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I

I

I

75-14,788
MELLINGER, Donald Lee, 1936A STUDY OF THE COEXISTENCE OF TWO SPECIES OF
DIAPTOMUS (COPEPODA:CALANOIDA) IN GULL LAKE,
MICHIGAN.
Michigan State University, Ph.D., 1974
Ecology

Xerox University Microfilms,

Ann Arbor, M ichigan 48105

STUDY OF THE COEXISTENCE OF TWO SPECIES OF DIAPTOMUS
(COPEPODA:CALANOIDA)

IN G U L L LAKE, MICH I G A N
By

D onald Lee M e l l i n g e r

A DISSERTATION

S ubmitted to
Mich i g a n State University
in partial fulfillment of the requirements
for the degree of
DOCTOR OF PH I L O S O P H Y
D epart m e n t of Zoology
1974

ABSTRACT
A STUDY OF THE COEXISTENCE OF TWO SPECIES OF DIAPTOMUS
(COPEPODA:CALANOIDA) IN GULL LAKE, MICHIGAN
By
Donald Lee M e l l i n g e r

The conditions of the coexistence of Diaptomus
mi n u t u s and D^_ oregonensis in Gull Lake, Michigan, were
ex a mined during the period 1972-1974.
from v e r t i c a l series of samples,

The d a t a obtained

using a van Dorn sampler,

i n d i cated that EK_ minutus and D^_ oregonensis occupied the
same v olume of water, had similar seasonal abundances,

and

o c c u r r e d w i t h essentially a 1:1 adult species ratio th r o u g h ­
out the course of the study.

Metas o m e length measureme n t s

did not ap p e a r to lend convincing support to the character
d i s p l a c e m e n t hypothesis as propo s e d by Cole

(1961).

By means of the radioisotope in situ grazing method
de v e l o p e d by Haney

(1970,

1971),

filtering rates were c a l ­

culated for the two species from feeding experiments
em p l oying five species of

l ^ C - l a b e l l e d

green algae.

The

p u r pose of these feeding experiments was to explore possible
food niche differentiation, based on cell size.
of exper iments using Chlorella sp.

The results

and Chlamydomonas

Donald Lee Mell i n g e r
reinhardtii indicated that

oregonensis females,

the

largest group, did not collect C h l o r e l l a - sized cells
(3-8 m i crons diameter)
sized cells.
accuminatus

as effectively as they did the larger

Both diaptomid species collected Scenedesmus
(18-26 microns diameter)

results suggest that,

effectively.

These

contrary to the Brooks and Dodson

(1965) h ypothesis of zooplankton food niche diffe r e n ­
tiation,

the area of overlap,

size, is between

in terms of food particle

8 and 2 2 microns w i t h the portion of the

size s p ectrum b e l o w 8 microns being util i z e d mainly by the
smaller species,

Dj_ minutus and the portion above 22

microns being available mainly to the larger species, D .
oregonensis.
During the summer stratification period,

female

daytime filtering rates in the me t a l i m n i o n were depres s e d
compared to the male rates.

This phenomenon may be

associated w i t h an alternating pattern of "encounterfeeding" and "filtering-feeding" modes.

Summer nighttime

filtering rates of migra t i n g individuals were higher than
daytime filtering rates.
The general conclusion is that there may be s u f ­
ficient differences in feeding patterns to account for the
coexistence of these two commonly co-occurring species.
There was little,

or no evidence of space niche or time

niche separation in Gull Lake.

To my father and mother, A b r a m and Mabel Mellinger,
I dedicate this work.

A CKNOWLEDGMENTS

I express my sincere appreciation and gratitude to
Dr.

Donald J. Hall, my m a j o r professor,

for his perceptive

guidance and support throughout m y research program.
grateful to Dr.

Robert G. Wetzel for his encouragemen t and

generosity in providing
ment.

I am

for the use of laboratory e q u i p ­

To D r s . Kenneth W. Cummins and W i l l i a m E. Cooper,

I

express m y thanks for their help and guidance during the
course of this study.

I w o u l d also like to thank Dr. Earl

E. W e r n e r for his assistance during the final stages of m y
program.

X am indebted to Dr. Patricia A. Lane for the use

of the grazing chamber.

I w i s h to extend special app r e ­

ciation to Dr. George H. Lauff,

Director, W. K. Kellogg

Biological Station for his e n c o u ragement and support in
numerous ways during the course o f my research program.
The assistance of the Depart m e n t of Zoology,
late Charles S. Thornton,

chairman,

the

and the W. K. Kellogg

Biolog i cal Station in providing graduate teaching assistantships during the early phases of m y graduate pro g r a m is
g r a t e f u l l y acknowledged.

During 1972-73,

I was supported

by a g r a n t from the National Science F o u n d a t i o n

H.

Lauff, et a l . , GB-15665,

GB-31018X,

supporting the Coh e r e n t

Areas Research Project in F r e s h w a t e r Ecosystems.
Finally,
Alta,

I have w a r m e s t appreciation for m y wife,

and daughters,

Donna and Sharon, w h o endured the

rigors of these years w i t h me.

TABLE OF CONTENTS

Page
LIST OF T A B L E S ..........................................

vi

LIST OF F I G U R E S ..........................................

vii

I N T R O D U C T I O N ..............................................

1

The Concept of Coexistence
.........................
The C o -occurrence of Diaptomus oregonensis and
D. m i n u t u s ..........................................
Scope of the S t u d y ...................................

1
9
11

STUDY A R E A ..............................................

14

M A T E RIALS AND M E T H O D S ...................................

17

R E S U L T S .................................................

24

T emporal D i s t ribution ................................
V e r tical D i s t ribution ................................
Size M e a s u r e m e n t s ...................................
G r azing E x p e r i m e n t s ...................................

24
27
32
37

D I S C U S S I O N ..............................................

55

Habitat C o e x i s t e n c e ...................................
Phylog enetic C o n s iderations .........................
Ch a r acter D i s p l a c e m e n t ................................
F i l t ering Rates .......................................

55
62
64
65

SUMMARY AND C O N C L USIONS

................................

82

B I B L I O G R A P H Y ..............................................

85

v

LIST OF TABLES

Table

Page

1 . V a r i a t i o n in m e a n meta s o m e length

(mm) of
Diaptomus minutus and
oregonensis in
February, 1972.
(n>20 for each
c a t e g o r y ) .......................................

35

2 . C o mpar i s o n of m e a n summer metas o m e lengths
(mm) of Diaptomus min u t u s and D_j_ o r e g o n ­
ensis of Gull Lake, Sherman Lake, and
Three M i l e Lake w i t h those reported by
Tur v e y (1968) from Ont a r i o
..................
3.

4.

36

Size m e a s urements of the five species of
green algae used in the in situ grazing
e x p e r i m e n t s ...................................

40

D a y-night filtering rates of Diaptomus
minutus in Gull Lake, Michigan.
All data
are from summer e x p e r iments ex c e p t where
noted.
Filtering rates are presented
as m e a n m l / a n i m a l / d a y
SE.
Animals
were grouped into pellets before c o m ­
b ustion to carbon d i o x i d e .....................

45

D a y-night filtering rates of Diaptomus
o r e g o n e n s i s in Gull Lake, Michigan.
All
data are from summer experiments except
w h e r e noted.
Filtering rates are given
as m e a n m l / a n i m a l / d a y + SE.
Animals
were grouped into pellets be f o r e c o m ­
bus t i o n to carbon d i o x i d e .....................

46

vi

LIST OF FIGURES

Figure
1.
2.

3.

4.

5.

6.

7.

8.

Page
M a p of Gull Lake, showing sampling
l o c a t i o n s .......................................

15

Seasonal d i s t r i b u t i o n of Diaptomus minutus
and
oregonensis adults m mean
n u m b e r s / 8 .8 liter sample.
Sample means
w e r e averaged on a mon t h l y basis
. . . .

25

V a riation in percentage of adult Diaptomus
m inutus and D_;_ o r e g o n e n s i s . Samples
were grouped on a m o n t h l y b a s i s .................

28

The vertical d i s t r i b u t i o n of adults of
Diaptomus minutus and D ^ oregonensis
in Gull L a k e ...................................

29

The vertical d i s t r i b u t i o n of adult
Diaptomus minutus and D^_ oregonensis
in two d a y - n i g h t series of July and
August, 1972.... .................................

31

V a r i a t i o n in size of Diaptomus min u t u s and
D . oregonensis in February, June, August,
and October, 1972.
(small peak = mean;
length of wh i t e bar = 4 SE; length of
underline = 4 S D ) ............................

33

C o mpar i s o n of the summer daytime and n i g h t ­
time filtering rates of Diaptomus
minutus ( # ) and D^_ oregonensis (♦ ) ,
using A n k i s t r o d e s m u s falcatus
(mean + SE)
I
I T .........................

39

The summer daytime filtering rates of
Diaptomus minu t u s ( • ) and D ^ o r e g o n ­
ensis
using Scenedesmus accuminatus
(mean + S E ) ...................................

41

vii

F igure
9.

10.

11.

12.

13.

Page
C o m p arison of the summer daytime and n i g h t ­
time filtering rates of Diaptomus
m inutus (# ) and D^_ oregonensis ( ♦ ) ,
using C h l a m ydomonas reinhardtii
(mean + S E ) ...................................

42

The summer daytime filtering rates of
D iaptomus minutus ( # ) and D^_ o r e g o n ensis ( ♦ ), using C h l o rella sp.
(mean + S E ) ...................................

44

C o m par i s o n of wi n t e r and summer daytime
filtering rates of Diaptomus minutus ( # )
and D^_ oregonensis ( ♦ ), using Scenedesmus
accuminatus
(mean + S E ) ....................

51

C o m p arison of w i n t e r daytime and nighttime
f iltering rates of Diaptomus minutus ( • )
and D^_ oregonensis ( ♦ ), using Scenedesmus
accuminatus (mean + SE) .....................

53

C o m par i s o n of wi n t e r daytime and nighttime
filtering rates of Diaptomus minutus ( • )
and D^_ o r e g o nensis T^F) , using
Chlamydomonas angulosa
.....................

54

viii

INTRODUCTION
The Concept of Coexistence
The p r i n ciple of competitive e x c l usion has i n t e r ­
e s t e d b iologists for more
p r i n ciple

than seventy years.

This

("Gause Hypothesis" or "Volterra-Gause Principle")

has b e e n v e r b alized as the proposition,

" . . .

that species

w i t h i d entical needs and habits cannot survive in the same
place if they compete for limited r e s o u r c e s — at least if
their needs and habits remain identical"
Hutchinson

(1965)

(Crombie,

1947).

stated that if two n o n - i nterbreedin g

popul a t ions o c c u p y i n g the same ecological niche are sympatric,

one w i l l ultimately exclude the other.

o b s e r v e d by several authors
1960;

Birch and Ehrlich,

(Gilbert,

1967)

It has been

et al^. , 1952; Hardin,

that if two population s are

suffi c i ently d i s t i n c t mo r p h o l o g i c a l l y to be recognized as
species,

they differ to some degree in their genetics,

physiology,

and eco l o g y as well.

So there is an a priori

as s u m p t i o n that no two species are e c o l o gically identical.
As a consequence,

the competitive exclu s i o n princ i p l e can

ne i t h e r be pr o v e d n o r disproved.
(1968)

indicates,

However,

as MacAr t h u r

the consequences of the princ i p l e may

1

2
still be valid and well w o r t h examining in some detail.
One w a y of proceeding w o u l d be to examine a natural si t u ­
ation and then infer the e x p l anation for the continuing
coexistence of closely related species,

and a second way

could be to simulate a simplified and controlled e n v i r o n ­
ment .
MacArthur's

(1958)

study of a group of warblers

living together in the northeastern coniferous
an example of the first approach.

forests is

He found that the five

species of warblers actually subdivided trees and each fed
m ainly in its section on a given tree.

The alternative

approach of controlled laboratory e x p e r imentation is e x e m ­
p l i f i e d by Gause
(1962).

(1934) , Frank

(1952,

1957)

and Park

These studies have shown that w h e n two similar

species are forced to live together in a simple enviro n m e n t
with a single

food resource, one species always wins out

over the other.
the experiment,

By increasing the physical complexity of
adding bits of macaroni,

for example,

outcome of the experi m e n t could be altered.

the

Both

approaches emphasize the importance of environmental
h e t e r o g e neity for the coexistence of two or more similar
species.
E n v i ronmental heter o g e n e i t y may be discussed in
terms of "niche".
"niche,"

Grinnell

(1924)

first used the word,

to describe the potential geographical d i s t r i ­

b u tion of a species.

The limits of the distribution w o u l d

3
be set by physical-climatic barriers rather than limits set
by interactions w i t h other organisms.

Elton

(1927) d e v e l ­

oped the idea that "niche" can be used to describe the food
habits of a species.

By this,

he referred to the o r g a ­

nism's actual or realized place in the e n v i ronment rather
than the potential position as suggested by Grinnell.
an attempt to formalize the notion of niche,

In

Hutchinson

(1957) p roposed that the niche of an o r g a n i s m may be r e p r e ­
sented as a hypervolume whose coordinates represent e c o ­
logical requisites

for its existence.

Since the concept

of niche is quite broad, some ecologists have subdivided
it into components,
and "place

(space)

Generally,

such as the "food niche,"
niche"

(Pianka,

"time niche,"

1969).

ecologists have exam i n e d two phenomena

which may permit coexistence:

(1) Habitat selection,

w h e r e b y two species attain some degree of spatial-temporal
separation thus generating differences in their place niche
and/or time niche;

and

(2) resource allocation, w h e n two

species use d i f f erent proportions of two or m o r e resources
(e.g.

food).

Resource allocation is also considered to

include the passive situation where the species are d i f ­
ferentially selected as a resource b y a predator.

These

two means of coexistence m a y often operate simultaneously
and in an interactive fashion.

It is i m p o rtant to e m p h a ­

size that coexistence per se implies nothing about

competition,

although coexistence is often the raison

d 1gtre for studies of competitive relationships.
Zooplankton, because of their seemingly identical
feeding behav i o r and hab i t a t utilization have long been
considered an enigma in competition theory
1961).

(Hutchinson,

Coexistence of two zooplankton species frequently

m a y occur if there is a temporary superabundance of food
w h i c h enables both species to thrive and increase sim u l ­
taneously

(Fryer,

1957; Pejler,

1962; Cole,

1966; S m r c h e k ,

1973), but other factors must be operating to pe r m i t the
l o n g -term coexistence of two closely related species
u tilizing the same or similar food resources.
ple, Lane and McNa u g h t

(1970)

As an e x a m ­

p e r f o r m e d a m a t h e matica l

analysis of the niches of Lake Mich i g a n zooplankton,
the equations of Levins

using

(1968), b a s e d on h a b i t a t selection

and resource allocation in similar species.
Pennak

(1957)

exam i n e d 148 vertical series of

samples taken from 2 7 lakes of C o l o r a d o and did not find
any single series of samples that contained more than one
species of D i a p t o m u s .

