Complex Interactions between Natural Coexploiters--Daphnia and Ceriodaphnia

Michael Lynch

Ecology, Vol. 59, No. 3. (Late Spring, 1978), pp. 552-564.

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E < o b ~ ?' .h 7 ) 1978. pp. 552-564
i 1978 b) the E c o l o g ~ c aSoc~etb
l of A r n e r ~ c a

COMPLEX INTERACTIONS BETWEEN NATURAL

COEXPLOITERS-DAPHNIA AND CERIODAPHNIA1,'

MICHAELL Y N C H
Department o f Ecology. Ethology, and Evolution, University of Illinois,

Urhunu, 1llinoi.s 61801 U S A

Abstract. This study concerns a seasonal succession of a large herbivore, Daphnia pule.^, by a
smaller one. Crrioduphniu reticulata, in a Minnesota pond. Based on a description of events in the
pond and results of several field experiments, one can explain this replacement in terms of a coex-
ploitative interaction between these 2 species. The field experiments. in which pairs of cladocerans
were isolated for 4 wk, gave several results which are inconsistent with the assumptions of contem-
porary competition theory. In the 1st experiment. Daphnia survived when solitary but went extinct
when paired with Cerioduphnia, regardless of starting densities or age structure. At the same. Daphnia
was declining in the pond while Ceriotluphniu was increasing. Four wk later, Duphniu coexisted in
pairs with both Cerioduphnia and B o ~ m i n ulongiro.stris, and at much greater densities than in its
controls. Not only did the competitive abilities of these species shift over this very short time period.
but the densities which they attained in control enclosures dramatically declined. Thus, static mea-
sures of competition (such as alphas) and carrying capacities are inappropriate for these species.
Furthermore. these interactions can be understood only in the context of a framework which considers
age structure. Generally, juveniles were more sensitive to coexploitative interactions while adults
were unaffected and sometimes even benefited. Since their resources interact, coexploitative inter-
actions between these species are not simply a result of resource depression but of resource alteration.
Despite the fact that they overlap extensively in resource utilization, an appropriate modification of
the resource base by I species can lead to enhanced conditions for a 2nd. I suggest that such facili-
tation may be an important process in these communities which merits further investigation.
Key words: age-specijic inteructions; Ceriodaphnia; coexploituti~~e interactions; community le\'c.l
evolrrtion; community ~trrrctrrre;competition; Crrr~tuceu;Daphnia;facilitation; intercrcting resources;
.Minnesota; :ooplunkton.

Pianka 1975). The attractiveness of these formulations

Population dynamics, distributional patterns, and stems from their simplicity, and they have been ma-
the evolution of community characteristics are fre- nipulated to produce a variety of relationships which

quently attributed to competition (Cody and Diamond predict such things as the limiting similarity of species,

1975). However, hardly any of the myriad of studies invasibility of habitats, and evolutionary convergence

which have invoked competition have examined the and divergence.

mechanism, i.e. the relation between resources and I emphasize 3 shortcomings of contemporary com-

