Resting Egg Production As a Life History Strategy of Marine Planktonic Copepods

BULLETIN OF MARINE SCIENCE, 37(2): 440-449,1985

RESTING EGG PRODUCTION AS A LIFE HISTORY STRATEGY OF MARINE PLANKTONIC COPEPODS

Shin-ichi Uye

ABSTRACT During the last decade, evidence of resting egg production by marine planktonic copepods has increased and provided a reasonable explanation as a mechanism by which a species repopulate regions after its disappearance from the plankton. So far, resting eggs have been found for 24 temperate coastal species belonging to Temoridae, Centropagidae, Pontellidae, Acartiidae and Tortanidae. Two types of resting eggs can be defined by the nature of hatching under various environmental conditions, i.e., diapause and quiescent eggs. Production of the former eggs has been confirmed for seven species. For three representative species (Tortanus jorcipatus, Labidocera aestiva and Acartia clausi), the seasonal life history is reviewed in relation to environmental variables. Acartia clausi (a. omorii) produces either type of resting eggs depending on its geographical distribution, which suggests that the remote populations are genetically differentiated. Strategic values of copepod resting eggs in the seasonal population biology are discussed.

In temperate coastal waters, it has long been postulated that there is some mechanism whereby a species can repopulate after its disappearance from the plankton, since the appearance of many species occurs on a seasonal basis (Fish and Johnson, 1937). Unlike freshwater copepods, resting eggs are rather new to science in marine copepods. Sazhina (1968) first indicated the presence of resting eggs for the marine calanoids Pontella mediterranea and Centropages ponticus in the Black Sea. Later, Zillioux and Gonzalez (1972) confirmed the production of resting eggs for Acartia tonsa from the east coast ofthe United States. Since then, records of resting eggs have been accumulated either by documenting their presence in bottom sediments or by demonstrating their production in nature or in the laboratory. At present, resting eggs are reported for 24 species belonging to the families Temoridae, Centropagidae, Pontellidae, Acartiidae and Tortanidae from world temperate and boreal waters (Table 1). It is now commonly accepted that resting eggs are a part of the life history of many copepod species in temperate and boreal coastal regions. Since resting eggs after release are deposited on the sea-bottom and spend a certain resting period until they hatch, the viability and development of benthic resting eggs are greatly influenced by environmental conditions of the bottom. Temperature, oxygen concentration and light condition are found to be major factors influencing their hatching (Landry, 1975; Uye, 1980; Dye and Fleminger, 1976; Uye et aI., 1979). The nature of hatching under various environmental conditions differs from species to species in the same season, and in the same species in different seasons. Two types of resting eggs can be defined. Although proper terminology to describe the state of dormancy of copepod eggs has not been established yet, these two types of dormancy can be termed respectively "diapause" and "quiescence" (Grice and Marcus, 1981). Diapause defines a state of arrested development which is genetically controlled. So far, six species (Acartia californiensis, A. tonsa, Labidocera aestiva, Pontella meadi, P. mediterranea and Tortanus !orcipatus) have been reported to produce diapause eggs. This type of egg is also produced by A. clausi in the Inland Sea of Japan, as will be described below. On the other hand, quiescence is a state of retarded development created by adverse environmental conditions. Consequently, quiescent eggs are identical 440 UYE: COPEPOD REPOPULATION STRATEGY 441