He concl u d e d that in North A m e r i c a

w h e n two limnetic calanoids are found together,

it is very

s e l d o m that they are both species of Diaptomus b u t rather
it is one Diaptomus and an additional species of
L i m n o c a l a n u s , E p i s c h u r a , or S e n e c e l l a .
exceptions to this rule,
them to be uncommon.

Wh i l e no t i n g some

Pennak suggested that he b e l i e v e d

On the o t h e r hand,

Cole

(1961)

5
compiled a list of 34 diffe r e n t combinations of two or more
Diaptomus species co-occurring in lakes and ponds.

Ten of

these combinations involved at least two members of the
same subgenus.

This list is based on his studies in

Ar izona and published reports from other parts of the
world.

Perhaps

the most extensive survey of the Diaptomus

co-occurrence phenomenon,

to date,

O n tario b y Higler, Langford,

was carried out in

and their students.

They

found that 51% of the 100 lakes studied conta i n e d two or
more species of Diaptomus
Turvey

(1968)

(Rigler and Langford,

1967).

listed the species composition of 226 lakes

in Ontario, w h i c h included those reported by Ri g l e r and
Langford,

and found that 38% contained two or m o r e species

of D i a p t o m u s .

His data show that of 144 h e a d w a t e r lakes,

only 21% conta i n e d two or more species of D i a p t o m u s .

In

82 n o n - h e adwater lakes, he found 65% contained two or more
species of D i a p t o m u s .

These data suggest that some

instances of co-occurrence may be the result of continuous
immigration.
V ertical and/or temporal separation has been
a d v anced to explain these congeneric c o - o c currences in
D i a p tomus
ford,

(Carl,

1967;

194 0; Hutchinson,

Sandercock,

1967;

1951;

Rigler and L a n g ­

Tash and Armitage,

1967).

It has also often been p o s t u l a t e d that related species of
zoopla n k t on of d i f f e r i n g body size do n o t occupy the same
food niche, presum a b l y due to d i f f e r e n t efficiencies in

6
"utilizing"

(collecting)

(Hutchinson,
Sprules,

diffe r e n t sizes of food particles

1951; Fryer,

1972).

1954; Brooks and Dodson,

Ha m m e r and Sawchyn

study of some Saskatchewan ponds,

(1968),

1965;

from their

concl u d e d that a min i m u m

length difference of 0.5 m m was necessary to allow co e x i s ­
tence of two species of D i a p t o m u s .
(1967)

Tash and Armitage

obser v e d that Diaptomus arcticus

frequently

c o - o c c u r red with EK_ pribilofensis in ponds and lakes of the
Cape T h o mpson area of Alaska.

A d u l t D^_ arcticus were about

twice as large as D^ pribilofensis wh i c h led the authors to
believe that congeneric coexistence depends upon size d i f ­
ferences of this magnitude.
In addition to observations that co-occurring c o n ­
g e neric species often display marked size differences,
Brown and W i l s o n
displacement"

(1956)

introd u c e d the term,

"character

to describe the diverg e n c e of m e t r i c c h a r ­

acters shown w h e n two partly allopatric species of c o m p a ­
rable niche requirements become sympatric in part of their
range.

Hutchi n s o n

(1959)

reviewed various studies of

m a mmals a n d birds w h i c h appe a r e d to exh i b i t the phenom e n o n
of character displacement.
r e l ated species co-occur,
small form is roughly 1.3.

He concl u d e d that w h e n closely
the ratio of the larger to the
This ratio,

he felt,

is in d i c a ­

tive of the kind of difference necessary to permit two
species to co-occur in diffe r e n t niches but at the same
trophic level.

Altho u g h the ratio was derived from mammal

7
and b i r d data, he beli e v e d that it had general application
to o t h e r animal groups,
(1961)

including aquatic insects.

Cole

suggested that character d i s p l a c e m e n t m a y permi t

closely related species of Diaptomus to parti t i o n and
c o nsequently share aquatic habitats.
Hutchinson

(1951)

He noted that

reported that in the case of the very

c l osely allied Arctodiaptomus w i e r z ejskii
A.

laticeps

(1.4 mm)

and

(1.3 mm), w h i c h generally have complete size

v a r i a t i o n overlap in lakes where they oc c u r alone,
was a slight length difference

(0.1 mm)

there

betw e e n the two

species when they co-occurred in a lake of the Outer
Hebrides,

Scotland.

The character d i s p l acement hypothesis as applied to
diaptomids by Cole suggests that if species A is larger
than species B then species A will be larger in lakes where
it coexists w i t h species B than it is in lakes where it
occurs alone and species B will be smaller in lakes wh e r e
it coexists w i t h species A than it is in lakes where it
occurs alone.

The functional consequence of the p r o p o s e d

c h a r a c t e r displacement phenom e n o n in diaptomids w o u l d be
that the increased difference in body lengths enables
species A to be more effective in collec t i n g larger food
p a r t icles from the size spectrum available and species B
to be more effective in collecting from the smaller end of
the food particle spec t r u m pre s e n t in lakes w h e r e they
coexist.

As a consequence,

data w h i c h w o u l d show character

8
displ a c e m ent in congeneric coexisting diaptomids could be
taken as indirect evidence that body length is indeed cor­
related w i t h the partitioning of the available food
resources into different food niches.
What is m e a n t by the term "coexistence"?
(1961)

Cole

does not differentiate between co-occurrence and

coexistence.

Pennak

(1957)

suggests that it is important

to consider species dominance when attempting to evaluate
coexistence.

He suggests that if one species is n u m e r ­

ically dominant and 20 or more times as abundant as the
o ther co-occurring species then the situation should not be
considered as an example of coexistence but rather the
typical situation of a community containing additional
species in the "rare" category w h o function as "seed"
nuclei for potential future population cycles.
and Sawchyn's study

(1968)

In Hamm e r

those diaptomid associations

w h i c h p e r sisted for at least three weeks were considered
as examples of true coexistence.

In many lakes,

this

p e r i o d of time w o u l d seem to be too short to preclude
situations w h i c h are really the overlap of the final phase
of one s p e c i e s 1 life cycle w i t h the begin n i n g phase of
another one.

Further,

one species m a y be restricted to the

hypoli m n i on while another may occur ma i n l y in the epilimnion and metalimnion.

During the summer, Sandercock

(1967)

found Diaptomus sanguineus to be e f f e ctively separated

9
from D_;_ oregonensis and D^_ minutus by the discontinuity
layer in Clarke Lake, Ontario.
M y operational defini t i o n of coexistence shall be
that two or more species may be considered to be coexisting
if they occupy the same volume of wa t e r for an extended
p eriod of time

(months)

and are present in relatively

similar proportions.
The Co-occurrence of Diaptomus oregonensis
and D . minutus
Diaptomus oregonensis Lilljeborg 1889 was used by
Light

(1939)

as the type species for the subgenus,

Skistodiaptomus.

Marsh

(1907)

suggested that

oregonensis

or its immediate ancestor inhabited the waters south of the
ice at the he i g h t of the glacial period and as the ice
retreated,

it gradually m o v e d north.

He beli e v e d that

d u r i n g this m o v e m e n t it ada p t e d itself only slightly to the
changes of the environment.
Diaptomus minutus Lilljeborg 1889 was included in
the subgenus, L e p t o d i a p t o m u s , by Light

(1939).

He based

his classification on the characteristics of the fifth pair
of legs of the male.

D ^ minutus has been descr i b e d from

collections made in Greenland,
(Marsh,

1929)

N e w York,

Iceland, N e w f o u n d l a n d

and its range extends w e s t thr o u g h Maine,

Ontario,

Michigan,

and Wisconsin.

Marsh

(1907)

recogn i z ed the specialized features of the fifth legs of
b o t h males and females b u t concluded that its wide

10
d i s t r i b u tion strongly suggested that it is an early form
of the tenuicudatus group of the genus D i a p t o m u s .
Marsh

(1895)

noted that D_;_ minutus was, perhaps,

the m o s t common of all the diaptomids in Lake St. Clair and
the Great Lakes.

He also off e r e d the o b s e r vation that

w h i l e D ^ oregonensis occurred in the G r e a t L a k e s , it was
not a b u ndant there but was the m o s t common limnetic species
in s m aller lakes of Michigan.

Robertson

(1966), however,

o b s e r v e d that D ^ oregonensis seemed to be abundant in the
warmer,

southerly parts of the G r e a t Lakes b u t decreased

in abundance in the cooler,

n o r t herly regions.

He found

D. m i nutus to be pre s e n t in all the G r e a t Lakes but sel d o m
seemed to be present in large numbers.

In Lake Erie,

D.

o regon e n s is was found to be the most common diaptomid w h i l e
D . minutus was somewhat less common
1954,

1962).

(Jahoda,

1949;

Davis,

In Parry Sound, Geor g i a n Bay, Carter

(1969)

ob s e r v e d approximately the same abundance for the two
species over an 18-month period.

Wells

(1960)

found si g ­

ni f i c a n t numbers of b o t h species in Lake Michigan.

He

found their seasonal abundance to be rather variable from
y e a r to year.

Langford

(19 38)

reported b o t h species had

p o p u l a t i o n peaks during July and A u g u s t in Lake Nipissing,
Ontario.
Turvey

(1968)

with EK_ oregonensis
in southern Ontario.

found that D. min u t u s co-occurred

in over 33% of the 226 lakes studied
The two species were identified in

11
20% of the 45 lakes in the Experimental Lake Area of N o r t h ­
w e s t e r n Ont a r i o by Patalas
(1967, 1968)

(1971).

Hall and Waterman

found the two species occurred toge t h e r in

three of the eleven Finger Lakes of New York.
lakes of the Adiron d a c k region of New York,

In selected

these authors

o b s e r v e d that D^_ minutus was abundant in m o s t of the 36
lakes and ponds studied while it occu r r e d w i t h D_^ o r e g o n ­
ensis in two of nine large lakes and none of the smaller
ones.

A survey of 28 lakes in southwestern lower Mich i g a n

revealed only three lakes,
both species were present

including Gull Lake,
(Shuba and Mellinger,

in which
unpub­

lished) .
Scope of the Study
The work of Rigler and Langf o r d
(1968), and Robertson

(1966)

(1967) , Turvey

has e s t a b lished the fact that

Diaptomus minu t u s and D_;_ oregonensis co-occur in numerous
lakes including the Great Lakes.
tively unstructured environment

While a lake is a re l a ­
(Hutchinson,

1961),

thermal

strat i f i cation does offer the potential for place niche
differentiation.

The initial stage of my study was

designed to determine whe t h e r these two species of d i a p ­
tomids co-occurring in Gull Lake,

Michigan,

actually fit the

o perational defini t i o n of coexistence w h i c h I proposed.
the two species occupy the same volume of water?

Do both

species mig r a t e into the epilim n i o n at night during the
summer?

Is there a seasonal difference between peaks in

Do

12
species abundances?

In short, w h a t biolog i c a l mechanisms

a p p e a r to pe r m i t the coexistence of these two closely
related species?
In order to answer these questions,

I took series

of v e r t i c a l samples at two stations w i t h a 8.8 liter van
Dorn sampler,

including several night series.

series of samples,

I measured meta s o m e

F r o m these

(cephalothorax)

lengths on four dates for the pur p o s e of examining possible
evidence of chara c t e r disp l a c e m e n t as suggested by Cole
(1961).

Several series of samples were also collected from

o t h e r lakes in this area in w h i c h one of the species was
found to be the sole diaptomid present.
The latter stage of my study was dev o t e d to a c o n ­
sider a t i on of filtering rates of the two diapt o m i d species.
These rates w e r e o b t a i n e d by using the radioisotope in situ
m e t h o d d e v e loped by Haney

(1970,

1971).

One of the o u t ­

standing features of this in situ method is that it p r o ­
vided a means of exami n i n g the filtering rates of both
species simultaneously in each experiment in their natural
h a b i t a t of the lake.

The experimental chamber,

therefore,

conta i n e d the complete spec t r u m of p h y t o p l a n k t o n , zoo­
p l a n k t o n p r e d a t o r s , other zooplankton,
of labelled green algae.

and the trace amount

Five species of green algae w e r e

used, r a nging from 36 pm^ to 4 300 ym^ in volume,

in an

attempt to identify prop o s e d differences in filtering
e f f ectiveness related to cell size.

These filtering rates

13
should provide some insight into the separation of food
niches of these two species based on body length as p r o ­
p o s e d by Hutchinson

(1951)

and Brooks and Dodson

(1965).

STUDY A R E A

Gull Lake

(Figure 1) is located in the southwestern

corner of lower Michigan,
b e t ween latitudes
85° 30' W.

in Kalamazoo and Ba r r y counties,

42° 20'-42° 30*

N and longitudes

85° 20'-

The lake basin was formed by glacial excavation

(Wisconsin glacier)

of a p r e e x isting valley.

The south end

o f the valley was dammed by a moraine and several large ice
b locks in the basin prevented filling by outwash of s e d i ­
ments from the mel t i n g glaciers

(Martin,

1957).

The lake

drainage b a s i n is small in compar i s o n w i t h surface area of
the lake.

The surrounding country is slightly rolling in

c h a r a c t e r and consists
drift.

largely of calcium-rich glacial

Gull Lake covers an area of 822 hectares and has a

m a x i m u m d e p t h of 33 meters

(Taube and Bacon,

1952).

lake is fed by springs and a few small streams.
drains into the Kalamazoo River which,
into Lake Michigan.

in turn,

The

Gull Lake
empties

The average January air temperature

is about -3.3°C a n d the average July air temperature is
22.5°C.

M e a n annual p r e c ipitation is 86.3 cm

(Senninger,

1963).
Deta i l e d p h y s i o - c h e m i c a l m e a s urements are available
from O c t o b e r 1968 to 1974

(Moss,

14

1972;

Lauff, et a l . , in

15

GULL LAKE

Figure 1.

M a p of Gull Lake,

showing sampling locations.

16
preparation).

Gull Lake is a dimictic deep lake c h a r a c t e r ­

istic of temperate continental regions
Loffler,

1956).

(Hutchinson and

Ice covers the lake from early January

until mid-March.

Ov ert urn occurs in early April and again

in late No ve m b e r or early December.

The s ummer epi lim nio n

was about 9 meters deep and the hyp oli mni on b e g a n about
13 m.

S urface temperature reached 26°C during late July,

1972.

The h y p o l i mni on temperature was 11°C in 1973.

During the summer stratification,

anoxic w a t e r has ext end ed

up as far as 15 meters be n e a t h the surface for a brief
period p rior to turnover

(Moss,

1972).

The alkalinity of

Gull Lake was about 3 m-e qu i v / 1 and the pH 8.0.
The p h y t o p l a n k t o n o f Gull Lake has b e e n i ntensively
investigated b y Moss

(1972).

major growth of diatoms

Spring is ch aracterized by a

(F r a g i l a r i a c r o t o n e n s i s , Asterio-

nella f o r m o s a , Cyclote lla m i c h i g a n i a n a ) and D i n o b r y o n .
During the summer,

green algae predominate.

and c hlamydomonad green flagellates
eter)

Cryptomonads

(less than 5 pm d i a m ­

a ppe are d in abundance in the thermocline.

green algae

Blue-

(Chroococcus d i s p e r s u s , Synechoc occ us s p . )

ap peared m a i n l y in late s u m m e r and autumn.

