must be attributable to (an)other factor(s), the most accessible of which is temperature. The latter approach has been adopted here. Ovigerous females of H. nilssoni (referred to as Hyafe hereafter) are generally present in Clyde Sea area populations from February to November, peaking from May-August, though in some years a small proportion of females may even carry eggs during December and January (P. G. Moore, unpubl.). Late February was chosen as the time most suitable for comparative sampling since by then the population usually shows clear evidence of resumed breeding activity. Besides considering the onset of spring breeding, attention was also directed to the possible role of autumnal temperatures in determining the sex of over-wintered adults. In amphipods, sex is usually not determined until a critical moult (which varies between species). Temperature differences at that time may have a marked effect on sex determination though temperature may not be the only pertinent factor (Bulnheim, 1978).

MATERIAL

AND

METHODS

&u/e were collected from site A 1, northwest of Westboume, Great Cumbrae Island (O.S. Grid: NS 14955484; lat. 55”45’ : long. 4’57’) usually between 0800-1000 G.M.T. Amphipods were extracted from the algae Pefvetiu cunuliculutu (L.) (predominantly) or Mucus spirulis L. (occasionally), which occupy adjacent zones at z H.W.N. (Moore, 1977), by repeated agitation of fragmented tufts in fresh water in a large white sorting tray. Amphipods were preserved in 5 y0 formalin in the dark prior to dissection and measurement. The antero-posterior length of the third epimeral plate, measured microscopically with an eyepiece graticule, was taken as a standard index of body length (1 graticule unit = 0.102 mm). This index is linearly related to the cube root of body dry weight and is not affected by problems of animal curling. Animals measured thus were sexed and the marsupia of ovigerous females emptied to determine the number, stage and size of eggs (as appropriate). Figures in this and earlier papers (e.g. Moore, 1977, 198 1) have been constructed on the convention that each category recognized is drawn to a common base line. This facilitates scale reading. It must be remembered, however, in the case of ovigerous vs. non-ovigerous females of the same size that the total number of females in that size range is the sum of their separate values.

TEMPERATURE AND HYALE BREEDING

239

RESULTS

Table I summarizes the population characteristics of Hyale sampled as nearly as possible on 20 February in 11 yr (data for 1977 were not collected). PROPORTION OF OVIGEROUS FEMALES

It can be seen from Table I that there is a wide variation in the percentage of females bearing eggs on the same date (virtually) from year to year. Such variability is independent of photoperiodic effects. Table II lists sea-water and aerial mean temperatures for (1) the periods between the previous winter solstice and the day prior to sampling and (2) the February conditions immediately antecedent to Hyde sampling dates. Regressions of the proportions of ovigerous females (cf. total females) on each of these factors yielded the equations in Table III. No significant relationship was found when the percentage of ovigerous females was regressed on air temperatures. A significant (P < 0.05) relationship, however, did emerge with post-solstice mean sea temperature (Fig. 1); although with the February sea temperature data alone, correlation just failed to reach significance at the 5% level. Mean February sea temperature and mean post-solstice sea temperature to late February proved, however, to be highly correlated (I = 0.90, d.f. 9, P < 0.01 whether Y on X or X on Y), so the weaker biological correlation with mean February sea temperatures may be due to reduced precision as a result of fewer February data points in 1982 and 1983. Alternatively, in a case such as this, where only one datum point is accrued per year, acceptance of the 10% probability level may not be unreasonable. In this instance neither variable in the bivariate plot can be regarded as independent and the reduced major axis method which considers variation in both variates may be preferable to least-squares regression. The variables, however, are highly correlated with zero difference on inversion, so least-squares regression was deemed presently to be satisfactory. SEX RATIO

Considerable differences were apparent in the sex ratios of the population in late February of different years (Table I). The majority of these ratios differed significantly from unity by chi-square tests. Consideration of size-frequency distributions taken at monthly intervals throughout the year (Moore, in prep.) showed that the February modal groups first became distinct sexually in early autumn (Sept./Ott.). If sex determination was temperature dependent then the explanation for the February sex ratios would lie in temperature conditions some months previous. To investigate this possibility, February sex ratios were regressed on monthly mean sea temperatures (air temperatures were not analysed, see above) separately for each of the preceding months of August to January (Table IV). February sex ratios did not correlate with either August or September mean sea

