Population differences in the timing of diapause: adaptation in a spatially heterogeneous environment

Summary Populations of the planktonic copepod, Diaptomus sanguineus, live in permanent and temporary freshwater ponds in Rhode Island. All ponds in which they occur become uninhabitable at some time during the year, but the nature and timing of the harsh period varies both spatially and temporally. Females produce discrete clutches either of subitaneous eggs which hatch immediately or of diapausing eggs which hatch the following season. The two egg types show distinct chorion morphologies under transmission electron microscopy. In permanent ponds the copepods start making diapausing eggs in March, one month before rising water temperatures induce planktivorous sunfish to become active. In temporary ponds diapausing eggs are produced, in a complex pattern from May to July, before the water disappears in late summer or early fall.We investigated the spatial scale at which D. sanguineus is adapted to this complex environment. In a reciprocal transfer experiment between temporary and permanent bodies of water, female copepods placed in new ponds made subies of water, female copepods placed in new ponds made subitaneous and diapausing eggs in the same sequence as control females retained in their home ponds. The copepod populations enter diapause at times appropriate for the local habitat conditions they experience, but inappropriate for other, nearby ponds. Transplanted females were unable to sense a change in pond type or to adjust egg production accordingly. We conclude that D. sanguineus populations are adapted to the specific conditions of isolated ponds rather than to a broader geographical region containing several pond types.     

Factors influencing the induction of diapausing egg production in the calanoid copepod Diaptomus leptopus

Field and laboratory studies were carried out between 1995 and 1997 on four populations of Diaptomus leptopus found in seasonally temporary, occasionally temporary, and a permanent environment to assess the relative importance of photoperiod and temperature regimes versus other proximate local cues in inducing diapause egg production. Patterns of diapausing and subitaneous egg production were determined by observation of individual females bearing clutches that were produced in the field. A laboratory common-garden experiment was performed to assess the effects of four different regimes of temperature and photoperiod on the induction of diapause. Patterns of diapausing egg production differed among ponds: diapause occurred early in the seasonally temporary environment and occurred rarely in the permanent environment. In the common-garden experiment, populations exhibited substantial changes in the onset of diapause when compared to patterns found under field conditions. These results provide indirect evidence that the different populations respond to available cues of environmental change in different ways in nature, or that environmental cues vary among habitats.     

Structure, development and induction of a new diapause stage in rotifers

1. This study shows that females of Synchaeta pectinata Ehrenberg can produce two morphologically and physiologically distinct kinds of amictic eggs that develop parthenogenetically into females. One kind, until now the only one known in monogonont rotifers, is a thin-shelled (about 1.4 μm) subitaneous egg that develops without arrest. The other kind is a thick-shelled (about 9 μm) egg that enters obligatory diapause after 1–3 cleavage divisions before resuming development. The thicker shell of the diapausing egg is due to an expansion of the outer sublayer of the single-layered shell. 2. The mean duration of the diapause at 19 °C (L : D 16 : 8) is about 14 days. This diapause is not broken by low temperature (5 °C), and it is not greatly extended by storage at low temperature (5 °C). 3. Diapausing eggs are induced immediately after a brief starvation period, and seem to be produced at no additional energetic cost. However, a population producing a high proportion of diapausing eggs has a much reduced reproductive potential. 4. Production of diapausing amictic eggs may be a strategy to increase the ability of clones to survive food limitation. 5. Diapausing amictic eggs differ markedly from fertilized resting eggs produced following bisexual reproduction during favourable conditions.     

