Starvation in Daphnia: Energy reserves and reproductive allocation

Starvation in Daphnia: Energy reserves and reproductive allocation*

Alan J. Tessier, Linda L. Henry, und Clyde E. Goulden Division of Environmental Research, Academy of Natural Sciences of Philadelphia, 19th and the Parkway, Philadelphia 19103

Murk W. Dumnd Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755

The relationship between energy reserves (1)iornass and triacylglyccrol) and starvation time is invcstigatcd for two planktonic Cladocera, Daphnicr. gcdeatu mendotae and Dclphnia mngna. ‘l’riacylglycerol storage is correlated to total individual biomass independently of body size. Adult biomass increases twofold to threefold during the intermolt, with triacylglycerol ac- counting for 16% of the total increase. The amount of triacylglyccrol transferred into each egg dcpcnds on the adult’s feeding success.

Starvation time is correlated to body mass; however, trixylglyccrol storage and rcproduc- tive allocation modify the relationship. Although adult biomass and percentage of lipid both increase during intermolt, animals in late intcrmolt starve sooner than those in early-middle intcrmolt because of the transfer of energy rcscrves to the ovaries for reproduction. Dclphnia mcancl neonates with high maternal lipid survived twice as long as neonates with low ma- te&l lipid lxlt similar body mass.

Food limitation and exploitative competition can be important factors in dc- tcrmining the structure of zooplankton assemblages (e.g. Ilrbackova-Esslova 1963; Weglenska 1971; Hebert 1977; Neil1 1978; Lampert 1978; Neil1 and Pea- cock 1980; Kerfoot and DeMott 1980). When regulated by food, the dynamics of zooplankton populations are frequently oscillatory (e.g. Pratt 1943; Slobodkin 1954; Clark and Carter 1974; Kwik and Carter 1975). At peak animal densities, food concentration may become so low that no individual can gather more than a small fraction of its daily needs so that ability to withstand starvation dcter- mines whether a spccics will persist in competition.

A central theory of zooplankton ecology (size-efficiency hypothesis) equates large body size with superior competitive

l Work supported in part by NSF grant DEB 80- 08918 and a fellowship from the University of Pennsylvania to A.J.T., NSF grant DEB 76-20119 to C.E.G., the supporting research fund of the Di- vision of Enviromnental Research, Academy of Nat- ural Sciences of Philadelphia, and the Klchcrg Folmdation.

ability and greater resistance to starvation (Brooks and Dodson 1965; Hall et al. 1976; Threlkeld 1976). However, the rc- lationship among body size, energy storage, and starvation time is poorly de- fined, and the prediction that large-bodied species are superior competitors has not always been substantiated (e.g. Frank 1957; Neil1 1975; Kcrfoot and Pastor-ok 1978). Differences in the way species allocate stored energy for survival and reproduction during starvation may explain exceptions to the size-efficiency hypothesis. We examine here the relative importance of energy storage, body mass, an d energy allocation strategies to starvation times of two species of Daphniti

For most species, the ability to withstand starvation is correlated with body mass (e.g. Kendeigh 1945; Oliver et al. 1979). This relationship holds both because greater body mass means greater amounts of expendable energy and because individuals of the same species use energy reserves in similar ways. In com- paring species which store different amounts or types of reserves or utilize energy in different ways or at different rates, bd o y mass may not be a good predictor

667

668 Tessier et al.

of relative starvation times (e.g. some copepods can outstarve humans).

Models of starvation time depend on knowledge of both the types and amounts of energy stored by organisms and the major processes and rates of energy ex- penditure (Calder 1974; Downhower 1976). Threlkeld (1976) summarized data on respiration rates and starvation times of zooplankton and empirically derived a model relating starvation time to body mass for cladocerans and copepods starving at 20°C (T = 2.9!5W”*2s, where T is starvation time in days, and W is body mass in pg). This model assumes that respiration is the only energy loss during total starvation and that protein catabolism is the major metabolic process. Both as- sumptions are apparently invalid for zooplankton.

Lipids (triacylglycerol and wax esters) are a major storage product of cladocerans and copepods (Farkas 1970; Lee 1975; Goulden and Hornig 1980; Gould- en and Henry in press). In cladocerans, lipid accumulates during the intermolt phase and is transferred to egg production toward the end of each molt cycle (Tessier and Gouldcn 1982). Neonates are born with a maternal lipid reserve, the amount of which varies according to species and the adult’s feeding success (Goulden and Henry in press). During starvation, adults and juveniles metabo- lize these lipid reserves in order to pro- long survival (Lemche and Lampert 1975). Since lipid is a more efficient energy storage product than either proteins or carbohydrates (more kcal * g-l), an as- sumption of protein catabolism would cause an underestimation of starvation times for animals utilizing stored lipid.

