Vol. 110, No.

971 The American Naturalist January-February 1976

LIFE HISTORY PATTERNS IN ZOOPLANKTON

J. DAVID ALLAN

Department of Zoology, University of Maryland, College Park, Maryland 20742

Variation in life historypatterns has proven amenable to analysis based on

the premise that such variation represents adaptive strategies (Cole 1954;
Gadgil and Bossert 1970). Highly unpredictable or seasonal environmentsmay
favor opportunisticspecies with high intrinsicrates of increase ("r selected"),
while more constant environments do not ("K selected" [MacArthur 1972]).
Inspection of a natural communitywithina single environmentreveals that the
problem of optimally allocating resources among such conflictingdemands as
maximizing the potential for rapid increase, predator avoidance, and com-
petitive ability may be met by a virtual continuum of compromises.Zooplank-
ton communities illustrate this well (Hutchinson 1967) and are particularly
amenable to quantitative analysis. Parthenogenetic and sexually reproducing
zooplankton populations are both well representedin freshwater.Rotifers and
cladocerans fall into the formercategory, have short multivoltine life cycles,
are rather unspecialized feeders, and develop large, transitory populations.
Other plankters, copepods for example, exhibit longer life cycles and fewer
generationsto the point of occasionally being biennial or triennial. Quantitative
comparisons have not been made, however, beyond the reasonably obvious
interpretationthat r is likely to be higherin the formercases.
This paper attempts to place the comparison of zooplankton life historieson
a quantitative basis by estimatingintrinsicrates of increase (r), thereby exam-
ining alternative life historieswhich apparently differin their trade-offsamong
reproductive potential, predator avoidance, and competitive ability. The
implications of this analysis will lend insight into seasonal abundance fluctua-
tions in zooplankton and into certain biogeographic observations, including the
composition of freshwaterand marine zooplankton communities.

ESTIMATION OF rmax

Survivorship and fecunditydata for Daphnia pulex (Frank et al. 1957) are
combined in the survivorship-weightedfecundityfunction,lmx (fig. 1). When
such complete informationis available, the intrinsicrate of exponential increase,
r, for a population with stable age distribution and unchanging survivorship
and fecundityfunctionsmay be estimated from

I xmxe-rxdx = 1. (1)
J0
Amer.Natur. 1976. Vol. 110, pp. 165-180.
?0 1976 by The Universityof Chicago.All rightsreserved.

165
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166 THE AMERICAN NATURALIST

SUfNIVORSHIP-WEIGHTED
FECUNDITY

3 I

*TT

10 20 30 40

AGE(x
FIG. l.-Survivorship-weighted fecundity forDaphnia pulex (data of Frank
et al. 1957). The area under the curve is lxonx,where lx is the probability of
survivingto age x and maxis the average number of female offspringper female
between ages x and x + 1. By eq. (1), r =0.295/day. The dotted line illustrates
the use of eq. (2) by selecting A = 6, T =14, W = 36, and S = 65 and gives
r = 0.287/day. See text fordiscussion.

Published data of this completeness are rare, however, and a simpler approach
must be found. Lewontin (1965) noted that such data from a wide variety of
organisms tend to have a general triangular shape, given which assumption r
could be derived from simple geometrical considerations. That is, if the 1,,m,
curve looks sufficientlylike the dashed line in figure1, then we must know only
A, the time to firstreproduction(egg -+egg); W. longevity; T. the age at which
survival-weightedreproduction peaks; and S. total female offSpringa born to a
female in her lifetime.These are combined in the formula (Lewontin 1965)

W- A 1 r 1 b- rA _ e T - rW e-rTl (2)
2S r2 LT- A V W - T VJ
and solved iteratively for r. Frank's data solved by (1) give r = 0.295/day;
solved by (2) they give r = 0.287/day. The discrepancy appears to be slight,
and comparisons should not sufferfromit.
From the standpoint of colonizing ability one wishes to know the maximal
rate of increase, r,,,. (Andrewartha and Birch 1954), representingthe physio-
logical capacity of the particular species population to increase in a given
environment. In this approach I assume that food is always in surplus and
predation does not occur, so that only temperature and the organism's physio-