Morphological differences between subitaneous and diapause eggs of Boeckella triarticulata (Copepoda: Calanoida)

1. Many calanoid copepods produce subitaneous eggs that hatch immediately and diapause eggs that remain dormant for long periods of time. Boeckella triarticulata (Copepoda: Calanoida) produces diapause eggs that hatch asynchronously over an extended period of time and appear identical under light microscopy to those that hatch immediately.
2. We compared the internal morphology of subitaneous and diapause eggs of B. triarticulata that had been prepared for transmission electron microscopy by four methods.
3. Subitaneous eggs had a thin, single-layered shell whereas diapause eggs had a thick, three-layered shell that appeared consistent over 3 months of diapause. Boeckella triarticulata appears to enter diapause at the multicellular stage.
4. Consistent morphological differences between subitaneous and diapause eggs of B. triarticulata suggest that these two egg types also have distinct differences in physiology, and are not merely extremes of a continuum from subitaneous to diapause eggs.     

Diapause dynamics of two diaptomid copepod species in a large lake

Skistodiaptomus oregonensis and Leptodiaptomus minutus produce diapausing eggs in a large lake, Oneida Lake, in New York State. The timing of the switch from production of subitaneous (immediately hatching) eggs to diapausing eggs for both species is in October. This timing is consistent with a pattern, reviewed here, for other populations of diaptomid copepods: populations living in large lakes tend to begin production of diapausing eggs later in the season than those living in small lakes. Populations living in temporary ponds tend to switch still earlier in the season. All populations reviewed here live in the north temperate zone. The sediments of Oneida Lake contain densities of diaptomid diapausing eggs on the order of 10⁵ m^–2 per cm below the sediment surface down to 5 cm. Below this sediment depth, egg densities decline. The highest egg densities were found in sediments under the deepest water. Diapausing eggs of L. minutus survive in the sediments at least two years, as shown by the recovery of the population after a year in which no new diapausing eggs were produced, and probably for two or more decades. Long-term dormancy can have the effect of ensuring the continuation of a population through periods of poor recruitment, and can help create conditions for the coexistence of competing species. Other investigators have suggested that S. oregonensis and L. minutus are competitors in other lakes when they co-occur.     

Egg development and diapause: ecophysiological and genetic basis of phenological polymorphism and adaptation to varied hosts in the green oak tortrix,Tortrix viridana L. (Lepidoptera: Tortricidae)

Experiments concerned 8 tortrix populations associated with varied oak species. They showed that the egg development included a phase of diapause. Completion of embryogenesis at 20 degrees C was used as a criterion for whether diapause was completed. Under semi-natural conditions diapause terminated in late autumn or early winter, then eggs developed continuously, without postdiapause winter quiescence, even in severe cold. The eggs from the populations associated with holm or cork oak completed diapause then hatched later than those from the populations associated with sessile or pubescent oak. Reciprocal crossbreedings confirmed that this phenological polymorphism was genetically determined. Under constant temperatures the physiological state of diapausing eggs, assessed by measuring their cold requirements to complete diapause by exposure to 8 degrees C, varied gradually with increasing age. This diapause development was strongly temperature-dependent. Cold requirements of diapausing eggs were much higher in a late-hatching than in an early-hatching population. This explains the phenological polymorphism of the tortrix: the more eggs need cold, the later they complete diapause in autumn, and the later they hatch in spring. Egg cold requirements varied widely within populations too, which resulted in large variations in the date of diapause end among individuals. The date of egg hatch was influenced by the temperatures occurring during diapause and postdiapause, but apparently not by photoperiod.     

Seasonal Variation in Diel Production Pattern of Centropages tenuiremis in Xiamen Waters, China

The seasonal variations in diel production pattern, and egg hatching time of the copepod Centropages tenuiremis in Xiamen waters, China, were investigated between January and June of 2003. The results show that in the winter–spring (January to early May) the adult females tended to lay subitaneous eggs at night, while in the beginning of summer (late May–June) they tended to lay diapause eggs as well as subitaneous eggs during the daytime. The egg hatching time negatively correlated with water temperature. These results, combined with the fact that C. tenuiremis migrates vertically in Xiamen waters, may explain the reproductive strategy of this dominant species in winter–spring.     