9.8

8.5

13.6

7.4

4.9

4.1

2.6

7.1

5.4

4.6

0

Date

17 Feb. 1972

20 Feb. 1973

20 Feb. 1974

25 Feb. 1975

20 Feb. 1976

23 Feb. 1978

24 Feb. 1979

21 Feb. 1980

22 Feb. 1981

22 Feb. 1982

20 Feb. 1983

32.8

55.4

60.2

52.2

25.5

45.2

66.8

60.5

52.4

57.9

53.9

0.9

1.0

4.0

11.8

1.4

0

0

0.8

0.3

0

Non-ovigerous females as y0 total

1.6

females as y0 total

Ovigerous

i 0.001 < 0.05 n.s.

to.001 < 0.00 1 -co.05

< 0.001 KS.

0.65 : 1 1.55 : 1 1.06: 1 0.46 : 1 0.54 : 1 0.78 : 1 0.52 : 1

0.85 : 1

36.4 57.8 49.3 30.7 32.5 41.4

30.6 46.1

31.6 2.9 0 0 1.4 0.6 0

7.7

<0.001

< 0.05

0.41 : 1

1.7

1

25.1

35.2

1.6

1.62:

Sex ratio significance


55.7

4.8

M/F

Sex ratio

0.62 : 1

% total

Males as

females as y0 total females

Ovigerous

(146)

(93)

5.43 + 0.08 5.66 f 0.05

(1)

4.8

(162)

4.52 f 0.05

(138)

4.73 + 0.05

(96)

4.66 ?r 0.06

(36)

4.76 f 0.08

(59)

5.37 + 0.07

(99)

5.09 f 0.07

(48)

4.76 f 0.09

(198)

4.83 + 0.04

(68)

4.26 f 0.07

Size of males

(171)

(176)

(3)

4.23 f 0.24

(1)

4.5

(12)

4.43 f 0.16

(11)

4.35 * 0.11

(2)

4.40 f 0.10

(5)

4.52 f 0.10

(2)

4.20 f 0.30

Size of ovigerous females

at P = 0.05; a, composite

4.32 f 0.04

4.31 i 0.04 (14)

(205) 2.64 f 0.08

3.53 f 0.03 (21)

(257) 2.53 + 0.04

3.54 * 0.02 (30)

(209) 2.35 + 0.05

3.62 f 0.03 (8)

(33) 2.56 + 0.06

3.65 k 0.08 (3)

(26)

2.57 k 0.03

4.15 i_ 0.11

(5)

(142)

1.82 f 0.12

3.89 f 0.04

(20)

(115)

2.66 f 0.06

3.76 f 0.04

(26)

(312)

2.57 f 0.06

3.69 f 0.02

(48)

(40)

2.67 k 0.04

3.37 k 0.06

(12)

Size of nonovigerous females

2.58 k 0.06

Size of juveniles

details for Hyde nilssoni from site Al, Millport: size (mean f SE) = length index (see text), numbers in parentheses; n.s., not significant including material from N. Keppel Pier, Millport; “, includes 20 individuals of undetermined sex.

Juveniles as y0 total

Population

TABLE I

317

304b

391

425

313

73”

102

272

191

563

122

number

Total

sample,

TABLE II

Temperature data for Keppel Pier, Millport (“C): sea temperature is for surface water, air temperature is dry bulb Stevenson screen, both taken daily at x0900 G.M.T.; first two columns show mean values from previous winter solstice to day prior to ffyale sampling; third and fourth columns show mean February temperatures to day prior to sampling.