Juvenile Dnphniu expend 55% of their net assimilation on growth, whereas adults invest as much as 70% in reproduction (Richman 1958). There is little evidence to suggest that expenditures for growth and reproduction are stopped during starvation. Lemche and Lampert (1975) noted that much of the energy lost by adult Duphniu in starvation was as reproduction. In both field and laboratory populations adult cladocerans continue to

reproduce even during starvation-in- duced population declines (Goulden and Hornig 1980; Tessier 1981). Continua- tion of growth or reproduction by starving individuals would reduce their survival times below those of individuals that expended energy only for maintenance.

We examine here the extent to which energy reserves affect the body mass and starvation times of Daphnia guleuta mendotue and Daphnia mugnu. Triacylglyc- erol and biomass accumulation during an adult’s molt cycle and allocation of triacylglycerol and biomass to reproduction are quantified. Starvation times are determined for neonates and adults having different amounts of lipid reserve and are then compared with predicted starvation times for zooplankton of similar total biomass (Threlkeld’s model). We discuss the significance of triacylglyccrol reserves and reproductive allocation to starvation times of Cladocera.

Methods Animals und Culture-Daphnia gu-

Zeutu mendotue used to establish cultures for these studies was collected from Marsh Creek Reservoir in Chester Coun- ty, Pennsylvania. Duphniu mugnu origi- nated from a culture that was maintained at McGill University by the late Frank Rigler and is descended from European animals initially established in culture by MacArthur and Bail lie ( 1929).

Water used in the cultures and experiments was collected from Marsh Creek Reservoir in 20-liter polyethylene car- boys, filtered through a No. 1 Whatman filter, autoclaved, cooled to 2O”C, and aer- ated before USC. All cultures and experiments were kept at 20°C with a 14:lO light : dark cycle. Two species of green algae were used in a 1:l concentration as food: Chlumydomonus reinhurdtii (neg- ative strain; Utex 90) and Ankistrodes- mus fulcutus (unknown origin). Algal culture techniques, media, and vitamins are described in detail elsewhere (Gouldcn and Hornig 1980; Goulden et al. 1982).

Animals used for growth, lipid, and starvation measurements were acclimat- cd to experimental conditions for two

Body muss und sturvution 669

generations before experiments. Juve- niles were isolated in vessels receiving the food concentration planned for the experiment, Neonates born in the second brood of these females were isolated for further culture and the original females and remaining young discarded. These F, females were then kept until their second brood was born and neonates of these F, generation animals used to begin the experiment.

Body muss und visible lipid-Juve- niles and adults of both species were haphazardly picked from mass cultures containing different quantities of food. Since body mass was expected to fluctu- ate with molt cycle, only adults of egg stage 1 (Threlkeld 1979) were used. Body length (from top of head to base of tail spine) was measured to the nearest 0.05 mm using a zoom stereoscope. Each individual was classified according to the amount of visible lipid in the body as 0, 1,2, or 3 (low to high lipid index: Tessier and Goulden 1982). The eggs carried by each female were counted but not removed. Each animal was dried at 60°C for 24 h and then weighed on a Cahn clec- trobalance, sensitive to 0.5 pg. Mean dry mass of stage 1 eggs was determined for each species (mean = 10.6 pg*egg-l for D. magna; mean = 189 ,ug.egg-r for D. galeata mendotue), multiplied by individual clutch sizes, and subtracted from body masses of adults. Body mass minus clutch mass was plotted as a function of body length.

Growth-Daphnia magna neonates were raised at a food concentration of 2.5 mg. liter-’ of Ankistrodesmus and Chlamydomonas (A/C). Animals were cultured singularly in 100 ml of water, fed daily, and changed to fresh jars and water every other day. A subsample of 10 animals was harvested at 2-d intervals until day 8 and then at 3-4-d intervals until day 28. The molt cycle of all animals was closely synchronized and adults were always harvested shortly after having laid a new brood of eggs (egg stage 1: Threl- keld 1979). The eggs carried by each female were counted and body length and dry mass determined for each individual

as described above. A mean egg mass of 10.6 pg was used to estimate clutch mass carried by each female.

