© 2002 by The Society for Integrative and Comparative Biology
Temporal Dispersal: Ecological and Evolutionary Aspects of Zooplankton Egg Banks and the Role of Sediment Mixing1
1 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853
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Zooplankton egg banks are the accumulation of diapausing embryos of planktonic animals buried in the sediments of many aquatic ecosystems. These eggs, which are analogous life history stages to the seeds of many plants, can survive in a ready-to-hatch state for periods ranging from a few years to greater than a century. Their presence in ponds, lakes and near-shore marine environments has substantial implications for understanding trajectories of ecological and evolutionary change. When the sediments of lakes are structured in historical sequence, diapausing eggs extracted from different sediment ages can provide a means of studying past changes in community or population-genetic structure. A completely different aspect of egg banks derives from the fact that hatching of diapausing eggs can influence, through what can be thought of as temporal dispersal, population and community response to environmental change. Eggs hatching from diapause introduce to current environments species or genotypes laid at times in the distant past. In addition, egg banks create extended generation overlap that can play an important role in maintaining diversity in a fluctuating environment when different types (species or genotypes) are favored at different times. These distinct aspects of egg banks (i.e., their direct impact on ecological and evolutionary processes versus their usefulness in reconstructing historical changes), are potentially in conflict because for old eggs to hatch, the sediments must be at least partially mixed. This same mixing, however, degrades the accuracy of the historical record. Both aspects are possible, however, even within a single lake when sediment-mixing intensity is spatially heterogeneous.
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INTRODUCTION |
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SYNOPSISINTRODUCTIONHISTORICAL RECORDS AND DYNAMICAL...A LOGICAL CONFLICT AND...METHODSRESULTSDISCUSSIONReferences |
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It has been appreciated for more than a century that many species of freshwater zooplankton produce diapausing eggs (e.g., Weismann, 1876; Sars, 1885
), and that these stages can form a significant part of the life cycle (Häcker, 1902; Wolf, 1903). Evidence for diapausing-egg production by some species of marine crustaceans has only come more recently (Sazhina, 1968; Zilloux and Gonzalez, 1972; see Marcus, 1996 for a review). For freshwater zooplankton, it was also recognized early on that diapausing eggs could survive for extended periods, at least in the laboratory: for example, the Norwegian zoologist, G. O. Sars, is well known for describing freshwater cladocerans and copepods using eggs obtained from dried mud shipped to him from localities throughout the world (e.g., Sars, 1885, 1901; see Christainsen, 1993). Despite this early start, the ecological and evolutionary significance of prolonged diapause for zooplankton has only been studied in any substantive way for the past couple of decades (e.g., Alekseev and Fryer, 1996; Brendonck et al., 1998). DeStasio (1989) was the first to use the term "egg bank" for zooplankton in analogy with plant seed banks (although some earlier studies clearly recognized the similarity), and its use has since grown steadily so that it has now become an accepted part of zooplankton terminology (Hairston, 2000).
Because zooplankton biologists were latecomers to studies of the role of prolonged embryonic dormancy, the seed-bank literature, both theoretical and empirical, has often served as inspiration and guide to explorations of the ecological and evolutionary significance of egg banks. Recent literature reviews exploring the distribution of prolonged dormancy among crustaceans (Brendonck, 1996; Hairston and Cáceres, 1996; Hairston, 1998), copepods (Hairston and Bohonak, 1998), and invertebrates generally (Cáceres, 1997a) have all drawn upon concepts developed for understanding seed banks. One key feature of the seed-bank literature is the insight that the three life-history traits, prolonged seed dormancy, iteroparity, and enhanced spatial dispersal, can act as alternative mechanisms for persistence in temporally varying environments (Templeton and Levin, 1979; Venable and Lawlor, 1980; Rees, 1993, 1994). Hairston and Cáceres (1996) used this theoretical framework to investigate the distribution of prolonged egg diapause among the Crustacea. They found in a literature survey of 159 taxa from both inland-water and marine habitats that species with an extended life span (i.e., duration >1 yr either as eggs or as adults) divided into two wholly distinct groups. Species had either prolonged egg diapause or they had long adult life span: there are apparently no crustaceans that possess both egg diapause lasting longer than one year and adult life span lasting longer than one year. Because it is difficult to envision any physiological constraint that would mediate against the co-occurrence of these traits in a single individual, it seems likely that the possession of either one alone is sufficient for survival in a temporally varying environment. It is interesting in this data set that Hairston and Cáceres (1996) also observed a relationship between habitat and the expression of prolonged egg diapause (Fig. 1). Sixty-two percent of crustacean species living in inland water habitats have prolonged egg diapause whereas only 6% have extended adult life span: just the opposite is found among marine crustaceans with 6% having prolonged egg diapause and 26% having extended adult life span. One interpretation of this pattern is that when conditions become uninhabitable in inland-water habitats, they go bad for both adults and juveniles, making diapause the only viable mechanism for survival until the return of good conditions. In contrast in marine habitats, it may be that adults survive through harsh periods much better than do juveniles, thus favoring iteroparity.