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 ZOOPLANKTON LIFE HISTORIES 167

logical capacities are at issue. The effectsof competition and predation xvillbe
considered later.
Estimates of the life historyparameters A, W, T, and S are discussed in con-
junction with life historydescriptions below. Certain problems are of a general
nature, however. All estimates were derived from laboratory culture experi-
ments with rotifers,cladocerans, and copepods, with an eye toward determining
maximal values. These parameters are highly temperature dependent, and an
effortwas made to achieve a representative range of estimates. The literature
was occasionally not complete with regard to particular taxa or particular
temperatures,and I indicate where values had to be approximated. Equation
(2) is most sensitive to changes in A, less so to S and T, and least of all to W
(Lewontin 1965), in accord with the general conclusion of life historyanalyses
that r is affectedmost by changes in prereproductivedevelopment time, less by
changes in brood size, and least of all by changes in longevity. Typically, the
literature is most complete regarding estimates of A; hence, parameters which
occasionally required guesswork were, fortuitously,less critical. A second prob-
lem lies in the adequacy of the culture medium, as slowed development, reduced
brood size, and highermortalityaccompany nutritionalinadequacy (Taub and
Dollar 1964). Some discrepancies in reported culture data undoubtedly stem
fromthis effect.In general I selected values reflectingmore rapid development
and higher survivorshipand based my calculations on what appeared to be a
reasonable range of values. However, it is possible that these are still under-
estimates. I assume that fora comparative approach the essential relationships
across groups are unchanged.

DESCRIPTION OF LIFE HISTORIES AND ESTIMATION OF PARAMETERS

Rotifera
The typical lifehistoryof species of the subclass Monogononta, which includes
all planktonic rotifers(Hutchinson 1967), consists of parthenogeneticreproduc-
tion in favorable circumstances and sexual reproduction in conjunction with,
or in anticipation of, unfavorable conditions. Beginning in the spring with the
hatching of a resting (mictic) egg, parthenogenetic (amictic) females appear.
In some cases, populations overwinter. A substantial number of generations
follow by diploid female parthenogenesis, as each female produces a series of
amictic eggs which develop without fertilization.After some period of time,
mictic females, morphologicallyindistinguishablefromthe amictic, appear and
produce haploid eggs by ordinary meiosis. Males develop from these small,
unfertilizedhaploid eggs. The fertilizationof a haploid egg by a male produces
the large, mictic, resting egg capable of undergoing a prolonged diapause and
carrying the population through overwinteringperiods. Although commonly
thought to occur once a year, the sexual phase may not occur each year or may
occur several times.

1 Hutchinson (1967) treats the biology of zooplankton with great thoroughness and
clearly recognizes (pp. 706-709) the variety in adaptive patterns which this paper addresses.

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168 THE AMERICAN NATURALIST

A quantitative evaluation of this life historyrequired knowledge of A, W, T,

and S (fig. 1). These parameters (table 1) were estimated from studies of
Brachionus calyciftorus(Birky 1963; Halbach 1970), Keratella valga (Kolisko
1938), and Euchlanis dilatata (King 1965). Development times are short and
broods are quite small. Usually, S is about 15 (King 1965; Halbach 1970), but
values as high as 25 female offspringper female were included as potential
maxima. Since brood size does not increase substantially with age, while sur-
vivorship must decrease, I assume that T closely followsA in time. This is sub-
stantiated by Halbach's (1970) lXmtdata.