A mod era te

growth of diatoms also appear ed in the autumn.

MA TERI ALS A N D METHODS

V e r t i c a l series of samples w e r e taken at two st a­
tions, w i t h an 8.8 liter van Dorn sampler.
located at the deepest point
(Figure 1, A)

(33 meters)

and the oth er one

One station was

of the lake

(16 meters)

was a p p r o x i ­

m a t e l y 200 meters south wes t of the W. K. Kellogg Bio log ica l
S t a t i o n b o a t house

(Figure 1, B ) .

Samples w e r e usually

taken at depths of 1, 3, 5, 7, 9, 11,
sionally,

13,

15 m.

Occa­

duplicate sets of samples w e r e taken as well as

samples of 17-m and 23-m strata at the deep station.

The

n umber of adults/8.8 liter sample ran ged fr om 0 to 227.
The sampler,

after being retrieved, was placed

v e r t i c a l l y into a 1 2-liter bu c k e t and emptied.

The sample

was then poured through an o verb o a r d d r a i n apparatus

in

wh i c h the zooplankton was collected on 75-micron netting
m o u n t e d in a piece of 7.6 cm

(I.D.)

plexi gla ss tubing.

The o v e r b o a r d drain apparatus c ons isted of a 25.4 cm ga l­
va niz ed funnel m o u n t e d against the top p o r t i o n of a 22.5 x
76 x 2.5 cm piece of wood.

The z o o p l a n k t o n-c oll ect ing net

was s upp o r t e d b e l o w the funnel by a 7.6 cm p la s t i c
elbow,

through the w o o d e n support,

17

(PVC)

and em p t i e d into the

18
lake.

This drain apparatus was attac hed to the tra n s o m of

the b oat w i t h two 15.3 cm clamps.
The zooplankton,

on the N i t e x net, were then rinsed

into a 115 ml bottle and pr ese r v e d with
malin

(Czaika and Robertson,

1968).

4%

b uff ere d for­

A Wild M-5 stereo-

di sse cti ng m i c r o s c o p e was used for sexing and counting all
diaptomids in the sample.
25X.

M o s t counting was per fo r m e d at

For m a k i n g m eta s o m e measurements,

a Leitz Or tho lux

Research M i c r o s c o p e fitted w i t h an o cular m i c r o m e t e r was
used.

Species identifications were b a s e d on the key to

freshwater calanoids by W i l s o n

(1959).

The in situ gr azing technique used in this study
was d e v e l o p e d and tested by Haney

(1970,

1971).

This

technique involves lowering a specially co n s t r u c t e d

(Plexi­

glas and stainless s t e e l ) , transparent pl ank ton trap to a
p a r t i c u l a r d e p t h in the lake.
to close the trap,

W h e n a m e s s e n g e r is dropped

a small a m o u n t of hi ghly radioactive

cells is a u t o m a tic all y released from the piston wi t h i n the
trap.

A f t e r a short experim ent al

feeding period

(10 m i n +

30 s e c ) , the trap is re trieved and the zooplankton c ol­
lected.

L a t e r the adult diapto mid s were s orted according

to species and sex,
activity.

oxidized,

and assayed for r a d i o ­

Fil te r i n g rates can be calculated by kn o w i n g the

exact r a d i o ac tiv ity of the labelled cells rel e a s e d in the
trap and the radioa ct ivi ty a cqu i r e d by the diaptomids
during the feeding period.

One of the m a j o r advantages of

19
this technique is that natural conditions are mai nta ine d
during the experi men t by using a large
pa rent grazing chamber
experimental

(8.8 liter)

trans­

(trap) w i t h an extremely short

feeding period.

L abe l l e d cells are added in

quantit ies so that the food concent rat ion in the lake w a t e r
is not significantly altered.
A n k i s tro des mus

falcatus

Ch lorella sp. (4 pm diameter)
carboys,

were c ultured in 20-liter

using Bristol's sol ution

extract.

(Starr,

1964)

and soil

These cultures were constantly aerated.

domonas reinhardtii
angulosa

(70-90 pm l o n g ) and

Chlamy-

(7-10 pm d i a m e t e r ) , Chlamydomonas

(11-15 pm d i a m e t e r ) , and Scened esm us accuminatus

(17-26 pm diameter)

were cu ltured in 500 ml E rle nme yer

flasks using Difco algal broth.

A l l cultures were ex pos ed

to a 12 -ho ur light,

12-hour dark cycle wit h "daylight"

fluorescent lamps.

Cultures were k e p t at r o o m temperature

(19-23°C).
A he mo c y t o m e t e r

(AO Spe n c e r Bright-Line)

to e stimate the c o n c e n tra tio n of cells.

was used

The labelling

process was st arted several days be f o r e the pro pos ed
ex p e r i men tal date.

An es timate of the m i n i m u m qua ntity of

cells req uired for each e x p e r i m e n t was made and an amount
approxi mat ely two times as great as this es timate was then
wi thd r a w n from the appropri ate culture.

The algal s us­

pe nsion was then centr ifu ged for 5 minutes and the culture
m e d i u m dec anted by means of a disposa ble syringe.

The

20
cells were then res usp end ed in di stilled w a t e r and usually
200 microcu rie s of aqueous 14c-NaHC0^ was added as ra dio ­
active label.
Incubation took place at room temperature w i t h two
60-watt incandescent lamps for illumination.

The s u s ­

pe nsion was st irred by means of an e lec t r i c m agn eti c
stirrer.

The period of incubat ion was usually 72 hours.

At the end of the incubation period,

the labelled su s­

pe nsion was centrifu ged for 5 minutes,

the liquid decanted,

and the cells resuspended in d i s t i lle d water.

This process

of centrifugation and resusp ens ion was re peated three times
to insure complete removal of n o n p a rt icu lat e ^ C .
the last centrifugation,

the cells were

After

resusp end ed in lake

w a t e r that had been filtered through a Mi llipore membrane
filter

(47 m m diameter,

0.45 pm pore size).

An aut omatic E p p e n d o r f m i c r o l i t e r pipette was used
to measure and transfer an exact a mount of
algae into the small g razing c hamber p i s t o n
ity) .

14

C- l a b e l l e d

(4 ml c a p a c ­

The final con cen tra tion of la belled cells in the

gr azing cha m b e r was 10^ cells/ml

for small cells

s p . , Chiamydomonas r e i n h a r d t i i ) and 10
larger cells.

(Chlorella

ce lls/ml for the

This qua nti ty of labelle d algae translates

to about 5-15% addition to the n umber of na tural cells
co ntained in the grazing chamber.
for an experimental series.

Four pistons w e r e used

These pistons w e r e filled in

21
the laboratory so as to max i m i z e the accuracy of the q u a n ­
tity of labelled cells pl a c e d in each piston.
Two 50-microliter samples of labelled cells were
filtered through Millipore mem brane
size)

filters

(0.45 pm pore

and the filters all o w e d to dry at r o o m temperature.

Two s imilar samples w ere taken at the end of the e x p e r i ­
mental day.

These filters were later assayed for r a d i o ­

activity in 15 ml Fluor all y T L A

(Beckman)/toluene.

experiments were performed, during the summer,
4-meter a l u m i n u m boat.
series.

The

using a

A tent was employed for the ice

A vertical series of samples was usually taken

several hours before b e g i n n i n g the feeding experiments for
the p urpose of identifying the d epth at w h i c h the adult
di aptomid density was the greatest.

Feeding experiments

were p e r f o r m e d on days w h e n the w e a t h e r was sunny.

Daytime

feeding experiments were con ducted be tween 1300 and 1700
hours and nighttime ones be t w e e n 2300 and 0200 hours.
A t the be gin n i n g of this study,

two series of

gr azi ng experim ent s were carried out to determine the
appropriate length of time for a dia ptomid feeding e x p e r i ­
ment.
times

Each series covered a range of e x p e r ime nta l feeding
(5 to 30 m i n u t e s ) .

The experim ent s were p erf orm ed at

the same depth and a cco rding to a rando miz ed scheme to
avoid a pos sible t i m e - r elat ed bias.

The results of these

time-series i ndi cated that a change in the adult d iap tom id
uptake rate o c c u r r e d after 15 minutes of feeding.

22
Therefore,

10-minutes was selected as the length of feeding

time for all future d iap tomid feeding experiments.
(1966)

Richman

reported that Diaptomus oregonensis adults did not

release fecal pellets during the first hour of feeding wi th
an experimental food concentration of 38,000 Chlamydomonas
cells/ml.
An individual experime nt involved the ins ertion of
a piston, previously filled w i t h labelled cells in the
laboratory,

into the grazing chamber and lowering the c h a m ­

b e r to the appropriate depth.

A me sse n g e r was immediately

d r opped to close the chamber and activate the experiment.
Af t e r 9 minutes,

the chamber was quickly r aised to the su r­

face and s trapped onto the e mptying apparatus

in the boat.

The w a t e r from the chamber was then allowed to pass through
a 75 pm Nitex net and the w a s t e w a t e r collected in a 12liter bucket.

A p p r o x ima tel y 40 seconds was required to

empty the chamber.

The N i t e x net with the zooplankton was

immediately p lunged into a container of soda w a t e r
and R i g l e r , 1967).

(Burns

The car bon a t e d soda w a t e r killed the

zooplankton wi tho ut causing defecati on or regurgitation.
After about one minute,

the zooplankton were rinsed into a

bottle and pre se r v e d w i t h 4% b u f f e r e d formalin.

Timing the

feeding p e r i o d began w h e n the cha mber doors closed and
ended w h e n the ch amber was completely empty.
was used for this timing.

A stop watch

The wa s t e w a t e r was transferred

from the b uck et to ci 2 0-liter plastic carboy.

23
The p res e r v e d samples w e r e examin ed with a W i l d
stereo-d iss ect ing microscope and by means of Irwin loops,
the adult diaptomids were sorted according to species

and

sex and then transf err ed onto 7 c m strips of filter pa per
(Whatman,

41 Smoke T e s t ) .

The cop epodid V stage of D.

oregone nsi s was also collected w h e n present.

These strips

of filter paper and animals w e r e then folded and pressed
into pellets by means of a p e l l e t press.

These pellets

were then combusted in a Packard Tri-C arb Sample O x i d i z e r
(Model 305).

The evolved CO

was collected into ethanola-

mine in 15 ml P P O / bis -MS B/t olu ene
lation mixture.

(15 g/1,

1 g/1)

scintil­

This p roc edure was used to avoid the

pr obl em of self-abs orp tio n of the w e a k beta radiation by
the animals.

A Beckman LS-150 equ i p p e d with A u t o m a t i c

Quench C o m p e n sat ion was used to assay sample radioactivity.
This Beckman s y s t e m automatically compensates for varying
quench by m eas u r i n g the degree of q uen ching for each sample
by the Ex ternal Standar d-C han nel s Ratio method.
carbon-14 efficiency is gr eater than 90%.

Its

Each vial was

counted for 20 minutes w h i c h y iel d e d a two-sigma s t a t i s ­
tical c ounting e r r o r of 2-7%.

B a c k g r o u n d radiation

(Beckman Reference Background,

Argon-Toluene)

was subtracted from each sample.

of 40 cpm

RESULTS
Te mporal D ist rib uti on
The data p r e s ent ed in Figure 2 represent 60 v e r ­
tical series of samples.

The total n um b e r of adults

c o lle c t e d in each series was di vided by the nu m b e r of sa m­
ples taken in that series.
mo nthly basis.

The means w e r e ave raged on a

The two species exh ibi ted st rik i n g l y sim i­

lar p op ula t i o n trends in Gull Lake during 1972 and 19 73.
The overwint eri ng adult populat ion s can be seen to have
almost d i s a p p e a r e d by June.

The fall crash of the sum mer

adult populations o c c u r r e d during October.

By November,

the adult p o p u la tio n of both species h a d reached a level
si milar to that of spring and summer.

Only D_^ minutus were

found carrying eggs during Nov e m b e r and December.

Since

the data p res ented here do not pr ovide a clear picture of
wi nte r pop ula t i o n levels,

it is di ffi c u l t to d isc ern

w h e t h e r these w i n t e r adult p o p u l a tio ns represe nt single
generations or the o v e r la ppi ng of two generations.
trivoltine

(three generations/annum)

The

hypothe sis w o u l d p r o ­

pose that the s pring r e p r o duc tio n gave rise to the summer
adults

(first g e n e r a t i o n ) .

gave rise to the fall adults

The early summer rep rod uct ion
(second g e n e r a t i o n ) .

24

The late

1973

1974

ADULTS

/ SAMPLE

20

20

MONTHS

Figure 2,

Seasonal distribution of Diaptomus minutus
and D. oregonensis adults in mean numbers/
8.8 Titer sample.
Sample means were
averaged on a monthly basis.

26
summer r e p r od uct ion developed much more slowly due to the
au tumn de crease in w a t e r temperature.

Alternatively,

a

di f f e r e n t type of egg may have been pro d u c e d during late
summer w h i c h required a cold stimulus
tr igger the b e g i n n i n g of d evel opm ent

(fall overturn)
(Cooley,

1971).

to
These

individuals r eached ma tur i t y about March and pro duced the
spring pulse of reprod uct ion
On the other hand,

(third g e n e r a t i o n ) .

the b ivo l t i n e hypoth esi s w oul d

pr opose that the w i n t e r p o p u l a t i o n levels are the result
of the e xte n d e d summer r eproductive period.

D e v e l op men t of

eggs p r o d u c e d during early summer p r o c e e d e d rapidly due to
hi g h e r w a t e r temperatures and gave rise to the fall adult
peaks.

As the w a t e r cooled during late summer and fall

de v e l o pme nt was ret arded so that there was

a continuing

input of individuals a t t a i nin g m a t u r i t y t hro ug h o u t the
period of ice cover.
ensis

Birge

(1898)

found that

oreqon-

pro d u c e d a fall g e n e r a t i o n only in some years in

Lake M e n d o t a and felt that this was c o r r e l a t e d to the w a t e r
temperat ure of late summer.

Lai and C a r t e r

the life cycle of EK_ oregonens is

(1970)

in S unf i s h Lake,

studied
Ontario,

and found three g e n e r a t i o n s / a n n u m d uring two of three years
studied.

These authors presume that D . o r e g o n e n s i s p r o ­

duced r esting eggs d uring the y e a r w h e n there was no fallw i n t e r generation.

The studies of Co m i t a and A n d e r s o n

(1959), H a z e l w o o d and P a r k e r
(1968)

as w e l l as others

(1961),

and Sa w c h y n and Ha mme r

indicate c learly that there is a

27
w i d e range of responses by diaptomids to the w h o l e complex
of e n v i r on men tal conditions.
mental time,

This wide range of d e v e l o p ­

nu m b e r of annual generations,

etc.,

is ind ica ­

tive of a large amount of p hys iol ogi cal plastici ty of
species of D i a p t o m u s .
Consequently,

in the absence of strong evidenc e for

the trivoltine hypothesis,

I p ropose that it is likely that

both species p r o d u c e d two generations/annum, while noting
that only D^_ minutus pr od u c e d eggs immediately after the
fall o v e r t u r n .
The adult patterns i ndi cated in F igure 2 fail to
su pport the hypothes is

that the life cycles of these two

species are temporally dis pl a c e d in Gull Lake.
of D^_ mi nutus to
both years

The ratio

oregone nsi s was very n early 1:1 for

(Figure 3).