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The remaining 32% of inland-water crustacean taxa and 68% of marine taxa all have diapause durations and adult life spans of less than one year. It would be consistent with seed-bank theory if these species were the ones with high spatial dispersal. In particular, the lower fraction of species without any prolonged life span (either as egg or adult) in inland waters compared with marine habitats might be a result of reduced dispersal ability among aquatic crustaceans that would have to move across land to reach another lake or wetland. Marine species presumably would be able to take advantage of currents and the interconnectedness of marine habitats to facilitate movement. In agreement with this interpretation, Hairston and Bohonak (1998)
found for calanoid copepod species that genetic data show lower dispersal rates among inland-water (Nei's genetic distance, D, averages 0.3) than among marine populations (mean D = 0.07).
Although general ecological and evolutionary theory should be the same for egg banks and seed banks. There are some specifics of the systems that can lead to important differences in the details. For example, freshwater egg banks are distinct from seed banks in the way that the dormant embryos are stored in the environment. This difference simultaneously makes the study of roles of prolonged dormancy both more tractable and more problematic. A key question in studies of seed and egg banks is how long do the propagules survive in dormancy? It is commonly the case that soils are too well mixed to provide any means of determining the ages of seeds, although there are exceptions (e.g., McGraw et al., 1991; Shen-Miller et al., 1995), and a new isotope ratio technique has been demonstrated by Moriuchi et al. (2000). In contrast, lake sediments are well known to contain depositional zones where material accumulates in temporal order. Thus, studies of historical changes are often possible and sediments can be aged by radioisotope dating, counting annual laminations, or by using other distinctive sediment characteristics (e.g., Davis, 1990, Brenchley and Harper, 1997). For the diapausing eggs of the freshwater copepod, Diaptomus sanguineus, recovered from the sediments of a small lake in Rhode Island (Fig. 2), 210Pb dating showed that the mean age of the eggs in this egg bank was 70 years, the oldest egg hatched was about 330 yr old, and the diapausing eggs had a 99% annual survival probability (Hairston et al., 1995). Other species of zooplankton in other lakes have been found to have viable egg ages ranging in age between 15 and 112 yr (reviewed by Hairston, 1996).
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Partly as a result of this tendency for sediment egg banks to accumulate in historical order, they are significant in the study of zooplankton ecology and evolution in two interesting and conflicting ways. Lake sediments store genotypes and species from the past and so can provide insight into the rates and trajectories of past ecological and evolutionary changes. At the same time, these eggs can hatch and influence on-going ecological and evolutionary dynamics. The conflict comes because for an egg bank to provide a reliable history, the sediments must be relatively undisturbed; for the egg bank to supply propagules dispersing through time, the sediments must be disturbed so that diapausing eggs buried in the past are brought to the sediment surface where they can hatch in the present. Here we review examples of four studies that demonstrate either the historical or the dynamical aspects for egg banks in studies of both ecological and evolutionary processes. We then propose a solution to the conflict by suggesting that both aspects of egg banks can operate within a single lake because each lake contains distinct depositional and erosional zones. We illustrate this resolution by providing some previously published and some new data on the sediment dynamics in Bullhead Pond, R.I., and their impact on the resident D. sanguineus population. We end by suggesting that our observations on Bullhead Pond are likely typical of many, perhaps most, other lakes.