the coexploiters' population processes (behavior and
demography). In the absence of sufficient information
on the biology of this interaction, contemporary com-
petition theory relies heavily on a simple set of math-
ematical constructs believed to mimic the outcome of
competition.
Almost all of these formulations follow the Mac-
Arthur-Levins extrapolations (MacArthur 1970, 1972,
MacArthur and Levins 1964, 1967) of Volterra's (1928)
equations (but see Grenney et al. 1973, Smith et al.
1975, Titman 1977). Overlap in resource utilization is
usually equated with competition, and several esti-
mates of "competition coefficients" based on utiliza-
tion functions have been proposed (Levins 1968,
MacArthur 1972, Schoener 1974, May 1975) and ap-
plied to natural communities (Culver 1974, Lane 1975,
' Manuscript received 1 l August 1977; accepted 6 March
1978.
' Contribution No. 170 from the Limnological Research
Center, University of Minnesota.
petition theory. ( 1 ) Conclusions drawn from this the-
ory are strictly dependent on the linearity assumptions
of the Lotka-Volterra equations. In the past, most in-
vestigators have set aside this caveat, stating that the
equations should be suitable for communities close to
equilibrium. However, as Armstrong and McGehee
(1976) pointed out, it may be entirely inappropriate to
analyze communities in terms of point equilibria. (2)
Models of interacting populations have traditionally
ignored age structure. Neil1 (19754) demonstrated with
laboratory populations of cladocerans that different
age classes are not equally sensitive to resource alter-
ation, and that the outcome of competition between
2 species may be based on a few critical age classes.
(3) The theory is probably least appropriate for spe-
cies whose resources interact. Most studies assume a
constant resource base or simply address the problem
of resource depression (MacArthur 1972). However,
since coexploitative interactions also often lead to a
qualitative shift in resources, it is necessary to under-
stand the implications of resource alteration as well as
Late Spring 1978 CLADOCERAN INTERACTIONS
resource depression. As I will demonstrate below, this
is a particularly serious problem because coexploita-
tion of interacting resources may actually lead to im-
proved conditions for some exploiters.
The relevance of each of these problems became
apparent in a study I did on the interactions between
3 species of filter-feeding cladocerans, L)(rphnicr prrle.u,
Ceriodophnia retic,ulata and Bostninrr longirosrris, in
a small Minnesota pond. Since the importance of com-
petition in structuring natural zooplankton communi-
ties has recently been questioned (Dodson et al. 1976).
the results I present are also of special significance in
their implications for plankton community theory.
Pleasant Pond lies in a small basin (50.25 ha, max-
imum depth = 2 m) located =16.1 km north of St.
Paul, Minnesota. It has no inlet o r outlet. The pond
was divided in half with polyethylene sheeting in 1976
as part of a large-scale fish manipulation experiment
(Lynch 1978). The studies I consider here are confined
to the northern (control) half of the pond where ver-
tebrate planktivores were rare.
Zooplankton was sampled weekly by taking dupli-
cate vertical hauls through the whole water column
using a Wisconsin net with a 15-cm diameter opening
and 64 p m netting. Samples were anesthetized with
carbonated water before fixing to prevent evacuation
of the guts, and then preserved with formalin and su-
crose (Haney and Hall 1973) to prevent loss of eggs.
At least 2 I-ml subsamples were counted in their en-
tirety under lOOx magnification to determine zooplank-
ton abundance. Size-frequency distributions were ob-
tained for the cladoceran populations by measuring
50 random individuals from the anterior margin of the
head to the base of the tail spine. Measurements
were made to the nearest .01 mm using an ocular
micrometer. Mean clutch sizes were determined for
size classes in which at least 3 separate measurements
were made.
Phytoplankton was sampled weekly at 0.3 m depth
and preserved with Lugol's solution.
The Daphnia-Ceriodaphnia succession
The seasonal fluctuations of the zooplankton species
in Pleasant Pond North are illustrated in Fig. 1. The
most dramatic event in 1976 was the replacement of
Drlphnia pules by the smaller Ceriodrrphni~lrericulrrtcr
at the end of July. The rarity of Ceriodcrphni~lin early
summer was most likely a result of Chaohorus (midge
larvae) predation (Lynch 1978). However, predators
were not responsible for D ~ p h n i a ' smidsummer de-
cline.
An enclosure experiment which I initiated on 3 Au-
gust substantiates this. Several I-m diameter poly-
553
ethylene bags suspended in the pond were closed at
the bottom and excluded all potential predators (the
salamander, Necturrrs, some walleye (Stizostedion \.it-
reutn) fry. and many arthropods). These enclosures
were filled with surface water so that zooplankton den-
sities were approximately equal to those in the pond.
In both the control enclosure and in 2 enclosures con-
taining an adult Necrrtrrr.7 (gut analyses indicated that
they did not consume zooplankton), Ceriodrrphnicl re-
mained numerically dominant over Dophnia through-
out the 4-wk experiment. The average densities in all
3 enclosures across all sampling dates were 2.0 Daph-
nirrilitre and 11.8 Ceriod~lphnicrilitre.Dnphnin re-
mained below a density of 3 individualsilitre except on
one occasion in 1 enclosure; this corresponds closely
to the density of Dophnicr in the pond at that time.
Since all other zooplankton species in the pond were
rare during this period (Fig. I), it is unlikely that they
were involved in the replacement of Daphnicr by
Ceriodrrphnia. This leaves the possibility that a direct
interaction between these 2 species was responsible
for their succession. However, before invoking ex-
ploitative competition as an explanation for this re-
placement, it is necessary to demonstrate ( 1 ) the ef-
fects which these species have on their resource base,
and (2) the significance of such resource alteration to
the coexploiting populations.
Alteration oj'thr resortrce h ~ l s e
In Pleasant Pond North, grazing by both D~lphnirr
and Ceriod~lphnirrhas a significant impact on the abun-
dance of phytoplankton. As shown in Fig. 2. several
algal species declined to below detectable levels in
mid-June when D~phnicr became abundant; they did
not reappear until August after D ~ p h n i ~declined.
l
Several other species, which were never noted early
in the summer, appeared immediatelv fnllowing the
decline of D ~ p h n i ~ ~ .
Associated with the dominance of D ~ p h n i ain early
summer was an intense bloom of the filamentous blue-
green Aphanizornenon jos-aqurre. In Pleasant Pond
(and other Minnesota ponds which have large h ~ p h -
nirr) this species forms large colonies (up to 2 x 15
mm) which cannot be ingested. I have evidence which
suggests that Dophnicr actually maintain these bloom5
by removing all potential algal competitors (Lynch,
person~lloh5 er\,crrion).
Division of the phytoplankton into size classes re-
veals a general pattern which is related to the relative
abundance of D ~ l p h n i ~and
l Ceriodaphnirr (Fig. 3).
Bacteria and 4-63 p m 3 particles (primarily small fla-
gellates) declined to very low densities just before the
D ~ l p h n i ~population
l peaked, and remained low after
Ceriodrlphnirr became dominant. No significant trend
is apparent with the next largest size class (consisting
of a variety of flagellates, diatoms, green and blue-
green algae). The largest size class (1,024-16,383 p m j
particles) consists of desmids, trachelomonads and
Late Spring 1978 CLADOCERAN INTERACTIONS 555

1 APP 1 MAY 1 JUN I JUL I AUG I SEP I I

I
80
L 1
........_-.-.-..-... CIYpfomonoJ obovofo
I
40
C L---.,.. ..........v Tloche/omono$ SP I Dapbnia Ceriodaphnia
L. ..-... .......... .
.. lo
. & Scenedesmus denflculofur Predominafe Predominafe
06[& a --A Gomphonemo 5 0

............. lo Schroderio sefiqero

Rhodomonos minum

O '[.-
A_ _ _ _ _ -&
-- - ]'0 dphonizamenon flos-oquoe

~ ~ c i ~ ~ o ti eonrui io~

lo T~ochelarnonorvo~ionr
'[,-"-
-- -
A.&-_--]~~
--
Chroococcus d i r p e ~ s u s

N,bsch,o Sp

.
F
02

-~----------
[--
--..-----.-._-- &
chiorn~dornonors p
a G i o e o c y ~ t ivesicoioso

l0

?\ 02
6 C......... ........& Heferochromoflos qioboso

Qq ~osrnoriurnsexnototurn
? I C.