Cladocera
The lifehistoryof cladocerans, typifiedby the water flea Daphnia, consists of
sexual and parthenogeneticgenerations. A typical cycle may commence in the
spring in a temperate lake froman overwinteringfemale or froma resting egg
which develops into a mature female. Eggs are produced which develop rapidly
and directly,without a larval stage, into miniatureversions of the parent. After
a variable number of instars, but typically five or six, these mature into repro-
ductive females, thus completing the parthenogenetic stage of the cycle. A
substantial number of such asexual generations are produced throughthe spring
and summer. Then, owing to crowdingor other environmentalstimuli, eggs are
laid which develop into males, other eggs develop into sexually reproducing
females, and, following fertilization, resting eggs (ephippia) are produced.
Although as a reproductivepattern this is the analogue of a rotifer'slifehistory,
the underlying cytological and development mechanisms differsubstantially,
testifyingto its independent derivation.
Estimates of A and W (table 1) require little discussion, as various studies are
in close agreement (Daphnia galeata mendotae[Hall 1964]; D. pulex [Frank et al.
1957]; D. laevis [Banta 1939]; D. magna [MacArthurand Baillie 1929; Anderson
and Jenkins 1942]). Estimates of S were more variable, ranging fromas high as
1,072 for D. magna (De Kerherve 1927, cited in Hutchinson 1967) to 300 for
D. laevis (Banta 1939), 160 for D. magna (Anderson and Jenkins 1942), and
about 600 for various species of Daphnia (Green 1956). Hall's (1964) data sug-
gest somewhat largerbroods at highertemperatures.I believe the values selected
for S (table 2) bracket the likely maxima. In contrast to rotifers,development
times are longer and broods much larger. The only available estimate of T was
for 200 C, and placed the peak of the 1lm,,curve at about day 14. Lower tem-
peratures would result in later maturation, essentially pushing the reproductive
period furtherinto the region of lower survivorship. Hence, I assume T to be
only 4 days after A at 100 C as opposed to 7 days after A at 200 C and 8 days
after A at 250 C.

Copepoda
The life cycle of the Copepoda differsstrikinglyfromthat of the Cladocera
and Rotifera in its obligate sexuality. Fertilized eggs hatch into a larval stage,
the nauplius. Six naupliar stages and six copepodite stages are recognized, of

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 ZOOPLANKTON LIFE HISTORIES 169

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170 THE AMERICAN NATURALIST

TABLE 2
SUMMARY OF CERTAIN ECOLOGICAL CHARACTERISTICS OF MAJOR ZOOPLANKTON TAXA

Rotifera Cladocera Copepoda

rmax (1/days). 0.2 1.5 0.2 0.6 0.1 0.4

Typical adult body size
(mm)............... 0.2 0.6 0.3 3.0 0.5 5.0
Largest species (mm) . . . 1.5 5.0 14.0
Food size range (,um) ... 1 -- 20 1 -- 50 5 -- 100
Mode of feeding........ Suspension feeding Filter feedingvia Filter and/or
via coronal cilia thoracic appendages raptorial
Filteringrate .......... Very low High Low
Susceptibilityto
vertebratepredators. . Very low High Low
Susceptibilityto
invertebratepredators High Moderate Moderate to high
Abundance pattern..... Vernal peak Vernal peak Variable
Biogeography (large lake
distribution)......... Surface and inshore Surface and inshore Deep, open water
Biogeography (global) .. Freshwater and Freshwater and Freshwater,
estuarine estuarine estuarine,and
marine