Reproduction strategies of <Emphasis Type="Italic">Daphnia pulicaria</Emphasis> population in a high mountain lake of Southern Spain

For three consecutive years, a population study of Daphnia pulicaria was undertaken in Río Seco Lake, a small high-mountain lake, in order to elucidate the reproductive strategies adopted by Daphnia in this system. Daphnia appears to colonize this lake every spring by hatching from ephippia and reproduce by means of subitaneous (non-diapausing) and ephippial (diapausing) eggs. D. pulicaria in this lake is an obligate parthenogenetic population. There is a short time period for subitaneous egg production and a much longer period for ephippial egg production. The contribution of subitaneous eggs to Daphnia population density and structure appears to be low. Diapause onset showed a high temporal synchronization in the three studied years in Río Seco Lake, and day-length emerged as the main cue triggering diapause onset and the main explanatory factor for the proportion of ephippial females observed. The development and reproduction of D. pulicaria in Río Seco Lake involves taking a gamble on resting forms to guarantee inter-annual Daphnia persistence in the lake, giving priority to investment in future generations. Guest editor: Piet Spaak Cladocera: Proceedings of the 7th International Symposium on Cladocera     

Induction of diapause egg production in Eurytemora affinis by their own metabolites

Chemically mediated crowding effect on induction of diapause egg production in the calanoid copepod Eurytemora affinis was investigated. Two types of eggs, i.e. subitaneous and diapause eggs, produced by females that were reared in crowded culture conditions or the water from crowded culture under excess food supply were examined. 2.3% of the females that were reared at a population density of 5 or 6 animals per 10 ml of filtered lake water (FLW) produced diapause eggs. Females that were reared individually in 2-ml containers with FLW did not produce diapause eggs while 72.7% of females that were individually reared in 2-ml containers, but with water from a crowded culture (500 ind. l^–1, culture medium was changed once a week), produced diapause eggs. These results demonstrate that accumulation of their own metabolic products in the medium induces diapause egg production by E. affinis.     

The effect of diapause emergence on the seasonal dynamics of a zooplankton assemblage

1. The role of seasonal phenology in the emergence of zooplankton from diapause in patterns of seasonal abundance in the water column was investigated in Oneida Lake, New York. Replicate emergence traps, placed in contact with the lake sediments at two locations (one at a shallow site and one at a deep site), were monitored between May and August.
2. Although six rotifer taxa showed a clear seasonal succession in the water column throughout the study period, all but one taxon emerged exclusively in spring. Three cladoceran and three calanoid copepod species, also present in the water column throughout the study period, again showed predominantly spring emergence. In contrast, three cyclopoid copepod species had distinct seasonal periods of emergence that corresponded, at least in part, to the timing of abundance peaks in the plankton.
3. These results for a single lake are largely consistent with patterns observed or inferred by other investigators for other lakes: variable dependence of abundance in the plankton on diapause emergence for species with long-lived diapausing eggs (i.e. rotifers, cladocerans and calanoid copepods), and much closer dependence for species with short-lived diapausing immature stages (i.e. cyclopoid copepods).     

Finding copepod footprints: a protocol for molecular identification of diapausing eggs in lake sediments

Even though calanoid copepods produce diapausing eggs that stay alive in lake sediments, these eggs have rarely been used paleolimnologically, as they lack diagnostic morphological features. In this study, we developed a method to identify copepod diapausing eggs in Japan as a clue toward reconstructing past plankton populations. We first determined a 28S ribosomal DNA (rDNA) (i.e., nc28S) regional sequence library (240 bp) of various calanoid copepod species using ethanol-fixed plankton samples collected from across the Japanese archipelago. Then we applied the UltraSHOT method to extract DNA from an individual diapausing egg. Finally, the nc28S region of diapausing eggs collected from various lakes was sequenced and compared with the regional library for species identification. In total, 21 haplotypes of the nc28S region were recovered from planktonic samples of 11 Japanese freshwater calanoid copepod species. Despite the short length of this region, no identical haplotypes were shared among the species analyzed, including the Acanthodiaptomus pacificus complex treated as a species. Even different lineages of A. pacificus could be separated. These results indicate that the nc28S region can be used as a barcode in Japan. A total of 112 diapausing eggs collected from various lakes and ponds was processed, and the nc28S region of each was successfully sequenced. All of these egg sequences matched one or the other of the nc28S haplotypes in the regional library mentioned above. The set of protocols we applied (i.e., preparing a comprehensive regional sequence library and sequencing egg DNA) is thus useful for involving copepod diapausing eggs in paleolimnological studies in lakes. The nc28S region treated in this study has a strong potential to uncover the paleodiversity of copepods, at least in Japan.     