D^_ m inutus appeared to m a t u r e more

slowly after the 1973 spring crash.

However, n e i t h e r

species was n u m e r ica lly sup erior for g rea t e r than two
months d uring the study period.
V e r t i c a l D ist rib uti on
F o r each species,

the n u m b e r at each depth sampled

was c onv e r t e d to a p e r c ent age of the total n umber of adults
of that species

(obtained by summing ove r d e p t h ) .

grouping was done from m i d m o n t h to midmonth.

The

The p e r ­

centages of the total numbers of the species for the m ont h
at each de p t h w e r e ca lcu l a t e d and gra phe d

(Figure 4).

1974

SPECIES

C O M P O S IT IO N

1973

»

i

J

F

> —'
M

A

~

i
M

I
J

/
J

A

I
S

1! 1
O

1■ 1
N

D

|

I
J

MONTHS

Figure 3.

Variation in percentage of adult Diaptomus minutus
and D^_ oregonensis. Samples were grouped on a
monthly basis.

M O NTHS
M

A

M

DEPTH

(METERS)

V i

a

1
3
5
7
9
11
13
15
17
19

i

J

1
t

P
o
1
J

Q ftinulm

EH

D . O O f l O W f t t il

□

soX

1

__ .

H
9
s

1972
A

1

S

0

1
b
ft
3
b
p
ips

3
5
3
?
?
}
1

N
Ji

5
■b
9
5
!
b

b
b
ft
3
J
P

1973
jg ”

pr

?

3

sa
7
9

b

I
i
E=i
g

S

¥

II'
13
15‘

17
19

Figure 4.

?
ft

b
b

¥

P

b
b
J

s
a.

p
ft
ft

?

The vertical distribution of adults of Diaptomus
minutus and D_;_ oregonensis in Gull Lake.

30
Both species w e r e rather u nif ormly distrib ute d
throughout the upper 13 meters of w a t e r during fall and
winter.

As the s ummer s t r a t ific ati on intensified,

the

adults beg an to concentrate in the m e t a l i m n i o n during
af ternoon

(1200-1700 h o u r s ) .

The d e p t h at w h i c h this co n­

centration o c c u r r e d was o bvi ously deeper in 1973 than in
1972.
disk,

Tr ansparency data,

co llected b y means of a Secchi

showed a s i g n i fic ant ly higher transparency in 1973

compared to 1972

(Lauff, et a l ^ , in p r e p a r a t i o n ) .

increased w a t e r clarity was

34% for the June 15-July 15

pe r i o d and 43% for the July 15-August 15 period.
gests that the diaptomids

The

This sug ­

responded to increased light

pe net rat ion by mo vin g into de e p e r w a t e r during the summer
afternoons since the summer temperature regimes for 1972
and 1973 were quite similar.
The ex tensive overlap of the v ertical di stributions
of the two species show clearly that they share the same
space during the 1200-1800 hours p ort i o n of the day.
this reason,

F or

no statistics were p e r f or med to e val u a t e the

overlap.
Da y-n i g h t series w e r e done at the nea r-s h o r e sta­
tion on two dates d uri ng the summer of 1972

(Figure 5).

The p urpose of these series was to a scer t a i n if the adults
of b o t h species mi gr a t e into the ep ilim n i o n at night.
During the day,
co llected were

5% of the total nu m b e r of adult D^_ minutus
found in the upper 5 meters w h i l e 9% of the

DAY

N IG H T

20

DEPTH

(M )

40

Figure 5.

The vertical distribution of adult Diaptomus minutus
and D^_ oregonensis in two day-night series of
July and August, 1972.

32
D. oregonen sis adults were

found in this layer.

The night

samples of the upper 5 meters conta ine d 55% of the adult
D. minutus and 37% of the adult

oregonensis.

The summer

nightti me be ha v i o r of these two diaptom ids co nsi s t e d of a
ge neral m ove m e n t into the epilimnion.

The ov e r a l l effect

was to p roduce a rather un iform dis t r i b u t i o n through out the
w a t e r column at the near-s hor e station.

This dis t r i b u t i o n

was similar to the daytime d i s t r ibu tio n d uring the winter.
The total nu mbers of adults col lected at n i g h t on
both dates w e r e be tw e e n two and three times as g r e a t as the
daytime totals.

The reason for the increase in numbers of

adults co lle c t e d at n i g h t was not obvious.

Nevertheless,

the species ratio was c o n s i ste ntl y 1:1 for day and ni ght
series.

If the night tim e ratios w e r e m a r k e d l y d i f f e r e n t

from the da ytime ones,

it w o u l d s uggest d i f f e r e n t i a l h o r i ­

zontal mo vements by one or both species.

This was not

i n dic a t e d by these two day -n i g h t series.
Size M eas ure men ts
The me an + 2 SE and the m e a n + 2 SD, p r e s e n t e d
gr aph ica lly

(after Hubbs and Hubbs,

1953)

in Figure 6,

in dicated no size ove rlap be t w e e n the two species.

D.

o r e g o n e n s i s males w e r e always larger than D^_ minutus
females by factors o f 1.29,
October).

1.26,

1.35,

1.27

D^_ o r e g o n e n s i s males w e r e always

mi nutus males by factors of 1.41,

1.38,

(Februarylarger than D.

1.36,

1.35

& niinytus

D. oregonensis

FEB

JUN

AUG

OCT

0.60
METASOME

Figure 6.

1.00

0.80
LENGTH

(mm)

Variation in size of Diaptomus minutus and
oregonensis
in February, June, August, and October, 1972.
(small peak = mean; length of white bar = 4 SE;
length of underline = 4 SD)

34
(February-October) .

D_;_ oregon ens is

larger than D^_ minutus
1.43,

1.32

females were always

females by factors of 1.43,

1.44,

(February-October).

The males and females of both species were larger
in w in t e r than in summer.

Males of

the least seasonal variation,

m inutus exhibited

12%, w h i l e the females of

D. oregone nsi s were 24% l arger in win t e r than in fall,
gr ea t e s t seasonal variation.

the

These seasonal changes in

body length are smaller than those reported by Tom ika wa
(1972)

for Sinodiaptomus volkanoni in small ponds in Hyogo

Prefecture,

Japan.

Turvey

(1968)

rep orted seasonal v a r i ­

ations of 8-13% in Clarke Lake,

Ontario, where

coexist ed w i t h D^_ o r e g o n e n s i s .

In a study of

in Lake Washington,

Comita and And er s o n

(1959)

minutus
ashlandi
found

seasonal variations similar to those in Gull Lake b u t the
summer adults wer e larger than the w i n t e r adults.
(1960)

Deevey

d isc u s s e d the relative effects of temperature and

food on seasonal var iat ion in b ody length in m a r i n e calanoid copepods.

While

the patte rns and degrees of seasonal

variation in body length are not u n i f o r m in expression,
signific ant seasonal var ia t i o n in bo dy length w o u l d appear
to be well d o c u m e n t e d and consequently,

it is essential

that any di scu s s i o n of pos s i b l e character d i s p l a c e m e n t in
diaptomids
factor.

include c o n s i de rat ion of this seasonal variation

35
The raetasome lengths of diaptomids
lections)
Lake,

of Gull Lake are c omp a r e d w i t h those of Sherman

in which D^_ minutus o c c u r r e d alone,

Lake and Three Mile Lake,
alone

(February col ­

and Big Gilkey

in w h i c h D^_ oregonensis occurred

(Table 1).

Table 1.— Var iation in mean m eta s o m e length (mm) of Diaptomus mi nutus and
oregone nsi s in February,
1972. (n>20 for each category)
D. minutus
male

D . o reg one nsi s

female

Gull Lake

0. 635

0. 694

Sherman Lake

0. 721

0.810

male

female

0. 896

0. 992

Big G ilkey Lake

0.868

0. 941

Three Mile Lake

0.938

1. Oil

The

minutus males and females of Gull Lake were

smaller than those of Sherman Lake by 12% and 14% r e s p e c ­
tively.

D_;_ o regonensis males and females of Gull Lake were

larger than those of Big Gilkey Lake by 3% an d 5% r es p e c ­
tively.

These differences are s ignificant at the 99% level

(P<0.01)

as judged by the Stu de n t ' s

"t" test.

The w i n t e r

data from these three lakes su p p o r t the ch aracter d i s p l a c e ­
ment hypoth esi s in that D_;_ min utus were s maller w h e n
coexisti ng in Gull Lake w i t h D^_ oregonen sis than w h e n they
oc cur red alone in Sherman L ake and

oregon ens is w ere

larger in Gull Lake w her e they c o e x i s t e d w i t h D_^ minutus

36
than w h e n they o ccu r r e d alone in Big G ilkey Lake.
w h e n the

However,

oregonen sis of Gull Lake are compared w i t h the

D . oregonensis of Three Mile Lake,

those occurring alone

are equal to o r larger than those coexisti ng with D_^ m i n ­
utus .
Turvey

(196 8) reported m e a n m etasome lengths

m e r collections)

for D^_ minutus and D_^ oregon ens is from six

headwater lakes where they co-occurred,

2 5 lakes where D .

oregone nsi s was found alone, and 18 lakes where
oc cu r r e d alone.

(sum­

These mean lengths,

minutus

together with m e a s u r e ­

ments I made of animals collect ed from several local lakes
are p r e s e n t e d in Table 2.
Table 2 .- - C o m p ari son of mean s um m e r met aso me lengths (mm)
of Di apt omu s minutus and
o reg one nsi s of Gull
Lake, Sherman Lake, and Three Mile Lake wi th
those report ed by Turvey (196 8) from Ontario.
D. minutus

D. oregonensis

male

female

male

female

Gull Lake

0.57

0.60

0. 77

0 .86

Turvey

0. 59

0.65

0.82

0. 89

Sh erman Lake

0. 61

0.65

Tu rvey

0.60

0.66

Three M i l e Lake

0. 80

0. 89

Turvey

0.79

0. 88

(6 lakes)

(18 lakes)

(25 lakes)

37
The diaptomids of Gull Lake are from 3% to 7%
sm aller than the means

from Tu rvey's study.

The Sherman

Lake data as well as those from Three Mil e Lake cor res pon d
closely to the means pre se n t e d by Turvey.

The males of

D. minutus of Gull Lake w e r e 6% smaller than the mean
length from Turvey*s 18 lakes w h e r e D^_ minutus oc cur red
alone and the females w e r e
o c c u r r i n g alone.

8% s maller compared to those

Al though the differen ces are r a t h e r s m a l l ,

the o b s e r va tio ns co n f o r m to the charac ter displace men t
hypothesis.

On the other hand,

ensis in Gull Lake are s mal ler

both sexes of D^_ o r e g o n ­
(2-3%)

than the Turvey means

for this species oc curring alone and thus do n o t support
the c har a c t e r d i s p l a cem ent hypothesis.
Gr azin g E xperiments
The iri situ gr azi ng technique of Haney

(1970,

1971)

was used to obtain all the feeding data of this study.

The

technique is d esi g n e d to collect inform ati on from w hic h
filtering rates of zooplankton can be calculated.

The size

and type of the algae chosen to be labelled s hould be
a p p r o pri ate for the animals of ex per ime nta l interest.

If

the species of zooplankton to be i n v e s tig ate d is known to
have a lower limit of filterable p article size of 100 u m ^ ,
it w o u l d be i l l - a d v i s e d to use a labelled cell of 60 um^
since this should result in a filtering rate of zero using
the in situ g razing technique.
to conclude that the organisms

It w o u l d not be ap propriate
in q ues t i o n were not

38
filtering during the experiment b u t r ather that they were
unable to handle cells with a volume of 60 ym^.
same manner,

In the

if a filtering rate of 3 m l/a n i m a l / d a y is

o b tained w h e n using a type of cell w i t h a volume of 1000
3
yin and a filtering rate of 1 m l / a ni mal /da y w h e n using a
cell w i t h a volume of 4 00 0 ym^,

the ap propriate co ncl usi on

w o u l d likely be that the o r g a n i s m under study is able to
handle the 1000 ym^ cell be t t e r than the 4000 ym^ one.
The five species of green algae used d u r i n g this
study are listed in Table 3.

Clearly,

size is only one of

several charac ter ist ics of labelled algae w h i c h m a y be
im portant to the test animals in terms of their ability to
handle the cells and consequently,
f i ltering rate
McQueen,

(Fryer,

to ef f e c t the resulting

1954; Conover,

1966; Pepita;

1970; P a f f e n h o f e r and Strickland,

1970).

1965;
Ankis-

trodesmus f a l c a t u s , a s olitary cell of a c i r c u l a r or semilunate shape

(2-3 ym diameter)

w i t h apices gra dually

tapering to fine p o i n t s , was used for 15 experi men ts on
four dates during July and August,
rates ob ta i n e d using A n k i s t r o d e s m u s
Figure

7.

The n igh ttime

19 73.

The filtering

falcatus are shown on

(2300-0200 hours)

results show the

e x p e c t e d pat t e r n of in cre a s i n g filtering rates w i t h
i n c r e a s i n g body lengths

(Brooks and Dodson,

1969; Burns and R i g l e r , 1967; McMahon,

1965; Burns,

1962).

The daytime

filtering rates, w h i l e lower than ni ghttime rates,

also

s e e m to follow this p a t t e r n except for the largest size

39

DAY
•*
NIGHT 0 0

3.0-

□
E
c

p

E

2.0-

LU
O
z
OC
UJ
►“
u.

0.80
F

M

METASOME

Fi gur e 7.

LENGTH

(mm)

C o m p a r i s o n of the summer d ayt ime and n i g h t ­
time filtering rates of Diaptomus
mi n u t u s ( # ) and
ore gone ns is C ^ ) » using
A n k i s t r o d e s m u s falcatus (mean + S E ) .

40
category,

D_^ oregonensis females.

tering rate for

The m e a n d aytime fil­

oregonensis females was only about 37%

of the e x p e c t e d filtering rate,

b a s e d on a linear r e g r e s ­

sion line fitted to the four sma ller size categories by the
least squares method.

This depress ion e ffect was ob ser ved

in all four experim ent al series,

using Ank is t r o d e s m u s

falcatus as w e l l as those using Scene des mus
(Figure 8) and Chlamy domo nas

reinhardtii

accuminatus

(Figure 9).

Table 3.— Size measurem ent s of the five species of green
algae used in the in si tu grazing e x p e r i m e n t s .

Cell Type

Diameter
(pm)

C h l o re lla sp.
Chlamydo mon as

3.6-4.5
reinhardtii

A n kis t r o d e s m u s falcatus

7.2-10.8
(68.0-90.5)
(length)

Range of
Volumes
(pm3)

Mean
Vo lum e
(pm3)

25-49

36.0

238-670

396. 3

354-466

418. 2

Chlamydo mon as angulosa

10.8-15.4

670-1906

1307.5

Scenedesmus accuminatus

17.5-26.3

1655-5406

4329.0

The results ob ta i n e d using the smallest alga,
3
C hlo rel la sp. (volume 36 pm ) are shown in F igure 10.
sm allest size category,

The

mi nutus males, h a d the highest

filtering rates and an apparen t trend of d ecr eas ing fil­
tering rates w i t h increasin g size is e vi d e n t in the ot her
four categories.