Table I. List of species for which resting eggs have been found

Family/species Locality Reference Temoridae Eurytmeora affinis Yaquina Bay, Oregon 9 E. pacifU:a Onagawa Bay, Japan 14 E. americana Buzzards Bay, Massachusetts 10 Centropagidae Centropages ponticus Black Sea I C. hamatus White Sea 3 Buzzards Bay, Massachusetts 10 C. abdominalis Inland Sea of Japan 4 C. yamadai Inland Sea of Japan 4 Sinocalanus tenellus Fukuyama, Japan 14 Pontellidae Pontella mediterranea Black Sea I Mediterranean Sea 8 P. meadi Woods Hole, Massachusetts 7 Labidocera bipinnata Inland Sea of Japan 13 L. trispinosa La Jolla, California 14 L. aestiva Woods Hole, Massachusetts 6 Epilabidocera longipedata Yaquina Bay, Oregon 9 Calanopia thompsoni Inland Sea of Japan 4 Acartiidae Acartia c/ausi Inland Sea of Japan 4 Onagawa Bay, Japan 11 Mission Bay, California 12 JakIe's Lagoon, Washington 5 Buzzards Bay, Massachusetts 10 A. tonsa Northeast U.S. 2 La Jolla, California 12 A, californiensis Mission Bay, California 12 Yaquina Bay, Oregon 9 A. erythraea Inland Sea of Japan 4 A. pacifU:a Inland Sea of Japan 14 A. pulmosa Inland Sea of Japan 14 A. tsuensis Inland Sea of Japan 14 A. steueri Onagawa Bay, Japan II Tortanidae Tortanus fordpatus Inland Sea of Japan 4

•.~"''';"' ""'Q\' ?' 7"li"". 1r~ Gonzalez (1972); 3: Pertzova (1974); 4: Kasahara et a!. (1974); 5: Landry (1975); 6: Grice and Lawson •.•.. - (,' ,,' ",~ (,""': ·1'/ '. 8: Grice and Gibson (1981); 9: Johnson (1980); 10: Marcus (1984); L 1: Uye (1980); 12: Uye and ! "",' ," .:0, '.. :: I .... ," " ,/79); 14: Uye (unpublished), to subitaneous eggs. I have found that A. clausi and A. steueri in Onagawa Bay produces only this type of egg throughout the year (Uye, 1980). There are many other species for which resting eggs are reported, but it is difficult to ascertain the type of their dormancy at present. In this paper I will review the seasonal life history of T. forcipatus, L. aestiva and A. clausi in temperate coastal waters, along with the strategic values of their resting eggs in the seasonal population biology.

Seasonal Life History of Representative Species Tortanus forcipatus in the Inland Sea of Japan. - T. forcipatus is distributed widely in tropical, subtropical and temperate waters of the Indo-Pacific. Rehman (1973) has reported this species to be present almost throughout the year in 442 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, 1985

30 Water temperature (OC)

Abundance in plankton

Type of eggs prod u ced .~~---- /Oiapause

Egg abundance in sediment

., , . ' . ;;:: Diapause ::::;::::::: ...... •...... 0· ... 00 .0_ .. • 0 ••• 0 •• 0 ••• 0 ••• 0 ••••••••• 0·· ••