Year

Mean sea temp. (“C)

Mean air temp. ( ’ C)

Mean Feb. sea temp. (“C)

Mean Feb. air temp. (‘C)

7.5 1.4 8.0 8.0 8.8 8.1 6.5 7.5 6.9 5.9 6.8

5.2 5.2 6.2 6.1 5.9 3.9 2.8 4.3 5.6 5.0 4.9

6.5 7.6 7.4 7.7 8.0 7.2 5.6 7.1 6.6 5.6 6.5

4.9 5.3 3.3 5.4 4.4 2.8 2.5 5.3 5.4 5.5 3.1

-1972 1973 1974 1975 1976 1978 1919 1980 1981 1982 1983

TABLE III

Least-squares regressions of per cent ovigerous female H. nifssmi(as a proportion of total sexable females) on post-solstice mean sea temperature, post-solstice mean air temperature, preceding February mean sea temperature and preceding February mean air temperature (all ‘C): d.f. = 9.

Equation of best tit

Correlation coefficient (r)

Level of significance

Post-solstice sea Y ovig. = 7.40X sea temp. - 50.03

0.66

0.02 > P < 0.05

Post-solstice air Y ovig. = 3.58X air temp. - 13.18

0.40

P> 0.1

February sea Y ovig. = 6.32X sea temp. - 38.77

0.56

0.05>P<0.1

February air Y ovig. = 0.25X air temp. + 3.63

0.00

ns.

Mean

Sea Temp.*C

Fig. 1. relationship between percentage of female fiyate n&so& with eggs in late February over 11 yr and mean post-winter solstice sea surface temperature: for equation of line of best fit, see Table III.

242

P.G. MOORE

temperatures (Table IV) providing no support for the idea that sea temperature differences at the time of sexual determination were in any way critical. Data for subsequent individual months, however, produced correlations which approximated to or exceeded the 10% probability level (Table IV). Accordingly, the overall mean TABLE IV

Least-squares

Period precedent Aug. Sept. Oct. Nov. Dec. Jan. Feb. Oct.-Jan. Oct.-Feb.

regressions of H. nilssoni February sex ratio (FSR) on mean sea surface temperature at Millport (MST) for different periods preceding sampling: d.f. = 9.

Equation

incl. incl.

Yrsa Yjsa raa Yrsa Yrsa Yrsa Yrsa Yrsa Yrsa

= = = = = = = = =

of best fit

0.21X,,, 0.29X,,, 0.41X,,, 0.38X,,, 0.42X,,, 0.26X,,,0.14X,,,0.45X,,, 0.43X,,,

-

2.07, 3.00, 4.05, 3.20, 2.95, 1.17, 0.16, - 3.58, - 3.20,

(“C)

Correlation coefficient (r)

Level of significance

0.49 0.41 0.52 0.55 0.62 0.52 0.28 0.61 0.61

n.s. ns. -0.1
(recalculated from raw data) sea temperatures for the period between sexual determination and late February sampling were calculated and February sex ratios regressed on these data. Regressions, which were just significant (P < 0.05), were obtained using data for the periods October-January (inclusive) and October-February (inclusive) (Fig. 2). Those winters which had warmer average sea surface temperatures tended also to have male dominated Hyale populations in the high shore PelvetialFucus spiralis zone in late February. The explanation for this trend probably resides in behavioural

Fig. 2. Relationship between sex ratio (M : F) of Hyale nilssoni population sampled in late February over 11 yr and mean winter sea surface temperatures averaged from previous October 1st: for equation of line of best fit, see Table IV; ratios above 1.0 indicate male dominance.

TEMPERATURE

AND HYALE

BREEDING

243

differences, not in temperature-dependent sex determination. Perhaps females move downshore in warmer winters preparatory to acceleration of egg laying (Fig. 1). Alternative explanations based on selective female mortality at higher winter temperatures cannot be sustained since females tolerate higher temperatures than these in summer. The converse logic, that males are less cold tolerant than females and only survive in high numbers in warmer winters, is also unlikely, since HyaZe nilssoni ranges as far north as the Arctic circle where winter temperatures sink far below those encountered in the Clyde. It is equally possible, however, that males could be selectively eliminated in colder years, perhaps by predation by rock pipits (Anthus spinokttupetrosus (Mont.)) (P. G. Moore, unpubl.). Preferential consumption of larger individuals (i.e. males c.f. smaller females, see Fig. 3) during adverse winters with foraging periods of limited duration would certainly make energetic sense so far as the birds are concerned and is a well-established foraging tactic in waders feeding on amphipods in sandy beaches (Hughes, 1982) or mud-flats (Goss-Custard, 1977). SIZE-FREQUENCY