Some of this reverse tendency m a y be

e x p l a i nab le in terms of the pre vio u s l y n o t e d daytime

41

2.0-

FILTERING

RATE

(m l/a n im a l/d o

3.0

1.0 -

M

0.60

0.80
F

CV

METASOME

Figure 8.

1.00
r

M

LENGTH

(m m )

The summer da ytime filtering rates of
Di aptomus m i n u t u s ( # ) and D .
oregone nsi s ( ♦ ) , using Scenedesmus
accuminatus (mean + S E ) .

42

day
♦ •
NIGHT 0 O

2.0

FILTERING

RATE

(m l/a n im a l/d a

3.0-

,o
1.0 -

* 0.60 ▼
M

F

C

▼
V

METASOME

Figure 9.

▼ 'oSo

'

▼

«

100

F

LENGTH

(m m )

Com par i s o n of the summer d aytime and n i g h t ­
time filtering rates of Diaptomus
mi nut us ( + ) and D^_ oregon ens is ( ♦ ) , using
C h l a m ydo mon as reinhar dti i (mean + S E ) .

43
filtering rate depress ion b u t there is the strong s u g ­
g e stion that

jninutus can handle or capture the C h l o r e l l a -

sized cells more e f f e c tively than can

oregonensis.

This hypothesis is based on the o b s e r vation that
D. oregonensis

females daytime filtering rates were c a l c u ­

lated to be 2 m l / a nimal/day
accuminatus
(Figure 10),

(Figure 8), using Scenedesmus

(volume 4300 pm ) and 0.66 ml/an i m a l / d a y
using Chl or e l l a sp.

(volume 36 p m ^ } .

Since

these experiments were p e r f o r m e d during the same time
period

(July-August)

and under sim i l a r conditions,

appears that the filtering rates of

oregonensis

it
females,

for the smaller C h l o r e l l a s p . , are much lower bec a u s e these
animals do not ha n d l e o r capture Chlor e l l a sp.

as e f f e c ­

tively as they capture larger cells like A n k i s trodesm u s and
Scenedesmus.

The filtering rates of D^_ o r e g onensis males

(Table 5) also support this hypothesis.
Scenedesmus accuminatus is typically a co l o n y of
four cells in a curved series, each cell s t r o n g l y lunate
w i t h sharply poi n t e d apices.

The co n v e x walls are a d j o i n e d

inwardly and the concave faces dire c t e d out w a r d
1962).

A l t h o u g h some fragmentation of colonies was

observed,
ones.
for

(Prescott,

less than 20% of the labelled cells w e r e single

W i t h the e x c e p t i o n of the filtering rates c a l c u l a t e d
minutus males,

the hig h e s t daytime filtering rates

were o b ta i n e d in experiments using the largest alga,
Scenedesmus accuminatus

(Table 4 and 5).

44

3.0-

c 2.0-

ac

0
U£
i

w
M

f

cv

METASOME

Figure 10.

0.80

1.00
t

M

LENGTH

(m m )

The summer daytime filtering rates of
Diaptomus minutus ( # ) and D .
o r e g onensis (+■), using Chlor e l l a sp.
(mean + SE) .

Table 4.— Day-night filtering rates of Diaptomus minutus in Gull Lake, Michigan. All data are from
summer experiments except where noted. Filtering rates are presented as mean ml/animal/day
+ SE. Animals were grouped into pellets before combustion to carbon dioxide.
Male
Day
Chlorella sp.
(36 ymJ)
Dates
Pellets
Animals

1.63+0.24

Chlamydomonas reinhardtii
(396 ym3)
Dates
Pellets
Animals

1.14+0.09

Ankistrodesmus falcatus
(418 yra3)
Dates
Pellets
Animals

1.01+0.11

Chlamydomonas angulosa
(1308 mh
Dates
Pellets
Animals

0.72(winter)

Scenedesmus accuminatus
(4329 Wm^)
Dates
Pellets
Animals

1.43+0.07

Female
Night

2
6
81

1
1
13

4
5
65

Night

0.95+0.07

2
7
85

1
2
25

Day

3
7
107
1.24
1
1
15
1.40+0.20
3
5
29
1.46(winter)
1
1
8
1.07+0.11(winter)
2
3
26

1.12+0.01
1
2
21
0.80+0.14
2
7
108
0.60(winter)
1
1
6
1.42+0.18
4
6
68

1.40+0.21
3
5
24
0.74(winter)
1
1
-5
w
0.93(winter)
1
1
8

Table 5.— Day-night filtering rats of Diaptomus oregonensis in Gull Lake, Michigan. All data are from
summer experiments except where noted. Filtering rates are given as mean ml/animal/day + SE.
Animals were grouped into pellets before combustion to carbon dioxide.
Stage V
Day
Chlorella sp.
(36 UmJ)
Dates
Pellets
Animals

0.63+0. 07

Chlamydomonas reinhardtii
(396 Pm3}
Dates
Pellets
Animals

1.04+0. 15

Ankistrodesmus falcatus
(418 ymJ)
Dates
Pellets
Animals

1.3.3+0.18

Night

Day

Female
Night

1
2
36

2
4
94

1.73
2
2
21

Day

Night

0.66+0. 05

2
6
136

Chlamydomonas angulosa
(1308 pm-*)
Dates
Pellets
Animals
Scenedesmus accuminatus
(4329 Pm3)
Dates
Pellets
Animals

Male

3
12
234
1.32
1
1
23
1.93+0.16
3
5
33

1.08+0.18

1.66+0.49

0.97+0. 17

3,31+0.46

1
2
47

1
2
48

1
2
52

1
2
46

1.72+0.11

1.85+0.33

0.95+0. 11

2.43+0.19

3
7
95

3
5
40

1.58
(winter)
1
1
9

2.42
(winter)
1
1
4

1.65
1
1
5

1
1
1

2.26+0.29

2.30*0.96
(winter)
2
2
8

2.08+0. 07

2.74+0.47
(winter)
2
2
9

3
4
33

3
8
139

3
4
43

3
5
26
2.10

47
Chlamydomonas r e i n h a r d t i i , a s p h e r ically-shap e d
alga

(volume 400 p m 3) , was used in the d a y - n i g h t series of

A u g u s t 3, 1973.

A c h a r acteristic of some of the species

of the genus Chlamydomonas is the habit of coming to rest,
losing their flagella,

and entering a q u i e s c e n t phase.

During this phase, vegetative cell divis i o n continues,
a c c o m p a nied by the secretion of mucilage w h i c h causes
c lumping

(Prescott,

1962).

While constant stirring and

the action of c e n t r ifugation tended to reduce the clumping
effect,

the size range of labelled particles was much

g r eater in experiments using cells of the genus, C h l a m y d o ­
monas , than in those using A n k i s t r o d e s m u s .
this clumping characteristic,
ut i lized only sparingly.
experiments,

the genus,

In light of

C h l a m y d o m o n a s , was

The results of the su m m e r daytime

using C h l a m ydomonas

reinhardtii

(Figure 9),

are very sim i l a r to those o b t a i n e d w i t h C h l o r e l l a sp.
(Figure 10).
ensis

The nighttime filtering rate of

oregon­

females appears to be h i g h e r than might be exp e c t e d

but since the mean represents only two pel l e t s on one date,
it is p ossible that additional e x p e r i m e n t a t i o n w o u l d show
the true m e a n to be some w h a t lower.

The n u m b e r of adult

D. minutus capt u r e d during the nighttime experi m e n t was
sufficient for only one p e l l e t for each sex.
The summer nighttime results using A n k i s t r o d e s m u s
falcatus
males,

(Figure 7) show that except for D^_ oregonens i s

all nighttime

filtering rates are h i g h e r than

48
daytime rates.

Since there was a w a t e r temperature d i f ­

ference of about 12°c
ments,

25°c)

betw e e n the surface

and the m e t a l i m n i o n

(night exp e r i ­

(day experiments,

13°C),

one m i g h t expect an increase in night t i m e filtering r a t e s .
The fact that nei t h e r of the male categories showed a s i g ­
n i f i c a n t day-night difference,

as judged by Student's

test, does not support this expectation,
night d iffer e n c e in the D^_ minutus

however.

female and

"t"

The dayoregon­

ensis V copepodid categories are significant at the 9 5%
level

(P<0.05)

and the difference for D^_ oregonensis

females was highly significant

(P<0.001).

The existence of increased summer nighttime fil­
tering rates was not enti r e l y a n t i c ipated w h e n this study
was proposed.

Nauwerck

(1959)

had actually

found h i g h e r

daytime than nighttime filtering rates for Eudiaptomus
g r a c i l o i d e s , a Eura s i a n d i a p t o m i d of comparable size to
D. m i nutus

and D^_ o r e g o n e n s i s , in Lake Erken,

Haney and Hall

(19 74)

Sweden.

Also,

could not detect day-n i g h t filtering

rate differences in Ch_ p a l l i d u s , using the in situ grazing
m e t h o d w i t h 22p - l a b e l l e d yeast cells.
Singh
calanoid,

(1972), however,

repo r t e d that the tropical

Rhinediaptomus i n d i c u s , in a shallow p o n d of

South India,

appeared to feed during the entire 24 hours

of the day but showed incre a s e d feeding activity during the
ni g h t hours.

He drew this conclusion from his study in

wh i c h he rated animals captured by placing t h e m into one of

49
three categories:
Wimpenny

(1938)

full gut,

50% full gut, empty gut.

noted that some of his data for the marine

calanoid, Paracalanus p a r v u s , suggested a greater ass i m i l a ­
tion by zooplankton at night, b a s e d on the percentage of
the gut filled w i t h food.

During laboratory experiments

to determine the filtering rates of four species of marine
plankt o nic c o p e p o d s , Gauld

(1951)

support the hypothesis of Fu l l e r

found some evidence to
(1937)

that marine c o p e ­

pods r e moved diatoms more rapidly at night.

Gauld

(1953)

attempted to explore this ques t i o n e x p e r imentally as well
as with field observations,
the test animal.

using Calanus

finmarchicus as

His laboratory observations indicated an

absence of any day-night feeding rhythm.

This observation

was supported by the experiments of Richman and Rogers
(1969).

However,

Gauld's field observations w e r e that

where vertical migration occurred,

feeding took place

m ainly at the surface and was restricted to the hours of
darkness.

In the absence of vertical migration,

he found

Calanus to be abundant at the surface and feeding c o n t i n u ­
ously throughout the 24-hour period.

These evaluations

were b a s e d on the perce ntage of the gut containing food.
Two experimental day-n i g h t feeding series were
c onducted during January and February,
was an ice cover on Gull Lake.

1974, w h e n there

During this period,

there

was no detectable vertical migra t i o n and the w a t e r t e m p e r a ­
ture was approximately 2°C

throughout the w a t e r column.

50
There was snow on top of the ice b u t due to melt i n g and
w i n d action,

it was

rather patchy.

The w i n t e r day-ni g h t

experiments were condu c t e d at 9-11 meters depth.
w i n t e r depth selection,

The

as w e l l as the summer ones, was

b a s e d on adult densities obser v e d from a vertical series
of samples

taken several hours p r i o r to the experiments.

Since the adult diapt o m i d populations w e r e quite d i s p e r s e d
throughout the w a t e r column during the winter,

it was n e c ­

essary to pool animals from several e x p e r iments in order to
o btain a suitable nu m b e r for radioactivity assay.
result,

As a

the w i n t e r data are not as extensive as those of

the summer and are more variable.
tering rates

(Figure 11),

The w i n t e r daytime fil­

using Scenedesmus a c c u m i n a t u s ,

are strikingly similar to those o b t a i n e d du r i n g the s u m m e r
even though the w a t e r temperature
w a r m as it was during summer

was only about 15% as

(14° + 2 ° C ) .

This o b s e r v a ­

tion would appear to be consistent w i t h the trend reported
by Kibby

(1971)

from his study of the effect of temperature

on filtering rate of Dap h n i a rosea after a long t e r m a c c l i ­
ma t i o n to low temperature.

On the other hand,

w h i c h u tilized a short pe r i o d

studies

(less than 48 hours)

of

temperature a c c l i mation have shown Dap h n i a to exh i b i t f i l ­
tering rate increases of 200% over 5°C
1967; McMahon,

1965;

Nauwerck,

(Burns and Rigler,

1959).

There w e r e no p_^ o r e g o nensis V copepodids
d u ring the w i n t e r experiments.

found

The d e p r e s s i o n of the

51

SUMMER • ♦
WINTER O O

3.0-

2.0

1L

1.00

0.80
M

F

CV

METASOME

Figure 11.

F

M

LENGTH

(m m )

C o m p a r i s o n of w i n t e r and summer daytime
filtering rates of Diaptomus minutus ( # )
and
oregonensis ( ♦ ), using
Scenedesmus accuminatus (mean + S E ) .

52
daytime filtering rates of D_^ oregonensis
d uring the w i n t e r

(Figure 11).

females pers i s t e d

The w i n t e r day-n i g h t d i f ­

ferences appear to be less obvious in experiments using
Scenedesmus accuminatus
C h 1amydomonas

angulosa

(Figure 12).
(Figure 13)

Alth o u g h the data for

suggest that the trend

of h igher nighttime rates p e r s i s t e d despite the absence of
w a t e r temperature difference.
a b r o a d l y ovoid cell

Chlamydomonas a n g u l o s a ,

(volume 1300

y m ^ ) , w a s used in the

d a y - n i g h t experiments of Janu a r y 16,

1974, only.

53

DAY
NIGHT 0 0

2.0

FILTERING

RATE

(m l/o nim al/day)

3.0-

1.0

\

▼ o.6o^

' r ~'-----^ “ aso

M

CV

t

M ETASO M E

F igure 12.

'

*

M

t.bo

F

LE N G TH

(m m )

C o m p a r i s o n of w i n t e r daytime and n i g h t ­
time filtering rates of Diaptomus
minutus (# ) and D_;_ or e g o n e n s i s C♦ ) #■
using Scenedesmus a c c u m inatus {mean + S E ) .

54

DAY
NIGHT O O

3.0.

2.0

oc

W

0.80

METASOME

Figure 13.

1.00
F

M

LENGTH

(m m )

C o m p a r i s o n of w i n t e r daytime and n i g h t ­
time filtering rates of Piaptomus
m inutus ( + ) and
oregonensis
)t
using C h l a m ydomonas a n g u l o s a .

DISCUSSION
Habitat Coexistence
The theory of competitive exclu s i o n w o u l d seem to
p r edict that in the relatively homogeneous limnetic zone
the p l a n k t o n communities w o u l d tend toward a species s t r u c ­
ture consisting of one species p e r genus.
(1961)

Hutchinson

discu s s e d the apparent p a r a d o x bet w e e n the p r e d i c ­

tion of this theory and the actual observations of numerous
species of p h y t o plankton coexisting in the same relatively
u n s t r u c tured limnetic environment.