• 0° .0 ••• "000 ••••••••• 0° •• •••

Hatching (OJ.) of diapause eggs at 15-20·C 100

°MJ J ASONDJ FMA Month

Figure 1. Schematic presentation of the seasonal life history of Tortanus !orcipatus in the Inland Sea of Japan. subtropical coastal waters off Karachi, Pakistan. In the Inland Sea of Japan, the occurrence of this species in the plankton is restricted to summer and fall seasons. From our previous investigations (Kasahara and Dye, 1979; Kasahara et aI., 1975), the seasonal life history of T. !orcipatus in this region can be reviewed as follows (Fig. 1). Planktonic T.jorcipatus begins to appear in May when water temperature warms to ca. 15°C, and increases in number until an annual maximum density is reached in September (water temperature: ca. 25°C). During the period from June to August, eggs spawned are exclusively subitaneous in nature, most of which will UYE: COPEPOD REPOPULATION STRATEGY 443 hatch within 1-2 days in the water column before sinking to the sea-bottom. These eggshave a case with a thin, flat disc surrounding the eggequator that aids flotation. Nauplii hatched from these eggs are recruited into the planktonic population. After the annual maximum in water temperature, the planktonic population decreases in size, and simultaneously the females begin to produce diapause eggs, which do not hatch immediately even when the temperature is still high, but undergo diapause. These eggs have a case with an incomplete disc that would provide less flotation. As water temperature decreases, the planktonic population is further reduced and completely disappears by mid-winter. In January, most of diapause eggs complete their refractory period, and they are then capable of hatching in a subitaneous manner when incubated at temperatures higher than 15°C.However, natural water temperature is at the annual minimum level at this time, and the eggs cannot hatch because of low temperature; they therefore overwinter on the sea-bottom until the temperature rises. In May, temperature at the sea-bottom warms up to 15°C and triggers the hatching of the eggs when these are resuspended from the mud by turbulence; a new planktonic population is thus formed. Environmental factors influencing the induction of diapause egg production in T. jorcipatus have not been elucidated yet. The effects of photoperiod and temperature may be important for switching the type of eggs from subitaneous to diapause, as has already been demonstrated for L. aestiva (Marcus, 1980; 1982b). Labidocera aestiva in Woods Hole Region.-L. aestiva is also a warm-water copepod reported to occur in waters along the east coast of the United States from the Gulf of St. Lawrence to the Gulf of Mexico (Turner, 1981). This species occurs year-round in waters south of Cape Hatteras, while it tends to occur sea- sonally in the plankton in the northern part of the habitat (Turner, 1981). Since the presence of resting eggs of this species was first demonstrated by Grice and Gibson (1975), intensive works have been carried out by Marcus (1979; 1980; 1982a; 1982b; 1984a; 1984b) on the ecology of its resting eggs. The following is a briefsummary ofthe seasonal life history of L. aestiva in the Woods Hole region. The pattern of life cycle of L. aestiva is very similar to that of T. jorcipatus. The planktonic population of this species appears in mid-June (water temperature: 18°C) and gives rise to a series of generations stemming from subitaneous eggs. The population is most abundant in August-September (water temperature: ca. 23°C). As temperature drops, the population begins to decrease largely owing to the decrease in egg hatching success. This is because the alternation from subitaneous to diapause egg production occurs. Marcus (1980; 1982b) has demonstrated that the type of eggs produced by the females is determined primarily by photoperiodic regulation, but the temperature regimen modifies the effect ofpho- toperiod. Under a long-day condition (18L-6D)1, L. aestiva produces exclusively subitaneous eggs, and under a short-day regimen (8L-16D), mostly diapause eggs. In the field, the major switch from subitaneous to diapause egg production occurs from late August to early September (Marcus, 1979), when daylength (maximum: 15L in June) is shortened to ca. 13L. The above-mentioned photoperiodic conditions tested by Marcus are not exactly identical to the field conditions experi- enced by L. aestiva, but it is suggested that the trend of photoperiod from long- day to short-day is important to produce diapause eggs. Although the diapause eggs do not hatch for several months when incubated at temperatures of 13-1 5°C

1 L ~ hours of light and D = hours of darkness. 444 BULLETIN OF MARINE SCIENCE. VOL. 37. NO.2. 1985

Akkeshi Bay Water temperature 20 (Oe)

I n land Sea of Japan 10

o 20 Abundance in plankton

Type of eggs produced Subitaneous .•..••.A Sa L:.j Diapause Egg abundance in sediment

F M A

Type of eggs produced Subitaneous (Quiescent)

Egg abundance in sediment

Hatching ('I.) of quiescent eggs 100

F M A M J J A SON 0 Month

Figure 2. Schematic presentation of the seasonal life history of Acartia clausi in Akkeshi Bay, Onagawa Bay and the Inland Sea of Japan.