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HISTORICAL RECORDS AND DYNAMICAL SYSTEMS |
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Retracing history
There are many examples of paleolimnological studies in which "microfossils" (various body parts) have been used to interpret past changes in zooplankton assemblages and the ecological processes that produced them (e.g., Kerfoot, 1974
; Kitchell and Kitchell, 1980; Jeppesen et al., 2001). In many ways diapausing eggs, if unhatched, are simply another microfossil that can be, and on occasion have been used for these purposes (e.g., Kerfoot et al., 1999), albeit with molecular sequences added to characters that can be studied (Duffy et al., 2000; Limburg and Weider, 2002). A more intensive use of the egg bank involves taking advantage of the fact that diapausing eggs from different time periods can be hatched and the live animals used to gain a fuller understanding of past processes. Hairston et al. (1999a) hatched the eggs of Daphnia exilis, an exotic species that invaded Onondaga Lake, N.Y., during a period of extreme industrial salt pollution. Analysis of allozyme loci, and comparison with genetic diversity of this species in its native habitat (shallow saline pools in the southwestern U.S.; Hebert and Finston, 1993), showed that although the population contained as many as several billion individuals in the plankton at one time, the lake was almost certainly colonized by the hatching of a single egg.
The pattern of past evolution was studied for a population of Daphnia galeata living in Lake Constance, central Europe. Weider et al. (1997) hatched diapausing eggs from a range of sediment ages that spanned a period of substantial eutrophication (1963–1979) followed by oligotrophication (1980–1997). They showed that allele frequencies at two loci tracked closely the changes in lake phosphorus content, and suggested that the Daphnia were responding to some unidentified natural selection pressure imposed by the changing environment. Hairston et al. (1999b, 2001) followed up this study by using the same D. galeata clonal isolates to show that animals hatched from eggs laid when cyanobacteria were scarce (or only recently abundant) in Lake Constance were significantly more sensitive to the presence of these toxic phytoplankton in their diets than were genotypes hatched from eggs laid after the population had been exposed to planktonic cyanobacteria for a decade or more. In this case, the egg bank provided a remarkable library of living propagules available for analyses of physiological and ecological characteristics. Similar kinds of studies should be possible for other lacustrine organisms that make long-lived dormant stages, for example algae and cyanobacteria.
Impacts on dynamics
The simplest and most direct way that an egg bank can influence ecological or evolutionary processes is by the one-time hatching of diapausing eggs laid at some period in the past. One excellent example of this was reported by Parker et al. (1996) who showed that the presence or absence of an egg bank for Hesperodiaptomus arcticus dictated whether or not this copepod species rapidly recolonized lakes following the extinction of introduced trout and char. The fish, originally stocked in lakes in the Canadian Rocky Mountains to enhance fishing, eliminated the copepods from the plankton. When the fish later died out, the copepods only reappeared quickly in lakes with a well-established diapausing egg bank.
In some instances, the egg bank can play a critical role in maintaining the coexistence of competing species over multiple years. In Oneida Lake, N.Y., Daphnia pulicaria and D. galeata mendotae compete for algae with the intensity of the interaction varying from one year to the next (Cáceres, 1998a). In a 22-yr study of the lake, Mills and Forney (1988) found that fish predation intensity also varied markedly from year to year, and that D. pulicaria was present in all years, whereas D. g. mendotae was absent for a continuous period of six years. Cáceres (1997b) then went on to show that while D. g. mendotae depended for its persistence on the combined presence of the egg bank with a temporally fluctuating environment, D. pulicaria did not. Thus the two species use their egg banks in different ways: both species require theirs for re-establishing presence in the water column in spring after winter absence, but only D. g. mendotae depends upon its for long-term persistence.
