Zooplankton egg banks as biotic reservoirs in changing environments
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1 Limnol. Oceanogr., 41(5), 1996, , by the American Society of Limnology and Oceanography, Inc. Zooplankton egg banks as biotic reservoirs in changing environments Nelson G. Hairston, Jr. Section of Ecology and Systematics, Cornell University, Ithaca, New York Abstract The long-lived diapausing eggs of zooplankton constitute an ecological and evolutionary reservoir that can impact the rate and direction of population, community, and ecosystem response to environmental change. Viable diapausing eggs are often extremely abundant and can survive in aquatic sediments for decades or longer. As the mean environment changes, the frequency of extreme conditions will likely increase, and species with prolonged diapause will be able to survive extreme years of no recruitment, whereas species lacking an egg bank will not. An altered environment may change which species have poor recruitment and even, through effects on thermal diapause cues, which species produce an egg bank. The interaction between environmental variation and generation overlap (produced by prolonged diapause) results in the maintenance of biotic diversity (both species richness and genetic variation), which forms the foundation for response to future environmental change. Environmental change is manifested as a directional alteration in the mean environment and, very likely, as a change (either up or down) in its variance (Mearns et al. 1992; Kerr 1995). The direction and rate of response of ecological communities to such changes is a product of at least four characteristics of the organisms present: their species diversity, the intrinsic physiological abilities of each species to deal with the changes, the amount of relevant genetic variation present that permits the populations to respond to altered natural selection, and the indirect effects of the first three categories on interspecific interactions. The second and third categories include both the organisms existing in the community at present and those capable of dispersing into it. One source of organism dispersal is from long-lived dormant stages; as Templeton and Levin (1979) pointed out, the emergence of these stages can be thought of as migration from the past. Here, I point out the potential importance of long-lived dormant stages of plankton to the response of pelagic lake communities as their environments are altered over time. My arguments and examples are largely restricted to a consideration of zooplankton, but the fundamental principles also apply to other members of the plankton, as well as to a large variety of aquatic organisms and indeed to residents of many other ecosystems. When the processes influencing the responses of particular species to environmental changes are understood, indirect effects on the ecosystem can be explored more informatively. Individual zooplankton species and individual genotypes have different impacts in pelagic lake ecosystems, and the trajectory of any change in populations or communities as a result of altered environments may have significance beyond biotic diversity. For ex- Acknowledgments 1 thank the editors for giving me the opportunity to write this article, M. V. Moore for advice, and C. M. Kearns and two referees for critical comments. Research was supported by Hatch Project (NYC-l ) USDA, NSF grant DEB 9 l to N.G.H. and S. Ellner, and EPA grant R O ample, within the zooplankton, taxa differ in being either generalists or specialists (DeMott 1988; Pace et al. 1990), in consumption efficiency (Hairston and Hairston 1993), in rates and routes of nutrient recycling (Lehman 1984; Sterner et al. 1992), and in vulnerability to predation (Zaret 1980; O Brien 1987). The net result is that the type of grazer present in a lake can have a large impact on trophic transfer efficiencies from algae to zooplankton and from zooplankton to fish (Hairston and Hairston 1993) and a large effect on nutrient dynamics (especially in a system near the N : P ratio at which it shifts between nitrogen and phosphorus limitation; Elser et al. 1988). Projected climatic changes in mean temperature and precipitation patterns in North America (elsewhere in this issue; see also Kerr 1995; Moore et al. in press) will impact aquatic organisms through direct and indirect effects on their abilities to