(Grice and Lawson, 1976), they synchronously hatch when warmed to 21-23°C after being chilled at 5°C for a minimum of 40 days (Marcus, 1979). In fact, immediate hatching success becomes higher after mid-December (Grice and Gib- son, 1975). The seasonal change in abundance of the resting eggs in the bottom sediment has not been fully investigated, but the most recent study (Marcus, 1984b) has reported that diapause eggs of L. aestiva can survive after passage through the gut of polycheates. This result may not lead to increased mortality, but rather may be important in promoting the translocation of the eggs. UYE: COPEPOD REPOPULATION STRATEGY 445

Acartia clausi (A. omorii) at Various Localities in Japan. -A complex of species called A. clausi are widespread over the world oceans, and they are common in estuarine-coastal waters. Bradford (1976) made a partial revision of the subgenus Acartiura and reclassified the specimens from Japan (Tokyo Bay) as A. omorii. Although she postulated the occurrence of other species of Acartiura besides A. omorii in Japanese waters, no detailed taxonomic examinations have been carried out. Thus, I tentatively assume that all the copepods which have been called A. clausi from Japanese waters belong to the single species (A. omorii). This species is widely distributed along the coast of the Japanese Archipelago except for Ryukyu Islands, but the time of its occurrence in the plankton varies from place to place. Unlike T. fordpatus and L. aestiva, A. clausi is a rather cold-water copepod; its upper critical thermal level falls within a range between 20 and 25°C. In Akkeshi Bay, east Hokkaido, A. clausi is reported to occur throughout the year. As shown in Figure 2, the planktonic population is significantly abundant during summer when water temperature ranges from 10 to 18°C, while in the other seasons the population is small; especially during winter only a few indi- viduals remain in the plankton (Koyama, 1975). The existence of benthic resting eggshas been investigated on only two occasions, i.e., in November and February; the eggsare present at densities of 104-105 eggs m-2• They are capable of hatching immediately when incubated at 20°e. In this bay, water temperature is too cold (minimum: ca. - 2°C) for this species to reproduce well in winter, and the population can overwinter in the form of cold-adapted adults and/or benthic resting eggs. In Onagawa Bay, northeast mainland of Japan, the seasonal life history of A. clausi has been fully elucidated (Uye, 1980; 1982). As illustrated in Figure 2, the planktonic population is continuous throughout the year; it is most abundant in summer (water temperature: 20-22°C) and least in winter (water temperature: 5- 7°C). Adult females of A. clausi spawn a single type of egg, i.e., subitaneous eggs, throughout the year. Some portion of the eggs sink to the sea-bottom and undergo quiescence owing to low oxygen concentration and darkness. No diapause eggs are produced by A. clausi in Onagawa Bay. Abundance of the eggs in the sediment varies closely with the seasonal abundance of the planktonic population; they are 6 2 highest in summer and early fall (maximum: ca. 2 x 10 eggs m- ) and lowest in winter and spring (minimum: ca. 0.5 x 106 eggs m-2). Resting egg production may be unnecessary for A. clausi in this bay as an overwintering strategy, since the planktonic population is perennial. However, such a large number of benthic eggs existing in sediments may play an important role in maintaining a more constant planktonic population since it provides a pool for time-released hatching that could lead to opportunistic resurgence into the plankton. Spending a greater length of time in the egg state results in high mortality. In fact, 80-90% of eggs are lost. Such a loss of eggs may not be a waste of a potential population, but may be an obligatory sacrifice in the interest of density-dependent population control. In the Inland Sea of Japan, southwest Japan, the planktonic population of A. clausi begins to appear in November when water temperature is ca. 20°C and increases gradually in number until May-June (water temperature: 15-20°C) and then suddenly disappears (Fig. 2). No A. clausi is present between August and October, since elevated temperature (> 22°C) during that period does not allow this species to exist as plankton. There are large numbers of resting eggs in the bottom sediment; they are most abundant shortly before the planktonic population disappears and sharply decrease to a minimum level just before the copepods are about to reappear in the plankton (Kasahara et aI., 1975). Hence, aestivation is performed in the form of resting egg. Recent study has elucidated that females of 446 BULLETIN OF MARINE SCIENCE, VOL. 37, NO.2, 1985