The effect of diapause on the genetic structure of Daphnia magna populations

For intermittent Daphnia magna populations embryonic diapause following bisexual reproduction is the means of surviving in harsh environmental conditions. Another advantage of bisexuality is genetic recombination which produces a variety of genotypes. Crowding and short-day photo-periods promote bisexual reproduction, but photoperiod, at least, can not be an obligatory factor in D. magna since some bisexual females have been found also during the periods of long daylength. Because the catastrophe dates vary considerably, the most advantageous reproductive strategy must be one with some flexibility in reacting to irregular catastrophes by producing ephippial resting eggs whenever the probability of a catastrophe exceeds a certain threshold value. Extensive genetic changes occurring during diapause suggest that there are considerable genetic differences in ephippial egg production and egg survival. Genetic drift alone can not account for the great genetic changes observed, although in populations reacting slowly to changing conditions the number of diapausing ephippia can be relatively low. If the ephippia hatch over a long period of time, they can act as a stabilizing mechanism for genotype frequencies.     

Ecological and evolutionary significance of resting eggs in marine copepods: past, present, and future studies

The occurrence of a resting egg phase in the life cycle of marine and freshwater planktonic copepods is well documented and receiving increasing attention by investigators. The species generally occur in coastal marine waters, freshwater ponds and lakes in areas that undergo strong seasonal fluctuations, though examples have been reported for tropical and sub-tropical areas not subject to such extreme fluctuations. Typically such species disappear from the water column for portions of the year, but remain in the region as benthic resting eggs. Studies to date have focused on the conditions that promote the occurrence of resting eggs, the factors that affect their survival and hatching from sediments, the existence of egg banks in sediments, and the impact of resting eggs on plankton community structure. Benthic resting eggs of copepods include diapause eggs as well as subitaneous (non-diapause) eggs that are quiescent due to conditions in the sediments. As with other groups of organisms the resting egg phase is viewed as being critical for the perpetuation of species year after year, especially those that disappear from the water column for portions of the year. Some data indicate that eggs can survive for many years in sediments which would expand their influence to evolutionary time scales. This paper summarizes our understanding of embryonic dormancy in marine copepods.     

The production of subitaneous and diapause eggs: a reproductive strategy for Acartia bifilosa (Copepods: Calanoida) in Southampton Water, UK

Acartia bifilosa from Southampton Water lays two morphologically distinct types of egg which are described for the first time. Eggs with a smooth surface are considered subitaneous, while eggs covered with thick 'spines' are diapause. During the seasonal occurrence of A.bifilosa in Southampton Water, from November/December to June, subitaneous eggs are laid during the first months of this period. The production of diapause eggs is restricted to a 2 month period before A.bifilosa disappears from the water column. There are significant differences between the response of the eggs produced at seasonal field temperatures (5-12C) and those reported for other Acartia species. In particular, the numbers of eggs female^-1 day^-1, both subitaneous and diapause, are lower and typically <4; and the hatching time of subitaneous eggs is longer, at up to 10 days, at optimum temperatures between 15 and 20°C and optimum salinity >20 PSU. Females acclimated to higher laboratory temperature regimes show higher egg production rates at field salinity. A delayed-hatch subitaneous egg is also reported. Results suggest that fecundity in A.bifilosa from Southampton Water might be limited to some degree by temperature and the responses of the eggs produced appear to offer A.bifilosa a reproductive repertoire to ensure its sustained presence in this seasonally influenced environment.      