Theory showing that generation overlap (via the egg bank in this case) interacting with environmental fluctuation can be a potent mechanism for maintaining coexistence among competing species was developed by Chesson and Warner (1981). Although it is likely to be of very general importance (Chesson, 1994; Hairston et al., 1996a), Cáceres' (1997b) study was the first to demonstrate unequivocally its operation in a natural system. Pake and Venable (1995) make a convincing case that the process may be acting in an assemblage of desert annual plants. Ellner and Hairston (1994) extended the theory to apply to the maintenance of genetic variation within a single population. The critical difference between the models of the "storage effect," as it is called, for community diversity and those for genetic variation lies in the requirement that in a genetic system, polymorphism must be maintained even when the theoretically most fit genotype (the Evolutionarily Stable Strategy) is present. Even with this constraint, the conditions supporting variation are quite robust. Hairston et al. (1996b) have shown for D. sanguineus in Bullhead Pond that polymorphism is maintained for a significant life-history trait, and Ellner et al. (1999) found that the expression of this trait in the population in each year is explainable as a combination of response to natural selection and the emergence of genetic variants from the egg bank. The change in phenotype from year to year, for a ten-year period, was only very poorly explained by changes in the direction and intensity of natural selection. However, when the effect of old genotypes hatching from the egg bank was factored in, the explanatory power was greatly increased. Interestingly, between some pairs of years the primary factor affecting life history change was natural selection, whereas between other pairs the primary effect came from "temporal dispersal" from the egg bank. On average, the two factors were roughly equal in importance over the 10-yr period of study.
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A LOGICAL CONFLICT AND ITS RESOLUTION |
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It is immediately striking that the historical and the dynamic significances of egg banks are in direct conflict. For an egg bank to maintain its value as a historical record, the sediments should have little or no disturbance. On the other hand, for diapausing eggs to influence water column processes, older and more deeply buried eggs must be mixed up to the sediment surface where they can hatch. Is it possible for both features of egg banks to exist within a single lake? Because sediment mixing rates differ markedly across different regions of a lake bottom, the answer is almost certainly yes, even for very small lakes. One explanation for the difference in hatching rate among sites lies in the difference in the amount of mixing that occurs in near-shore versus deep-water sediments. There is increasing evidence that diapausing eggs require cues of light and oxygen in order to hatch (B. T. De Stasio, N. G. Hairston and C. M. Kearns, unpublished data for light; see Marcus, 1996
for a review of the effects of dissolved oxygen). Thus, eggs buried under more than a small amount of sediment may be inhibited from hatching. In addition, it might be physically impossible for newly hatched zooplankton to emerge into the water column were they to hatch more than a few millimeters deep in the mud. Marcus (1984) and Marcus and Schmidt-Gengenbach (1986) proposed for marine copepods that bottom disturbance would carry eggs to the sediment surface and thus stimulate hatching, and similar processes ought to be important in lakes. Here, we present evidence for different sediment mixing rates between the central deep and the near-shore shallow portions of Bullhead Pond. And, we show the effect of mixing on the egg bank of D. sanguineus, and the expression of phenotypic variance in this population.
Diaptomus sanguineus and Bullhead Pond
Bullhead Pond is a small (2.3 ha surface area, 4 m maximum depth) permanent lake in southern Rhode Island, USA (for a more complete description, see Hairston et al., 1983; De Stasio, 1989). D. sanguineus is an herbivorous planktonic calanoid copepod distributed in lakes and temporary ponds throughout much of eastern North America. In Bullhead Pond, individuals are active in the water column from November through June. Adults make immediately-hatching eggs during winter, switch to making diapausing eggs in late March and continue to produce them until the population is eliminated by fish predation in May or June (Hairston and Munns, 1984; Hairston, 1988). Diapausing eggs hatch continuously between November and May (De Stasio, 1989). The species is absent from the water column throughout summer when zooplanktivorous fish are most active, and the diapausing eggs that settle to the lake bottom are not exposed to predation by fish. Active individuals only reappear in the water column in autumn when diapausing eggs begin hatching in autumn after fish predation intensity declines (Hairston, 1988).
Two lines of evidence strongly support the conclusion that the springtime switch from production of immediately-hatching eggs to diapausing eggs is an adaptation to avoid the seasonal onset of fish predation. First, timing of the switch observed in the lake matches closely the theoretical ESS timing (Hairston and Munns, 1984), and second, small year-to-year variation in the switch date is predicted by calculations of natural selection intensity and response based in part upon interannual variation in the timing and intensity of the onset of fish predation (Hairston and Dillon, 1990; Ellner et al., 1999). We will show below that another critical factor influencing the expression of the copepod population's diapause-timing phenotype is the amount of variation that enters the water column each year through temporal dispersal from the egg bank.