Basically,

he p o s t u ­

lates that due to the constant changes of the limnetic
environment,
ibrium.

there is a perma n e n t failure to achieve e q u i l ­

He also developed the idea that in freshwater,

species of phytoplankton may have w e l l - d e f i n e d benthi c
littoral niches from w h i c h they may invade the limnetic
zone.
P ennak

(1957)

found that the limnetic zooplankton

communities w h i c h he studied in Colo r a d o confo r m e d to the
expectations of the e x c l usion principle.

However, other

studies have shown that the co-occurrence of sympatric
p opulations of planktonic copepods of the same trophic

55

56
level are not rare
1960;

(Langford,

Rigler and Langford,

Turvey,

1968; Smrchek,

19 38; Davis,

1954; Wells,

1967; H a m m e r and Sawchyn;

1973).

Anderson

19 68;

(1970) has d e m o n ­

s t rated that the larger species of the genus Diaptomus
at least facultative,

predators.

Consequently,

are,

the a s s u m p ­

tion should not automatically be made that all diaptomids
b e l o n g to the same trophic level.
(1972)

As an example,

found D^_ shoshone co-occurred with

in a shallow pond of Colorado.

Sprules

coloradensis

Although some of the d e v e l ­

o p m ental stages of these two species may w e l l b e l o n g to the
same trophic level,

the adult D^_ shoshone

(2.47 mm)

are

functionally predators w h i l e the adult Dj_ coloradensis
(1.26 mm)

are filter-feeding omnivores.

Since numerous examples of diapt o m i d coexistence
are well-known,
are r e lated to

it is of interest to determine w h a t factors
(or responsible for)

this coexistence.

The

inter e st in this situation is h e i g h t e n e d by the rather
limited possibilities

for separation of "habitat"

(place)

niches in the relatively unstructured plankt o n i c e n v i r o n ­
ment

(Elton,

1946; Pennak,

1957; Hutchinson,

cock

(196 7) concluded that in Clarke Lake, Ontario,

mi nutus successfully coexi s t e d w i t h
of at least two mechanisms:
separation.

SanderD.

oregonensis by means

size difference and seasonal

She found that, wh i l e there was considerable

ov erlap of adult numbers,
of

1961).

the pattern of change in numbers

minutus was significantly different from that of D.

57
o r e g o n e n s i s in all four years of her study as tested in the
analysis of variance.

In Clarke Lake,

seasonal m a x i m u m in spring w h i l e
m a x i m u m in summer.

In contrast,

D^_ minutus had a

oregonensis had its
the two species in Gull

Lake did not exhibit this separation during the presen t
study.

The studies of these two lakes agree that the two

species were not separated vertically.
(1967)

Rigler and Lan g f o r d

found a statistically significant difference of

2.5 + 0.8 meters between the daytime mean depth for D.
minutus and iK_ oregonensis adults in 19 lakes of southern
Ontario.

However,

Turvey

(1968)

obse r v e d that a frequency

d i s t r i b u tion of m e a n depth difference in the Ri g l e r and
L a n g f o r d survey w o u l d show that for over 50% of the lakes
in question,
event,

the difference was a m e t e r or less.

In any

since the epilimnion is defined as a w a t e r mass

w i t h little or no thermal s t r a t ification and w i t h constant
m i xing

(Ruttner,

1963),

it w o u l d seem to be diffi c u l t to

ascribe a functional meaning to a difference betw e e n m e a n
depths if both means were loc a t e d in the epilimnion.
tainly,

Cer­

a more careful evalua t i o n of conditions existi n g

1 o r 2 m eters apart is necessary before statistical d i f ­
ferences can be i n t e r preted biologically.
Recall that only the adults of these two species
were considered in this study.

With a comp l e x life cycle

consi s t i ng of 12 p o s t - e m b r y o n i c life history stages,

it is

clear that conclusions based on a study restricted to the

58
a dult stage m u s t be held as tentative until m o r e info r m a ­
tion about the dynamics of at least the last three copep o d i d stages is obtained.

Mul l i n and Brooks

(1970)

sug­

g e s t e d that the marine c a l a n o i d s , Rhincalanus and Calanus
may achieve niche separation during the naupliar stages
rather than as adults.

These authors were unable to rear

Calanus pacificus nauplii on D i t y l u m brightwelli but were
successful in rearing Rhincalanus nasutus nauplii on this
diatom.
occur,

While separation of food niches of nauplii may
the hypothesis has not y e t been suppo r t e d by data.

Czaika and Robertson

(196 8) have developed a key for the

i d e n t i f ication of the s i x copepodid stages of the diaptomids of the Great Lakes.

They note that there is c u r ­

rently no way to separate the six naup l i a r stages to
species.
H utchi n s o n

(1967),

citing the w o r k of Ravera

(1954),

o b s e r v e d that even though each coexisting diaptomid species
may share the same e n v i r onment

(biocoenosis), each species

m a y e x hibit a diffe r e n t generation time and/or numbers of
generations/annum.

So that the regularity of the seasonal

ecological variations may enable a univoltine species to
coexist w i t h a m u l t i v o l t i n e one.
In summary,

the pres e n t study has not revealed the

two species occup y i n g different space niches.

In the

terms of my operational definition of coexistence,
minutus

and D^_ oregonensis adults in Gull Lake had

D.

59
e x t e n s i vely ov e r l a p p i n g vertical distributions and adults
of b o t h species m o v e d into the epilim n i o n at ni g h t

(summer).

The third criterion of the defini t i o n prop o s e d that both
species should be p r e s e n t in relatively similar p r o p o r ­
tions.

Figure 3 shows that this condi t i o n is also met.
The popula t i o n curves

quite closely.

(Figure 2) track each other

A spring and fall die-off of adult p o p u l a ­

tions was observed in 1972 and 1973.

While no defini t i v e

reason for these events can be given,

their occurrenc e

seems to coincide w i t h the formation of the summer thermal
s t r a t i f ication and its subseq u e n t b r e a k u p in the fall.
Al t h o u g h these events may well be synergistic phenome n a
involving other factors,

in addi t i o n to w a t e r temperature.

To w h a t factor may the contro l l e d amplitude of the
intervening periods be attributed?

Paine

(1966)

offered

an h ypothesis w h i c h stated that local species diversity
is d i r ectly related to the e f f i c i e n c y w i t h which predators
p r e v e n t the m o n o p o l i z a t i o n of the m a j o r environmental
requisites by one species.

He was able to show that the

removal of the top carnivore from an intertidal community
p r o d u c e d a decrease in species diversity.
of p r e d a t i o n allowed for a "winner"

The absence

in the competitio n for

space.
Burbidge

(1967)

reported that A m e r i c a n smelt in

Gull Lake consumed copepods ma i n l y du r i n g fall and winter.
He did not routinely d i f f e r e n t i a t e betw e e n cyclo p o i d and

60
c a l anoid copepods but he did observe that diaptomids were
i n c luded in the smelt diet.
stratification,

During the pe r i o d of summer

smelt occu r r e d p r i m arily in the h y p o l i m n i o n

d u ring the daytime but moved into the m e t a l imnion at night.
Consequently,

smelt and adult diaptomids did not appear to

share the same space niche during summer.

His gut analysis

data show that copepods represented less than 1% of the
average total volume of food in the gut during summer,
during fall and 11% during winter.
and o t h e r planktivorous

6%

The role of y o u n g smelt

fishes pre s e n t in Gull Lake is as

yet unknown.
A m o n g the zooplankton of Gull Lake,
p r e d ators pre s e n t in significant numbers,
the summer.

there w e r e four

at least during

They w e r e Mesocyclops e d a x and Cyclops bicus-

pidatus thomasi

{cyclopoid c o p e p o d s ) , L e p t o d o r a kindtii

(clad o c eran), and Epischura lacustris

(calanoid c o p e p o d ) .

The p r e d a t i o n effect of Mesocyclops e d a x on a popula t i o n of
Diaptomus

floridanus has been exam i n e d by Co n f e r

(1971).

He found that the preda tion by M_;_ e d a x was highly selective
for diaptomids rather than for cladocerans.

The m a x i m u m

estimates of in situ pr edation rate for two Florida lakes
were 1% a n d 6% of the s tanding crop of copepodids per day.
In Mar i o n Lake, British Columbia,
e s t i m a t e d that the Cyclops b i c u spidatus

McQu e e n

(1969)

thomasi copepodids

IV and V and adults could have eaten 30% of the standing
crop of D^_ oregonensis nauplii during the summer of 1967.

61
L a b o r a t o r y experiments indicated that C_;_ b_^ thomasi did
n o t eat m a n y diaptomid c o p e p o d i d s .
Episc h u r a lacustris was p r e s e n t in Gull Lake in
low densities during the present study but they have been
shown to be predators upon diaptomid nauplii and,
extent,

early copepodids

(Main,

to some

1962).

Lepto d o r a kindtii is a fluid feeding predaceous
cl a d o c e r a n w h i c h was also found in low density in Gull Lake.
A study by Cummins,
as a p r e d a t o r

et al.

(1969)

suggested that L e p t o d o r a ,

(6-12 m m l o n g ) , crops the most readily

a v a i lable prey,

usually the most abun d a n t prey zooplanktor.

In S a n c tuary Lake,

Pennsylvania,

the principal prey zoo-

pl a n ktors included Diaptomus s i c i l o i d e s .
In the process of counting and sorting samples
during the pre s e n t study,

I have obse r v e d both Mesocyclops

e d a x and Cyclops b i c u s pidatus thomasi preserved in the act
of c o n s uming adult diaptomids as w e l l as copepodids and
nauplii.

In light of the preda t i o n effects reported by

Co n f e r and McQueen,

it wo u l d s e e m plausible to suggest that

c y c l o p o i d predation in Gull Lake may have b e e n a dominant
factor in preven t i n g ei t h e r species from achieving a h i g h e r
seasonal maximum.

This hypothesis states that the cycloid

predators w o u l d always consume a h i g h e r nu m b e r of the most
ab u n d a n t species of Diaptomus and then "switch" to the
o t h e r d i a p t o m i d if the numbers of the second species began
to increase.

A rather similar hypothesis was experimentally

62
ex p l o r e d by Slobodkin
experi m e ntal removal

(1964).

He was able to show that

(predation by the experimenter, p r o ­

p o r t ional to popula t i o n densities)

of H y d r a in two-species

laboratory cultures p r e v ented densities from reaching
ex c l u s i o n levels,

thus enabling two species to coexist

where o n ly one could d o so in the absence of predation.
This i n t e r pretation of p r e d a t o r - c o n t r o l l e d c o m p e tition of
Diaptomus remains very tentative due to insufficient q u a n ­
titative data.
P h y l o genetic Considerations
As a p a r t of a revision of the North American
Species of D i a p t o m u s , Marsh
genus occurs world-wide,

(1907)

no t e d that although the

all the N o r t h American species

w e r e p e c u l i a r to this continent.

This suggested that the

genus is quite susceptible to the influences of its e n v i ­
ronment.

Marsh acknowledged that it w a s speculative to

co mment upon the affinities of the North Amer i c a n species
of Diaptomus b u t he felt that some reasonable observations,
nevertheless,

could be made.

He felt that a p h y l o g e n e t i c

scheme could be composed b a s e d on c o n s i d e r a t i o n of s t r u c ­
tural relationships and species d i s t r ibution patterns.

He

d i s c u s s e d his criteria for primi t i v e structural c h a r a c t e r ­
istics though he n o t e d they are of necessity,

largely

conjecture.
Of inte r e s t to the di s c u s s i o n of the results of
the p r e s e n t study is the opinion of M a r s h that b o t h D^

63
oregon e n sis and

minutus are the primitive form of their

respective groups wi t h i n the phylogeny of the genus,
Diaptomus.

D. minutus was noted as somewhat of a par a d o x

b e c a u s e the fifth p a i r of legs of the males show ma r k e d
re d u ction that could be considered indicative of high
s p e c i a l i zation but its w i d e geographical distribution,
noted e a rlier in this paper,

strongly suggests that it

represents an early form of its group.

Marsh felt the wide

g e o g r a p h ical d i s t r ibution should carry more w e i g h t than its
structural reductions.
D. minutus was identified as a highly variable
species,

in terms of periods of reproduction and seasonal

p o p u l a t i o n dynamics,

by Schin d l e r and Noven

(1971).

authors were attemp t i n g to establish baselines

These

for future

f e r tilization experiments in two shallow lakes of the
E x p e r i m e ntal Lakes Area,

northwestern Ontario.

They c o n ­

cluded that the seasonal dynamics of D^_ minutus in the two
lakes studied appe a r e d to b e a r little relation to eith e r
p h y t o p l a n k t o n abundance o r temperature and thus attempts
to identify changes in

minutus populations due to

fertilization w o u l d most probably prove futile.

This

o b s e r v a t ion of apparent plasticity of reproductive capacity,
along w i t h the opi n i o n of Marsh,
that

minutus

tend to support the idea

functions as a genera l i s t

in zooplankton communities.

(Pianka,

1974)

D^_ oregonensis also has a

r a t h e r wide g e o g r a p h i c a l distribution as reported by Marsh

64
(1929)

and thus also qualifies as a generalist.

The o r i g ­

inal i d e n tification was made from a collec t i o n from P o r t ­
land#

Oregon, b u t it apparently is not common w e s t of the

Rocky Mountains.

It has b e e n reported east as far as New

B r u n swick and the N o r t h w e s t Territories on the north
al t hough it is m o s t common in the Great Lakes region.
Chara c t e r Displacement
The term,
Brown and Wi l s o n

chara c t e r displacement, was introduce d by
(1956)

to describe the pattern that results

w h e n two closely related species have o v e r lapping ranges.
W h e n the one species occurs alone,

it tends to converge

upon or be quite similar to the other species.
trast,

however,

In con­

in the area where the two species co-occur,

the p o pulations are more divergent and easily distinguished.
That is to say,
characters.

they "displace"

one another in one or more

It should be noted that contrary to the e x a m ­

ples of v ertebrates cited b y Br o w n and W i l s o n and Hutchinson
(1959) , the metasome lengths of

minutus and

oregon-

ensis do not overlap in lakes w h e r e they occur alone.
R igler and L a n g f o r d

(1967)

p e r f o r m e d measuremen t s

of body length on animals colle c t e d in their survey of 100
lakes in southern Ontario.
lakes in which

minutus and

w i t h 13 lakes in which
lakes w i t h

They compa r e d data from 33
oregonensis co-occurre d

minutus was found alone and 13

oregonensis alone.

There was no difference

n o t e d for Dj_ oregonensis and in the case of D^_ m i n u t u s ,

65
r ather than divergence,
gence!

they found a significant conv e r ­

When it occu r r e d w i t h D^_ o r e g o n e n s i s , it was

l onger than w h e n it occurred alone.

Turvey

8-10%

(19 6 8) also was

unable to find any evidence of chara c t e r displacement,

in

terms of body l e n g t h s .
The length m e a s urements p r e s e n t e d in this study
(Table 1 and 2)

indicate that while diaptomids exhibi t

ge n e r a l l y simi l a r measurements,

the varia t i o n from lake to

lake tends to be large enough to obscure evidence of c h a r ­
acter displacement even if it did occur.
Cole

(1966)

re ported that the c e p h a l o t h o r a x length

of diaptomids o c c u r r i n g in temporary ponds of Ari z o n a w e r e
s ignif i cantly grea t e r than those of the same species
o c c u r r i n g in p e r m a n e n t lakes.
n o t e d a popula t i o n of
u n u s ually small.
occurrence.