which the last is the adult. Only five naupliar stages occur in Pseudodiaptomuus
coronatus(Jacobs 1961). Typically, however, the number of stages is constant,
unlike cladocerans, with a more variable number of instars. Mating follows
sexual maturity,and the female may store sperm in a spermathecal sac, thus
minimizingthe need forsubsequent mating. Eggs develop into males or females,
completing the life cycle.
Life history parameter estimates (table 1) are plentiful for copepods, par-
ticularly marine calanoid species, and my statements about copepods refer
primarilyto that subgroup. Values for A are based on Pseudocalanus minutus
(McLaren 1974), Acartia tonsa (Heinle 1969), Eurytemoraaffinis(Heinle 1969;
Katona 1970), P. coronatus (Jacobs 1961), and Calanus helgolandicus (Paffen-
hofer1970). The large C. helgolandicuswas comparable to other,smaller species.
Longevity data were selected fromthe above studies and appear reasonable for
growing,reproducingpopulations. Longevities of a year or more occur in nature,
but typically not with continuous reproduction. Fecundity data show wide
variation, in part because egg output correlates with body size, and copepods
exhibit a wide range of body sizes. From 10 to 20 broods are commonlyobserved
(P. minutus [McLaren 1974]; P. coronatus [Jacobs 1961]; Calanus plumchrus
[Fulton 1973]). Various estimates of interbrood duration (Burgis 1970; Heinle
1969; Jacobs 1961; McLaren 1974), divided into adult life span, are supportive.
Total fecundity observations include 60 eggs for P. coronatus (Jacobs 1961),
up to 586 eggs but more typically 200-300 eggs for individual Calanus fin-
marchicus (Marshall and Orr 1952), an average of 535 and a maximum of 835
for C. plumchrus (Fulton 1973), and up to 2,000 eggs per female for C. helgo-

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 ZOOPLANKTON LIFE HISTORIES 171

1.5
.15

IA
1.25 .10 ROTIFERA

/ P. minutus
1,0 .05

2 6 10 14
.75

rmax
('/days)
O .50 CAOR

COPEODA

.25

I
10 20 25
(TC)
TBPERATURE

FIG. 2.-Maximal intrinsic rates of increase (r,,JaX) for major zooplankton taxa.
Insert -r max for Pseudocalanus minutus assuming that the number of broods
per lifetimeis constant (A) or increases with temperature(B).

landicus (Paffenhdfer1970). I assume 20 broods of 25 eggs each, or 500 eggs, is

reasonable for a small (- 1 mm) female, and 20 broods of 50 eggs each, or
1,000 eggs, is reasonable for a large (- 3 mm) female. With a 1: 1 sex ratio at
hatching, only half will be female offspring.The larger estimate of 750 female
eggs per female at 25? C was included to give an upper limit to copepod rn.ax.
Estimates of T are, as usual, hard to acquire. Heinle's (1969) data suggest about
10 days afterA at 25? C (E. affinis).Marshall and Orr (1952) suggest that max-
imum egg laying occurred within the first7 days after maturityat 15? C, often
by day 3, but theirdata indicate egg production to be ratheruniformover time.
However, decreasing survivorship must force a peak in the lm. graph, and I
assume it is 10 days after A at all temperatures.

RESULTS OF T'rax CALCULATIONS

Estimates of rmaxbased on equation (2) utilized a combination of life history

parameters fromtable 1 which would provide the highest and lowest estimates
of rmaxat each temperature (fig. 2). In this manner a band of values was ob-
tained which represents variation owing to species characteristicsand culture