Lipid analysis -Triacylglycerol content of animals was determined quanti- tatively (Goulden and Henry in press). Daphnia mugnu was acclimated to high food levels (~5 mg * liter-l A/C) and fourth brood adults (body length = 4.7 mm) were harvested either at egg stage 1 or at egg stage 5 (beginning and end of intermolt). The eggs carried by each female were counted and removed, adults freeze-dried, and dry masses determined on an elec- trobalancc. Animals were ground and either extracted immediately or stored at -80°C under nitrogen with 2:l chloroform-methanol (v/v). After extraction at room temperature with this solvent, the crude extract was washed with 0.9% so- dium chloride (Folch ct al. 1956). The volume was reduced under nitrogen and the triacylglycerol separated out by thin- layer chromatography in a two-solvent system on silica gel (Kritchevsky et al. 1973). After detection with iodine, the triacylglycerol was eluted from the silica gel with 2: 1 chloroform-methanol and the solvent evaporated by nitrogen gas bub- bling. Triacylglycerol was measured col- orimetrically (Van Handel and Zilversmit 1957). Triolein standard was used for cal- ibration.

S turvution times -Animals were acclimated to either a high (>5 mg. liter-1 A/C) or low (0.1 mg. liter-’ A/C) food level. Neonates were born in 0.22-Frn filtered lake water and classified according to the amount of visible maternal lipid (maternal lipid index = 0, 1,2, or 3: Tessier and Goulden 1982). Neonates were kept at a density of 1 animal. 10 ml-r (D. magna), or 1 animal.4 ml-’ (D. guleutu mendotue) and changed every 12 h to fresh, O.22-pm filtered water and clean vials. Adults were selected according to the number of hours after having laid the third clutch. For D. magna, 0-, 14-, 36-, and 60-h animals were used; for D. galeata mendotue, 0-, 12-, 29-, and 50-h animals were used. Adults were transferred to 0.22~pm filtered lake water at a density of 1 animal. 30 ml-l (D. magna), or 1 animal’ 10 ml-’ (D. guleutu

670 Tessier et ul.

6

5

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2

1

T

D. MAGNA

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. 0 0

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00 0.

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0.2 0.4 0.6 0.8 1.0 1.2 1.4

LN SIZE

D. GALEATA

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0

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0 l 0 l : : 0% v .

: 0

0 Q 0

0 0

-1T--- r------7---- - I I I I I - 0.4 - 0.1 0.2 0.5 0.8

LN SIZE

Fig. 1. Relationship between body mass (mg) and body length (mm) in D. gnlecltcl mendottre and II. magna. O-Animals with visible lipid index = 3; 0 --animals with visible lipid index = 1 or 0 (low or 110 lipid observed). For both species, overall regressions and regressions considering only animals with lipid = 3 or lipid = 0 or 1 are significant: P < 0.001. For both species, comparisons of animals with lipid = 3 with those with lipid = 0 or 1 show no difference in slopes of the regressions but a significant difference in clcvation: P < 0.001 (ANCOVA).

Body mass and starvation 671

1000: Pg

100 -

ii _ a

I

E

z . 0

q

10 f

2 I ,,p I I

3 ,’

F ,,’ ,,’ , _’ ., _ _ _ ,’

i’ ’ ,’ . . ,’ . .

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5 IO 15 20 25 213

AGE IDAYSI

Fig. 2. Biomass accumulation vs. age in D. mg- nm f&l 2.5 mg* liter-l of Ankistrorlesmzcs and Chla- mydomonus (AC) in equal amounts. Bars on solid points, f 1 SE. Dashed lines connect calculated mass of adults minus clutch mass (lower points) to mea- surcd mass.of adults at egg stage 1 with clutch mass included (upper points).

mendotae) and changed to freshly filtered water and clean jars every 24 h. Ex- periments were continued until all animals died. A mean starvation time was calculated. Life table data on the same clones of D. magna and D. galeata mendotae cultured at high food levels of A/C, under identical environmental conditions, were used as a control for rates of senescence (Goulden et al. in press).