=t
.......--.-&-. .
...
.

'0
0
'
2-

___--I2 ~ i o t h r i xosciiiormo
04

c ...... .-..-..---.. A Characlurn ombigoorn

I

:Lfi
__-_-A
--_- ]04 Ochrornonor voiiesioco I
I
08
C. ....................... A sphoerocyslis schroeteri
1 1024 - 16,383 pm3
_M,
, *----
dcm
I6 socterlo
I Particles
1 I 1

APR MAY JUN JUL AUG SEP

I I
FIG.'2 . Major phytoplankton species in Pleasant Pond
North. 1976.
0

JUN JUL AUG

obtain a full complement of the large herbivores when FIG.3. Abundance of 4 size classes of bacteria and phy-
toplankton capable of being ingested by Drrphnirr and Cf,rio-
filling the control chambers; these were generally most daphnia. Vertical dashed line denotes date of maximum den-
abundant at a depth of .= 1 m. Two differences between sity of Duphniu after which it sharply declined and was
treatments were consistent in all experiments. Chroo- replaced by Ceriodaphnia.
coccus mitlut~ts( a small coccoid blue-green) was al-
ways most abundant in chambers with zooplankton,
supporting Porter's (1976) contention that such gelat- I analyzed gut contents by squashing individuals
inous forms may accrue a competitive advantage by gently under a cover slip and examining the extruded
absorbing nutrients as they viably pass through her- bolus. Gut contents consisted largely of a homoge-
bivore guts. Bacteria were consistently lowest in neous brown material of unknown origin (bacteria,
chambers with zooplankton. detritus. o r partially digested algae). Those phyto-
The density of zooplankton in the pond was very plankton cells which were intact were identified and
low during experiment 2 (29 June-3 July), and few enumerated. and notes were made regarding remnants
additional differences were noted between treatments. of broken and partially digested cells. Although bac-
However, during experiment 3 (18 July-22 July), the teria and detritus were likely to have been important
Dapht1ia population was at its peak and most phyto- components of the diet, they could not be quantified.
plankton species increased upon removal of zooplank- The proportions of intact algal types in the foreguts of
ton. Most significant was the dramatic increase of a juveniles and adults of both species are presented in
tiny species of Srlrr~u.~trirm w hich occurred upon re- Table 1. All of these algae, except Truchelornot1rt.r and
moval of zooplankton; this species was only rarely the gelatinous forms. were frequently found partially
noted in the pond. Daphtlia were scarce during ex- digested. suggesting that they are important compo-
periment 4 (19 August-26 August), while Ceriodaph- nents of the food supply.
niii were at their maximum density. With the excep- All sized individuals of both species were capable
tion of the gelatinous forms, all species increased in of ingesting the whole spectrum of algae found in the
the absence of herbivores. guts; only the largest Cosrnari~trn species were not
Examination of the food ingested by Dapht1iu and found in the guts of immature Ceriodaphnia. In July,
Ceriodaphrlia verified that they share the same re- adult Ceriodaphr~iuand adult and juvenile Drtphnirt
source base, i.e., that they are potential competitors. had very similar diets, while immature Ceriodapht1ia
 MICHAEL LYNCH Ecology. Vol. 59. No. 3

EXPERIMENT 2 (JUN 2 9 - JUL 3 , 1976) Thus, Driphniri and Ceriodriphnici share the same
' O O C N -----
02
---a-.-
Llphonizomenon flos-aquae resource base, and both are able to limit the abun-
L Q-.@ Characium omb~guum dance of these resources in Pleasant Pond. Both spe-
08
C- ---------- m%, Chroococcus minutus cies are capable of depressing the small food particles
08
C ----.
, m--a
-----. Heterochromonas globosa to very low levels. However. Cerioduphtliu cannot re-
02
02
C B! Monochrysis Sp duce the abundance of large phytoplankton to the ex-
I--- R-.m
--rr;s--..--- Ochromonas valles~aca tent that Daphtliu can.
4
,E. 6X.N Oscillatoria tenuis
-6
C.n..im..~-~ Rhodomonas minuto The mec,huni.t rn of' competition
02
C-N.-m-.rn--m!- Schroderia setigera The reduction in small food particles throughout the
08
CH . ..---. ,-: Trachelomonas varians summer was reflected in the amount of food observed
08
b..,- -
H.;-P.- Bacter~a in the guts of both species. On 8 July. the guts of all
individuals were visibly full. When the Driphnici pop-
EXPERIMENT 3 ( J U L 1 8 - 2 2 , 1976) ulation peaked on 22 July, the guts of adult Duphnici
8
F,. m.-rr;s Aohan~zomenonflos -aouae
were all full, whereas those of immatures averaged
I
02
C--- R-- Chroococcus minuta <ZW full; the guts of all Ceriodapht~iuwere < 2 5 9
L------- ------- Cryptomonas obovata full, and many were empty. On 13 August, after Cerio-
01
--------- 6Q-.m..m Gomphonemo Sp daphtliri had become abundant, guts of immature
04
C----. , Heterochromonas olobosa Daphtliri averaged 20% full, those of adult Duphtliu
I
-----my5 Nilzschio Sp 60%. and those of Cerioduphnici 15%. The Crriodaph-
08
02
[-- m-.m Oscillatoria tenuis niu population had become very dense on 20 August.
L - ~ - - -.----.
I z ~ m . . ~Rhodomonas minufa and the guts of all individuals of both species were
04
-,- 6i-B - Sch ,r o d e- r ~ as e t- near1
~ g e r a-- - y empty.
-
08
C Selenastrum ~p While the quantity of food ingested declined for both
I
C m!.--?rn Bacter~a species throughout the summer, Ceriodriphtlia were
apparently less sensitive to these low food levels as
EXPERIMENT 4 (AUG 19-26, 1976) evidenced by their high rate of population growth
2
[ ax,
- - .. Chroococcus mlnutus throughout this period (Fig. 1). High clutch sizes were
maintained in mid-July when Driphtliu were most
abundant and only began to decline in August after
2
C .--.-.._- -.:-- .YH Cosmar~umsexnotatum Ceriodriphtlia had reached high densities (Fig. 5).
rr;s H-H Gloeocystls vesiculosa Although Duphtlici appear to have had little effect
08
------.--.,-. m..m Heterochromonos alobosa on Crriodaphtliu, significant changes occurred in the
04 Daphtliri population when Ceriodciphtliri were abun-
L-----,-.--: - ---Y N ~ o c y s t i sI U C U S ~ ~ I S
04
4