Diapause in Monogonont Rotifers

This review focuses on more recent findings on the diapause in Monogonont rotifers, since the major reviews by Pourriot & Snell (1983, Hydrobiologia 104: 213–224) and Gilbert (1992, Rotifera. In Adiyodi, K. G. & R. G. Adiyodi (eds), Reproductive Biology of Invertebrates, Vol. 5 – Sexual Differentiation and Behaviour. IBH Publishing Co., Oxford: 115–136; Vol. 6A – Asexual Propagation and Reproductive Strategies. IBH Publishing Co., Oxford: 231–263.). It covers diapausing egg formation, diapausing egg survival, and diapausing egg hatching as well as possible strategies involved in these processes. Data from laboratory and field studies exist, but little information is available on diapausing egg hatching in the field. Resting or diapausing egg production can be mictic and in some cases amictic. Mictic diapausing egg production depends on the balance between cues promoting and inhibiting mictic female production. Such cues can be either environmental or endogenous. Our knowledge on factors inducing mixis is still limited to a few species, but effects of crowding on mixis induction may be more widespread. Recent results also show that male mating behavior may play an important role in the successful production of diapausing eggs. Hatching may be induced by factors related to temperature and light conditions; also desiccation may have a role. However, desiccation of temporary habitats may also be damaging to diapausing stages. Although few data are available, those existing point to distinct differences between populations and the importance of clonal variation within populations regarding the initiation as well as the termination of diapause.     

Selection of low investment in sex in a cyclically parthenogenetic rotifer

Cyclical parthenogens, which combine asexual and sexual reproduction, are good models for research into the ecological and population processes affecting the evolutionary maintenance of sex. Sex in cyclically parthenogenetic rotifers is necessary for diapausing egg production, which is essential to survive adverse conditions between planktonic growing seasons. However, within a planktonic season sexual reproduction prevents clonal proliferation. Hence, clones with a low propensity for sex should be selected, becoming dominant in the population as the growing season progresses. In this context, we studied the dynamics of the heritable variation in propensity for sexual reproduction among clones of a Brachionus plicatilis rotifer population in a temporary Mediterranean pond during the period the species occurred in plankton. Clonal isolates displayed high heritable variation in their propensity for sex. Moreover, the frequency of clones with low propensity for sex increased during the growing season, which supports the hypothesized short‐term selection for low investment in sex within a growing season. These results demonstrate (1) the inherent instability of the cyclical parthenogenetic life cycle, (2) the cost of sexual reproduction in cyclical parthenogens where sex produces diapausing eggs and (3) the role of the association between sexual reproduction and diapause in maintaining sex in these cyclical parthenogens.     

Dormancy, dispersal and the survival of cyclopoid copepods (Cyclopoida, Copepoda) in a lowland floodplain

1. The survival of cyclopoid copepods was investigated in a floodplain for 2 years where flooding occurred during the cold season. The cyclopoid community was studied in three waterbodies with distinct hydroperiods: a permanent pond connected to the flooded area during inundation, a temporary pool that is part of the flooded area and an isolated temporary pool.
2. Field studies, including data obtained from samples of water, sediment and soil, showed the overall predominance of species with a summer diapause over those with a winter diapause or without diapause. Emergence of cyclopoid copepods at the onset of flooding, examined using emergence traps and data from recently filled or still isolated temporary pools, showed that some species can survive several months of drying.
3. The ability of the diapausing fourth copepodid stages of Cyclops strenuus and C. insignis , the two cyclopoids most abundant during winter and spring flooding, to survive terrestrial conditions was tested in laboratory experiments. Both species survived for several months, but rates differed among the species. A higher percentage of C. strenuus survived for a longer period, possibly explaining why this species was relatively more abundant in more temporary habitats.
4. Both dormancy and dispersal facilitated survival of cyclopoid copepods in transient habitats connected to each other during flood periods. Dormancy was the most important survival strategy, whereas dispersal could be more important following prolonged periods without flooding.     

