or arrested development of nonencysted copepodids or adults . Ecologically ... is defined as retarded development in direct response to a limiting factor (e.g. low ...
199
Hydrobiologia 306: 199-211, 1995 . © 1995 Kluwer Academic Publishers. Printed in Belgium.
Dormancy in the Copepoda - an overview Hans-U . Dahms Department of Biology, University of Waterloo, Waterloo, Ontario, N2L 3G1 Canada Received 15 June 1994 ; in revised form 15 June 1994 ; accepted 21 June 1994
Key words : Diapause, ecology, evolution, life history, marine, freshwater, Copepoda
Abstract Dormancy affects copepods in their anatomy, physiology, genetics, population biology, community ecology, evolution and local and geographic distribution . It is known from freeliving representatives of three copepod taxa, namely the Harpacticoida, Cyclopoida and Calanoida . Species showing dormancy occur in various realms and habitats, both freshwater and marine, being benthic, planktic or ice-dwelling . Depending on the taxon, dormancy occurs at various times of the year, prevailing in higher and temperate latitudes . Copepod dormancy is expressed in various ontogenetic stages, such as resting eggs, arrested larval development, juvenile and adult encystment, or arrested development of nonencysted copepodids or adults . Ecologically, dormancy is an energy saving trait, allowing the individual to bridge periods of environmental harshness . Adverse environmental conditions could be abiotic (e .g . desiccation, temperature, oxygen availability) or biotic in nature (e .g . food availability, predation) . Diapause s . str. i s initiated, maintained and terminated by triggering factors (e .g . photoperiod, temperature, chemical cues, population density/physiological factors) . The dormant state and emergence patterns directly affect reproduction, population dynamics, community composition, coexistence and distribution of copepods, as well as the phenology of their predators and living food items . Populations having dormancy, in most cases belong to and affect communities of two realms : the water column and the bottom . Dormant stages may provide means for dispersal as well as for staying in special localities . The variability of dormancy permits flexible and complex life histories. Dormancy is subjected to and on the other hand affects copepod evolution . Introduction Organisms living in occasionally deteriorating environments either have to improve the environment to their needs, migrate to more suitable areas, or must become dormant for the time of environmental deterioration . For small organisms, like the Copepoda, dormancy is the only strategy to bridge adverse seasons . Adverse conditions refer not only to the physical environment but also to biotic interactions like competition or predation . Dormancy is not simply a cessation of development, but involves structural and physiological changes . Danks (1987) broadly defined `dormancy' as a `state of suppressed development' presenting either `quiescence' or 'diapause' s . str. The latter is defined here as arrested development which is triggered by environmental factors, but is compulsory and ulti-
mately genetically determined . It is a response to predictable, cyclic changes in the habitat and is initiated by fixed ontogenetic instars . Diapause is distinguished from quiescence (i . e. pseudo-diapause), which is defined as retarded development in direct response to a limiting factor (e .g . low temperature, scarcity of food) without prior acclimation . It is a short-term and irregular phenomenon, does not ensure long term viability, is not fixed to a certain ontogenetic stage, and may be induced repeatedly in the same individual . As a life history phenomenon of the Copepoda, dormancy varies considerably in relation to taxon, ontogenetic stage, latitude, climate (both the latter factors are mainly characterized by shifts of photoperiod and temperature) and other abiotic and biotic factors . Being flexible, dormancy may be regarded as a buffer system of the life cycle, providing survival in unfavourable times .
200 Because most studies on dormancy in Copepoda do not distinguish between diapause s . str ., and quiescence, this overview reports of all `forms of suspended development' in the Copepoda .
and Cyclopoida, and towards species from the marine realm in the Calanoida (Table 1) . Whether the total lack of dormancy reports from marine Cyclopoida is real or simply has not been documented, remains to be shown .