----.. rn-.m-.H
..--
Scenedesmus denticulatus dant. Both the size at 1st reproduction and the maxi-
---m-.m Sphoerocystis schroeter~ mum adult size of Dapht~ia declined throughout the
2
- - - - a . Stourastrum p a r a d o ~ u m
summer (Fig. 5). This is characteristic of all food-lim-
ited populations of cladocerans that have been studied
(Ingle et al. 1937, Richman 1958, Hall 1964, Weglenska
1971). It also tends to equalize the number of eggs
carried by equal-sized (but different-aged) individuals
exposed to different nutritional conditions. Thus, the
relation of clutch size to body size does not vary great-
FIG. 4. Response of phytoplankton to zooplankton re- ly throughout the summer (Fig. 5).
moval experiments. First 3 columns are counts from pond
samples; last 2 columns are means of duplicate treatments. The most significant effect of food depression is its
Significant differences between columns are denoted by 1 influence on the survival of immature Daphniri. This
( P > . O O or 2 inverted diamonds (P > .01). Experiment conclusion arises from the observation that newborn
2: Daphnirr and Cerioduphniu rare: experiment 3: Daphnin Daphnici were often very rare on days when adults
abundant. Crriodaphniu rare; experiment 4: Dnphnia rare. were carrying many eggs (for instance, on 29 June and
Ceriodnphnin abundant.
13 August). It also follows from an index I constructed
ingested higher proportions of diatoms and delicate as a relative estimate of survival for newborn (0.6-0.8
flagellates. There was some difference in resource uti- mm) Driphnici.
lization between the 2 species in August. Cerioduph- The expected influx of newborns (N,,,) on day x
niu feeding more intensively on diatoms. Duphnici was calculated according to:
more o n delicate flagellates and Cosmariirm sps.
Nonetheless, these types were shared to some extent.
and all other categories were shared considerably.
Late Spring 1978 CLADOCERAN IN TERACrIONS

JUL 8 JUL 15 JUL 30 AUG 13 AUG 2 SEP 6

2 Daphnia pu/ex

Ceriadaphnio reticulafa

Carapace Length (mm)

FIG. 5. Size-frequency distributions for Dophnia pu1e.u and Ceriodcrphr~ierretic~rrlatcr(A' =50) presented as histogram\:
mean clutch sizes (A'3 3. but usually between 10 and 30) given in insets for different size classes. Abscissas of insets start
at 1 .5 mm for Dcrphnicr: 0.53 mm for Ceriodllphniu.

where E,.., = average number of eggs carriedlfemale borns from ephippia (resting eggs). Since food levels
on day x - 1 . declined throughout the summer, it is likely that
? ,_ ,= population size of females on day x - 1 . growth rates also declined. causing the late summer
D,.., = duration of egg development on day ratios to be the most overestimated ones. Nonethe-
x - 1 ( a function of temperature, taken less. these ratios declined dramatically throughout the
from Knutson 1970). summer (Fig. 6).
Two additional points emphasize the vulnerability
Animals also leave this size class as they grow larger. of juvenile Dcipiznirr to competitive interactions with
Since the shortest period of growth to 0.8 mm is 1 day Ceriodciphn~a:
for Dciphnici pulex, then the minimum expected den- 1. The restriction of juvenile Daphrlia to feeding on
sity of 0.6-0.8 mm Daphnirr can be estimated with the same small particles which Crriodaplznirr use
equation 1. Dividing this estimate into the actual num- poses a developmental problem for Dciphnici since the
ber of 0.6-0.8 mm individuals on day x gives a relative smaller species are more efficient at gathering these
estimate of the survival of newborns. Values > 1 occur small particles (Gliwicz 1969. Neill 197%). Neill
both because of the maximum growth rate assumption ( 1 9 7 5 ~ f)ound in laboratory microcosms that survival
and also because of an unaccounted influx of new- and reproduction of adult Daphnici rncignu were un-
TABLE1. Average proportion of intact phytoplankton biomasq in the foreguts of Duphfricr and Ceriodaphniu for major
groups of algae. Immature Daphoicr < 1.4 mm long: immature Ceriodaphnia < .56 mm. Sample size denoted by N

Proportion of total intact phytoplankton biomass in the foregut?