Spatial variation in egg bank density and copepod emergence
De Stasio (1989) surveyed both the distribution of the diapausing eggs of D. sanguineus and their annual hatching rates along two transects from shallow to deep water in Bullhead Pond. Whereas diapausing eggs are most dense under sediments away from the shallow, near-shore sediments, hatching rates decline markedly from near-shore to the lake center (Fig. 3). Indeed, De Stasio (1989) concluded that the low density of eggs in near-shore sediments was caused by a combination of high hatching rates and low input rates in this region of the lake. The trend in hatching along the transects is not due to differences in egg viability among sites, as De Stasio (1989) found that egg viability in the top 5 cm of sediment was relatively constant.
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A variety of processes may disturb the lake bottom in shallow water near shore. In large lakes, physical mixing processes due to energy transfer from surface waves and currents are greatest at the shore. In Bullhead Pond, however, which is small and relatively well protected by trees from wind action so that waves are never more that one or two centimeters in height, biological mixing processes must dominate. The roots of submersed and emergent macrophytes provide passageways into the sediment through which benthic invertebrates may travel carrying small particles like copepod diapausing eggs (ca. 100 µm diameter) with them. Nest construction and maintenance by centrarchid sunfish causes considerable redistribution of the top five to ten centimeters of sediment, which has been shown to lead to substantial movement of diapausing-egg sized particles from the center of a nest to its raised margin (Cáceres and Hairston, 1998
). Terrestrial animals (e.g., raccoons, deer, and dogs) that come to the lake shore may wade into the water mixing lake sediments. In Bullhead Pond, biologically-mediated sediment mixing processes may be accentuated by fluctuations in lake water depth that can leave shore sediments alternately exposed to water and air. Finally, human activities at Bullhead Pond (i.e., swimming, fishing, canoe launching), though modest in extent are concentrated at the lake shore. In contrast, sediment mixing processes at the lake center are much less extensive. Bioturbation by benthic invertebrates in soft sediments is generally limited to the top few centimeters in most lakes (e.g., McCall and Tevesz, 1982; Kearns et al., 1996). In Bullhead Pond, occasional surface disturbance by turtles and deeper burrowing by catfish is limited in spatial extent, as is occasional sediment disruption when fishermen and limnologists anchor their boats. After recognizing the potential effects of anchoring on egg bank dynamics, the limnologists studying Bullhead Pond (i.e., the authors) began using a permanently-moored buoy. |
METHODS |
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Sediment mixing depth
Spatial variation in sediment mixing depth was measured in two ways. First, we took two sediment cores (7 cm diameter) for 210Pb dating, one (collected 13 November 1993) at the lake center and the other (collected 27 June 1994) near shore in 1 m of water. Both were piston cores taken by SCUBA diver. Both cores were wrapped in aluminum foil and stored in the laboratory at 4°C until they were sliced. Each core was extruded and sliced at 1-cm intervals down to 20 cm. For each slice, the outer layer of sediment that had dragged along the wall of the core tube was removed and discarded. The sediment retained was stirred and subsampled. 210Pb was measured on selected slices by D. R. Engstrom (personal communication) using 210Po distillation and alpha spectrometry methods (for details see Hairston et al., 1995
). By plotting the logarithm of unsupported 210Pb activity as a function of sediment depth, mixing depth can be inferred from a change in slope: slope should be constant without mixing, and should be steeper near the sediment surface if mixing has taken place.
The second method by which we measured sediment mixing was by determining the depth to which polystyrene beads, of approximately the same size (ca. 100 µm diameter) and specific gravity (1.03) as copepod diapausing eggs, are mixed over time. On 17 June 1992, 5.6 x 108 white beads were distributed as evenly as possible into the surface water of the main basin of Bullhead Pond at all regions 
1 m deep. We followed the distributions of the beads within the lake sediments by taking cores along the same transects sampled by De Stasio (1989) for egg density and hatching. Bead densities in each core were analyzed at 1-cm intervals (for details see Cáceres and Hairston, 1998). Bead distributions were sampled on 5 dates: 22 days, and 4.5, 12, 17 and 24 mo after the beads were added to the lake. Here we discuss only the distributions of beads from cores taken after 4.5 mo, because these illustrate well the results relevant to mixing depth. A more detailed analysis will be undertaken elsewhere.