Copepod taxa performing dormancy Developmental stages initiating dormancy Dormancy is known exclusively from freeliving taxa of the Harpacticoida, Cyclopoida and Calanoida (Table 1) . It is noteworthy that there are no symbiotic copepod taxa among Copepoda known to show dormancy. There is no report hitherto from the Platycopioida, Mormonilloida, Poecilostomatoida, Siphonostomatoida, Monstrilloida, Misophrioida or the Gellyelloida . There are 3 harpacticoid genera that exhibit dormancy, namely Canthocamptus from freshwater and Heteropsyllus and Drescheriella from marine waters . All cyclopoid taxa known to have dormancy belong to the Eucyclopinae (Cyclopidae) . The 3 cyclopoid genera with encysting copepodids are Cyclops, Microcyclops and Metacyclops . Nonencysted dormancy involves species of Thermocyclops, Mesocyclops, Cyclops, Acanthocyclops, Diacyclops, Eucyclops, and Macrocyclops . There are 16 species of the freshwater Calanoida, where there is proof for resting eggs . They belong to the genera Diaptomus, Onychodiaptomus, Leptodiaptomus, Aglaodiaptomus, Acanthodiaptomus, Scotodiaptomus, Eurytemora, Epischura and Limnocalanus . Genera from marine environments with resting eggs include 27 species belonging to Pontella, Labidocera, Anomalocera, Tortanus, Calanopia, Acartia, Centropages, Temora, Eurytemora, and Sinocalanus . Four species of Acartia, Epilabidocera and Eurytemora with resting eggs are reported from brackish waters . The calanoid genera belong to the Centropagidae, Temoridae, Pontellidae, Acartiidae and Tortanidae ; all of these families belong to the Centropagoidea (Bowman & Abele, 1982) . Calanoids which possess nonencysting resting copepodids are reported from 7 marine species of Calanus, Neocalanus, Calanoides and Pseudocalanus . It seems likely, though, that several other species can undergo a form of dormancy as well (cf . Conover, 1988 ; Miller et al ., 1991) . There are some indications of dormant calanoid copepodids resting on the sea bottom (cf . Elgmork, 1967) . There is a bias of dormancy reports towards freshwater species in the Harpacticoida
Dormant instars may comprise resting eggs, naupliar stages arrested in their development, and freeswimming or encysted copepodids and adults . Resting eggs Most of the copepod dormancy studies deal with resting eggs as dormant stages in the Calanoida (cf . Grice & Marcus, 1981) . These can be diapause as well as quiescent eggs . Both types of eggs are actually fertilized eggs or zygotes . lanora & Santella (1991) show that the resting egg capsules of Anomalocera patersoni even contain advanced dormant embryos . A morphological distinction between egg types can be difficult, though diapause eggs of some species are reported to be slightly larger, ornamented, or of darker colour than subitaneous eggs (= hatching without delay) . Uye (1985) shows that 7 out of 24 marine calanoids develop through diapause s . str. eggs ; the remaining species produce subitaneous eggs which become quiescent in the sediment for variable periods . The thicker chorion of diapause eggs may provide a protection against digestion by predators (Hairston & Olds, 1984 ; Marcus & Schmidt-Gegenbach, 1986), desiccation and bacterial degradation . Calanoid diapausing eggs can remain viable for at least 3 years and perhaps for more than 15 years (Hairston & De Stasio, 1988) . Resting eggs can be produced at faster rates by the females of Diaptomus leptopus, because subitaneous egg clutches have to be carried for longer than resting egg clutches (Watras, 1980) . Dormant nauplii Delayed naupliar development is reported from four species of marine Harpacticoida (Coull & Dudley, 1976) and two species of marine Calanoida (Uye, 1980) (Tab. 1) . This life habit enables the nauplii to survive longer in a particular habitat in order to extend the utilization of resources or to ensure a more stable population density . It remains to be shown, however, whether prolonged naupliar periods represent a form of dormancy, or are just immediate responses to
20 1
QUIESCENCE
DIAPAUSE
Direct response to adverse conditions .e .g . : -low temperature -food shortage
Induction at sensitive stages by the following possible triggering factors : A . External factors -photoperiod -temperature -population density
COMMUNITY E}FECTS Community composition and dynamics of plankton and benthos : -migration/emergence -predator/prey dynamics -co-existence
B . Internal factors -"biological clock" -neurosecretions -lipids -metabolites
ADAPTIVE SIGNIFICANCE A . Bridging periods of environmental stress : -drought -high/low temperatures -oxygen deficiency -starvation -predation -competition Fig . 1 .
B . Other arguments of adaptive value -energy saving -temporal resource partitioning -reproduction timed for food pulses -synchronized reproduction -genetic variability and storage -dispersal/persistence -complex life histories/bet hedging
Copepod dormancy - mechanisms, effects and functions .