桡足类滞育规律研究

首次提出用滞育指数对桡足类滞育能力进行相对量化处理 ,并对 10 2种桡足类的滞育能力同迁移能力、体长、栖息地之间的关系进行了数学分析 ,初步得出了滞育在桡足类中的分布规律 :在桡足类中滞育与迁移呈负相关 ,两者之间存在一定程度的置换 ;个体较小的桡足类一般具有较强的滞育能力和较弱的迁移能力 ,个体较大的桡足类一般具有较弱的滞育能力和较强的迁移能力 ;淡水桡足类一般比海洋桡足类具有较强的滞育能力。最后探讨了这种分布模式的成因     

Diapause of Cyclops vicinus (Uljanin) in Lake Søbygård: Indication of a Risk-spreading Strategy

Cyclops vicinus is reported to enter summer diapause triggered by day length in order to survive food scarcity and fish predation. Development ceases and the fourth or fifth copepodid stages persist in the sediment for several weeks. In Lake Søbygård, however, a small eutrophic lake in Denmark, C. vicinus is found in the sediment as well as in the open water throughout the year. We performed laboratory experiments to elucidate the life cycle strategy of this population. In order to find the factors that induce diapause we tested the influence of food composition and light regime on the proportion of copepods entering diapause. Further we examined the diapause pattern of the offspring from diapausing and non-diapausing parents to see whether the co-occurrence of diapausing and non-diapausing copepods results from genetic differentiation within the population. In all experiments some of the copepods developed directly into adults, while others remained at the fourth or fifth copepodid stage and displayed diapause features. The proportion of copepods that developed directly into adults was influenced by food supply. Fewer individuals entered diapause when they received a mixed diet of algae and ciliates or algae, ciliates and seston compared with a pure algal diet. The response to light was different than described in literature: about 30% of the copepods entered diapause under dark conditions, and the diapause frequency was not higher when copepods had been exposed to continuous light. The offspring from diapausing parents showed no higher tendency to enter diapause than the offspring of non-diapausing parents, indicating no genetic differentiation. We conclude that diapause in C. vicinus represents a risk-spreading strategy, modified by food. The simultaneous production of diapausing and non-diapausing offspring ensures survival under harsh conditions; the influence of the food supply on the proportion of individuals entering diapause may adjust the population to the actual environmental condition. This flexible life cycle strategy might contribute to the exclusive dominance of C. vicinus in Lake Søbygård.     

Geographic Variation of Photoperiodic Diapause but Not Adult Survival or Reproduction of the Invasive Mosquito Aedes albopictus (Diptera: Culicidae) in North America

Climate differences across latitude can result in seasonal constraints and selection on life-history characters. Because Aedes albopictus (Skuse) invaded North America in the mid-1980s, it has spread across a range of ≈14° latitude and populations in the north experience complete adult mortality because of cold winter temperatures that are absent in the south. Life-table experiments were conducted to test for differences in the adult survival and reproductive schedules of Ae. albopictus females from three populations from the northern (Salem, NJ; Springfield, IL; Eureka, MO; ≈39° N) and southern (Palm Beach, Palmetto, Tampa, FL; ≈27-28° N) extremes of the species distribution in North America. There were consistent differences between northern and southern populations in incidence of photoperiodically-induced egg diapause. Under short daylength, diapause eggs constituted twice the proportion of total viable eggs from northern females (81.9-92.1%) than southern females (35.9-42.7%). There were no consistent differences between northern and southern populations in resource allocation between reproduction and maintenance, reproduction over time, and reproductive investment among offspring, and no apparent trade-offs between diapause incidence with reproduction or longevity. Our results suggest that the main response of North American Ae. albopictus to unfavorable winter climates is via the life history strategy of producing diapausing eggs, rather than quantitative variation in reproduction, and that there are no detectable costs to adult survival. Inherent geographic variation in the expression of diapause, consistent with the latitudinal extremes of A. albopictus, indicates evolutionary loss of diapause response in southern populations because of the invasion of A. albopictus in North America.