RELATIONSHIPS

Size-frequency histograms for the late February samples over 11 yr are presented for comparison in Fig. 3. Their general consistency is remarkable (see also Table I). Most year-to-year heterogeneity is seen in the size of males. Female size is much more conservative, with only the 1982 and 1983 females being significantly larger than in other years. The two sexes differed when size was correlated with environmental variables (Fig. 4). Mean size of males was significantly negatively correlated (r = - 0.70, d.f., 9, P < 0.02) with mean sea temperatures (averaged over the previous October, November, December, January and preceding days of February) for the .l 1 yr studied. Mean size of non-ovigerous females, by contrast, showed no significant correlation (r = - 0.13, d.f., 9, P > 0.1). Were year-to-year differences in February modal sizes to reflect temperature-dependent growth rates over the immediate past, then it would not seem unreasonable to expect that male and female trends would be correlated. That this is not so leads to other speculations. The most reasonable hypothesis is that colder winters support fewer males (for whatever reason, see above) and that males remaining, freed from competitive inter-male rivalries (P. G. Moore, unpubl.) are enabled to forage more efficiently, or over a wider area, and thus attain a greater size by virtue of increased food consumption. Spring breeding is initiated by the largest animals in the population. Females lay bright green eggs. Prior to their appearance in the brood pouch, these can be seen in the ovaries of the female without recourse to dissection. Fig. 5 shows data collected in two years (1974,1983) on the size distribution of females with prominent green ovaries in late February. Clearly not all the sexable females are mature and only large individuals participate in reproduction this early in the season. Hyale engages in precopula (or amplexus), during which period the male carries the passive female tucked under his ventral surface, until such time as the female moults and copulation can occur. Effective

TEMPERATURE

AND HYALE

BREEDING

245

mating therefore demands that males be bigger than females. Fig. 6 illustrates late February (1975) and mid-March (1973) size-frequency histograms in which the sizes of pairs in precopula were recorded. The sizes of linked pairs are shown as diagonal lines in Fig. 6. As would be expected, only the largest males are capable of covering the largest females. During precopula, pairs are especially vulnerable to predation (Strong, 1972) and it is interesting to note in passing that pairs in precopula were consistently the last to emerge from hiding during the extraction procedure. Given that early spring female size is independent of preceding winter temperatures (Fig. 4), yet males are scarce after harsher winters (Fig. 2), it is clearly essential for successful breeding that males remaining are of a large size (Fig. 6). Fig. 4 shows that this indeed proved to be the case. 6

I

3 1 8

I

Mea;

1’1

sea +efAOp°C

Fig. 4. Relationship between late February mean length index of males (closed stars) and non-ovigerous females (open stars) and mean winter sea surface temperatures averaged from previous October 1st over 11 yr: regression line for males indicated, equation of best fit, y = - 0.71x + 11.34; equation for females, y = - 0.07x + 4.45.

Length index Fig. 5. Size-frequency (length index) histograms of non-ovigerous female Hyale nihoni in late February of 2 yr, 1974 (top) and 1983 (bottom), indicating females with prominent green ovaries (0).

246

P. G. MOORE

The mechanisms underlying these observations now require elucidation, (1) by experimental observations on gonad maturation of Hyale kept under different daylength/temperature regimes, (2) by detailed observations on differential dispersive

Length index Fig. 6. Size-frequency (length index) histograms of Hyde nilssoni in mid-March 1973 (top) and late February 1975 (bottom), indicating the sizes ofpairs linked in precopula (diagonal lines): for shading convention, see legend to Fig. 3.

tendencies and social interactions of different reproductive categories (c.f. Moore, 1977), and (3) by observations on prey size selectivity by predators, the most significant of which is the rock pipit. DISCUSSION