Results Body mass and visible lipid-When

standardized for genotype, body size, and even molt stage, individual Duphnia from different food regimes carry different quantities of visible lipid. These differences in body lipid arc associated with large differences in body mass (Fig. 1). Daphnia galeata mendotae adults of high body lipid (lipid index = 3) weighed twice as much as similar-sized individuals of low body lipid (lipid index = 0). In D. magna differences were even greater. For both species, regressions of In length to In mass for animals with a lipid index = 0 vs. lipid index = 3 differ signifi- cantly in elevation (P < 0.001) although not in slope (ANCOVA). Lipid per se is certainly not the single cause of’ variation in mass, but visible lipid is apparently

Table 1. Body mass (pg) and trixylglycerol (pg equiv;llent triolein) incrcasc during molt cycle of fourth-brood adult D. mclgnc~. All eggs were rc- moved from brood pouch. Mass 1 1 SE.

Egg I,ipicl st.qe hdy ImIss Triacylglyccral W)

: 537.6+ 16.4 36.38k3.1 6.7kO.5

1,164.1+30.6 136.8k5.8 11.8kO.5 5-l 626.5 100.42 16.3

positively correlated with other compo- nents of body mass.

Growth-In addition to differences between individuals in energy reserves, the molting cycle of cladocerans also causes variation in length-mass relations (Fig. 2). During intermolt, the accumulation of energy reserves causes a twofold-threefold increase in the body mass of adult D. magna. After molting, most of this accumulated mass is lost as eggs, extruded from the ovaries into the brood pouch. Therefore, throughout adult life, body mass fluctuates in a zig-zag fashion, the highs associated with late molt position (egg stage 5: Threlkeld 1979) and the lows with early molt position (egg stage 1).

Lipid analysis -Triacylglycerol ac- counts for 16% of the biomass increase during the fourth-brood intermolt of D. magna (Table 1). Dry weights, dctcr- mined at the start and end of the molt cycle, indicate a doubling of biomass (from 537.6 to 1,164.l pg*animal -I); however, the amount of triacylglycerol in- crcascs from 36.38 to 136.8 pg. animal-‘, a 3.8-fold increase. Whereas udlllts contain only 6.7% triacylglycerol at the start of the molt cycle, 1)~ late intermolt adults are 11.8% triucylgl ycerol.

Calculation of triacylglycerol present in eggs in the brood pouch (mean of46 eggs per fourth brood x 2.4 pg of triacylglycerol per egg = 110.4 r_cg: Goulden and Henry in pl’ess) is remarkably close to the direct estimate of total triacylglycerol ilc- cumulation during intermolt (100.4 ,.,,g: Table 1). This suggests that well fed adults allocate to reproduction almost all the lipid reserve uccumulatcd during intcrmolt. The total increase in biomass during intermolt does not however get

672 Tessier et al.

0 (0) 14 (1) 36 (2) 60 (5)

0 (0) 12 (1) 29 (2) 50 (5) 50 (5)

D. mclgna 198k8 246+11 18026 160+5

3 3 3 3

Mean 2 2

Mean

D. gdeata 105+-3 3 134+-7 3 140+-4 3 12624 Mean 114-14

1461~2 12023 14724 12524 134k6 105k8 104L3 105-co.4 66k4

52+-2 5625 70+-3 60+-4

incorporated into eggs. Of the 626.5 pg of mass accumulated during the fourth- brood intermolt, only 78% is transferred into egg biomass (10.6 kg. egg-l x 46 eggs per fourth brood = 487.6 pg). The pref- erential transfer of lipid to eggs results in a higher percentage of lipid in eggs and neonates than in adults (22.6% triacylglycerol in eggs, 13.9% in neonates: Goulden and Henry in press; compared to 6.7% in D. magnn adults: Table 1). This high percentage of maternal lipid in neonates is visible as large triacylglycerol droplets anterior and dorso-lateral to the gut.

The quantity of maternal lipid transferred to neonates is variable. Adult Duphniu in low food env ironments give less maternal lipid to each egg than adults of the same clone from high food cnvi- ronments (4.3% triacylglycerol in D. mugnu neonates from mothers from low food cultures vs. 13.9% in neonates from mothers from high food cultures: Gould- en and Henry in press).

S turva tion-Fluctuation of biomass and

lipid associated with food regime, molt cycle, and reproductive allocation suggests that these latter processes influence starvation times of Cladocera. Mean starvation times of D. mugnu and D. guleutu mendotue, adults and neonates, are given in Table 2. In general, individuals died only after all visible lipid in the body had disappeared.