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172 THE AMERICAN NATURALIST

conditions. Although not a confidence band in a statistical sense, this method

generates the maximum range of values associated with the range of life history
parameters available in the literature. Clearly, the resulting curves differin
magnitude and degree of curvature.
Over all temperatures,the ranking of maximal rates of natural increase is:
Rotifera > Cladocera > Copepoda. Although rotifersand cladocerans exhibit
identical life history patterns, the rapid development of rotifersmore than
compensates for their miniscule broods. The three curves in figure2 show no
overlap, a degree of distinctness which I feel is realistic for the species in ques-
tion but not necessarily for all species. Quite possibly the species utilized for
laboratory culturingdo not representthe extremes of their taxonomic groups.
At least one cladoceran, the tiny (- 0.35 mm) Bosmina longirostrismay be
capable of rotifer-likevalues of r (Kerfoot 1975), and the cladoceran Cerio-
daphnia quadrangula also may achieve per capita growthrates in excess of those
suggested by figure2 (Heinle 1966).
In terms of curve shape, rotifersshow the greatest response of rmaxto in-
creasing temperature. Organisms which depend on short development times
rather than large brood size to achieve high rates of increase may in general
show a greatersensitivityto temperaturechanges. This stems fromthe observa-
tion that development times are highlytemperaturedependent, and the ranking
of rmaxshows a clear relationship to the ranking of 1/A. Cladocerans and cope-
pods rely more on large S than on small A to achieve rapid rates of increase;
hence their curves with temperature are flatter. Whether the slightly more
linear response of cladocerans compared with copepods represents a real
differenceawaits furtherdata.
Another point affectingthe shape of these curves, particularly with clado-
cerans and copepods, is the relationship among temperature, body size, and
brood size. Lower temperatures, in addition to postponing firstreproduction,
result in larger body sizes (Deevey 1960; McLaren 1963). In turn, larger indi-
viduals have larger clutches. These larger clutches, typically associated with
lower temperatures, are laid and hatched at lower rates, while longevity is
simultaneously increased. It is difficultto ascertain whether the number of
broods is then rather constant owing to these opposing effects,as MacLaren
(1974) indicates, or whethermore broods are laid at highertemperatures.If the
number of broods remains constant, S will decrease with increasingtemperature
because individual body size and brood size decrease. If the number of broods
increases with temperature,S will remain fairlyconstant or increase. McLaren's
(1974) data on Pseudocalanus minutes are uniquely detailed for examining this
question, and figure2 shows how rmax increases less steeply with temperatureon
the assumption that S decreases (insert, curve A), compared with the assump-
tion that S remains constant (insert, curve B). Hall's (1964) study of Daphnia
galeata mendotaesuggests larger broods at higher temperatures; on the other
hand, great longevity at very low temperaturesmakes it questionable whether
laboratory techniques were able to maintain individuals sufficientlylong to
observe maximum S.
How do estimates of rmax fromfigure2 conformto fielddata? Another unique

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 ZOOPLANKTON LIFE HISTORIES 173

advantage of these taxa is their visible, brooding eggs which affordaquatic

investigatorsthe opportunity to estimate instantaneous birth rates in natural
populations. The egg ratio method of Edmondson (1960) utilizes egg/total
female population x egg development time-1 to estimate female births/
female/day. This estimate, or a minor modification (see Allan 1973; Caswell
1973; Edmondson 1973 fordiscussion), is the instantaneous birthrate, b, which,
if we ignore all mortalityof a nonphysiological nature (i.e., predation, etc.), is
is the maximum rate of increase under those field conditions. Rotifers show
values of b (r rmax)in excess of 0.6/day, often0.4 or higher (Edmondson 1965)
and as high as 1.2 (Walker 1973); and in laboratory populations, growth may
attain values as high as 0.8 (Brachionus plicatilis at 24? C [Theilacker and
McMaster 1971) to 1.4 (Euchianis dilatata at 22? C [King 1965]). Cladocerans
attain values of b as high as 0.6 (Hall 1964), but more commonly, maxima are
around 0.3 (Allan 1973; Hall 1964; Wright 1965). Copepods have been in-
frequentlystudied, but three species of Diaptomus attained values of b of about
0.25-0.4 (Edmondson et al. 1962).

COMPETITION AND PREDATOR ESCAPE ABILITY

Differencesin reproductivecapacity are obviously only part of the lifehistory

strategy. We must also include feeding biology as it relates to competitive
relationships, and predator escape ability. As relatively little is known about
competitionamong membersof the three major taxa under consideration,what
follows will emphasize the functional morphologyof feeding, the size range of
food particles, and feeding rates. Predator escape ability will be considered
from the standpoint of body size, swimming agility, and observations on
predator selectivity.