Sediment mixing and egg hatching
We studied the effect of sediment mixing on egg hatching in the laboratory. Sediment naturally containing D. sanguineus diapausing eggs was collected by SCUBA diver from center of Bullhead Pond using six 16.6-cm diameter box cores. The cores, wrapped in aluminum foil, were returned to the laboratory, where the top 5 cm of sediment was removed, mixed thoroughly among all cores and then introduced into a series of shallow plastic pans (8.4 cm x 11.5 cm). Glass-fiber filtered Bullhead Pond water was added to each pan to a depth of 1 cm above the sediment surface. Two sediment-depth treatments (2.2 cm and 0.8 cm) and two mixing regimes (stirred and not-stirred), were studied in a factorial design. The pans used were made of translucent plastic that permitted light to pass through the sides, so we painted black the bottom portion of each that contained sediment. All treatments (5 replicate pans each) were incubated at 10 ± 0.5°C and 13.25:10.75 L:D photoperiod. Egg hatching was detected by siphoning the water lying above the sediment in each pan weekly for 53 wk, filtering and checking for nauplii. Water was immediately reintroduced to each pan and the sediment was thoroughly stirred with a plastic spatula in the "stirred" treatments. In the "not-stirred" treatments, the water was slowly reintroduced through a diffusing filter to minimize sediment disturbance.
Egg hatching and phenotype distribution
To determine how the abundance of diapausing eggs hatching in any given year affects the D. sanguineus population in the water column, we explored data reported in previous studies (Hairston, 1988; Hairston and Dillon, 1990; Ellner et al., 1999) for an important fitness character, the springtime switch-to-diapause date. For the years 1979–1989 (with 1987 omitted, see Hairston and Dillon, 1990) we calculated the distribution of switch dates from data on the fraction of female copepods carrying diapausing versus immediately-hatching eggs in plankton samples collected approximately weekly in each year (see Hairston [1988] for details). We do not have direct estimates of year-to-year variation in the numbers of eggs hatching from the sediments to compare with these phenotypic variances. Instead we use data on water depth as a surrogate. Bullhead Pond fluctuates greatly in water depth between years because it lies on a relatively porous Pleistocene-aged moraine (Hairston, 1988), and we argue that change in water level between years determines the exposure of the egg bank to hatching cues. When water level is high, there should be little hatching of diapausing eggs because near-shore sediment mixing processes act on sediments with very few eggs (see Fig. 3). When lake level is low, shoreline mixing processes include sediments that have many eggs and are normally less exposed. Change in water depth between years should be a better predictor of egg hatching than absolute water depth because multi-year exposure to the same conditions (whether low or high water) should tend to dilute these effects. Thus, we investigate egg bank effects on phenotype distribution by plotting the standard deviation of D. sanguineus switch-to-diapause date as a function of the change in the depth of Bullhead Pond.
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RESULTS |
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Sediment mixing depth
Both the 210Pb and the polystyrene bead data show substantial differences in the mixing depth of sediments near shore compared with those from the center of the lake. Plots of log(210Pb activity) versus sediment depth show a change in slope between 5 and 6 cm in the near-shore sediments but at only about 2 cm at the lake center (Fig. 4). These changes in slope could be attributed either to surface sediment mixing, which would cause near-surface sediments with higher 210Pb activity to mix with deeper sediments of lower activity, or to an increase in sedimentation rate over the past several decades, which would dilute the 210Pb activity of recently deposited sediments. The bead data, however, support only a difference in mixing depth. Within four months of being added to the water column, beads were found as deep as 6–7 cm in the near-shore sediments, but only in the top 2–3 cm in sediments closer to the lake center (Fig. 5). Because the beads have a lower specific gravity than many of the natural sediment particles in Bullhead Pond (Kearns et al., 1996
; Cáceres and Hairston, 1998), they do not sink through the bottom sediments. In laboratory experiments, bioturbation moved beads up as well as down through Bullhead Pond sediments (Kearns et al., 1996). Taken together, the radioisotope and the bead data indicate deeper sediment mixing near shore than at the lake center, which means that diapausing eggs buried in near-shore sediments are more likely to be mixed to the sediment surface and so are more likely to receive the hatching cue than are buried eggs at the lake center.