The author is unaware of any other published field data on breeding initiation in amphipods covering such an extended period of time as those here presented, although Barnett’s (1971, unpubl.) data on Urothoe brevicomis and Bathyporeia spp. should eventually provide material for fruitful comparison. Barnett (1971) has reported already that breeding can be advanced artificially in the field by elevated sea temperatures (caused by the discharge of a warm water, power station eflluent). Photoperiodic effects could be disregarded in his case too, being equivalent between his polluted and control areas. Accepting the universal caution about correlation not proving causation, it can yet be fairly stated that “climate”, as evidenced here by temperature variation, has an important impact on breeding response in littoral amphipods. This response may be direct: it could also be indirect and mediated through intermediate links, e.g. food availability (Fish & Preece, 1970; de March, 1977; Sheader, 1978).

TEMPERATUREAND

HYALE

BREEDING

247

Purely by serendipity, the period investigated encompassed the warmest winter locally for 30 yr (Barnes, 1955; Moore, 1980), so the range of response recorded is probably maximal. The collated field data now establish clear guidelines for the design of future relevant experiments. These findings do not deny the potential importance of photoperiodism in amphipod breeding cycles. A number of authors have established this to be significant in amphipods (see p. 237) isopods (Madhavan & Shribbs, 1981) and decapods (Rice & Armitage, 1974; other references in Madhavan & Shribbs, 1981). It is quite likely also to be a factor of importance to Hyale. In this respect, field data on H. nilssoni breeding cycles over a wide latitudinal range would be of great interest. Some information bearing on the latter topic is available to the author and will be considered in a subsequent contribution. As de March (1977) has shown by elegant experimentation, it is likely that the controversy over photoperiodism vs. temperature effects in arnphipod breeding will be resolved eventually in terms of combinational hypotheses (see also Madhavan & Shribbs, 1981). Moore (1981), working on other species, summarized the position thus, “photoperiod, or more likely, rate of change of photoperiod (Steele et al., 1977) is responsible for gonad maturation late in the year, i.e. at a period of low sea temperatures (Segerstrale, 1970, 197 1). The expression of this physiological breeding potential is, however, held in check in spring by low temperatures. Increasing temperatures release this block, allowing peak reproduction to take place before peak temperatures are experienced”. More data on a variety of amphipods are required before we can establish firm ground rules governing the roles of photoperiodic and temperature cycles in amphipod breeding biology.

REFERENCES BAR&ES,H., lY55. Climatology and salinity data for Millport, Scotland. Glasgow Nat., Vol. 17, pp. 193-204. BARNETT, P.R.O., 1971. Some changes in intertidal sand communities due to thermal pollution. froc. R. Sot. London, iI, Vol. 177, pp. 353-364. BULNHEIM,H.-P., 1978. Interaction between genetic, external and parasitic factors in sex determination of the crustacean amphipod Gammarus duebeni. Helgol. Wk. Meeresunrers., Vol. 31,pp. l-33. FISH, J.D. Kc A. MILLS, 1979. The reproductive biology of Corophium volurator and C. arenarium (Crustacea: Amphipoda). J. Mar. Biol. Assoc. U.K., Vol. 59, pp. 355-368. FISH, J. D. & G. S. PREECE, 1970. The annual reproductive patterns of Barhyporeia pilosa and Bathyporeia pelagica (Crustacea: Amphipoda). J. Mar. Biol. Assoc. U.K., Vol. 50, pp. 475-488. GOSS-CUSTARD,J. D., 1977. Predator responses and prey mortality in redshank, Tringa rotanus (L.), and a preferred prey, Corophium volutaror (Pallas). J. Anim. Ecol.. Vol. 46, pp. 21-35. HUGIIES, J. E., 1982. Life history of the sandy-beach amphipod Dogielinorus loquax (Crustacea : Dogiclinotidae) from the outer coast of Washington, U.S.A. Mar. Biol.. Vol. 71, pp. 167-175. HYNES, H.B.N., 1955. The reproductive cycle of some British freshwater Gammaridae. J. Anim. Ecol.. Vol. 24, pp. 352-387. KINNE, O., 1961. Die Geschlechtsbestimmung des Flohkrebses Gammarus duebeni Lillj. (Amphipods) ist temperaturabhlngig - eine Entgegnung. Crustaceana, Vol. 3, pp. 56-69. LEWIS,J. R., R. S. BOWMAN,M. A. KENDALL & P. WILLIAMSON, 1982. Some geographical components in