Feeding and Competition

The majority of planktonic rotifersare suspension feeders collectingparticles

as a result of the action of the coronal cilia, or they are raptorial (Hutchinson
1967). Edmondson (1965) showed by correlative analyses that several non-
raptorial species specialized on fine particles < 10-12 pm in diameter. Most
planktonic cladocerans are filtrationfeederson finesuspended material,utilizing
their four to six thoracic appendages to create a feeding current (Jorgensen
1966). Functional mouth parts are reduced to only the mandibles, to which the
thoracic filtrationappendages deliver a bolus of food. Almost certainly,rotifers
and cladocerans overlap broadly in food intake. However, the upper limit to
particle size appears to be about 20 jim forrotifers(Edmondson 1965; Jorgensen
1966; Gliwicz 1969), as compared with 50 ,m forcladocerans (Burns 1968).
Copepods must be treated in two very differentcategories: the Calanoida,
which are primarily filterfeeders on smaller particles and raptorial on larger
particles, and the Cyclopoida, which are solely raptorial. Copepods typically
feed on coarser particles. If the smallest gap between setae may be taken as the
lower limit to particles collected, then calanoid copepods probably concentrate

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174 THE AMERICAN NATURALIST

on particles > 5-10 jym(Jorgensen 1966). The upper limit forfiltrationis prob-
ably 50 um,with raptorial feeding taking over for larger particles (Parsons and
Takahashi 1973). Copepods are flexible in their feeding behavior and capable
of "tracking" biomass peaks in the size distribution of food (Wilson 1973;
Poulet 1974), and cladocerans appear to show this ability as well (Berman and
Richman 1974). Cyclopoids apparently sense and grasp particles (Fryer 1957).
Like the calanoids, their feeding is more specialized and may involve larger
particles. In short, rotifers and cladocerans are similar in feeding on small
particles; copepods may show a greater degree of specialization in their feeding,
a preferencefor larger particles, and quite possibly a greater ability to sense
prey (Stricklerand Bal 1973).
Filteringrate estimates indicate that cladocerans are capable of filteringrates
up to an order of magnitude higherthan copepods of similar size (Haney 1973),
while observed rotiferfilteringrates are as much as one to two orders of mag-
nitude lower than copepods (King 1965; Edmondson and Winberg 1971).
In a nutritionallyrich medium, competition would of course be minimal. As
populations become abundant followinga vernal peak of primaryproductivity,
or in a perennially nutritionallydilute environment,food shortages may occur
for all three taxa. We might expect the higher filteringrates and greater food
range of cladocerans relative to rotifersto convey some advantage. Hurlbert
et al. (1972) provide evidence that the cladoceran community of a small pond
may limit rotiferpopulations considerably. As food becomes scarcer, the ability
of copepods to capture a wider range of particles, especially large items, should
convey an advantage relative to both rotifersand cladocerans.

Predator Escape
The ability to avoid predators seems to be most critically affected by size
(Brooks and Dodson 1965), mobility, and visibility (Zaret 1972). Rotifers,
cladocerans, and copepods may or may not vary systematically in visibility,
but do in size and mobility. Rotifers are distinctly smaller (0.1-0.6 mm) than
cladocerans and copepods which are roughly similar in size in freshwaters
(0.4-4.0 mm). In marine systems, cladocerans are few and small and copepods
are plentifuland may be much larger. Rotifershave a decided advantage in the
presence of vertebrate predators and typically increase in abundance with fish
stock, while larger cladocerans and copepods are eliminated (Hrba'cek et al.
1961; Brooks and Dodson 1965). Invertebrate predation is most likely the
reverse,selecting smaller species (Anderson 1971; Allan 1973; Dodson 1974).
Cladocerans and copepods may oftenbe similar in size but differstrikinglyin
mobility. While cladocerans swim in a hopping fashion (hence the name "water
flea") with their second antennae, copepods propel themselves with their first
antennae, by paddle-like thrusts of their thoracic limbs and by flickingtheir
abdomen in a rapid movement. Some idea of their movement can be gained by
attempting to catch one with an eyedropper. Swimming speeds for adult
Daphnia have been estimated at 0.74 cm/sec (Jacobs 1967). A variety of esti-
mates for adult copepods show much higher values, for example, 20 cm/sec

