ENHANCEMENT
HERBIVORE
OF NET PRIMARY PRODUCTIVITY
GRAZING IN AQUATIC
LABORATORY
MICROCOSMS
David
Department
of Biological
Sciences,
BY
C. Cooper2
State University
of New
York
at Binghamton
13901
ABSTRACT
The role of herbivore
grazing intensity
as a factor affecting
net primary
productivity
was investigated
by introducing
varying
biomasses of a starved herbivore
(Notropis
spilopterzcs) into replicate autotrophic
microcosms,
After 20 clays, the enhancement
of
net primary productivity
in the experimental
microcosms was directly related to herbivore
biomass up to a certain density and inversely related above this. The relationship
approximates the first derivative
of a sigmoid population
growth model. Enhancement
of primary
production under these experimental
conditions appears to be due to reductions of standing
crop and increased turnover rates of producer populations.
The results suggest that these
responses were independent
of increased nutrient
regeneration
rates brought
about by
grazing.
The distinction between productivity
(a
rate function) and standing crop (a static
mcasurcment) has often been made. Yet,
the notion that reduction in producer standing crop corresponds to a reduction in food
material for a consumer population is taken
as axiomatic in many investigations
of
production-consumption
relationships.
Several observations of changes in productivity of producer populations immediately following rapid removal of consumers
suggest that measurements of standing crop
are not necessarily indicative of the amount
of food material available for consumption
by a consumer population.
For example,
Paine and Vadas ( 1969) found that removal
of sea urchins ( StrongyZocentrotus spp, )
resulted in significant alterations in benthic
algal species composition and increases in
primary productivity.
Also, the high mortality of limpets on the Cornish shorts subsequent to detergent spraying following
the Terre!/ Canyon oil spill in 1967 resulted
in enhanced primary productivity
by attached green algae (Smith 1968).
But thcrc has been little direct invcstigation of the dynamic effects of hcrbivorc
1 This research was supported
by a research
fellowship
and grant-in-aid
from the SUNY Research Foundation
JAC/UAC
365-570.
’ Prcscnt address:
Battelle
Columbus
Laborntories, 505 King Avenue, Columbus, Ohio 43201.
LIMNOLOGY
AND
OCEANOGRAPIIY
31
consumption on rates of primary productivity.
Hargrave ( 1970) varied numbers
of the herbivorous
amphipod
Hyalda
axteca in sediment cores. The productivity
of the sediment microflora was stimulated
with increased amphipod numbers within
the range of natural density. Above this
lcvcl, with increased numbers of amphipods,
algal production declined. The results suggest that increased grazing, within the range
of natural grazing intensities, scrvcs to increase the primary productivity
of benthic
microflora.
One explanation for the cnhancemcnt of
net primary productivity
by low level
grazing is that herbivores might increase
nutrient cycling rates in nutrient-limited
situations. Nutrient rcgcncration by aquatic
consumers has been discussed by Johanncs
( 1968) and is undoubtedly
important for
producer populations in situations of nutricnt limitation.
However, several reports
suggest that the cnhanccmcnt of net primary productivity by grazing might bc due
to other factors. Welch ( 1968) found that
nutrient reserves in sand recdgrass bccamc
deplctcd in rcsponsc to grazing and deduced that the plants wcrc utilizing thcsc
rcscrves to satisfy a newfound growth potential in the aftermath of standing crop rcductions due to grazing. Examples such as
this from tcrrcstrial habitats may or may
JANUARY
1973, V. 18( 1)
32
DAVID
not bc appropriate to aquatic ccosystcms,
but some investigations
suggest that the
same relationships
do hold for aquatic
production-consumption
relationships.
For
cxamplc, the work of DC Amczaga et al.
( 1972) on primary productivity and rates of
change of biomass in various spccics of
phytoplankton
in Castle Lake, California,
suggests that many incrcascs in net primary
productivity
arc due to factors other than
nutrient rcgcneration rates and arc strongly
related to reductions in standing crops OF
producer populations,
In certain situations, it seems probable
that cnhancemcnt of net primary productivity is instigated by a reduction in produccr standing crop due to grazing by a
consumer population. The following invcstigation was conducted to cvaluatc this
premise.
METHODS
AND
MATERIALS
I used the laboratory microcosm to facili tatc replicabili ty, control, and manipulation impossible in field conditions.
A
single large water sample was used to
inocula tc 15 rcplicatc aquaria containing
15 liters of water each. The water sample
came from a depth of 0.5 m in Krajan’s
Pond, a small eutrophic farm pond in
Broome County, New York. Filtration
through No. 20-mesh plankton netting rcmoved zooplankton nauplii and rcs ting eggs
as well as adult plankters, but allowed
much of the phytoplankton
in the sample
to pass through and bc included in the
To each microcosm I
initial inoculum.
added 250 g of autoclavcd sediment (also
from Krajan’s Pond). The microcosms were
aerated for 2 days to prcvcnt colonization
by anacrobcs since the sediments wcrc
quite reducing (redox potential = -150
mV vs. saturated calomcl clcctrodc); acration was then discontinued.