Ri g l e r and Lang f o r d

(1967)

oregonensis in one lake that was

They w e r e not able to explain this

Examples such as these tend to reinforce the

o p i n i o n of Turvey

(1968)

may i ndeed take place,

that w h i l e c h a r a c t e r disp l a c e m e n t

controlled e x p e r iments will be

n e c e s s a ry in o r d e r to p r e s e n t convin c i n g evidence of its
reality in calanoid copepods.
Filte r i n g Rates
In a review of respiration and feeding in copepods,
Marshall

(19 7 3) noted the a s s u mption that,

freshwater,

at least in

size of b o d y is c o r r elated w i t h size of food

and so that small copepods can eat only small food

66
particles,

large copepods can eat b o t h small and large ones

(Brooks and Dodson,

1965).

ence in diaptomid body

The hypoth e s i s that a d i f f e r ­

length represents a difference in

food niche is supported by very few data.
case was reported by F r y e r
laticeps

(1.54-1.65 mm)

(1.14-1.23 mm)

(1954).

One supporting

He found that Diaptomus

c o - o c curred with Diaptomus gracilis

in Lake Windermere,

p e r i o d January through March,

1953.

England,

during the

His study of gut

contents revea l e d that D^_ laticeps fed almost exclusively
on the d i a t o m Melosira italica during the time of the
study w h i l e D_;_ gracilis fed ma i n l y on "tiny spherical green
algal cells and fine detritus
w i t h very few diatoms.

. . .

of vegetable origin"

He also o b s e r v e d that neither

species colle c t e d the diatom, A s t e r i o n e l l a f o r m o s a ,
al t hough it was abun d a n t during the pe r i o d of his study.
The results of the experiments in the present
study,

using Chlor e l l a

l arger diaptomid,

(volume 40 pm ) indicate that the

D^_ o r e g o n e n s i s , was unable to collect

this s m a l l - s i z e d food particle as effectively as did the
sm a l l e r diaptomid,

D^_ minutus

(Figure 10).

While no

pr e c i s e estimate of this decre a s e d effectiveness can be
calculated,

a c o m p a r i s o n of the C h l o r e l l a d a t a w i t h those

of S c e n edesmus

(Figure

on the o r d e r of 50%.
the B rooks

8) suggests that the decrease was
This o b s e rvation tends to show that

and Dodson hypothesis m e n t ioned above is an

o v e r s i m p l i f i c a t i o n of the true relationship bet w e e n larger

67
and s m aller d i a p t o m i d s .
(1970)

found that

In laboratory e x p e r i m e n t s , M c Q u e e n

oregonensis females and stage V

copepodids did not filter small diatoms, volume less than
3
125 ym , in experiments in w h i c h they were off e r e d a m i x e d
culture of diatoms,

genus N a v i c u l a .

This size threshold,

however, was not as distinctly evident w h e n they were fed
n a t u r a l p h y t o p l a n k t o n from Ma r i o n Lake,
A l t h o u g h Calanus is much larger
than D i a p t o m u s , Marshall and O r r

B r i t i s h Columbia.

(3.2-5.4 mm,
(1955a)

total length)

found a sim i l a r

decrease in effectiveness, b e l o w 10 ym diameter.

These

results, w h i l e hardly conclusive, do tend to support the
hypoth esis I have proposed,

small cells are collected less

e f f e c t i v e l y than larger cells b y EK_ o r e g onensis

(larger

diaptomid).
The Brooks and Dodson hypoth e s i s p r o p o s e d that the
upper particle size limit for small he r b i v o r o u s zooplankton
w o u l d be approximately 15 ym diameter.
(1965)
length)

of Eudiaptmus qraciloides

Bogatova's study

(1.0-1.3 mm, overall

showed selec t i o n of algae in the 4 to 20 ym d i a m ­

e t e r range.

Jorge n s e n

(1966)

e x p r e s s e d the opi n i o n that

p a r t icles b e l o w 30-50 ym d i a m e t e r can be filtered by
Calanus whe r e a s larger cells are seized raptorially.
study of zooplankton grazing, P o r t e r
analysis of

(1973)

found that gut

minutus y i e l d e d results w h i c h tended to c o n ­

f i r m the upper limit of 30-50 ym d i a m e t e r sugge s t e d by
Jorgensen.

In a

It cannot, of course, be determined by gut

68
analysis w h e t h e r the large cells w e r e filtered or seized
r aptorially b u t h e r results indicate that the smaller
diaptomid,

minutus,

can collect cells considerably

larger than prop o s e d by Brooks and Dodson.

In addition,

the fact that A n k i s t r o d e s m u s falcatus was successfully
collected by b o t h species in the pres e n t study offers
evidence that both species can consistently handle larger
cells since this species of green algae is usually be t w e e n
60 and 90 ym long.

Gauld

b e l i e v e d that particles

(1964)

as well as Jorge n s e n

larger than 40 ym diam e t e r were

e x c l u d e d from the filter chamber by short setae.
setae might not be effective,
A n k i s t r odesmus falcatus

however,

These

in preventing

from ente r i n g the filter chamber

due to its nee d l e - l i k e shape.
In terms of cell volume, S c e n e desmus accuminatus
was the largest cell
study.

(4300 ym^)

used during the present

The filtering rates calculated from experiments

using this large cell were the high e s t obta i n e d for all
categories ex c e p t for D^_ minutus males.

The results seem

to indicate that both species are capable of handling
larger cells more e f f e c tively than smaller ones although
there is the h i n t that D_;_ minutus males may handle cells
of the volume of Scenedesmus accuminatus and larger ones
s o m ewhat less ef f e c t i v e l y than sma l l e r ones.
In summary,

the range of overlap in particle size

collec t ion appears to be betw e e n 8 ym (mean diameter of

69
Chlamydomonas r e i n h a r d t i i ) and 22 pm diameter
of Scenedesmus a c c u m i n a t u s ) .

(mean diameter

D^_ minutus e x h i b i t e d e f f e c ­

tive collection be l o w that size range and it appears likely
that future experiments will d e m o n strate that

oregonensis

e ffectively collect cells larger than those in the range of
overlap.

McQ u e e n

(1970)

has already shown that D^_ o r e g o n ­

ensis females are capable of collecting cells with a mean
3
cell volume of 10,000 pm .
In order to evaluate this size - p a r t i t i o n i n g h y p o t h ­
esis, it w o u l d be helpful to know the nature of the size
s p e ctrum of food particles available.

The d i s t r ibut i o n of

p h y t o p lankton in Gull Lake during 1973 has been intensively
studied by Moss

(personal c o m m u n i c a t i o n ) .

He found 1000

cells/ml at the surface and 300 cells/ml in the metalimnion
in the 2-8 pm size category during July and August.
size category included Rhodomonas minuta,
lates,

This

green flag e l ­

and several colonial bacteria.
The principal genera in the 8-22 p m size category

were C y c l o t e l l a , P e r i d i n i u m , C r y p t o m o n a s , and O o c y s t i s .
A t the surface,
metalimnion,

the density w a s

320 cells/ml and in the

260 cells/ml.

In the 25-50 pm size category,

the density was 1260

cells/ml at the surface and 430 cells/ml in the metalimnion.
Dinobryon was the m a j o r contributor in this size range,
however,

the presence of a lorica aro u n d the protopl a s t

and the tendency to form b r a n c h i n g colonies may m a k e this

70
species unattractive as a diapt o m i d food item.

Even though

a q u a n t itative statement descri b i n g the 25-50 ym size
category is difficult to make because the relative palatability of algal species is unknown,

it does appear that a

s i g n i f icant num b e r of cells are pres e n t in this size c a t ­
egory for

oregonensis to exp l o i t during the per i o d of

s ummer stratification.
Relatively few studies have been conducted to
d etermine the filtering rates of freshwater diaptomids
a lthough there is a large literature on the feeding o f
m arine calanoids
(1959)

(see Marshall and Orr,

19 5 5 b ) .

Nauwerck

reported filtering rates b e t w e e n 0.3 and 2.8

m l / a n i m a l / d a y for Eudiaptomus g r a c i l o i d e s , using an in
situ m e t h o d w i t h

cells.

^ c - l a b e l l e d

These results agree

q uite w e l l w i t h those reported b y M a l o v i t s k a y a and Sorokin
(1961)

for E^_ graciloides and E^_ gracilis

animal/day).

Richman

(1966)

(0.7-4.1 ml/

studied the effect of p h y t o ­

p l a n k t o n c o n c e ntration on the filtering rates of adult D.
oregon e nsis and repo r t e d a range of filtering rates b e t w e e n
0.3 and 2.5 ml/animal/day.

F r o m a study of the energy

b u d g e t of D^_ s i c i l o i d e s , Comita

(1964)

obtained filtering

rates b e t w e e n 1.0 and 2.0 ml/animal/day.
c o n d ucted feeding experiments,

using

McQ u e e n

oregonensis

and stage V copepodids as test organisms.
variety of types of cells,

(1970)
females

Employing a

he reported that the filtering

rates i ncre a s e d w i t h increa s i n g cell volume until a m a x i m u m

71
rate was reached.

Beyond this opt i m u m size,

rates decreased w i t h incre a s e d cell size.

the filtering

He reported

m a x i m u m filtering rates of 11.2-12.9 m l / a n i m a l / d a y for
natural phyt o p l a n k t o n

(mean volume 179-524

p m ).

The

largest size category reported in his natural p h y t o p l a n k t o n
experiments was

12-15 ym d i a m e t e r

(mean volume,

1150 y m ^ ) .

M c Queen obta i n e d a similar p a t t e r n in experiments using
a m i x t u r e of Navi c u l a diatoms instead of natural p h y t o ­
plankton;

however,

the m a x i m u m filtering rate was 2.1 m l /

animal/day for the Nav icula mixture compared to 12.9 ml/
animal/day for the natural phytoplankton.

It is of interest

to note that w h i l e both rates w e r e calculated by the d i f ­
ferential cell count method,

the Navi c u l a mixture data

was o b t a i n e d by using a C o u l t e r cou n t e r w h i l e counts of the
natural p h y t o p l a n k t o n experiments w e r e obtained using an
i n v e r t e d microscope.

Wh i l e filtering rates over 100 ml/

animal/day for marine calanoids have b e e n reported
(Marshall and Orr,

1962;

Richman and Rogers,

M c Queen study is the only one,

to date,

1969),

the

reporting rates of

o v e r 5 m l / a n i m a l / d a y for freshwater calanoids.
The filtering rates obta i n e d during the p r e s e n t
study agree very well w i t h previous studies except for the
natural p h y t o p l a n k t o n portion of McQueen's work.

This

seems rather remarkable in light of the variety of e x p e r i ­
m ental techniques used in the studies m e n t i o n e d above.

72
The r e l a t ions hip bet w e e n filtering rate and body
size for bap h n i a rosea can be descr i b e d a p p r oximatel y by
the Power Law:
Y = aXb ,
w here Y is filtering rate,
of the line,

X is body length, b is the slope

and a is the inter c e p t on the y axis

(Burns

and Rigler,

196 7).

3.02 for

rosea o v e r a body length range o f 0.64 to

1.60 mm.

In a study involving four species of D a p h n i a ,

Burns

(1969)

and 2.38

These authors calcul a t e d a slope of

reported slopes of 2.16

(15°C), 2.80

(20°C),

(25°C).
Brooks and Do d s o n

(1965)

suggest that the food-

collec ting surfaces are proportional to the square of the
body length.

Egl o f f and Palmer

(1971)

found that the area

of the filtering setae of thoracic limbs 3 and 4 of D a p h n i a
m a g n a and D_;_ rosea indeed supported the Brooks and Dodson
hypothesis.
(1969)

These authors noted, however,

that w h e n Burns

comp a r e d the filtering rates of these two daphnids

to their b o d y lengths,

the slope values w e r e distinc t l y

g r eater than p r e d i c t e d by the Brooks and Do d s o n hypothesis.
These studies sug g e s t that the filtering rates of Da p h n i a
i ncrease p r o p o rtional to numbers betw e e n the square and
the cube of body length.
Using the least squares fit method,

a slope of 2.28

was o b t a i n e d for daytime experiments e m p l o y i n g

73
A n k i s t r o d e s m u s falcatus and 2.33 for those using Scenedesmus
accum i natus w h e n the
included.

o r e g o nensis female cate g o r y was not

A l t h o u g h the d i a p t o m i d day t i m e filtering rates

of this study are lower than those repo r t e d for D a p h n i a ,
the b o d y length-f i l t e r i n g rate r e l a t ionship is v e r y similar
(excluding

oregonensis

females).

The day t i m e filtering

rate d epres s i o n of D^_ o r e g o nensis females is very striking.
A l t h o u g h perhaps less extreme,

the D_^ m i n u t u s females also

e x h i b i t e d daytime filtering rate depression.

I have been

u nable to locate any similar cases of d e p r e s s e d female fil­
t ering rates alth o u g h v e r y few studies have investigated
sexual d i f f e r e n c e s in the filtering rates of freshwater
diaptomids.

Nauw e r c k

(1959) o b s e r v e d similar filtering

rates for b o t h m a l e s a nd females of E u d i aptomus g r a c i l o i d e s .
Invest i gations of sexual d i f f e rences in mar i n e calanoids
have shown m a l e filtering rate depression.

Mu l l i n

(1963)

r e p o r t e d that the graz ing rates of m a l e Cala n u s helgoland i c u s , feeding o n the diatom, D i t y l u m , w e r e o n l y b e t w e e n
10% and 33% as great as females of the same species under
ident i c al laboratory conditions.
L a b o r a t o r y feeding e x p e r i m e n t s by Ric h m a n and
Rogers

(1969)

yiel d e d d a t a that suggest that Calanus

h e l g o l a n d i c u s , feeding on the diatom,

Ditylum brightwellii,

u t ilize a c o m b i n a t i o n of passi v e l y filtering small cells
and a c t i v e l y hunt i n g large ones.

Conover

(1966,

1968)

found that in Calanus hyp e r b o r e u s " e n c o u n t e r ” feeding and

74
"filter"

feeding were separate and m u t u a l l y exclusive

processes.

His evidence indicated that the percenta g e of

time spent in one mode va r i e d according to external c o n d i ­
tions.

"Encounter"

feeding was proposed by Cus h i n g

(1951)

to describe the capture of large cells that come into c o n ­
t a c t w i t h the feeding appendages.

Wilson

(1973)

ac c epted the existence of two feeding modes,
filtering and selective grasping,

also

nonsele c t i v e

and h y p o t hesized that

there is a constant alternation of modes in the calanoid
feeding pattern.
In light of the above hypothesis,

one possible

e x p l a n ation of the daytime d e p r essing of the female f i l ­
tering rates of the p r e s e n t study m i g h t be that du r i n g the
daytime,

while residing in the metalimnion,

the females

switch from a pred o m i n a t e l y filtering mode of feeding to a
m a i n l y "encounter-feeding" mode or to a regime of a l t e r ­
n a t i o n of these two modes.