obtain resources and hence on their interactions with prey, competitors, and predators. Furthermore, when the mean climate changes, the distribution of environmental year-types may also change; conditions that were formerly considered extreme are likely to become more common (Mearns et al. 1984, 1992). Because most holoplanktonic species are multivoltine, a change in environmental variance can lead to rapid shortterm changes in population dynamics and community interactions. For example, the copepod Diaptomus sanguineus living in a small lake in New England experiences changes in seasonal precipitation via changes in lake volume, which in turn significantly alter the densities of zooplanktivorous fish and thus copepod mortality rates (Hairston 1988). Planktonic organisms are typically thought of as ephemeral with short generation times (Allan and Goulden 1980; Banse and Mosher 1980) and the potential to respond sensitively to short-term changes in the environment (Peters 1983; Moore and Folt 1993; Locke and Sprules 1993). Although this perspective is correct in many respects, it is also true that virtually all species living in inland water bodies possess some means of entering dormancy (Hairston and Caceres 1996). Many species have been shown to be capable of remaining dormant for very
2 1088 Hairston Table 1. Densities of zooplankton diapausing eggs in pond, lake, and nearshore marine sediments. Taxon Density (m-2) Location Reference Rotifers Seven species Brachionus plicatilis Branchiopoda Streptocephalus vitreus Holopedium gibberum. Three Daphnia sp. Ceriodaphnia pulchella Bosmina longirostris Copepoda Diaptomus sanguineus Two Diaptomus species Diaptomus pallidus Eurytemora afinis Rotifers Brachionus sp. Branchiopoda Penilia avirostris Evadne tergestina Evadne nordmanni Podon polyphemoides Bosmina longispina mar. Copepoda Two copepod species Two copepod species Acartia clausi Acartia erythraea Acartia steueri Acartia tonsa Calanopia thompsoni Centropages abdominalis Centropages hamatus Labidocera aestiva Labidocera bipinnata Labidocera wollastoni Tortanus forcipatus 1-40x X lo6 up to 1.6x lo x lo x lo X lo x x lo4 up to 1.0x lo x lo5 up to 6.5 x lo x lo5 2.9-l 3.6 x lo x x 1 o5 0.3-l 8.8 x lo x lo3 O-l.1 X X lo3 O-6.5x lo x x lo4 up to 13.0 x lo x lo3 up to 3.7x lo x 1 O6 up to 1.0x lo x lo x lo x lo5 O-2.5 x lo x 10s o-7.3 X lo4 O-2.8x lo x lo x lo x lo x lo4 Inland waters Ztirichsee, Switzerland 15 ponds, Japan temporary pond, Kenya Windgfallweiher, Germany Schijhsee and Kellersee, Germany Piburger See, Austria Piburger See Bullhead Pond, RI Little Bullhead Pond, RI Oneida Lake, NY small pond, New York Lake Ohnuma, Japan Marine waters Pettaquamscutt estuary, RI Pettaquamscutt estuary, RI Baltic Sea Pettaquamscutt estuary, RI Baltic Sea California coast Onagawa Bay, Japan Apalachicola estuary, Florida California coast British coast Buzzards Bay, MA British coast Nipkow Ito 1958 cited by Gilbert 1974 Hildrew Lampert and Krause 1976 Carvalho and Wolf 1989 Moritz 1988 Moritz 1988 De Stasio 1989; Hairston et al Hairston and De Stasio 1988 Hairston and Van Brunt 1994 Dowel1 in press Ban 1992 Onbe 1978 OnbC 1985 OnbC 1978 Onbe 1985 OnbC 1978 OnbC 1985 Onbe 1978 Onbe 1985 Kankaala 1983 Katajisto 1996 Marcus 1990 Uye 1983 Marcus Marcus 1990 Lindley 1990 Marcus 1989 Lindley 1990 long periods of time: decades or even centuries for bacteria, phytoplankton, and zooplankton (see Hairston et al. 1996). This dormancy increases generation time-often substantially-and slows population growth rate. For zooplankton sediment egg banks, there are now a substantial number of taxa in a variety of freshwater and nearshore marine environments for which egg densities have been reported (Table 1). The viable eggs of Calanoid
