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The Ecology of Optimal Dormancy and Environmental Constraint

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The Ecology of Optimal Dormancy and Environmental Constraint Ecology, 84(5), 2003, pp. 1189±1198 q 2003 by the Ecological Society of America HOW LONG TO REST: THE ECOLOGY OF OPTIMAL DORMANCY AND ENVIRONMENTAL CONSTRAINT CARLA E. CAÂ CERES1,3 AND ALAN J. TESSIER2 1School of Integrative Biology, 515 Morrill Hall, University of Illinois, Urbana, Illinois 61801 USA 2W. K. Kellogg Biological Station and Zoology Department, Michigan State University, Hickory Corners, Michigan 49060 USA Abstract. Dormancy is a common mechanism employed by short-lived organisms for persistence in a variable environment. Theory suggests that the fraction of propagules that terminate dormancy each year should be ,100% when recruitment success varies tem- porally. Moreover, the fraction of propagules that resumes development should vary across habitats that differ in the probability of successful recruitment or the probability of survival during dormancy. We tested these predictions by using dormant eggs from ®ve populations of the freshwater cladoceran Daphnia pulicaria that differ in their ability to recruit to and persist in the water column. In two separate experiments, newly produced dormant eggs were incubated in situ for one year at various sites on the bottom of the lakes. A series of reciprocal transplants among four of these populations separated the effects of lake-speci®c environmental cues from the genetic and maternal effects of the different populations. Additional eggs were incubated in the laboratory under photoperiod±temperature combi- nations representative of those in the ®eld. We found that the annual hatching fraction ranged from 6% to 50% among lakes, and that hatching fraction was primarily driven by environmental cues rather than being a result of the source of the eggs. However, laboratory incubations demonstrated signi®cant differences among populations in the trajectories of the hatching curves, and a much higher rate of hatching than the ®eld incubations. Our results suggest that variation in dormancy strategies within these systems is likely in¯uenced both by the seasonal risk experienced by the active individuals and by risks associated with entering the dormant egg bank. Key words: bet hedging; Daphnia pulicaria; diapause; dormancy, optimal; dormancy termination and environmental cues; resting eggs; zooplankton. INTRODUCTION If this theory is correct and dormancy termination Most organisms live in variable environments and schedules can be shaped by selection, habitats that dif- have evolved life-history traits that facilitate survival fer dramatically in either the frequency of ``bad'' con- and reproduction in habitats of ¯uctuating quality. For ditions or the mortality rate of propagules should select example, many species produce long-lived dormant for populations that differ in their dormancy strategies. propagules such as seeds, eggs, or cysts that can not Annual plants have served as the primary model system only survive conditions that are lethal to active indi- for testing this theory, and variation in germination viduals, but can also create overlapping generations fractions at the level of species, population, and ge- with the formation of persistent seed or egg banks notype is well established (Went 1949, Grime et al. (Leck et al. 1989, Hairston et al. 1995, CaÂceres 1997). 1981, Phillipi 1993a). The studies that have rigorously When only a fraction of propagules resume develop- addressed the theory indicate that delayed germination ment at the ®rst available opportunity (e.g., ®rst rainfall is consistent with a bet-hedging strategy, and some after seed drop), short-term ®tness gains are sacri®ced, suggest the occurrence of ``predictive germination'' in but this bet-hedging strategy of variable germination which phenotypic plasticity in response to the hatching pays off in habitats that are occasionally so bad that cues results in the highest germination fractions in recruitment back to the dormant stage fails entirely years that are favorable for recruitment (Rice 1985, (Cohen 1966, Seger and Brockmann 1987). Just what Phillipi 1993b, Evans and Cabin 1995, Pake and Ven- fraction of propagules should forgo resuming devel- able 1995, Clauss and Venable 2000). opment is predicted by theory to be related to the fre- Much like annual plants, many species of freshwater quency of favorable habitat conditions and the prob- and nearshore marine zooplankton produce long-lived ability of survival in the dormant stage (Cohen 1966, dormant eggs that accumulate in vast numbers in sed- iment egg banks (De Stasio 1989, Marcus et al. 1994, Ellner 1985a). Hairston 1996, CaÂceres 1998). The existence of these Manuscript received 10 May 2002; revised 16 September egg banks indicates that