Since small cells, C h l o r e l l a sp.

and C h l a m ydomonas r e i n h a r d t i i , w e r e colle c t e d by the
females,

alth o u g h at reduced rates,

a const a n t alter n a t i o n

b e t w e e n a filtering m o d e o f feeding and an "encounterfeeding" m o d e w o u l d s e e m to offer a more plausible h y p o t h ­
esis than a ma i n l y "encounter-feeding" mode.

The hypothesis

p r o poses that while in the "encounter-feeding" mode,

small

cells cannot be colle c t e d since a large cell is bein g
ha ndled by the feeding appendages.
feeding mode,

During the filtering

small cells are colle c t e d by the feeding

75
appendages and large cells are ignored or prevented from
en t e r i n g the filtering chamber by setae as proposed by
Gauld

(1964).

This hypothesis tends to support the p r o ­

posal that I made earlier in this section that

oreqon-

ensis utilizes cells larger than those found in the range
of overlap.

This daytime feeding behavior of altern a t i n g

"encounter-feeding" m o d e w i t h a "filter-feeding" mo d e could
thus serve as a m e c h a n i s m of food niche differentiation.
The daytime d e p r e s s i o n of female filtering rates
was e vi d e n t during the wi n t e r as w e l l as the summer
11).

(Figure

The wi n t e r conditions of light w e r e generally similar

to those of summer b u t there was no obv i o u s migra t i o n under
the ice and the temperature was a p p r o x i m a t e l y 10°C less
than in summer

(metalimnion).

Light w o u l d s e e m to be the

only cons t a n t p a r a meter that could serve as the signal
m e c h a n i s m for this proposed daytime switch in feeding
s t r ategy that wo u l d be p r e s e n t in summer as well as w i n t e r
unless there w o u l d be an innate d a y - night filtering r h y t h m
in D i a p t o m u s .

This condition, however, doe s n ' t seem likely

in light of the experimental w o r k of Ric h m a n and Rogers
(1969)

and the o b s e r vations of Gauld

(1953) w h i c h support

the idea that there is no innate d a y - n i g h t filtering rhythm
in the ma r i n e calanoid,

Calanus.

The summer ni ght t i m e experiments w e r e c o n d uc t e d at
a d epth of 1 meter.

This was in cont r a s t to the daytime

e x p e r i mental depth of 11-15 meters.

The summer nighttime

76
rates

(Figures 7, 9) are hi g h e r than the summer daytime

ones.

The day-night d i f f e r e n c e is m o s t striking in the

female and stage V categories.

I propose that the d i f ­

ference b e t w e e n the day and night filtering rates of D.
oregonensis females,
ponents.

for example, was comp o s e d of two c o m ­

The first, a dayt i m e filtering rate depre s s i o n

and the second,

a night t i m e filtering increase.

This

hypothesis is based on the comparative p e r f o rmances of the
o t h e r size categories of this study.

I bel i e v e these c o m ­

paris ons are especi a l l y appropriate since all diapto m i d
size categories p a r t i c i p a t e d together in e a c h experiment.
The nighttime increases obse r v e d in the pre s e n t
study are directly oppo s i t e from those of N a u w e r c k

(1959)

w ho r epo r t e d higher day t i m e than nighttime filtering rates
f°r
rates

graciloides alth o u g h he did find hi g h e r nighttime
for D a p h n i a .

show a m u t i n g

The w i n t e r day-n i g h t d a t a

(or absence)

(Figure 12)

of d a y - n i g h t differences.

This

c ould suggest that the incre a s e d summer night t i m e filtering
rates w e r e the result of the large temperature diffe r e n c e
b e t w e e n the metalimnion
epilimnion

(daytime experiments)

(nighttime experiments)

and the

since there was no

tempe rature difference b e t w e e n the day and n i g h t exper i m e n t s
u n d e r ice cover.

Alternatively,

the hig h e r night t i m e fil­

t ering rates m a y be a s s o c i a t e d w i t h the d a y - n i g h t mi g r a t i o n
event.

77
M u c h has been w r i t t e n about the significance of
v e r tical m i g r ations of marine crustaceans in p a r t i c u l a r
(Cushing,

1951;

Hardy,

1956; Bainbridge,

W y n n e - E d w a r d s , 1962; McLaren,
1969;

Kerfoot,

1970).

tative approach,
of potential
intensity,

Kerfoot

1961;

David,

1961;

196 3; M a u c h l i n e and Fisher,
(1970) devel o p e d a q u a n t i ­

"pathway analysis,"

for deri v i n g curves

food energy c o n s idering the varia b l e s of light

productivity,

time, and depth.

a p p r o a c h leads to some interesting ideas,

While this
a stated c o n ­

straint was that the mo m e n t the isolumes reach the surface,
feeding of individuals wi t h i n that light range ceased.
Consequently,

the data of the pres e n t study are unsu i t e d

for a p p l i cation of the above hypothesis.

Kerfoot's c o n ­

t e n tion that light is the dominating stimulus for m i g r a t i o n
m a y well be correct.
McLaren

(1963)

examined the then exis t i n g theories

about the adaptive values of vertical m i g r a t i o n and found
them inadequate.

He prop o s e d his own theory that an e n e r g y

bonus m a y be achieved as a consequence of the more e f f i c i e n t
uptake of food at higher temperatures
night)

(surface w a t e r at

and the more effic i e n t d i r e cting of en e r g y to g r o w t h

at lower temperatures

(metalimnion dur i n g d a y t i m e ) .

He

as s u m e d that m i g r a n t zooplankton do not feed consta n t l y and
can fill their daily n u t r itional needs during the time
spent in surface w a t e r if food is sufficiently rich.
ever, McL a r e n

(1974)

How­

indicates that he now beli e v e s that

78
his e ar l i e r e x p l anation of the d e m o g raphic consequences of
v e r t i c a l m i g r a t i o n involved a p r o b a b l y erroneous m e t a b o l i c
model.

He offers data to support the p r o p o s i t i o n that

i ncreased fecundity does re s u l t from part-time resi d e n c e in
c older w a t e r but notes that there are exceptions d e p e n d i n g
upon the type of life cycle,

amount of food present,

and

n a u pliar m o r t a l i t y rates.
In a re v i e w of the bio l o g y of euphausiids, M a u c h l i n e
and F isher

(1969) make a number of perceptive statements

about the importance of vert i c a l m i g r a t i o n in light of the
co mplex literature and o f t e n c o n t r a d i c t o r y observat i o n s and
generalizations.

T h e s e authors offer the opinion that v e r ­

tical m i g r a t i o n p r o b a b l y confers a number of benefi t s on
the organisms rather than one of great significance.

They

consi der it unli k e l y that a p r o v e n general reason for dayn ight m i g r a t i o n of planktonic organisms will be found since
they believe it is quite probable that the m o s t important
b e n efits der i v e d b y one species
those deri v e d by another species

(group) w i l l differ from
(group).

Th e i r co n c l u s i o n

w as that the various theories previo u s l y offe r e d to e x p l a i n
v e r tical m i g r a t i o n m a y all be true rather than any one
b e i n g of p a r a m o u n t importance.
A l t h o u g h the phys i c a l parameters are genera l l y
similar for m i g r a t i n g organ i s m s in Gull Lake,

the s t r a t e g y

of survival or p r o s p e r i t y for D a p h n i a , w h i c h has a short
life expectancy,

high r e p r o ductive capacity via

79
parthenogenesis,

and short d e v e l opmental time w o u l d i n t u ­

itively seem to be quite diffe r e n t from C h a o b o r u s , w h i c h
m i g rates as larvae,

then m e t a m o r p h o s e s into pupae,

later into flying sexual adults.

and

In a similar way, d i a p ­

tomids, w i t h only sexual adults, ma t i n g rituals,

and 12

p o s t - embryonic free living life his t o r y stages w o u l d seem
likely to need yet another strategy.

So that it seems

r e a s o n a b l e to accept the hypothesis that for the d i f f e r e n t
groups of m i g r a n t s there will be var y i n g c o m b i n a t i o n s of
be n e f i t s der i v e d from stammer vertical m i g r a t i o n eve n w i t h i n
a single lake.
A d d i t i o n a l summer nighttime feeding e x p e r im e n t s p e r ­
formed in a vert i c a l series may produce a m o r e defini t i v e
pi cture of night t i m e filtering rates and thus support or
refute the theory that increased n i g h ttime rates are
d i r e c t l y related to temperature.

Por t e r

(1973)

reported

v e r y few diatoms as part of the gut contents of D^_ minutus
while M c Q u e e n

(1970)

found that

r e adily filtered diatoms.
ments,

o r e g o n e n s i s females

Fur t h e r in s i t u feeding e x p e r i ­

using diatoms as labelled cells, m i g h t show selection

based on cell-type that c o u l d enhance the food niche d i f ­
ferent iation of these two species of D i a p t o m u s .
As n o t e d earlier,

Rigler and L a n g f o r d

r e p orted D^_ minutus c o - o c c u r r e d w i t h
of 100 lakes w h i c h they studied.

(1967)

oregonensis

in 4 5%

o r e g o n e n s i s occ u r r e d

alone in 24 lakes and D. minutus occu r r e d alone in 19

80
lakes.

Clearly,

always occur.

coexistence is quite possible b u t does not

M y study d i d not produce evidence that w o u l d

indicate w h y some lakes have o n l y one diapt o m i d species
present.
It m a y be suggested that the condition of c o e x i s ­
tence of two species of Diaptomus reflects a tempor a r y
p hase in the e u t r o p h i c a t i o n process of a lake.

W i t h the

e x c e p tion of the Gr e a t Lakes, v e r y little sampling data is
a v a i l able to use in considering this hypothesis.

However,

it seems reasonable to infer from the study of Rigler and
Langford

(1967)

that diapt o m i d c o e x i stence is not a t e m ­

p o r a r y condition since the 100 lakes included in their
study ranged from extreme o l i g o t r o p h y to extreme eutrophy.
MacArthur

(1972)

pointed out that several c o m p e t i ­

tors can m u c h m o r e easily outcom p e t e and eliminate a
species than can a single competitor.

This concept of

d i ffuse c o m p e t i t i o n m a y help to exp l a i n the dis t r i b u t i o n
of diaptomids.

I have prop o s e d that the range of food

p a r t i c l e sizes for D_;_ min u t u s is 3 to 22 pm d i a m e t e r and
that the range of D_^ o r e g o nensis overlaps from 8 to 22 pm
d i a m e t e r and extends beyond to larger cells.

If these two

species of Diaptomus w e r e the only herbivores in the l i m ­
n etic zone,

it could be propo s e d that while there is a

zone of o v e r l a p in the food part i c l e size spec t r u m
d i a m e t e r ) , D ^ m i n u t u s has a relative refuge
diameter)

(8-22 pm

(3-8 pm

b e l o w the o v e r l a p zone as p a r t of its food niche

81
while

oregonensis prob a b l y has one above the overlap

zone as part of its food niche.

However,

since the h e r ­

b i v orous zooplankton communities usually con s i s t of varying
combinations of rotifers,

cladocerans,

and ot h e r cala n o i d copepods,

cyclo p o i d copepods,

the p o s s i b i l i t y of one or the

other species of Diaptomus b e i n g "sandwiched" bet w e e n s e v ­
eral competitors and being unable to survive w o u l d seem
intuitively q u i t e possible.

To date no investigati o n s of

di ffuse c o m p e t i t i o n have b e e n carried out w i t h the zoo­
plankton .

SUMMARY A N D CONCLUSIONS

Factors related to the coexistence of Diaptomus
mi nutus
mm)

(0.84-0.93 mm)

and Diaptomus oregonensis

(1.15-1.34

in Gull Lake, Michigan, w e r e explored du r i n g 1972-1974.

Conditions requisite for using the term, coexistence, w e r e
de fined since its usage in the literature has been rather
imprecise.

The in situ grazing m e t h o d of Haney

(1971),

using ^ C - l a b e l l e d algae, was employed in an effort to
determine w h e t h e r resource alloca t i o n was accomplished on
the basis of cell size.

Advant a g e s of this technique

include very short experimental time,
ditions,

high sensitivity,

naturalness of c o n ­

and the ability to include b o t h

species together in e a c h experiment.

The following c o n ­

clusions eme r g e d from this study:
1.

In Gull Lake, D_;_ oregonensis and D ^ minutus o c c upied
the same space niche.

There was extensive o v e r l a p

of vertical d i s t r i b u t i o n s as well as an absence of
pronounced seasonal popula t i o n maxima.
summer s t r a t ification period,
into the e p i l i m n i o n at night.

82

During the

b o t h species m i g rated

83
2.

D_;_ oregonensis was shown to filter small cells
(3-8 ym diameter)
minutus.

less effectively than d i d D *

This indicates a partitioning of the size

c o n t i n u u m of food particles present.
3.

B o t h species w e r e able to capture large green algae,
A n k i s t r o d e s m u s falcatus
esmus accuminatus

(60-90 ym long)

and S c e n e d ­

(18-26 ym d i a m e t e r ) , effectively.

This study did n o t attempt to explore the p o s s i b i l ­
ity of raptorial feeding of large particles b y one
or both species, which may enhance food niche d i f ­
ferences .
4.

D u r i n g the summer stratification period,

female d a y ­

time filtering rates in the m e t a l imnion were m a r k ­
edly depressed compared to the m a l e rates.

This

filtering rate d e p r ession was m o s t pronou n c e d in
D. oregonensis females and m a y represent an example
of an a l t e r nating pattern of an "encounter-feeding"
m o d e w i t h a "filter-feeding" mode.
5.

D a y - n i g h t m i g r a t i o n was evi d e n t during the summer
s t r a t ification period.

The hi g h e r nighttime f i l ­

tering rates w e r e consistent w i t h the higher t e m p ­
erat u r e s e x p e r i e n c e d by the migr a n t s near the s u r ­
face at night.
6.

W i n t e r daytime filtering rates,

under ice cover,

w e r e quite similar to those obta i n e d dur i n g the
summer.

This o b s e r vation appears to support the

84
trend reported by Kibby

(1971)

for Daphnia rosea

and also to be consis t e n t w i t h the findings of
Conover

(1956)

and H a l c r o w

(1963)

r e g a r d i n g the

acclimation of r e s p iration rates b y ma r i n e calanoid
copepods to seasonal temperature changes.
7.

The general conclusion,

although tentative,

is that

there m a y be sufficient d i f f e rences in feeding to
account for the c o e x istence of these commonly
co-occuring species.

Spatial or seasonal s e g r e ­

gation is not involved.

Character displaceme n t

(size) m a y poss i b l y be occur r i n g in D_j_ minutus b u t
is not e v i d e n t in D^_ o r e g o n e n s i s .
8.

The quest i o n of their respec t i v e distributions;
i.e., alone or together,

remains unanswered,

but it

seems clear that taken by themselves coexistence
is indeed possible.
species

Dif f u s e com p e t i t i o n from other

(including cladocerans)

mi g h t acco u n t for

the absence of one or the o t h e r species in a given
lake system.

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