unfavourable conditions . Suspended growth may also be due to the fact that these stages are non-feeding and can rely on their stored yolk for energy requirements . Dormant copepodids Diapausing nonencysted calanoid and harpacticoid copepodids do not feed, there is no movement of the intestine, they survive on stored lipid resources, and they usually drift in the water with infrequent swimming motions (Hirche, 1983 ; Dahms et al., 1990) . In diapausing copepodids of two Calanus species, mor-
phological changes in the gut epithelium are observed as well as a reduction in digestive enzymes greater than normally associated with starvation (Hallberg & Hirche, 1980) . Low amylase and trypsin activity, together with almost undetectable ammonia excretion of copepodids V of Calanus finmarchicus, indicates a very low metabolic activity (Tande, 1982) . As for the Cyclopoida, Fryer & Smyly (1954) describe nonencysted dormant copepodids with a bent abdomen, the swimming legs directed forward, having a rigid body, and being motionless and colourless . Even fertilized females of Cyclops strenuus are shown
202 Table 1 . Copepod species from different habitats showing various types of dormancy (after
the records of 178 publications) . Marine (brackish) HARPACTICOIDA
CYCLOPOIDA
CALANOIDA
resting eggs : dormant nauplii : nonencysted copep . : encysted copepodids : resting eggs : dormant nauplii : nonencysted copep . : encysted copepodids : resting eggs : dormant nauplii: nonencysted copep . : encysted copepodids :
to be dormant (Naess & Nilssen, 1991), although copepodid IV is most frequently observed to diapause in this species (Elgmork, 1980) . The time in diapause is 2 .5 months and up to 1 year for a portion of the population of C. strenuus (Elgmork, 1959) . Elgmork & Nilssen (1978) discuss the equivalence of copepod and insect diapause. They suggest for nonencysted freshwater Cyclopoida that their dormancy phases consist of a preparatory phase (a), induction phase (b), refractory phase (c), activated phase (d), and a termination phase (e) ; characteristics of each phase are : - (a) where the gut is emptied, the number and size of lipid globules increase in the body cavity and the instars accumulate above the bottom sediments - (b) where populations show a rapid increase in number of dormant instars - (c) with deep torpor (= lethargy) and low metabolic rate, and enhanced ability to survive anaerobiosis ; here development cannot resume even if environmental conditions are favourable - (d) with diminishing torpor and gradually rising emergence - (e) all dormant stages leaving the sediment, a short period with subsequent growth, development and reproduction . Copepods, however, deviate from the insects in that different developmental stages are usually capable of dormancy in the same species . Elgmork (1962) even shows that 4 stages are found in dormancy for Cyclops scutifer .
Freshwater resting eggs : 4 1 1
27(4) 2 7
dormant nauplii : nonencysted copep . : encysted copepodids : resting eggs : dormant nauplii : nonencysted copep . : encysted copepodids : resting eggs : dormant nauplii :
1
6
24 3 15
nonencysted copep . : encysted copepodids :
Encysted copepodids are known from the Harpacticoida and the Cyclopoida . With one exception they are exclusively freshwater. The exception is the marine harpacticoid Heteropsyllus nunni known to encyst primarily during summer, exclusively as adults (Coull & Grant, 1981) . A gross chemical analysis of the cyst wall of Canthocamptus staphilinoides shows that it is composed of cuticulin, but does not contain protein, lipid, mucin nor chitin (Deevey, 1941) . Encysted dormant stages enhance the dispersal potential of organisms when being transported on the feathers, fur or in the intestine of larger animals (e .g . Thienemann, 1950 ; Marcus, 1984a), or by currents, waves and wind . There is, however, no conclusive evidence about the frequency and success of such dispersal pathways . Hairston & Munns (1984) suggest for eggs of freshwater Calanoida, that dispersal events happen only occasionally, and are not a viable adaptive strategy maintaining the dormancy trait . On the other hand, benthic dormant stages may be advantageous in keeping a planktic population in a certain area which is otherwise subjected to currents or drift . This may especially hold for planktic resting eggs of coastal Calanoida retained under the pelagic range of their parents in the bottom substrate .
20 3 Occurrence of dormancy as defined by habitat, latitude and season Habitat Except for one species, all of the diapausing Harpacticoida are mud-dwelling forms of shallow fresh and marine waters (Table 1) . The exception is provided by non-encysted copepodids of Drescheriella racovitzai (Dahms & Schminke, 1992) from high Antarctic melting pools, suspected to be planktic during their nonsympagic (= sea-ice-dwelling) existence (Dahms, 1991) . Dormancy among freshwater copepods is not restricted to ephemeral habitats, but occurs also in deeper water bodies . Dormant freshwater Cyclopoida are represented mainly as nonencysted or encysted copepodids . Migration is intimately connected with cyclopoid diapause as is emphasized by Elgmork (1967) . He noted that diapausing cyclopoid copepodids select a particular area of a lake, and actively penetrate deep into the bottom substrate . Some species seem to concentrate in the deepest part of the lake while others are confined to the slope, depending