8 and ?? July 13 and ?O August
Daplrnicr Cerioeinr~hnicr Dclllhnicl Ceriodaphnicr
Major Immature Mature immature Mature immature Mature Immature Mature
phytoplankton - -- -- - --
types (A'= 16) (A' = 14) (.V = 6) (A' = 10) (A' = 13) (h' = 13) (A' = 9) (.V = 20)
Cosmarirrni spp. .O5 .40 .25 .I3 .?7
Trcrchclomoncrs spp. .68 .72 .60 .03 .08 .?3 .?I
Diatoms .08 .03 .35 .03 .04 .07 .32 .I4
Gelatinous forms .09 .06 .09 .07 .43 .32 .--
77
.30
Delicate flagellates .O1 .03 .54 .20 .02
Greens. non-gelatinous .O1 .04 .01 .03 .0S
Filamentous blue-greens .I4 .I0 .02 .30
Ulothriu oscillarincr .06 .07 .07 .O1
 MICHAEL L Y N C H
-
JUN JUL AUG
FIG.6. Relative index of survival for newborn Daphnicr.
Low values indicate poor juvenile survivorship; see text for
the method of computation.
affected by the presence of Ceriodaphnia, whereas ju-
venile Daphnia did not survive >4 days.
2. At low food concentrations Ceriodaphnia have
an "encounter rate" for food particles -2x as great
as juvenile Daphnia. O'Brien and deNoyelles (1974)
find that at 25C (a close approximation to summer
temperatures in Pleasant Pond) C . reticulata (length
= 0.8 mm) may filter 0.29 ml per animal per h. Mea-
surements made for Daphnia pulex at the same tem-
perature show that 0.8 mm individuals filter at a max-
imum rate of e 0 . 1 5 mllh, and 0.6 mm individuals at
< 0.10 mllh (Burns 1969).
The data presented in the previous sections provide
strong evidence for a coexploitative interaction be-
tween Daphnia and Ceriodaphnia. I examined the role
and mechanism of this interaction more directly in 2
sets of field experiments.
Methods
Enclosure experiments were done in 3.5-1 plexiglass
cylinders suspended at a depth of 0.5 m in a part of
the pond clear of vascular plants. These chambers
' ~ and bottoms and two 10 x 10 cm
have P l e x i g l a ~ lids
windows of 102-pm Nitex netting near the upper end.
Cladocerans were selected from pond samples and iso-
lated into their appropriate chambers in pond water
which had previously been filtered through 64-pm net-
ting to remove all zooplankton. I generally used initial
Ecology. Vol. 59. No. 3
EXPERIMENT I (JUL 19- AUG 14)
Starting
O
"zr:
400 (mat. D.)
19 ,
; : : ; , /8[
(mat. D.)
Dl
?h
--- . -**o--.= //
10 D . 1 0 C
(10 mat. + 10 irn. D.)
.-*-.
800 I 4 (im. D.)
400k;
/
I,,_:
15 (mat. D)
Days
FIG. 7. Results of the 1st zooplankton competition ex-
periment; solid line-Daphnia, dashed l i n e 4 e r i o d u p h n i a .
Initial numbers of animals per chamber are designated in the
right column. Initial age classes of Daphnia are indicated.
Ceriodaphnia and control Daphnia were not selected ac-
cording to size. Inset numbers designate chamber numbers.
densities of 10 individuals of each species in their re-
spective chambers, although starting densities varied
in experiment 1. All treatments were done in duplicate
or triplicate.
Interactions of Duphniu and Ceriodaphnia with
Bosminu lon~irostriswere also examined in experi-
ment 2. This small (<0.6 mm) cladoceran was obtained
from Loch Loso, a small enriched pond north of Min-
neapolis. Bosmina were relatively abundant in Pleas-
ant Pond in early 1975; their total absence in 1976 was
most likely a result of Chaoborus predation (Lynch
1978).
These experiments lasted =4 wk, samples being tak-
en after 2 wk and on the final sampling date. Only
small subsamples were removed on the 1st sampling
date. After thorough mixing, 3 subsamples were rap-
idly removed from the bottom, middle and surface of
the chamber for a total sample volume of 85 ml, =4%
of the chamber's content. On the final sampling date,
the chamber was mixed well, 60 ml was removed as
a phytoplankton sample, and the remainder was con-
centrated with a 64-pm net and preserved with sucrose
and Formalin. Samples from the 2nd wk were counted
in their entirety; 3 I-ml subsamples of the final samples
Late Spring 1978 CLADOCERAN INTERACTIONS
EXPERIMENT I
AUG 4 AUG 14
0.4
Daphnlb pu/ex
Single
04r
I
Ceriodaphnio reficulata
P, Single
Paired
02r - = 0.024
Carapace Length (mm)
FIG. 8. Size-frequency distributions of Daphnia and
Ceriodaphnia in competition experiment 1 (pooled data from
replicates). Instantaneous birth rates of the populations (cal-
culated according to Paloheimo 1974) are in units of days-';
sample size is denoted by N . (Daphnia was extinct in all
paired chambers on August 14).
were enumerated. Comparison of the 2 sampling meth-
ods in 4 chambers gave estimated densities which were
not significantly different.
The Nitex windows were installed to allow some
passage of food and to prevent stagnation of the cham-
bers. However, the mesh size used was apparently not
fine encough to prevent the entrance of rotifers o r of
the small copepod, Cyclops \,ernalis, and its nauplii.
Although their densities were much lower in the pond,
Cyclops (mostly nauplii and early copepodids) ranged
between 200 and 50011itre and rotifers between 1,000
and 3,00011itre in the chambers. There were no signif-
icant differences in densities of either of these between
treatments, and there is no indication that they had
any effect on the outcome of the experiments.
It is difficult to say how much flow the Nitex win-
dows permitted. It seems likely that significant flow
occurred at the beginning of the experiments but was
EXPERIMENT I (AUG 14)
TREATMENTS
-
o- -0 Daphnia ( 3 , 5 )
A--a Ceriodaphnia ( 2,4, 6 )
Ceriodaohnia (Daohnia extinct) (7,8,9)
Food Size Classes
(pm3)
FIG. 9. Mean density of algae and bacteria in different
size classes for different treatments in competition experi-
ment 1 (14 August).
quickly restricted by periphytic growth on the win-
dows. By the 2nd wk of an experiment, the chambers
could be lifted from the water without any loss of
water through the windows.
Experiment I
The results of this experiment are in accord with the
hypothesis of competitive displacement of Duphnia by
Cerioduphniu in the pond. It was started on 19 July
(just prior to the peak of Daphnia) and continued
throughout the replacement of Daphniu by Cerio-
duphnia until 14 August. Regardless of initial densi-
ties, relative frequencies o r age structure of the Duph-
niu populations, Daphnia always went extinct when
paired with Ceriodaphnia (Fig. 7). Cerioduphnia ap-
parently invaded one of the Daphnia controls (no. 1)
and in that case the 2 coexisted. The reduction of the
maximum size of Daphnia in the presence of Cerio-
duphnia (Fig. 8) also conforms with the results for the
pond.
The disappearance of Daphniu from the chambers
containing Ceriodaphniu appears to be a result of re-
duced survival at an early stage in their life history,
since the few female Daphnia that were mature in the
presence of Ceriodaphnia were investing more in re-
production than control animals were (compare in-
stantaneous birth rates for August 4 in Fig. 8). The
fact that a smaller proportion of Duphnia were mature
in the paired case emphasizes the difference between
these estimates. The same result was obtained for
Ceriodaphnia-a higher b in the paired situation de-
spite the similarity in age structure with the controls.
Examination of the food-size distribution in these
chambers shows that Daphnia and Crriodaphnicl had
F 60 MICHAEL L Y N C H Ecology. Vol. 59. No. 3