Neon&es --In both species, neonates continued to grow while starving; most individuals molted into the second instar before dying. Neonates of D. mugnu lived longer in starvation than the smaller ones of D. guleutu me,ndotue. However, the amount of maternal lipid greatly influ- enced starvation time. Duphniu mugnu neonates containing low maternal lipid (lipid index = 1) starved as quickly as D. guleutu mendotue neonates of high maternal lipid (lipid index = 3). Further- more, D. mugnu neonates of high maternal lipid survived as long as adults of D. galeutu mendotue, a larger, much heavier animal. This implies that body size or even biomass alone are not good predic- tors of starvation times in Cladocera; lipid content is equally significant.

Adults-Despite biomass accumulation during intcrmolt, adult starvation times increased only in the first half of the intermolt and then decreased sub- stantially in late intermolt (Table 2). Adult D. magna that began starvation in egg stage 5 (60 h into intermolt) had nearly twice the biomass, yet starved in two- thirds the time, of animals that began starvation in egg stage 1 (14 h into intermolt), This general pattern was evident in both spccics and is apparently associated with continued reproductive activity during starvation (Table 3). Initiation of starvation at later stages of the intermolt is correlated with increased clutch sizes produced while starving. Assuming a linear increase in adult biomass during intermolt, we calculate the fraction of this biomass used in reproduction during starvation (Table 3). Kegardless of when during the intermolt starvation began, fc- males always allocated a high percentage of l,iomass accumulated during that intermolt to egg production. This fraction

Body muss und starvation 673

Table 3. Observed clutch sizes and reproductive biomass calculations for D. magntl during starvation. h-Hours after laying third brood that starvation began; calculated biomass accumulation (CBA) assumes II linear increase in biomass during intcrmolt; a mean egg weight of 10.6 /.~g was used to calculate clutch biomass (CCB); FAR-fraction of accumulated biomass allocated to reproduction during starvation.

h

0 14 36 60

Mean clutch

CBA size cm FAR

0 31.8 1.0 117 :: 74.2 0.63 301 18 191 0.63 501 26 275.6 0.55

Mean 0.70

of biomass allocation (ca. 70%) is similar to the pattern of reproductive allocation in well fed Dnphniu (Richman 1958; Fig. 2). Apparently, with regard to energy allocation, an individual Duphniu is insen- sitive to rapid changes in food availability.

Overall, starvation time is positively correlated to body mass (T = 66.0W0*1”5, r = 0.86, P < 0.001; where T is starvation time in h and W is body mass in pg), However, almost all survival times observed are shorter than those predicted from a model based on respiration costs (Fig. 3; Thrclkeld 1976). Only D. magna neonates having the highest maternal lipid index survived as long as the model predicts.

The slope of the observed relationship between starvation time and body mass is also less than that predicted. Observed values indicate less of an advantage (starvation resistance) with increasing body mass than prcdictcd from the model (predicted slope of 0.25 vs. actual slope of 0.165). Senescence does not explain the brief starvation times of D. mngnu adults, Life table data on both D. mugnu and D. gale&a mendotue indicate that at high food levels survival is >95% in the first 25 days (Goulden et al. in press). No animals survived for more than 25 days in our experiments.

In summary, mean starvation times de- pended on lipid reserves and the molt

MASS lUgI

Fig. 3. Starvation time (h) vs. body mass of D. magna adults (+) and nconntes (0), and D. gnleclta menclotc~e adults (A) and neonates (A). Numbers on LI. mngnfi neonate points refer to matcrnnl lipid index assigned to each group (1, 2, or 3). Solid line is predicted starvation time of animals catabolizing protein for maintenance (T = 70.8W”.25, where ?’ is starvation time in h and W is body mass in ~6: Thrclkeld 1976).

cycle. Adults expend most reserve biomass on reproduction, whereas neonates utilized some maternal lipid for development into second instars. Continued growth and reproduction during starvation results in death from starvation sooner than expected from a model based on respiration losses alone.

Discussion The quantity of lipid stored by an in-

dividual cladoceran is indicative of its total energy reserves. Body size alone is not an adequate predictor of body mass, let alone resistance to starvation. Length- mass regressions for zooplankton can be quite variable; a threefold-fourfold range in mass at a given size is not unusual (Burns 1969; Dumont et al. 1975; Bottrell et al. 1976; Fig. 1). Storage of energy at high food 1 evels is apparently the cause of this variance. Previous work dcmon- stratcd how a visual assessment of individual triacylglyccrol reserves (lipid index) can bc used to estimate food availability in natural populations of cladocerans (Tessier 1981; Tessier and Gouldcn 1982). Our present results suggest that the lipid index is also correlated to total energy reserves and resistance to starvation.