also on the abiotic conditions . Resting eggs, accumulating at the bottom refugium, are produced by freshwater Harpacticoida and Calanoida and marine neritic calanoid species . In freshwater Calanoida, diapausing eggs are concentrated in the deepest sediments (De Stasio, 1989 ; Ban, 1992) . Miller et al. (1991) found the resting stock of copepodid V of a Calanus finmarchicus population consistently centered near the 500 m isobath . Latitude There is a latitudinal tendency for dormancy ; it prevails in higher latitudes and decreases towards the tropics (Watson, 1986) . Burgis (pers . comm. cit. Nilssen, 1980) states that freshwater Cyclopoida show no dormancy under tropical conditions . Nilssen (1980) argues that diapause would not be of selective advantage in the tropics, for most environmental factors, like predation patterns and food availability, remain constant . However, Rzoska (1961) reports encysted copepodids of Metacyclops minutus from temporary rainpools of tropical Sudan . Miller et al. (1991) mention copepodid V dormancy for the tropical marine calanoid Calanoides carinatus. Important environmental factors, whether abiotic or biotic, seem to be not constant or stable, but rather are often less predictable in the tropics . Wyngaard (1988) shows a complete shift in dormancy phenology in populations of Mesocyclops edax
from Michigan lakes, where they are dormant during winter, to continuous reproduction in more southern Florida lakes . Crossbreeding experiments demonstrated a genetic differentiation in the dormancy performance between the Michigan and Florida populations of this species . In Calanus finmarchicus, arrested development always occurs in the later (= preadult) copepodid stages, but the stages involved differ within the species with latitude (Tande, 1982) . This species is found to overwinter as copepodid III or IV under arctic and subarctic conditions, but as copepodid IV or V at lower latitudes . Season As mentioned earlier, most reports of copepod dormancy are from temperate regions or higher latitudes, which show marked annual cycles . Here, the timing of life history phenomena is important . One can differentiate between two groups : `summer resting stages' and `winter resting stages' and some intermediate and overlapping cases (Elgmork, 1967) . As for the Harpacticoida, Canthocamptus arcticus is reported to diapause as resting eggs for 10 months from July to April (Borutzky, 1929) . The seasonal phenology of Drescheriella racovitzai is not clarified as yet (Dahms et al., 1990) . Encysted adult harpacticoids prevail in summer. As for the Cyclopoida, encysted and nonencysted forms are reported throughout the year . Many of the studies mention summer encystment . Two genera show exclusive winter dormancy as nonencysted copepodids : Mesocyclops and Thermocyclops, with the exception of the North American Mesocyclops edax, which develops a copepodid IV summer resting stage (Wyngaard, 1988) . Marine calanoid resting eggs usually are released after the population declines from the plankton; this is in autumn for most of the species (cf . Uye, 1985) .
Induction and termination of diapause Proximate factors Several environmental factors are hypothesized to be responsible for the onset of diapause . For populations of Cyclops strenuus, Elgmork (1967) observes diapause to start at the same time in small littoral, warm, well aerated ponds and in a stratified lakelet with an anaerobic hypolimnion . This led him to the hypothesis that diapause is primarily cued by the length of day .
2 04 There is also strong experimental evidence for the regulation by photoperiod (e .g . Einsle, 1964) . Spindler (1971) demonstrates that diapause for Cyclops vicinus is induced by a long-day regime, but can be terminated earlier by short-day conditions . The marine calanoid Labidocera aestiva reared at 15 °C produced subitaneous eggs under a photoperiod regime of 18L :6D, whereas copepods exposed to a shortday regime of 8L : 16D produced mainly diapause eggs (Marcus, 1980) . Temperature may modify the effect of the photoperiod (e .g . Hairston et al., 1990 ; Marcus, 1982) . Studying temperature and salinity effects on resting eggs of Acartia californiensis, Johnson (1980) argues that the production of dormant eggs and the termination of dormancy is temperature dependent, and eggs may become dormant below 15 °C . Salinity does not induce dormancy in this species . For Cyclops vicinus a response to environmental stimuli is sexually differentiated, with the majority observed entering diapause in this species being males (George, 1973) . There is a positive correlation between the degree of torpidity in freshwater cyclopoids and the duration of the period spend in torpor . However, according to Elgmork & Nilssen (1978) the degree of torpidity is not correlated with depth, trophic level or humic content, nor with the type of circulation in the water body. Diapause eggs cannot be induced to hatch for a certain period (i .e . the refractory phase), even if environmental conditions are favourable (Ban & Minoda, 1991) . Williams-Howze & Coull (1992) could not confirm effects of photoperiod or temperature cues on the induction or inhibition of encystment in the marine harpacticoid Heteropsyllus nunni . They suggested that internal genetic cues, connected to specific ontogenetic stages, must be responsible for diapause induction in this species . Annual seasonality characterized by a change of photoperiod and temperature is the most common cycle associated with diapause, but other cycles are possible, such as the lunar cycle or its associated tidal cycle (cf . Hairston, 1987) . Diapause termination for resting eggs has been hypothesized to be stimulated by the following factors : temperature increase, desiccation, light, high or low oxygen concentration and coverage by bottom sediments (Ban & Minoda, 1991) . For bottom resting stages it seems unlikely that the termination of diapause is a response to changes in photoperiod . Although the optical density of natural waters is frequently low early in the year, only dormant instars near the surface would detect incident light (George, 1973) . Also, resting eggs