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Sediment mixing and egg hatching
In the laboratory, sediment stirring had a marked and highly significant effect on the number of D. sanguineus eggs hatching from lake sediments (Fig. 6; Repeated Measures ANOVA; 2.2 cm: F = 54.6, df = 1, P = 0.0018; 0.8 cm: F = 107.6, df = 1, P = 0.0005). This is consistent with the hypothesis that stirring brings eggs to the sediment-water interface where they are exposed to the hatching cue. In both sediment-depth treatments, there was an initial burst of hatching in the absence of stirring that subsequently declined. These were presumably the eggs that initially lay close enough to the surface to receive the hatching cue. According to this interpretation, hatching then continued for an extended period in the stirred treatments because new eggs were brought to the surface and exposed to the hatching cue.
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If the difference in the number of eggs hatching between the stirred and the not-stirred treatments is entirely due to the relative exposure of the eggs to the hatching cue, the data can be used to estimate the depth into the sediment that the hatching cue penetrates as: ([total number hatched in "no-stir"]/[total number hatched in "stir"]) x (total sediment depth). For the 2.2-cm and the 0.8 cm deep treatments, the estimated depths of cue penetration are 3.3 mm and 1.5 mm respectively. The reason for the difference between the two treatments is unclear, but both estimates suggest that the hatching cue does not penetrate more than a few millimeters and supports the interpretation that the depth of sediment mixing must be critical for determining the number of eggs that hatch.
Egg hatching and phenotype distribution
There is a significant relationship between the magnitude of the change in the depth of Bullhead Pond between consecutive years and the phenotypic variation in seasonal diapause timing (Fig. 7; Spearman Rank Correlation, rs = –0.76, p < 0.01). In particular, the copepod population in the water column in years for which there was a substantial decline in water depth from the previous year had high levels of trait variation. The three years in which trait variation was greatest were also the years in which water level in Bullhead Pond were the lowest values for the preceding two, three or > four years (Fig. 7).
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pond depth = –0.3 m), 3 yr ( |
DISCUSSION |
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SYNOPSISINTRODUCTIONHISTORICAL RECORDS AND DYNAMICAL...A LOGICAL CONFLICT AND...METHODSRESULTSDISCUSSIONReferences |
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The diapausing eggs produced by zooplankton have important implications for our understanding of ecological and evolutionary processes. We have explored the logical conflict between the proposition that egg banks are an accurate historical record, which requires that there be little sediment mixing, and the possibility that eggs laid many years in the past can hatch naturally and influence on-going dynamics, which requires mixing of eggs to the sediment surface. This is not a conflict for the animals. They simply experience the effects of prolonged dormancy whatever the processes that bury eggs and mix them back up again might be. Rather, since egg banks have been studied both for their historical content and for their ecological and evolutionary potential, it is a conflict in what we understand about egg banks. Our detailed studies of D. sanguineus at Bullhead Pond, R.I., however, illustrate for a single system how both historically reliable records and temporal dispersal can be present for a single population within a single lake.
In Bullhead Pond, a small, shallow and sheltered lake, there is significant spatial variation in sediment dynamics that leads to important differences in the way that the egg bank acts in ecological and evolutionary processes. In the lake center, sediment mixing by bioturbation, though present, is relatively slight (Figs. 4 and 5). A substantial fraction of the diapausing eggs that settle to the bottom there become buried below the mixed zone before they receive the hatch cue and so an egg bank, deposited in historical order (with some smearing), accumulates (Fig. 2). In contrast, sediment mixing processes near shore are greater as is the depth of regular sediment disturbance. Most diapausing eggs receive the cue to hatch and so few eggs accumulate in the egg bank. In the laboratory, sediment mixing stimulates hatching (Fig. 6), and in the lake, it is in the more mixed near-shore region of the lake where the greatest amount of hatching occurs (Fig. 3). Near-shore sediments must be where the primary contributions of the egg bank to on-going ecological and evolutionary processes are most important. In Bullhead Pond, which fluctuates markedly in depth from one year to the next, sediments are subjected to near-shore mixing processes that vary through time. In years of extremely low water level, even the deep egg bank can be exposed to increased disturbance. In these low-water years, the variance in phenotypes observed in the water column is elevated (Fig. 7) presumably because the egg bank contains a greater variety of genotypes and phenotypes than is present in the water column population in most years.