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 ZOOPLANKTON LIFE HISTORIES 175

swimmingspeed and 30 cm/secforan abdominal flick(Cyclopsscutifer[Strickler

and Bal 1973]). Hence, at least over short distances, copepods can achieve
a velocity 10-50 times as great as that of cladocerans and accomplish
rapid changes in direction. Predator avoidance ability should be enhanced
substantially.
Prey selection experiments utilizing young bluegills (Lepomis macrochirus)
revealed that reaction distances were longer and strike success higher with
cladocerans as prey as compared with copepods (Confer and Blades 1974).
Stomach analysis of bluegills in a Wisconsin lake revealed that over 900% of the
zooplankton prey were cladocerans (Baumann and Kitchell 1974). The effectof
an invasion by alewives into some Connecticut lakes was to favor smaller zoo-
plankters, but the copepods able to coexist with alewives were considerably
larger than the cladocerans (Brooks and Dodson 1965). Presumably, greater
mobility compensated for greater body size. These data support the contention
that planktivorous fish select cladocerans over copepods; however, species-
specificvariation in visibilityand body morphology(Zaret 1972) may complicate
the picture.
Invertebrate predators appear to be the reverse of vertebrate predators in
freshwatersystems,selecting small prey over large. Anderson (1971) concluded
that predaceous copepods preferredrotifersand immature copepods to clado-
cerans. Another major invertebrate predator on plankton, the midge larva
Chaoborus,has been found to prefersmall copepods to similar-sizecladocerans,
rejecting the latter after capture (Swiiste et al. 1973). In some cases, however,
cladocerans appeared to be the preferredprey (Allan 1973; Dodson 1974).
Since small copepods may include immatures, especially those at naupliar
stages, their swimmingrates relative to cladocerans can only be compared with
furtherdirect measurements.

DISCUSSION

Brooks and Dodson (1965) proposed that body size was a principal determi-
nant of a zooplankter's susceptibility to predation and success in gathering
food. Much aquatic researchin the subsequent decade has verifiedand expanded
their basic hypothesis. Although considerable insight into the workings of
plankton communities can be gained from examination of a single critical
variable size, differencesamong the principal taxa add an additional com-
plication to life historypatterns.
Consideration of the combined informationon zooplankton life historydata
suggests the following patterns (table 2): Rotifers are highly opportunistic,
have a reproductive advantage at all temperatures, probably share common
food resources with cladocerans and smaller copepods, and are vulnerable
primarilyto invertebratepredation owing to their small body size. Cladocerans
are also opportunistic,although unable to equal the biotic potential of rotifers,
probably share common food resources with rotifersand small copepods, and
are vulnerable primarilyto vertebratepredation. Smaller cladocerans encounter
invertebratepredation in some circumstances.Copepods, with theirlower poten-