3 Egg banks as biotic reservoirs 1089 Table 2. The ages of zooplankton diapausing eggs collected from lake and estuarine sediments (Table 1 gives locations and egg densities). Egg age (yr> Taxon Mean Max Dating method Reference Rotifers Brachionus sp. Polyarthra dolichoptera Asplanchna pridonta Pompholyx sulcata Synchaeta pectinata Trichocerca capucina Keratella quadrata Branchiopoda Podon polyphemoides Ceriodaphnia pulchella Bosmina longirostris Copepoda copepod 1 copepod 2 Tortanus discaudatus Diaptomus oregonensis and Diaptomus minutus Diaptomus sanguineus D. sanguineus Pb < Pb Moritz 1987 Moritz 1988 Hairston and Van Brunt 1994 Hairston et al Hairston et al copepods, cladocerans (and other branchiopods), and rotifers are consistently found in numbers ranging between 1 O3 and 1 O6 rnd2. Where the multiplication has been done, these convert to staggering population sizes (e.g. 6.5 x lo9 viable diapausing eggs of D. sanguineus in the sediments of a small lake in Rhode Island; Hairston et al. 1995). Assigning ages to these eggs has been attempted less frequently. In most cases where ages have been reported, the maximum age of viable eggs has been found to be on the order of decades (Table 2), but my colleagues and I have recently found that the eggs of D. sanguineus can survive longer than three centuries in the sediments of Bullhead Pond, Rhode Island. The mean egg age in this lake is >70 yr (Table 2). Not all, zooplankton make diapausing stages and not all diapausing stages have the ability to survive for years. Marcus et al. (1994) found little evidence for prolonged dormancy in the copepod Tortanus discaudatus and the cladoceran Podon polyphemoides in the sediments underlying the anaerobic monomolimnion of a meromictic estuarine basin, whereas other taxa survived as diapausing eggs in the same environment for yr (Table 2). Freshwater cyclopoid copepods, which typically enter diapause in a late copepodid stage, may not exhibit prolonged diapause in permanent bodies of water, although they can survive for several years in the dry sediments of temporary ponds (Rylov 1963; Wyngaard et al. 1991). Many marine pelagic copepods appear not to exhibit diapause, whereas those in the neritic environment often do. Copepod eggs in nearshore marine sediments well mixed by bioturbation may be brought to the sediment surface frequently (Marcus 1984) and so hatch after only a relatively brief period (I 1 yr) of dormancy. Thus, shortterm changes in the environment or, equally, extremes of existing environmental variance that lead to poor recruitment, may cause the elimination of some species while those with egg banks can persist. On the other hand, planktonic species lacking dormancy ( dispersal in time ) may have an enhanced ability to disperse spatially, thus avoiding locally harsh conditions. Regional climate change, however, may decrease the efficacy of spatial dispersal if all habitats within a region are similarly impacted. Prolonged dormancy (i.e. dormancy extending past the next reproductive season) is significant in the context of environmental change for two reasons. First, as suggested, some species and genotypes may be excluded from the water column of a lake in some years, but their dormant stages in the sediments act as a reservoir for seeding the active community when conditions favorable for growth and reproduction return (provided of course that good recruitment years return while the dormant individuals are still alive). Environmental change may alter the frequency of years that are favorable for a particular species, but so long as that species has an egg bank, it is protected from extinction. For example, Chen and Folt (1996) suggested that an increase in autumn water temperature in a small Vermont lake may cue the eggs of the copepod Epischura Zacustris to hatch at a maladaptive time of year leading to the loss of the species from that lake. This would be most likely if all or nearly all years have warm autumns. Alternatively, if climate change leads to in-
4 1090 Hairston creased variance, cooler years will be interspersed among the warm ones and the E. lacustris egg bank may permit it to survive this thermal stress. At the community level, May (1986) found that the assemblage of rotifer diapausing eggs found in the sediments of Loch Leven, Scotland, contained a diversity of species broader than that found in the water column in any single year, but fully concordant with the total assemblage observed over a 6-yr period. The egg bank thus can act as a reservoir of the biotic diversity present in the plankton of a lake over multiple years. As a simple matter of surviving a harsh period of low or zero recruitment, it is necessary that only some diapausing eggs survive and hatch. Because the seed population serves to establish a cohort of individuals that grows and reproduces in the water column, to a very great extent the numbers of eggs hatching from the sediments are not critical. In contrast, the second reason that prolonged dormancy is important in understanding zooplankton response