Table 2. Seasonal change in composition of eggs spawned by Acartia clausi

% Composition of spawned eggs Surface water Day length Date of collection temperature ("C) (h) Subitaneous Diapause Non·viable 6 January 1982 9.6 10.0 81 0 19 3 February 8.2 10.6 85 0 15 12 April 11.7 12,9 76 0 24 6 May 14.7 13.7 77 0 23 19 May 16.2 14.1 77 0 23 5 June 17.5 14.4 69 5 26 9 June 18.1 14.4 51 32 17 17 June 20.3 14.4 58 18 24 23 June 21.4 14.4 54 14 32 30 June 22.2 14.4 52 18 30 7 July 23.2 14.3 No A. clausi present

A. clausi produce diapause eggs just before disappearance from the plankton in this region.

RESULTS First, I have examined the seasonal change in hatching success and time required for hatching of eggs newly spawned by field collected females between January and July. About 100-200 adult females of A. clausi were isolated from the plankton samples collected in Fukuyama Harbor, and transferred to Pyrex beakers containing 900 ml ofMillipore-filtered seawater at temperatures close to the sampling site. Eggs produced by these females within 4-5 h were incubated at different temperatures between 4.7 and 26.0°C. The results of the experiment are shown in Table 2. All the eggs produced during the period between January and May were subitaneous since their hatching success was usually higher than 80% at appropriate temperatures and the time to hatching clearly followed the Belehnl- dek's temperature function. However, after June, there were more eggs that did not hatch even within 14 days of incubation at respective temperatures. Some fraction of these eggs could hatch after they were reincubated at 15°C for 2 weeks. I, therefore, distinguished these eggs from subitaneous ones and presumed these to be diapause eggs. Second, I have investigated the influence of photoperiod on egg production in laboratory-reared A. clausi. In this experiment, the copepods were reared from egg to maturity under various temperature (15 and 20 ± 1°C) and photoperiod (10L-14D, l2L-12D, l4L-lOD) combinations. The experiments were initiated from several hundreds of eggs spawned by females taken in February. Rearing was made in 2-liter Pyrex beakers containing filtered seawater and cultured Iso- chrysis galbana (1-5 x 105 cells ml-1) and Thalassiosira weissj/ogii (1-4 x 104 cells ml-I). After copepods became mature, adult females were transferred to freshly prepared media, and eggs spawned during recent 10-12 h were incubated at various temperatures. As shown in Table 3, at both temperatures, the eggs produced by females under 1OL-14D and l2L-12D photoperiodic conditions were mostly subitaneous. However, the eggs from the beakers of l4L-10D contained many diapause eggs, although small numbers ofsubitaneous eggs and large numbers of non-viable eggs (eggs that did not hatch during 100 or 120 days of experimental period) were noted. From these results, long-day photoperiod is effective in in- ducing diapause production in A. clausi. Eggs produced under l4L-10D were incubated at 25°C; only a few eggs were observed to hatch under this condition. UYE: COPEPOD REPOPULATION STRATEGY 447

Table 3. Photoperiodic control to induce diapause egg production in Acartia clausi

% Composition of spawned eggs Temperature ("C) Photoperiod Subitaneous Diapause Non·ylable

15 ± 1 10L-14D 83 0 17 12L-12D 84 0 16 14L-I0D 4 47 49 20 ± 1 lOL-14D 82 0 18 12L-12D 84 2 14 14L-lOD 2 59 39

However, the hatching synchronously occurred at 15°C after ca. 1 month of preincubation at 25°e. Third, the seasonal change in hatching of the eggs recovered from freshly collected bottom sediments was also investigated between May and January, by incubating them at various temperatures. Hatching success during initial 2 weeks of incubation declined in June at all temperatures tested. In July, many eggs were capable of hatching immediately, but the eggs incubated at 20 and 25°C were still in diapause phase; it is especially remarkable for eggs at 25°C, whose hatching did not take place until late August. These results imply that most of eggs produced in June stay in the bottom sediment in diapause condition until late August. After that, hatching is possible, although hatched nauplii may not survive well since water temperature is still higher than 20°e. In November when water temperature drops to 20°C, the formation of a new planktonic population is possible.