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176 THE AMERICAN NATURALIST

tial forexponential increase, are probably capable of more selective feeding for
larger particles and may possess the greatest predator escape ability. We may
now ask what consequences these life history patterns bear for distributions
and seasonal abundances.
Biogeography
While freshwaterzooplankton communities are notable in their substantial
representation of cladocerans, rotifers, and copepods and nearly complete
absence of planktonic larvae, marine zooplankton communities are dominated
by copepods, planktonic larvae are common, and rotifersand cladocerans are
virtually absent. The few marine cladocerans exist only secondarily, and when
present appear to be rare and seasonal, as with Evadne spiniferain Sargasso Sea
collections (Deevey 1971). Rotifers and cladocerans may show a substantial
presence in coastal waters and estuaries, but, as with freshwatersystems, the
formersystemsare stronglypulsed seasonally in temperate latitudes. Copepods,
in contrast,are even more abundantly representedin marine systems.
If we ask what has kept cladocerans fromgreater success in invading marine
habitats, or why copepods do not dominate the freshwaterplankton as com-
pletely as they dominate the oceanic plankton, the answer seems to lie in the
abundance and seasonality of the food supply. Ryther's (1969) estimates of total
carbon production per square meter of surface area show that the open ocean is
lower in productivitythan are coastal zones, which are in turn much lower than
estuaries. Temperate waters, marine and freshwater,are furtherinfluencedby
the highly predictable vernal peak of productivity.
Environments which are stronglypulsed seasonally, such as temperate lakes,
are essentiallyempty islands fora period of time equivalent to numerous genera-
tions for some zooplankters. Adaptation to regular colonizing events through
high r would be advantageous. The open ocean is nutritionallydilute (Conover
1968), too deep forthorough nutrientmixing, and bufferedby size and salinity
against extreme climatic influences; hence, an opportunisticstrategy would be
less adaptive. On these arguments,rotifersand cladocerans should be associated
with freshwatersand estuaries and copepods with oceans. Furthermore, this
interpretation is consistent with the observation that in the Great Lakes
cladocerans make up a greater fractionof the plankton in surface and shoreline
waters while copepods predominate in deep and open waters (Watson 1974).
As tropical lakes become better known, a similar trend toward copepod domin-
ance may emerge.
The comparative absence from marine systems of rotifersand cladocerans
might also be explained by salinity and evolutionary arguments. Salinity can
not be the only barrier,however, as a few members of these taxa have success-
fully made the transition. Interestingly,the fraction of sexual individuals in
parthenogeneticgroups seems to increase among cladocerans in marine systems
(Bainbridge 1958; Bosch and Taylor 1973), as does the frequencyof sexuality in
rotifers(Hutchinson 1967). Marine systems may impose more intense and un-
predictable selection pressures,thus necessitating the recombination advantage
of sexual reproduction (Williams 1975).

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 ZOOPLANKTON LIFE HISTORIES 177

Seasonality
One would expect rotifersand cladoceransto undergogreaterpopulation
increases than copepods and to begin the increase sooner. Although not always
the case, this is well illustrated by Davis's (1962) study of Lake Erie zooplank-
ton. Exceptions may be attributed to the fact that, during the major part of an
annual cycle when food is not superabundant, rotifersand cladocerans take
advantage of resting stages while copepods continue development. Over-
winteringadults may produce eggs which hatch into nauplii in readiness for a
vernal phytoplanktonbloom. This capacity to overwinterand continue develop-
ment for as long as 7 months on stored food (Fulton 1973; Heinrich 1962),
coupled with the predictability of seasonal blooms in some environments,
prevents taxa with higher r from achieving as great a head start. The cohort
structureof copepod populations at the onset of a bloom allows a more rapid
rate of increase than would be achieved under stable age conditions.

SUMMARY

Freshwater zooplankton exhibit a continuum of compromisesin their means

of meetingthe presumably conflictingdemands of maximizing the potential for
rapid increase, predator avoidance, and competitive ability. Rotifersand clado-
cerans both alternate parthenogeneticand sexual reproduction and attain high
rates of increase relative to copepods. The rapidly developing small-clutch
rotifers surpass more slowly developing large-clutch cladocerans in rrax.
Copepods appear to consume food in a wider range of particle sizes, exhibit a
greater capacity for selective feeding, and possess a greater ability in predator
avoidance. Hence, ranking of three major taxa of freshwaterzooplankton with
respect to opportunism is: rotifers > cladocerans > copepods. These results
are utilized to interpretsome principal biogeographic trends in plankton com-
position, including the rarity or nearly complete absence of rotifersand clado-
cerans fromthe open oceans and deeper waters of large lakes. Patterns in the
timingand sharpness of seasonal abundance peaks are also consistent with this
interpretation, although complexities in timing occur owing to intrataxon
variation in keying to seasonal fluctuations.

ACKNOWLEDGMENTS

I thank R. Strathmann, D. Gill, D. Heinle, T. Kinsey, I. McLaren, S. Smith-

Gill, T. Zaret, T. Bowman, and a reviewer for helpful advice.

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