probably lack appropriate receptors to perceive light . Uye et al. (1979) argue that the hatching inhibition in the sediment is mainly caused by microaerobic sediment conditions . However, burying the eggs in the mud also creates darkness . Darkness completely and immediately suppresses hatching of the eggs of the marine calanoid Acartia clausi (Landry, 1975) . According to Marcus (1984a), turbulence due to bioturbation is sufficient to promote hatching . Bioturbation may provide a mechanism for the continuous turnover of sediments and the gradual release of individuals from the seabottom . According to Brewer (1964), the specific stimulus inducing the hatching of diapause eggs in Diaptomus stagnalis and D. caducus is the reduction of oxygen . He suggests that this is effected by the biological environment of the eggs, such as the bacteria . Smyly (1962), finds similar rates of revival of resting copepodids of Mesocyclops leuckarti in aerated and stagnant substrate samples . Copepods are well equipped with mechanical and chemical receptors (cf. Strickler & Twombly, 1975) that are likely to detect other qualities of environmental information, for example the presence of predators, changes of phytoplankton concentrations, or population density . Such complex stimuli could directly affect the induction and termination of individual dormancy phenologies . However, Hairston et al. (1990) could not confirm any direct onset of diapause or any more subtle effects of fish predators on diapause timing in field experiments with Diaptomus sanguineus . Still other factors, such as crowding and food limitation, may be responsible for diapause induction . Ban (1992) provides evidence that high density in Eurytemora affinis cultures induces diapause egg production . However, he did not find food quality and quantity to affect diapause egg production of E. affinis. In this laboratory study competition for food was excluded, and excretory metabolic products or pheromones are discussed as dormancy induction factors . Walton (1985) shows that females of Onychodiaptomus birgei make subitaneous eggs first, then diapausing eggs as they age . Internal conditions The mechanisms responsible for diapause induction or termination are poorly studied in the Copepoda . lanora & Santella (1991) mention the hypothesis developed for insects that diapause results from an accumulation of an inhibiting substance and ceases when this is destroyed . As for most temperate-zone insects, Tauber
2 05 et al. (1988 cit . Miller et al., 1991) find no specific diapause-terminating stimuli . Insects cease to respond to diapause-maintaining factors, thus terminating diapause gradually and spontaneously . Internal stimuli would be helpful for the induction or arousal of diapause in uniform environments, as with constant temperature and light conditions (e .g . in the sediment or deep water layers of large water bodies) . Timing of diapause is possibly coupled with still unknown internal triggers . Corkett & McLaren (1969) propose for Pseudocalanus sp . that the nutritional state (i.e. lipid content) of the copepodid V cues physiological events which induce diapause . Busa & Crowe (1983) suggest that embryonic diapause is regulated by intracellular pH in Artemia salina cysts. An abundant granular secretion in neurosecretory cells of the cerebral region of Calanus finmarchicus and C. helgolandicus is found to be responsible for the control of diapause, moulting and overwintering metabolism and behaviour (Carlisle & Pitman, 1961) . Also, there is widespread mention in the literature (e .g . Elgmork, 1967, Miller et al., 1991, Williams-Howze & Coull, 1992) of a long-term endogeneous timer (i.e . an internal or biological clock) cueing the arousal and especially the termination of copepod diapause . Sensitive stages Ban (1992) suggests that the type of eggs (subitaneous or diapause eggs) being produced by Eurytemora affinis are determined by the environmental conditions experienced during the naupliar stages of their mothers . Hairston & Olds (1987) were able to induce individual females to switch between subitaneous and diapausing eggs by changing temperature and photoperiod . Uye (1980) argues for marine calanoid resting eggs that the variability in hatching time is due to arrested embryonic development, probably at various sensitive stages of the eggs . However, it is also possible that the active phase is of different duration once dormancy is cued, depending on the individual history of the resting eggs . Spindler (1971) does not find any particular sensitive stage in photoperiod experiments with Cyclops vicinus . The whole predormant period is said to be susceptible to triggering conditions .