The bank of
15 microcosms was maintained at 21°C on
a 12-hr photopcriod from an overhead bank
of fluorescent lights (Sylvania, kool white)
at a surface light intensity of 1,850 2 25 lux.
Water (25 ml) and scdimcnts (2 g) wcrc
cross-cultured daily for the first 2 weeks
to ensure uniformity.
Community mctab-
C.
COOPER
olism was measured by the di.urnal changes
of oxygen concentration (Odum 1956).
A laboratory
stock of the herbivore
Notropis spilopterus (Cyprinidac)
was obtaincd by seining and the USC of a slurp
gun in Krajan’s Pond and the backwaters of
nearby Choconut Creek. The range of
body weights was rather small in both the
natural and labora tory populations-minimum weight cncountcrcd was 0.62 g, maximum 0.93 g. Various biomasses of this
hcrbivorc wcrc added after a constant P: R
ratio had been achieved and maintained
for 15 days in all microcosms. The fish wcrc
starved for 1 week before introduction into
the microcosms to minimize the contribution of gastrointestinally derived nutrients
to the nutrient budgets of the microcosms.
Scvcral of the many survivors of the starvation regime were disscctcd. Stomach contents in all casts were nil; intestinal contents
wcrc not examined.
Ten of the microcosms were divided into
five groups of two replicates each and the
other five wcrc used as controls. Three
Notropis (2.3 g) wcrc added to group la, b;
4.55 g (6 individuals)
to group 2a, b; 6.92 g
( 9 individuals ) to group 3a, b; 9.18 g ( 12
individuals)
to group 4a, 1); and 11.5 g ( 15
individuals)
to group 5a, b. This range of
biomass was well within the natural variation in Krajan’s Pond and Choconut Creek
( O-1,425 gnl-” ) .
All microcosms were kept under the same
After Notropis
environmental
conditions.
had been allowed to graze for 20 days, they
were rcmovcd. Net primary productivity in
all microcosms was measured for three
diurnal cycles af tcr Notropis removal. Stomach contents of the fish were examined.
Fecal pcllcts wcrc subjected to scmimicro
calorimetry and analyzed for total nitrogen
and total phosphorus ( Strickland and Parsons 1968).
RESULTS
AND
Autotrophic
DISCUSSION
succession
The dominant primary producers in the
microcosms wcrc coccoid green algae.
Spirogyra was also frcqucntly
obscrvcd,
but its standing crops were always very
ENIIANCEMENT
OF NET PRIMARY
low ( < lo--,’ those of the coccoid forms in
all Hcnscn-Scmpcl samples and ScdgwickRafter counts ) . Two blue-green algae,
Anccbuena and Aphunixomenon, formed thin
discontinuous
mats on the walls of the
aquaria, and filaments were found, infrcquently, in the water. It is somewhat surprising that coccoid green forms rcmaincd
dominant, since the high surface arcavolume ratio in vcsscls such as thcsc typitally results in the dominance of attached
blue-green mats (cl;. Odum and IIoskin
1957; McIntirc ct al. 1964).
Primary consumers rapidly increased in
numbers after incrcascs in standing crops
of primary producers. Two populations of
rotifers ( Testuclinellu, Gustropus), olw spctics of cladoceran (Ceriodaphnia reticulata),
and two populations of copepods (Cyclops
sp., Epischura sp.) wcrc found in samples
taken at irregular intervals from all microcosms. IIowcvcr, regular dctcrminations of
zooplankton biomass, spccics number, and
diversity were not made.
The succession of community metabolism
in the microcosms hcforc the addition of
herbivores is illustrated in Fig. 1. Rcspiration was initially greater than net primary productivity,
but rates of incrcnsc in
net primary procluctivity
cxcccdcd rates
of incrcasc in community
respiration.
After about 40 days, a state of autotrophy
( @ P:R 1 1) was attained and maintained
in the microcosms, and the slopes of all
community metabolic paramctcrs wcrc csscntially zero; they rcmaincd that way in
the five microcosms used as controls. The
pattern of autotrophic succession is similar
to that obscrvcd by Abbott ( 1966). The
cocfficicnts of variation of respiration (6.2%)
and gross primary productivity
( 8.4%)
between all microcosms wcrc slightly lower
than those dctcrmincd by Abbott ( 7.1%
+
FIG. 1. Development
of community metabolism
in the microcosms before herbivore
addition, and
maintenance
of community
metabolism
in control
microcosms.
Dnrkcned arcns indicate two standard
deviations
about the mean.
Rrnckcts
inclicatc
range. N inclicntcs the number of indcpcndent
mcasurcments
consCituting each mean.