How general is this spatial variation in egg bank dynamics, documented here for a single system? Although the egg bank of no other lake has been studied as extensively as Bullhead Pond, one aspect of the spatial structure can be explored. If the processes observed in Bullhead Pond are common, then there should be a general tendency for sediment densities of diapausing eggs to be greater in sediments at the center of lakes than at their margins. A survey of lakes in which the distributions of diapausing eggs have been investigated shows that the pattern in Bullhead Pond is quite general (Table 1). For eight zooplankton populations from six lakes (including D. sanguineus in Bullhead Pond), the ratio of egg densities in central deep sediments versus shallow near-shore sediments is uniformly greater than one, and ranges as high as 25. This means that it is likely to be quite common to find within-lake spatial variation in the role that the egg bank plays in ecological and evolutionary processes.
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Although zooplankton diapausing egg banks are similar in many ways to plant seed banks, lacustrine environments impose constraints on the functioning of egg banks that may be distinct from their terrestrial plant counterparts. Distinct zones of net deposition and mixing or resuspension within a single water body create opportunities both for the long-lived dormant stages to influence ecological and evolutionary processes, and for the long-term storage of these diapausing eggs to provide a record of past ecological and evolutionary processes. It is possible that in at least some seed-bank-producing plant populations there exist analogous regions of deposition, storage, germination and loss. As with the action of fish and invertebrates in redistributing eggs (e.g., Cáceres and Hairston, 1998
), terrestrial animals can have significant effects on seed dispersal, locally patchy storage and germination (e.g., Louda, 1989). Similarly, effects of submersed aquatic plants on egg distribution and movement (Cáceres and Hairston, 1998) have clear counterparts in the dynamics of seeds, where plants can trap seeds as well as influence their germination success (Evans and Cabin, 1995; Pake and Venable, 1995). However, there appear to be few instances in which plant seeds are deposited in a temporally reliable sequence from which ecological or evolutionary histories can be inferred (see McGraw et al., 1991 for a striking exception). If the soils in which seeds are buried are typically more thoroughly mixed than the bottom sediments of lakes, seed populations probably turn over more rapidly than diapausing egg populations, and the mean age of seeds in seed banks is likely to be considerably less than the mean of eggs in egg banks, even if the physiological capacities of each for survival during dormancy is equivalent. The dynamics of seed banks should be more similar to those of egg banks near shore than to those in deep water, with the result that generation overlap produced by seed banks is probably substantially less that that produced by egg banks.
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ACKNOWLEDGMENTS |
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We thank C. E. Cáceres, B. T. De Stasio, D. R. Engstrom, S. P. Ellner, W. Lampert, E. L. Mills, and L. J. Weider for stimulating discussions and sharing data. K. D. Kearns, K. Batson, P. Jester and T. Groman helped with data collection. NGH thanks M. E. Feder for the invitation to participate and for patience, and the National Science Foundation and the Society for Integrative and Comparative Biology for symposium travel funds. The research reported here was supported by the National Science Foundation (grants DEB-9119984 and DEB-9815365 to NGH and S. P. Ellner, and grant INT-9603204 to NGH), the Environmental Protection Agency/National Science Foundation program on Water and Watersheds (EPA grant R82-4771-010 to NGH and E. L. Mills), and the U.S. Department of Agriculture (Hatch Project NY(C)-1837409 to NGH).
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FOOTNOTES |
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1 From the Symposium Plant/Animal Physiology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
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SYNOPSISINTRODUCTIONHISTORICAL RECORDS AND DYNAMICAL...A LOGICAL CONFLICT AND...METHODSRESULTSDISCUSSIONReferences |
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