Ecological significance of dormancy Adaptive significance on the population level A low metabolic cost of the diapause phase (Watson & Smallman, 1971) assures that diapausing individuals have more energy available than those remaining active. A temporary retreat during dormancy may enable species also to partition resources on a temporal scale, and allow them to co-exist within a given habitat (cf. Marcus, 1984b ; Watson, 1986) . Under extreme conditions, dormant stages may be the only means of survival and recruitment in a given locality. Therefore, dormancy enables the members of a population to bridge periods of environmental harshness in order to occupy niches in regions which would otherwise be less accessible . Summer resting stages of freshwater copepods, for instance, are means to withstand draught in temporary water bodies or high summer temperatures and accompanying low oxygen concentrations . Deevey (1941) concludes that encystment is an efficient way of surviving summer anaerobiosis in the harpacticoid Canthocamptus staphylinus . However, a low oxygen consumption of encysted individuals may only be an associated factor following a slowed down metabolism, and not the ultimate adaptation . Dormancy is also proposed to be a mechanism to avoid predators (e .g . Strickler & Twombly, 1975 ; Hairston, 1987) . The latter author shows for Diaptomus sanguineus a close fit between the dates that females switch from producing subitaneous eggs to diapausing eggs and the presence or increased activity of predators . These findings are further supported by a theoretical model which predicts similar switching dates to those observed in the field by incorporating seasonal increases in predation . Also, dormant individuals can bridge unfavourable periods between seasonal pulses of food abundance . This may hold for polar oceans, which are characterized by markedly seasonal primary production cycles, followed by seasonal vertical migrations, seasonal reproduction, and overwintering stages of marine Calanoida (Smith & Schnack-Schiel, 1990) . Resting eggs of Labidocera aestiva (Grice & Gibson, 1975) are said to serve as a means to overwinter, and to provide a mechanism of repopulation in spring after the population totally disappears from the plankton during winter. Grigg & Bardwell (1982) state that metabolic variations with dormancy are evidently small in Calanus finmarchicus (in contrast to the findings of, e .g ., Watson & Smallman, 1971 ; Tande, 1982), and
206 find it unlikely that dormancy is a metabolic adaptation that enhances the survival of overwintering individuals. They interpret dormancy as an adaptation that synchronizes breeding with phytoplankton productivity . Advanced ontogenetic stages may have an advantage in the spring when their young can be released during the vernal phytoplankton bloom (Allan, 1976) . Hence, dormancy provides also a means of synchronized emergence . Marcus (1979) argues that this promotes the reproductive success of the first generation to appear in the plankton again, by ensuring that individuals will attain reproductive maturity at the same time . As Nilssen (1980) emphasizes, the timing of co-occurrence of individuals is necessary for efficient reproduction . This will be difficult to accomplish in low density populations with asynchronous development. Community effects The timing of dormancy and patterns of emergence are important in determining community structure and dynamics, even during periods when there is little environmental stress (De Stasio, 1990) . This author also gives the example of resting eggs being dormant for several years . With the annual production of new dormant eggs, several generations may be present in the sediments . In combination with environmental variability affecting reproductive success, this situation can lead to the co-existence of competing species in communities through what is called the `storage effect' (Warner & Chesson, 1985) . Reproductive success from good years can be stored, acting as a buffer, and subsequently allow persistence through years when reproductive success is poor . Dormant stages and the benthos Benthic resting stages represent an important source of recruitment to the plankton . They also have an impact on benthic processes . Benthic resting stages are regarded here as another component of `temporary meiofauna' . They will not use benthic food resources, but their presence adds to the potential prey available to benthic consumers . Kasahara et al. (1974) estimate maximum density of marine copepod eggs in the sea bottom to be as high as 3 .4 x 106 x m -2 from a sample collected in early summer in the Seto Inland Sea, Japan . Resting copepodids of cyclopoids are found as deep as 30 cm into the mud (Elgmork, 1959) . Lacroix & LescherMoutoue (1984) found the mean biomass of benthic resting stages to be equal to 36% (15%-80%) of the
total cyclopoid biomass in the shallow Lake Creteil, France. The benthic abundance varied from 27 000 m_2 individuals x m-2 to 350000 individuals x and gave a potential recolonization level of the open water area of 6-78 individuals x 1 -1 . However, a study by Sarvala (1979) on a Finnish lake shows that the contribution of cyclopoid resting stages to the benthos is only a few percent of the overall benthic animal production . Marcus (1984a) demonstrated that both subitaneous and diapause eggs of Labidocera aestiva remain viable after being consumed by the polychaetes Capitella sp . or Streblospio benedicti. She suggests that the temporal decline in egg abundance reported for the uppermost sediment layer is more likely due to the translocation of eggs from the surface than to mortality caused by predators . Benthic resting stages themselves are greatly influenced by environmental conditions at the bottom . Temperature, oxygen concentration and light conditions are found to be major factors influencing the viability and hatching of resting eggs (cf . Uye, 1985) .