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population dynamics: possibilities and realities in some littoral species. Neth. J. Sea Res., Vol. 16, pp. 18-28. MADHAVAN,K. &J. M. SHRIBBS,1981. Role ofphotope~od and low temperature in the control of ovigerous molt in the terrestrial isopod, ~~udillidju~ &gore (Latreille, 1804). Cnrrmceuna, Voi. 41, pp. 263-270. MARCH, B.G. E. DE, 1977. The effects of photoperiod and temperature on the induction and termination of reproductive resting stage in the freshwater amphipod Hyalella azrecu (Saussure). Can. J. Zool., Vol. 55, pp. 1595-1600. MARCH. B. G. E. DE. 1982. Decreased day length and light intensity as factors inducing reproduction in Gammarus kx.wis iacusrris Sars. Can. .I. Zool., Vol. 60, pp. 2962-2965. MOORE, P.G., 1977. Org~ization in simple communities: observations on the natural history of Hyuie niksoni (Amphipoda) in high littoral seaweeds. In, Biologi ofbenrhic orgunf.sm.s,Proc. I Ith Eur. Mar. Biol. Symp., edited by B. F. Keegan, P. O’Ceidigh & P. J. S. Boaden, Pergamon Press, Oxford, pp. 443-45 I. MOORE, P.G., 1980. Sea surface temperatures at Millport. 1959-1979. Wesfern Naf., Vol. 9, pp. 53-61. MOORE,P. G., 1981. The life histories of the amphipods Lembos websteri Bate and Corophium bonnellii Milne Edwards in kelp holdfasts. J. Exp. Mar. Biol. Ecol., Vol. 49, pp. I-50. RICE, P. R. & K. B. ARMITAGE,1974. The influence of photoperiod on processes associated with molting and reproduction in the crayfish Orcotrecres nais (Faxon). Camp. Biochem. Physioi., Vol. 47A. pp. 243-259. SEGERSTR~LE, S.G., 1970. Light control of the reproductive cycle of Ponroporeia u&u% Lindstriim (Crustacea, Amphipoda). J. Exp. Mar. Biot. Ecol., Vol. 5, pp. 272-275. SEGERSTRALE, S. G.. 1971. Light and gonad development in Pontoporeia offinis. In, 4rh Eur. Mar. Biol. Symp., edited by D.J. Crisp, Cambridge University Press, Cambridge, pp. 573-581. SHEAD~R, M., 1978. Distribution and reproductive biology of Corophium insidiosum (Amphipoda) on the north-east coast of England. J. Mar. Biol. Assoc. U.K., Vol. 58, pp. 585-596. S.I-EEI.E,V. J., 1981.The effect of photoperiod on the reproductive cycle of Gummanrs ~a~renci~nus Bousfield. J. Exp. Mar. Biol. Ecof., Vol. 53, pp. l-7. STEELE,V. J., D. H. STEELE& B. R. MCPHERSON,1977. The effect ofphotoperiod on the reproductive cycle of Gammarus serosus Dementieva, 1931. Crustaceana, Suppl. 4, pp. 58-63. STRONG, D.R. JR.. 1972. Life history variation among populations of an amphipod (Hyulella ozteca). Ecology, Vol. 53, pp. 1103-l I I I. WA-TKIN,E. E., 1941. The yearly life cycle of the amphipod, Corophium volurnfor. J. Anim. Ecol., Vol. IO, pp. 77-93. WILLIAMS,J. A., 1978.The annual pattern of reproduction of Tulifrussulfuror (Crustacea : Amphipoda : Talitridae). J. Zool., Vol. 184, pp. 231-244.