Variation in the amount of maternal lip-

674 Tessier et al.

id caused substantial differences in nco- nate starvation times. Daphnia magna neonates with high maternal lipid survived twice as long as neonates with low maternal lipid. Despite much lower body mass, D. galeata mendotae neonates with high maternal lipid survived as long in starvation as D. magna neonates with low maternal lipid. Interestingly, actual csti- mates of triacylglycerol for these animals are also similar. Daphnia galeata mendotae neonates of lipid index = 3 contain 6.3% triacylglycerol by weight and D. magna neonates of lipid index = 1 contain 4.3% triacylglycerol (Gouldcn and Henry in press). Starvation resistance apparently depends more on lipid content than on body mass, and consequently, reproductive success in conditions of low food or starvation would depend on the quantity of lipid invested in each egg.

Large-bodied species, such as D. magna, produce neonates with higher percentages of lipid than do smaller cladocerans such as Bosmina longirostris (Goulden and Henry in press). However, with respect to mass, larger species produce relatively cheaper eggs (Lynch 1980). For example, D. magna produces eggs which are only 0.0197 of third-brood adult mass at egg stage 1, whereas D. galeata mendotae makes eggs which are 0.0815 of third-brood adult mass at egg stage 1. Why large species should pro- vide their young with the advantage of a higher percentage of lipid is unknown, but may be related to the longer juvenile development period of these larger species. Ironically, the longer dcvelop- mcnt time would seem a consequence of producing relatively smaller, lighter eggs.

Greater starvation resistance should enable large-bodied species to outcom- pcte small species in low or fluctuating food environments. However, our results concern only two species of Daphnia. Other species may have more conserva- tive strategies of allocating reproductive energy, enhancing survival during starvation, In addition, population age and size structure can influence competitive outcomes among species of different body size (Neil1 1975; Lynch 1978). The sig-

nificance of strategies of cncrgy allocation and of demography to competitive interactions among cladocerans is dis- cussed elsewhere (Goulden et al. in press; Goulden and Henry in press),

The effect of molt cycle position on starvation time of adults illustrates the discreteness of reproductive allocation in Cladocera. The transfer of body reserves (especially triacylglycerol) to the ovaries for egg production occurs late in the intcrmolt (Tessier and Goulden 1982). Therefore, susceptibility to starvation should increase as an individual moves closer to the end of intermolt. IIowever, during inter-molt, individual biomass is being accumulated. The compromise is that starvation time increases to a maxi- mum in egg stage l-2 and then decreases in late intermolt (egg stage 5). Daphnia magna, with its longer intermolt period, shows this effect most strongly.

Despite the lowering of individual resistance to starvation, reproduction during starvation may have certain advan- tages for large Cladocera. Parthenogenic reproduction increases the number of individuals with the same genotype. An increased numhcr of animals can be important in an environment with a significant probability of mortality from factors other than starvation (senescence, predation, and parasitism). Large species of Daphnia produce neonates containing high percentages of maternal lipid and therefore can survive for a substantial time without food. For both D. magna and D. galeata mendotae, if we add gestation time to mean neonate starvation time, we find that neonates survived as long as adults of the same species. We do not know how long an adult could survive starvation if it refrained from reproduc- ing, but the advantage of this additional time would be weighed against an increased probability of mortality from senescence or other causes. Finally, if juveniles and adults partition resources, then parthenogenic reproduction by an adult genotype will increase the niche breadth of that genotype. For example, if juveniles use the habitat space different- ly (Tessier 1981) or can feed on different

Body mass and starvation 675

food particles (Gcller and Miiller 1981), Cladocer;~ and their consequences to competi-

then parthenogenic reproduction by a tion. Proc. Natl. Acad, Sci. 77: 1716-1720.

large individual could increase the re- IIALL, D. J., S. T. THHEI,KELD, C. W. BURNS, AND

sources available to that genotype. De- ,P. H. CROWI,EY. 1976. The size-efficiency

termining the relative validity of these hypothesis nnd the size structure of zooplankton communities. Rnnu. Rev. Ecol. Syst. 7: 177-

hypotheses will require comparative 208.

studies of energy allocation among var- IIEDERT, P. D. 1977. Niche overlap among species

ious species of Cladocera. in the Dtrphnia cwinato complex. J. Anim. Ecol. 46: 399409.

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Submitted: 22 July 1982 Accepted: 6 December 1982

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Starvation in Daphnia: Energy reserves and reproductive allocation