Variable dormancy responses and complex life histories Dormancy in copepod species is characterized by a remarkable intra- and interspecific variability of occurrence and timing . This may allow copepod populations to respond to particular niche requirements in a spatially or temporally variable environment . According to Watson (1986) there are two major patterns of variability, which follow a latitudinal gradient or are present in different sized waterbodies of the same locality . Interpopulational examples of latitudinal difference are given above . Another case study is provided by Marcus (1980), who finds populations of Labidocera aestiva from Woods Hole to produce resting eggs, whereas more southern populations from Florida do not. The calanoid Acartia clausi does not produce diapause eggs in Onagawa Bay in contrast to more southern populations in the Inland Sea of Japan (Uye, 1985) . This differentiation is thought to be genetically based and to be a response to different selection pressures in each region . An example of different life cycles in waterbodies of the same region is provided by Elgmork (1980) for Cyclops scutifer . These extend from a simple annual cycle to a complex life history, with and without diapause, and life cycles of 2 and 3 years . The different life history strategies and the varying proportions of
207 ontogenetic stages in the plankton and diapause stages in the sediment are said to be regulated by a complex interplay of abiotic and biotic factors, such as a lack of oxygen or food and enhanced predation . In one population of C. scutifer both a period of reproduction and dormancy of bottom resting stages occurs during the winter. Nilssen (1980) interprets the adaptive significance of fractionating the C. scutifer population as being a compromise between avoiding size-selective predation and the expectation of future offspring production . A larger-sized, biennial fraction exhibits a 'big-bang' strategy with larger clutches within a short period of time when food is in abundance, while a smaller-sized, annual fraction produces smaller clutches over a longer part of the life period . Fryer & Smyly (1954) explain dormancy differences of a Mesocyclops leuckarti population in the same habitat by the differential exposure of parts of the population to an environmental gradient, in this case temperature . Hairston & Olds (1984) conclude from reciprocal transfer experiments with Diaptomus sanguineus, which show population differences in the timing of diapause, that their respective populations are genetically adapted to the specific conditions of isolated ponds . The same authors (1980 ; 1987) show distinct photoperiod responses in the populations they studied . Watson (1986), on the other hand, argues that variability in diapause is a response to prior environmental signals resulting in different proportions of populations entering diapause in different localities at different times of the year. The environmental signals are said to be interactions of photoperiod and temperature . When reared under some combinations of these two factors, either all or none of the individuals from the same population may enter diapause . An intermediate range of conditions produces a varying proportion of animals entering diapause . According to Watson & Smallman (1971) there is a considerable flexibility in the physiological basis of diapause control within local populations . Although there is unquestionably a genetic basis for diapause control, authors disagree to what extent environmental factors modify diapause and are responsible for the observed variability of the diapause response . Any conclusions on the hereditary basis of dormancy response, however, should be made with caution . Even the environment of mothers (e .g . their exposure to different temperature or light regimes) is suggested to influence the diapause response of their offspring (Ban, 1992) .
There are several other mechanisms indicated in the litterature that allow dormancy to be temporally and spatially variable, for instance : facultative diapause, the necessity of a suitable induction factor, reversibility potential, different stages being sensitive for induction, or 'bet-hedging' (sensu Stearns, 1977) . In Cyclops strenuus only copepodids of the first spring generation perform diapause (Elgmork, 1959) . Wierzbicka (1962) states that cyclopoid copepodids kept without access to mud may omit the resting stage and subsequently reach maturity without diapause . Many calanoid species switch between subitaneous and diapause egg production (e .g . Hairston & Olds, 1986) . Coker (1933) shows that an exposure to low temperatures promotes a resumption of development in Cyclops vernalis in the free swimming state . Dormant cyclopoid copepodids removed from a reservoir before the onset of winter can be induced to break diapause by increasing the temperature after a short period of exposure to cold (George, 1973) . Uye (1980) observes a high variability in hatching time of resting eggs, indicating possibly that the embryonic development is not arrested at a fixed developmental stage . Hairston et al. (1985) proposed a model for highly variable periods of adverse conditions, where the ESS (=evolutionary stable strategy) for females to lay both subitaneous and diapausing eggs regardless of the time of the year is a bet-hedging trait . Walton (1985) observed just this kind of response in a small pond population of Onychodiaptomus birgei . Insects provide evidence for a complex polygenic control of diapause (Hoy, 1978 cit . Grice & Marcus, 1981) . Wyngaard (1988) showed the same for freshwater Cyclopoida, and Hairston & Dillon (1990) show heritability of the diapause timing trait in Diaptomus sanguineus both in the laboratory and in the field . It should be mentioned, finally, that some of the observations indicating `variability in diapause' may in fact be reports on quiescence, and therefore immediate short-term responses to environmental deterioration .