T A B L E2. Mean final densities ( 2 . 9 5 confidence limits) of cladocerans in the 2 competition experiments. Numbers in
parentheses under D a p h n i a + Ceriodaphnia in Experiment 1 are the final densities in the one chamber in which the 2
coexisted. Number of replicates denoted by N

Mean final densities k0.95 confidence limits (individualsilitre)

TREATMENT
Ctjrio- Daphnia +
Daphnia + Dapl~nirr + d a p l ~ n i a+ Ceriodaphnia +
D a ~ h t ~ i u Crriodanhnicr Bosrnincr Ci~riodanl~niu Bosmit~u Bosrninu Bosrnit~u

EXPERlMENT l
( 14
.4ugujt)

'V = 3 3 9

~ ( l ~ 1 / l l l ~ ( l 95.0 -+ 19.0 0 (80)

C'c,riodop/~t~i(~ 462.0 -+ 53.4 265.0 t 42.3

(193)
EXPERIMENT 2
( 10 September)
h'= 3 3 2 2 3 3 4
Dcrpl~nia 19.0 -+ 10.8 48.5 -+ 14 38.3 -+ 15.4 17.5 -+ 6.7
C(,riod(~pl~nici 262.0 t 40.2 61.5 -+ 16 137.0 -+ 29.1 2.8 -+ 2.6
Bosmintr 202.0 2 127.6 6.3 -t 6.2 89.7 -+ 23.5 12.2 -+ 5.6

very different impacts on the food supply (Fig. 9).
Very small particles were rare in all chambers. Large
particles were scarce in all chambers containing Daph-
nia, but were abundant in those containing only Cerio-
daphnia. These large particles remained rare even af-
ter Daphnia had gone extinct, and were scarcest in
the one chamber in which Daphnia and Ceriodaphnia
coexisted. Thus, it appears that together the 2 species
depressed the food supply to a lower density than
either could d o alone-to the point at which Cerio-
daphtlia outlasted Daphnia.
E.xperiment 2
The 2nd experiment was initiated immediately fol-
lowing the 1st but yielded significantly different re-
sults. Both Daphnia and Ceriodaphnia persisted
alone, but at considerably lower densities than in the
1st experiment (Table 2). Furthermore, Daphnia not
only survived when enclosed with Ceriodaphnia, but
it reached densities twice those in the Daphnia con-
trols; in these same enclosures Ceriodaphnia declined
significantly relative to their controls. Similarly, when
Daphnia and Bosmina were paired, Daphnia attained
twice their control densities, while Bosnlina nearly
went extinct. Densities of all 3 species remained low
when they were enclosed together, although the abun-
dance of Daphnia was not significantly different from
its control density.
The enhancement of conditions for Daphnia in the
presence of either Ceriodaphnia or Bosmina in this

T A B L E3. Mean and range of major food groups within treatments in Experiment 2, 10 September a s lo5 CLm:l/ml.Flagellates
include all such species without hard outer walls: Chlorococcales include Scer~edesrnlisand Pedicrstrrm~species: desmids
include Cosmaririrn species and S t a ~ r r u s t r ~ i rpna r u o ' o x ~ i m :diatoms include Coc,coneis sp., Cyrnhellu sp.. Gornphot~rmcr
sp.. ,Vcr~.iclilasp. and Nitzschia sp.: gelatinous forms are Chrooc~occrisdisperslis, Gloeocystis ~ ~ r s i c . r i l o sand
a Spl~arroc~.stis
.scl~roetrri

Mean and range of major food groups (10" p d i m l ) on final sampling date, Experiment 2
TREATMENT
Taxon D C B D + C D + B C +B D + C +B Control
Flagellates .58
(0-.91)
Chlorococcales 1.02
(.52-1.45)
Desm~ds 9.84
(4.02-15.92)
D~atoms 2.44
(1.563.76)
Gelat~nousForms 1.51
(.40-2.10)
Bacter~a 1.04
( . ? G I .89)
Late Spring 1978 CLADOCERAN INTERACTIONS 6 1

EXPERIMENT 2, SEP 10 males carrying eggs were numerous in the chambers

Daphnlb pulex with all 3 species, juvenile Daphnia were rare. This
Solitary ( N - 5 5 ) + Ceriodaphnia ( N = 103)
suggests that low juvenile survival was responsible for
maintaining Daphnia at low densities in the 3 species
chambers.
Complexities associated with age structure also