not all eggs resume devel- 2002; accepted 27 September 2002. opment soon after they were produced, raising the 3 E-mail: [email protected] question of whether or not this accumulation of viable 1189 1190 CARLA E. CAÂ CERES AND ALAN J. TESSIER Ecology, Vol. 84, No. 5 offspring represents a bet-hedging strategy parallel to marily the result of genetic or environmental effects? that seen in annual plants. Laboratory studies have in- Is there any evidence that egg banks represent an op- dicated substantial variation in response to hatching timal strategy for these populations? Our results sug- cues across species, populations, and genotypes of zoo- gest that despite differential responses to environmen- plankton (Pancella and Stross 1963, Schwartz and He- tal cues both within and between populations, the op- bert 1987, Van Dooren and Brendonck 1998) and have timal hatching strategies predicted by theory are con- documented signi®cant genetic effects on the hatching strained by among-lake variation in availability of fraction (De Meester and De Jager 1993a). A few ®eld environmental cues. studies have directly estimated hatching rates from the sediment egg bank, and all conclude that a very small METHODS fraction of the viable eggs terminate dormancy within a given year (De Stasio 1989, CaÂceres 1998, Hairston Study systems et al. 2000). Our study lakes are small glacial kettles in southwest If dormancy schedules in zooplankton populations Michigan (Barry and Kalamazoo Counties) that vary are shaped by selection, then we would expect the in surface area (4.8 ha±67.6 ha) and maximum depth hatching fraction of eggs to vary among lakes, de- (9 m±14 m). The zooplankton assemblage of each lake pending on the probability of successful recruitment is dominated by Daphnia pulicaria during spring. Four back to the egg bank (sensu Cohen 1966, Ellner 1985a, of the lakes thermally stratify in summer, creating a b). Successful recruitment is likely in¯uenced by a deep-water refuge in which the D. pulicaria can avoid number of ecological factors (e.g., resource levels, competition and predation (Wright and Shapiro 1990) abundance of competitors, and predation risks) known and therefore persist year-round (perennial popula- to vary widely among lakes in the same geographic tions: Bristol Lake, Lawrence Lake, Warner Lake, 3 region. Alternatively, rather than genotypes bet hedg- Lakes 2). Among these perennial populations, however, ing by producing some fraction of offspring that will there is considerable variation in the annual water-col- delay hatching, diapausing eggs may accumulate in the umn abundance and seasonal dynamics of D. pulicaria. sediments simply because some fail to get the ``right'' This variation is in part associated with the fact that cue soon enough and are subsequently buried. Since in some lakes, deep-water anoxia reduces the size of eggs may need to be within the top few millimeters of available refuge, leading to a decline of summer den- sediment to receive the hatching cue and terminate dia- sities (Tessier and Welser 1991, C. E. CaÂceres and A. pause, the majority of the eggs produced can quickly J. Tessier, unpublished data). The ®fth lake, Little become buried too deeply to contribute to the active Long, has a large surface area and therefore does not population (Kasahara et al. 1975, CaÂceres and Hairston stratify thermally during the summer. The water-col- 1998). If this is the case, mother and offspring may umn abundance of D. pulicaria in this lake typically have little control over hatching schedules and the pres- falls below detection by mid-summer due to a lack of ence or absence of egg banks in a particular system may be driven to a large extent by physical processes deep-water refuge (annual population). These differ- such as the degree to which sediments accumulate and ences in water-column dynamics likely create annual are subsequently mixed. Hence, if diapause strategies variation within and among lakes in a population's abil- are shaped by selection in these populations, the risks ity to hatch from the egg bank and successfully recruit experienced in the water column balanced against the back to the dormant stage, thereby creating variation risks in the sediment will determine the optimal strat- in the frequency of ``good'' and ``bad'' years among egy. populations. Moreover, differences in basin shape and Our research focuses on the variation in diapause productivity among the lakes likely in¯uence the rates strategies of several populations of Daphnia pulicaria of sedimentation and re-suspension in these lakes, two inhabiting small lakes in southwest Michigan (USA). key processes in determining the risk of eggs being More than six years of ®eld sampling indicate that the buried too deeply to ever receive a hatching cue (CaÂ- annual phenology of the Daphnia pulicaria in the
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