DISCUSSION Marine copepods are often distributed widely extending throughout a broad latitudinal range. In northern or southern parts of their range, their appearance is confined to a certain period of the year which is favorable for their existence in the plankton. If the environment in these waters fluctuates in a predictable way, some cope pods may evolve adaptations that adjust their life cycle to cope with environmental adversity. Diapause egg production is apparently one of the strategies the species have evolved, whereby the endemic perpetuation of the population is possible. Prior to the onset of unfavorable conditions, the copepods should be able to forecast the environmental change. Previous study by Marcus (1980; 1982b) for L. aestiva and the present study for A. clausi have demonstrated that the seasonal photoperiodic variation is a primary stimuli that triggers diapause egg production. Short-day photoperiod is important for warm-water cope pods which overwinter as resting eggs, and conversely long-day photoperiod is effective for cold-water species which aestivate as resting eggs. For these species, adaptation to the fluctuating environment of their habitat has been completed. Variation in the diapause response between remotely separated populations has been found. Marcus (1984a) has investigated the effects of photoperiodicity and temperature on diapause egg production for four distantly separated populations of L. aestiva along the Atlantic coast of the United States. The population from the waters south of Cape Hatteras, where the planktonic stage tends to occur year- round, have a weak ability of producing diapause eggs under short-day photoperiod, whereas the populations north of Cape Hatteras produce diapause eggs under the same photoperiodic condition. Similarly, in the present study, A. clausi in Onagawa Bay, where the planktonic population is continuous, does not produce diapause eggs in contrast to more southern populations in the Inland Sea of Japan. 448 BULLETIN OF MARINE SCIENCE. VOL. 37. NO.2. 1985

Since diapause is a genetic trait, these results suggest that the remote populations are genetically differentiated. In the home range where the planktonic population is perennial, some species lay subitaneous eggs which are capable of surviving in the sea-bottom sediment for certain periods. Such benthic quiescent eggs are often much more numerous than the planktonic stages in the overlying water column. Since these eggs are considered as seeds for the planktonic population, it is necessary to investigate not only the planktonic process but also the benthic process for more complete understanding of the population dynamics of the marine planktonic copepods.

ACKNOWLEDGMENTS

I wish to thank Drs. T. Onbe and N. H. Marcus for critical review of the manuscript. Gratitude is also due to Mr. T. Horimoto for help in the hatching experiment of A. clausi eggs, and Dr. S. Kasahara for encouragement.