,
arose for Ceriodaphnia populations under different
treatments (Fig. 10). The reduced population size in
+ Bosrnino ( N = 104 ) + Ceriodaphnia +Bosrnlna the presence of Daphnia appears to be largely a result
2 I 2 ~ : , :N=89) of the reduced clutch sizes. However, the few Cerio-
0.2 Q, 0.2 oo daphnia which were present in chambers containing
0
all 3 species were carrying large clutches. The con-
spicuous absence of juveniles under this treatment
again emphasizes the importance of juvenile mortality
in maintaining these populations at low densities.
Finally, the density of Bosmina was significantly
depressed by the presence of other species in all cases.
Cerlbdaphnlb reticulafa Its reproductive capacity was much more severely af-
I Solitary (N=143) + Daphnia (N=85)
fected in paired situations than was that of Daphnia
P, 2 r 2r
or Ceriodaphnia.
The precise mechanisms leading to the outcome of
this experiment are less clear than for the 1st experi-
ment. However, it is clear that the impact of the her-
bivores on their food supply in this experiment was
+ Bosmlna (N=142) + Daphnia + Bosrnina one of resource alteration rather than simple depres-
2 1 , ;o (Y=,12) sion. Although the food-size distribution was very
similar in all treatments on the final sampling date (Fig.
l l ) , there were significant differences in the abun-
dances of specific food groups (Table 3).
The enhancement of conditions for Daphnia when
paired with Ceriodaphnia o r with Bosmina was asso-
ciated with an increase in the abundance of flagellates,
Chlorococcales and desmids and a decrease in bacteria
Solitary (N-91) and gelatinous forms relative to Daphnia controls.
These algae are significant contributors KO the food
supply of Daphnia, and could explain the increased
clutch sizes and population densities for Daphtlia in
0.2 paired chambers. Flagellates, Chlorococcales, and
desmids were also more abundant in the 3 species
treatments where Daphnia clutch sizes were high, yet
+ Ceriodaphnio ( N = 9 1) + Daphnia + Ceriodaphnia the data are not sufficient to explain the much lower
0,4~[N~001 , 0,4~5[oO~o I N=50) abundance of Daphnirc in these chambers.
Significant shifts in the quality of the food supply
also occurred between treatments with Ceriodaphnia
(Table 3). Bacteria and diatoms, which are significant
components of Ceriodaphnia's diet (Gophen et al.
1974, Smyly and Collins 1975), were lower in the
Carapace Length ( m m ) Daphtlia + Ceriodaphnia treatments than in Cerio-
FIG. 10. Size-frequency distributions and mean clutch dapht~irccontrols and may be responsible for reduced
sizes for individuals of different sizes in experiment 2 (pooled clutch sizes in these chambers. Abundances of most
data from replicates). Abscissas of insets start at carapace
lengths directly below their ordinates. Sample sizes for size- +
food types in Ceriodaphtlia B o s m i t l ~and Daphnirc
frequency distributions are denoted by N. Mean clutch sizes + Ceriodaphnia + Bosmitla treatments were nearly
are for sample sizes 3 3 , and usually between 10 and 30. equal to those in the Ceriodrcphnia controls, and clutch
sizes approximated those in the controls. Again, this
experiment is further supported by the larger clutches information is not sufficient to explain the lower num-
carried by females in paired chambers (Fig. 10). N o bers of Ceriodaphtlia (a probable result of reduced
Daphnia were carrying eggs in the controls at the end juvenile survival) in the paired chambers.
of the experiment. However, despite the fact that fe- The lack of explanation for several population char-
562 MICHAEL L Y N C H Ecology. Vol. 59, No. 3

acteristics in this experiment is probably a result of

temporal variability in the food supply in these cham-
EXPERIMENT 2 (SEP 10)
bers. Because the generation time of cladocerans is
greater than that of their food supply, their population
Control
characteristics could have been regulated by earlier
(and perhaps different) resources than those I oh-
served. Furthermore, since I was unable to quantify
detritus, its significance as a dietary component for
these species remains unknown.
Two discrepancies appear when the results of the
competition experiments are related to the actual pond
data. (1) T h e estimated densities of Daphnia and
Ceriodaphnia were generally much higher in the
chambers than in the pond. Thus, while competition
between these 2 species was clearly demonstrated in
experiment 1, the question remains as to whether
Daphnicr was really competitively displaced by Cerio-
daphnia at lower densities in the pond. I found no
evidence to indicate that increased predation was re-
sponsible for the demise of Daphnia. Several physical
and chemical factors have been suggested to be im-
portant in determining the distribution of zooplankton
(Hutchinson 1967): temperature, oxygen concentra-
tion and pH. All of these remained quite stable before
and while Daphnia was displaced (Lynch and Shapiro,
personal observarion). More significantly, while the
estimated densities of both species were much lower
in the pond than in the experimental chambers, the Cerioduphnio
food supply also declined to much lower levels in the
pond (compare Figs. 3 and 9).
This discrepancy may simply be an artifact of the
method I used to estimate pond densities, i.e. densities
per unit surface area divided by the depth of the water
column. Because 0, concentrations below 1 m were
often very low, the cladocerans were probably con-
fined to a narrow surface layer, in which case my cal-
culated volumetric densities would be underestimated.
(2) Although conditions for Daphnia were enhanced
in the presence of Ceriodaphnia in the 2nd experi-
ment, densities of Daphnia remained very low in the
pond. It is possible that the very high densities of
Ceriodaphnia in the pond maintained a bottleneck
which prevented an increase of Daphnia. The low
starting densities in the chambers would have alle-
viated such a problem. Cerioduphnio