to environment change depends not only on survival through a harsh period, but more sensitively on the amount of generation overlap created by the egg bank. Taxa that would otherwise not coexist due to competition can do so if the organisms involved have sufficient generation overlap, and if they are exposed to environments that vary from one reproductive season to the next, with each type of competitor having greatest recruitment in different years. This storage-effect process (Chesson 1983) can be a powerful mechanism for maintaining both species diversity within communities (Chesson and Warner 1981; Chesson 1994) and genetic diversity within populations (Chesson 1994; Ellner and Hairston 1994; Hairston et al. 1996). For short-lived zooplankton, the egg bank provides the necessary generation overlap, and, as the extent of overlap increases, so does the likelihood of coexistence (Ellner and Hairston 1994). The extent of generation overlap, y, produced by diapause depends on both the fraction of dormant individuals that emerges or hatches each year (H), and the survival probability (s) of those that remain dormant: y = (1 - H)s (Ellner and Hairston 1994). At present, however, few studies provide data that can be used to assign values to either H or s. One exception is De Stasio s (1989) budget for the egg bank of D. sanguineus, which suggests that only a small fraction of the eggs produced hatch the following year. De Stasio also found that many of the remaining unhatched eggs die within a year after they are produced. However, once the eggs are in the sediments, survival is quite high, on the order of 99% yr-l (Hairston et al. 1995). Most theoretical models of the storage effect ask only whether diversity is maintained, but Sasaki and Ellner (1995) have recently shown that the number of different organism types that can coexist in a single habitat increases as a direct positive function of amount of environmental variation. Environmental changes that lead to either increased or decreased year-to-year variation in temperature, precipitation, or other climatic variables can have a direct impact on the amount of biotic diversity (whether species richness or genetic variation) maintained in the future. This indirect effect of environmental change on the capacity of populations and communities to respond to future changes may be quite important. Long-lived diapausing stages and the egg banks they produce may or may not be specific adaptations for survival in varying environments. In theory, the fraction of individuals emerging from diapause in each year should be a direct function of the probability of any given year being favorable for growth and reproduction (Ellner 1985). It is also possible, however, that eggs buried in aquatic sediments often do not emerge simply because buried eggs have to be uncovered to receive the hatch cue. The physical and biological processes affecting sediment mixing dynamics differ temporally and spatially and thus create different emergence patterns within and between habitats. Indeed, climate change itself may have an impact on sediment dynamics in small lakes (e.g. through changes in sediment disturbance in drought years; Hairston 1988). Whether diapause duration is an evolved life-history trait or a by-product of sediment dynamics, the generational overlap essential for the operation of the storage effect is produced. Understanding the processes underlying changes in zooplankton populations and communities is critical to projecting the effects of changing environments in aquatic ecosystems as a whole. The rate and direction of response of aquatic communities as lake environments change will depend on the ecological and evolutionary potential of the resident organisms. Much of this potential resides in the long-lived dormant stages and the generational overlap produced. References ALLAN, J. D., AND C. E. GOULDEN Some aspects of reproductive variation among freshwater zooplankton. Am. Sot. Limnol. Oceanogr. Spec. Symp. 3: New England. BAN, S Seasonal distribution, abundance and viability of diapause eggs of Eurytemora afinis (Copepoda: Calanoida) in the sediment of Lake Ohnuma, Hokkaido. Bull. Plankton Sot. Jpn. 39: BANSE, K., AND S. MOSHER Adult body mass and annual production/biomass relationships of field populations. Ecol. Monogr. 50: CARVALHO, G. R., AND H. G. 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