LITERATURE CITED Bradford, J. M. 1976. Partial revision of the Acartia subgenus Acartiura (Copepoda: Calanoida: Acartiidae). N.Z. J. Mar. Freshwater Res. 10: 159-202. Fish, C. and M. Johnson. 1937. The biology of zooplankton populations in the Bay of Fundy and Gulf of Maine with special reference to production and distribution. J. Fish. Res. Bd. Can. 3: 189-233. Grice, G. D. and V. R. Gibson. 1975. Occurrence, variability, and significance of resting eggs of the calanoid copepod, Labidocera aestiva. Mar. BioI. 31: 335-337. -- and --. 1977. Resting eggs in Pontella meadi (Copepoda: Calanoida). J. Fish. Res. Bd. Can. 34: 410-412. -- and T. J. Lawson. 1976. Resting eggs in the marine calanoid copepod, Labidocera aestiva Wheeler. Crustaceana 30: 9-12. -- and N. H. Marcus. 1981. Dormant eggs of marine copepods. Oceanogr. Mar. BioI. Ann. Rev. 19: 125-140. Johnson, J. K. 1980. Effects of temperature and salinity on production and hatching of dormant eggs of Acartia californiensis (Copepoda) in an Oregon estuary. Fish. Bull. 77: 567-584. Kasahara, S. and S. Uye. 1979. Calanoid copepod eggs in sea-bottom muds. V. Seasonal changes in hatching of subitaneous and diapause eggs of Tortanua !orcipatus. Mar. BioI. 55: 63-68. --, -- and T. Onbe. 1974. Calanoid copepod eggs in sea-bottom muds. Mar. BioI. 26: 167- 171. --, -- and --. 1975. Calanoid copepod eggs in sea-bottom muds. II. Seasonal cycles of abundance in the populations of several species of copepods and their eggs in the Inland Sea ofJapan. Mar. BioI. 31: 25-29. Koyama, A. 1975. Studies on zooplankton community in Akkeshi Bay, Hokkaido. Ph.D. Thesis, Hokkaido Univ. (in Japanese). Landry, M. R. 1975. Dark inhibition of egg hatching of the marine copepod Acartia clausi Giesbr. J. Exp. Mar. BioI. Ecol. 20: 43-47. Marcus, N. H. 1979. On the population biology and nature of diapause of Labidocera aestiva (Copepoda: Calanoida). BioI. Bull. 157: 297-305. --. 1980. Photoperiodic control of diapause in the marine calanoid copepod Labidocera aestiva. BioI. Bull. 159: 311-318. --. 1982a. The reversibility of subitaneous and diapause egg production by individual females of Labidocera aestiva (Copepoda: Calanoida). BioI. Bull. 162: 39-44. --. 1982b. Photoperiodic and temperature regulation of diapause of Labidocera aestiva (Co- pepoda: Calanoida). BioI. Bull. 162: 45-52. --. 1984a. Variation in the diapause response of Labidocera aestiva (Copepoda: Calanoida) from different latitudes and its importance in the evolutionary process. BioI. Bull. 166: 127-139. --. 1984b. Recruitment of copepod nauplii into the plankton: importance of diapause eggs and benthic processes. Mar. Ecol. Prog. Ser. 15: 47-54. Pertzova, N. M. 1974. Life cycle and ecology ofa thermophilous copepod Centropages hamatus in the White Sea. Zool. Zh. 53: 1013-1022 (in Russian). Rehman, F. U. 1973. Observations on variation in a planktonic copepod, Tortanus !orcipatus (Giesbrecht, 1889) from the inshore water of the Karachi coast, Pakistan. Crustaceana 25: 113- 117. UYE:COPEPODREPOPULATIONSTRATEGY 449

Sazhina, L. I. 1968. On hibernating eggs of marine Calanoida. Zool. Zh. 47: 1554-1556 (English translation by the Fish. Res. Bd. Can.). Turner, J. T. 1981. Latitudinal patterns ofcalanoid and cyclopoid copepod diversity in estuarine waters of eastern North America. J. Biogeogr. 8: 369-382. Dye, S. 1980. Development of neritic copepods Acartia clausi and A. steueri. I. Some environmental factors affecting egg development and the nature of resting eggs. Bull. Plankton Soc. Japan 27: 1-9. ---. 1982. Population dynamics and production of Acartia clausi Giesbrecht (Copepoda: Cal- anoida) in inlet waters. J. Exp. Mar. Biol. Ecol. 57: 55-83. --- and A. Fleminger. 1976. Effect of various environmental factors on egg development of several species of Acartia in Southern California. Mar. BioI. 38: 253-262. ---, S. Kasahara and T. Onbe. 1979. Calanoid copepod eggs in sea-bottom muds. IV. Effects of some environmental factors on the hatching of resting eggs. Mar. BioI. 51: 151-156. Zillioux, E. J. and J. G. Gonzalez. 1972. Egg dormancy in a neritic calanoid copepod and its implications to overwintering in boreal wates. Pages 217-230 in B. Battagia, ed. Fifth European marine biology symposium. Piccin Editore, Padova.

DATEACCEPTED: January 28, 1985.

ADDRESS: Faculty of Applied Biological Science, Hiroshima University, Fukuyama 720, Japan.