Although the mechanisms leading to certain out-

comes of the competition experiments are not entirely oo*wowPwPwP "
clear, the results themselves are significant. An un- -wInCUa,arQ* 2
N O 0 mu-)--
0
ambiguous interpretation of the interactions between - * ,-mcu- E
- w wCU .-2
LL

Food Size Classes

FIG. 11. Mean density of algae and bacteria in different
size classes for different treatments in competition experi-
ment 2 (10 September). Vertical lines denote the range. Con-
(p n 31
trol is one chamber which received no cladocerans.
Late Spring 1978 CLADOCERAN 1INTERACTIONS
Daphnia and Ceriodaphnia involves several complex-
ities which are not generally appreciated in theoretical
investigations of competition: (1) seasonality, (2) age
structure, and (3) resource interactions.
I . There was a shift in the competitive abilities of
Daphnia and Ceriodaphnia over a very short time pe-
riod. Over the same period there was a dramatic de-
cline in the densities to which each species could grow
in the absence of competitors. Such disparities be-
tween experiments show the artificiality of considering
"competition coefficients" and "carrying capacities"
as time invariant.
The shift in the competitive ability of Daphnia be-
tween experiments may be related to a seasonal de-
cline in water temperature. Daphnia pulex has a max-
imum feeding efficiency (food intake divided by
metabolic demands) at a temperature of =20C; feed-
ing efficiency drops off very sharply above this tem-
perature, declining to very low values at 25'C (Lynch
1977). Temperatures during the 1st experiment often
exceeded X C , and Daphnia always went extinct
when paired with Ceriodaphnia. Temperatures had
dropped below 25C by the 2nd experiment and ap-
proached 20C on 6 September; Daphnia increased at
the expense of Ceriodaphnia in this experiment.
2. Because different age classes are not equally
prone to coexploitative interactions, the interactions
of these species can be understood only in the context
of a framework which considers age structure. While
certain age classes were severely affected by resource
alteration, others were unaffected and sometimes even
benefited. The competitive displacement of most spe-
cies in the experiments appeared to be not s o much a
result of any adverse conditions for adults as a con-
sequence of reduced juvenile survival.
3. The frequent enhancement of conditions for cer-
tain age classes in the presence of coexploiters further
emphasizes the complexity of these interactions.
When paired with Ceriodaphnia or Bosmina in the 2nd
experiment, Daphnia attained a density twice as great
as in their controls. However, an enhancement of con-
ditions for adults is not sufficient for an increase in
population size. In the presence of both Ceriodccphnia
and to.smina in experiment 2, Daphnia females car-
ried many more eggs than in Daphnia control cham-
bers. but their final population levels were similar.
Thus, the improved conditions for adults in that case
must have been balanced by a reduced survival at an
earlier age.
Such enhancement effects mediated by coexploiters
are not consistent with our present concept of com-
petition. The assumption that resources are indepen-
dent of each other prevents a direct enhancement of
conditions for one species by a coexploiter from aris-
ing in theoretical investigations. Thus, an assumption
implicit in most studies of competition is that ex-
ploitative interactions are based sloelq on resource
depression. However, many studies have shown that
563
the removal of 1 prey species often results in quanti-
tative, qualitative or distributional changes in other
prey (Brooks and Dodson 1965, Paine 1966, Harper
1969). Such results occur when the presence of a pred-
ator alleviates competition between prey species by
removing the competitive dominant. In those cases,
coexploitative interactions are more accurately de-
scribed in terms of resource alteration than simple
depression.
When the restriction of resource independence is
relaxed, the predictions drawn from various compe-
tition formulations may be altered significantly (Lev-
ine 1976). Under such conditions it becomes theoret-
ically possible for one species to alter the resource
base in a way that directly benefits a 2nd coexploiter
(e.g. Charnov, Orians and Hyatt, 1976). The results of
these experiments clearly demonstrate the potential
for such facilitation to occur in natural communities.
The simple depression of all resources in the 1st
experiment may have been related to the relatively
high levels of nutrients present then (Lynch and Sha-
piro, personal observation). If the algae in the Daph-
nia coritrol chambers were not competitively con-
strained, the activity of a 2nd grazer would be unlikely
to benefit any alga. The fact that almost all algal spe-
cies increased in Ceriodaphnia controls relative to
Daphnia controls provides further evidence that these
algae were not tightly constrained by nutrients.
Phosphorus (dissolved and total) and dissolved in-
organic nitrogen (ammonia, nitrate, nitrite) levels de-
clined very significantly in August, resulting in a sharp
decline in species specific algal productivities (Lynch
and Shapiro, personal observation). These changes
may be responsible for the decline in the carrying ca-
pacities for Daphnia and Ceriodaphnia in the 2nd ex-
periment. This also suggests that the algae were more
competitively constrained than in the 1st experiment,
and that some species would have benefited from the
depression of their competitors, conditions necessary
for the establishment of facilitation between 2 exploit-
ers.
It is entirely plausible that the facilitation noted in
this study was simply a transient phenomenon result-
ing from environmental vagaries. However, such fa-
cilitation between species may in some cases have an
evolutionary basis. There would be a distinct advan-
tage for an organism which benefits from the resource
alteration mediated by a coexploiter.
The results of this study emphasize the importance
of studying species in the context of their natural en-
vironment. While facilitation appears to be widespread
in nature ( M . Lynch, personal observation), it has not
generally arisen in laboratory investigations, probably
due to the simplified communities used in such studies.
Consequently, contemporary ecological theory em-
phasizes the selective nature of negative interactions
between species-competition and predation. 1 stress
that our present understanding of community structure
564 MICHAEL LYNCH Ecology. Vol. 59. No. 3

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