Evolutionary significance of dormancy Dormancy evolution One may assume that obligate dormancy has evolved from a more optional state of quiescence gradually to a genetically compulsory form of diapause . Quiescence and other types of dormancy may occur, per-
2 08 haps because these forms of suspended activity are more flexible than diapauses s . str. Elgmork (1980) describes an intermediate form of restricted development, that he termed `active diapause', where certain cyclopoid instars show an arrest in development and reproduction, but not in activity . He regards this as an evolutionary step towards diapause s . str. Once diapausing behaviour has become a developmental necessity, its subsequent evolution may then be controlled by other factors . Winter diapause (i.e . hibernation) seems to be a relatively recent acquisition since the appearance of the glacial climate . Hibernation, therefore, may have been substituted for diapause which was proximately caused by other factors, such as food shortage, drought, or predation pressure (Levins, 1969) . Another example for a functional shift of dormancy performance is the occurrence of dormancy in permanent water bodies . Dormancy may have evolved first in temporary waters . But in permanent water bodies, the primary causes of dormancy have probably become biotic factors such as the predictably seasonal cycling of food availability or those of predation pressure (Sarvala, 1979) . Some truly limnetic cyclopoids, namely Diacyclops thomasi, Cyclops scutifer, Mesocyclops leuckarti and M. oithonoides, occurring in the largest lakes of Europe and America, show dormant copepodids (Elgmork, 1967) . The more seasonally predictable a period of adverse conditions is over an evolutionary time scale, the more likely will be the evolution of an inheritable diapause response . The constancy of the arrival of adverse conditions will permit the copepods to use a correlated environmental cue as a reliable predictor of future repetitions of the adverse event . Evolution of diapause will then depend in part on the abiotic and biotic environment and on the physiological and developmental properties of the organism (cf . Hairston, 1987) . This author also mentions the possibility that although the ecological or evolutionary forces forming the dormant phenology of an ancestral population may no longer exist, present populations could retain the trait, only because they are stuck with it . He gives the example of Diaptomus sanguineus, which produces diapausing eggs in spring, and is said to do so because some ancestral population made diapausing eggs at that time of the year . In any case must an adaptation be rigorously demonstrated as such (Hairston, pers . comm.) . Diapause may provide a sufficient means of intra- and inter-population variability and differentiation . If diapause in a given locality is genetically controlled, for instance by selection for critical photoperiods, and
gene flow is reduced on a temporal scale, then many potentially isolated populations could evolve within the range of a species (e .g . Marcus, 1984b ; Hairston & Olds, 1984) . Dormant stages can also maintain the genetic variability of a population and may affect the rate of evolution . Hairston & De Stasio (1988) demonstrated for Diaptomus sanguineus that the storage of genetic variation in the pool of dormant eggs slowed the rate of evolution when responding to a switch in selection pressures . Phylogenetic evidence Lindley (1992) argues that most calanoid species found in nonmarine environments are referred to the superfamily Centropagoidea, which also includes most of the abundant neritic marine species . Species within this group can produce eggs which survive in the sediment and resist chemical, osmotic and mechanical stresses . He suggests that this has enabled them to maintain populations in shallow marine and estuarine habitats more readily than other calanoids and has preadapted them to colonize inland waters . Defined dormancy traits, therefore, may provide useful autapomorphies for the consideration of phylogenetic relationships among taxa (e .g . Centropagoidea, Eucyclopinae) . However, dormancy is widespread, and is realized in different ways by various copepod taxa (Table 1 ; e .g . different ontogenetic stages, various types and taxa, encysted or nonencysted, winter or summer, marine or freshwater, benthic or planktonic) . This may suggest the likelihood of its independent or parallel mode of evolution, following the ecological selection forces discussed above .
Perspectives The proximate and ultimate mechanisms controlling copepod diapause are, as yet, far from clear . Also, internal mechanisms, such as the neurological, endocrine, and metabolic physiology of dormant copepod stages, are largely unknown . Knowledge about these mechanisms may provide clues of possible external triggering factors . As pointed out by Hairston (1987), instances of dormancy as adaptations to avoid intense community interactions, most likely will be discovered in dormant organisms from environments that appear to be physically unstressed . Dormancy may be not only the result of predation responses, but could be caused by intra-
209 and interspecific competition as well . Ban's (1992) data support competition as the ultimate cause, and Walton (1985) showed a mild increase in diapause function under a low food condition . Mathematical models, besides their affirmative and predictive value for dormancy phenologies and functions, are of heuristic importance . They indicate, a priori, conditions where dormancy is advantageous, and triggers for dormancy, which subsequently could be verified by observations and appropriate experiments in the field or in the laboratory . There are quite a few models on dormancy available waiting to be applied and tested for the Copepoda. As this overview shows, there is a range of possible ultimate and proximate ecological causes . There may be developmental, genetic and environmental constraints to the realization of copepod dormancy, as well as contingencies allowing a more flexible response . Therefore, each diapausing population may reveal different mechanisms underlying the origin and maintenance of dormancy traits . Copepod dormancy also has implications for methodological approaches . Dormant stages affect the ecology of the respective realms from where dormant stages disappear or emerge to, i .e . in most cases the water column and the bottom . Hence, for a planktologist, neglecting temporary benthic resting stages may provide misleading results for geographic distribution, population dynamics, secondary production, community composition, and the evolution of local populations (cf. Elgmork, 1967) . Future studies should consider both the phenology and the genetics of dormancy. This may help us to understand intra- and interpopulational differences and elucidate the microevolution of dormancy traits . If interdisciplinary studies can be made of a broad spectrum of copepod taxa, habitats, and geographic sites, it may be possible to draw conclusions and make generalizations relating aspects of dormant development in the Copepoda to dormancy in other groups of organisms . Due to their small size, ubiquitous availability and suitability for cultivation in the laboratory, copepods may also serve as a good model for observational and experimental studies of dormancy phenomena in general .
Acknowledgments Dr W. Taylor (Waterloo) is thanked for constructive recommendations on the manuscript . I will
also acknowledge the helpful criticism of Dr Nelson G. Hairston, Jr. and two further anonymous referees . The author acknowledges an Natural Sciences and Engineering Research Council (NSERC) international postdoctoral fellowship in Canada.
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