PRODUCTIVITY
2
.s
3 ,-, 3 2 ‘;’
EI FZ’
Q+ a 22’;’
G
2 N
.r(
L O ILJ 2
$
l-l
‘a
g .$I
*;’ $3
2 2
‘2 $
g g 2
2
.$ i
2 hl I
$& 1E
V-l c\I
z
0
$’ Z
12
$
62
L r\
hPI I 2 4 % a
3 “:
k ’ 2m o”
g by
s -
33
30
60
I
30
I
60
N45
I
N=5
I
30
60
.F g
.z ‘;’
2 2
2 $,
~
ha)
2 3
.j u
I-
"az0.5
v1 ‘2
b
’
N
N=l5
I
30
DAYS
N=5
I
60
34
DAVID
C. COOPER
to.8 UPPER LIMIT
u -0.4
w
’
OF
LOWER LIMIT OF
CONTROL RANGE
t
-0.8 i
0
\
2.30
4.55
HERBIVORE
6.92
BIOMASS
9.18
I I.50
(g)
FIG. 2. Difference
in net primary productivity
in experimental
( E ) microcosms and control ( C )
microcosms vs. grazing biomass of NO~TO@S ~@Zopterus. Brackets indicate range.
and 12.7%, rcspcctively ), perhaps bccausc
under
my microcosms wcrc maintained
more rigidly defined and maintained photoperiods and thermal regimes, and crossculturing was conducted during the first
2 weeks.
Effects of herbivore
addition
After the Notropis were allowed to graze
for 20 days, the grazing populations were
removed, and net primary productivity was
measured for three diurnal cycles in all
in net primary
microcosms. Diffcrenccs
vs. control
productivity
in experimental
microcosms during these diurnal cycles
were related to the biomass of the herbivores that had grazed in any particular set
of microcosms (Fig. 2). Enhancement of
net primary productivity by herbivore grazing was directly related to the biomass of
the hcrbivorc populations up to a certain
point, beyond which rates of net primary
productivity
were substantially lower than
those of the control microcosms (0.78 g
O2 rnd2 day-l difference bctwcen the control mean and the mean of experimental
microcosms 5a, b) . Thus, although grazing
in microcosms la, b, 2a, b, and 3a, b apparently enhanced net primary productivity,
overgrazing in 4 a,b and 5 a,b rcsultcd in
HERBIVORE
BIOMASS
(g 1
FIG. 3. Total dry weight stomach contents of
all grazing populations of Notropis vs. grazing stock
biomass.
statis tically significant
decreases in net
primary productivity.
Growth of the herbivore during the 20day grazing period was negligible, according to weight measurements of Notropis
before and after.
Stomach contents of all Notropis populations that had grazed in each of the experimcntal microcosm groups were dried
for 48 hr at 60°C and then weighed (Fig. 3).
The total weight of stomach contents was
directly related to grazing biomass, vcrifying the initial assumption that grazing
intensity of Notropis populations would bc
directly related to their biomasses (at least
within the period of the experiment).
Microscopic examination of fresh stomach contents showed chitinous exoskeleton material
in only two individuals (one from 4a, b and
one from 5a, b ) ; this rcinforccs the assumption that Notropis was deriving food matcrial almost exclusively from primary producers.
Fecal pcllct production by grazing populations of Notropis was watched for five
2-hr periods during the 20 days. The fecal
material was quite cohcsivc. The length
of the fecal pellets varied by several orders
of magnitude, and there was a significant
ENHANCEMENT
OF
NET
PRIMARY
Tuble 1.
pellets
0
2.30
4.55
6.92
HERBIVORE
9.18
II.50
BIOMASS(g)
FIG. 4. Fecal pellet production
rates (mg dry
wt hr-l of Notropis
populations
grazing in the
microcosms at various dcnsitics.
Darkened
areas
indicate two standard deviations about the mean.
Brackets indicate range.
correlation bctwecn length and dry weight:
Fl = O.BF, (r = O-92), where Fl = length
in millimeters and F, = dry weight in milligrams. The production rate of fecal pellets
by Notropis was directly related to the
biomass of the grazing population (Fig. 4).
Since the food sources for Notropis were,
and qualitatively,
nearly
quantitatively
identical in all microcosms, my hypothesis
was that rates of nutrient regeneration
would be directly related to fecal pellet
production by the fish. This hypothesis was
tested by semimicro, calorimetry and analyses for total nitrogen and phosphorus in
fecal material from each set of microcosms
in which Notropis populations had grazed
(Table 1). There was no significant diffcrencc in caloric content, nitrogen, or phosphorus content of the fecal material from
the diffcrcnt microcosms. The regeneration
rates of nitrogen and phosphorus were thus
directly related to the amount of fecal
pellets produced, which was in turn directly
related to the biomass of the grazing hcrbivorc populations.
If increases in nutrient regeneration were
responsible for the enhancement of net
primary productivity,
experimental groups
Analysis of samples of Notropis
obtained
Microcosm
No.
la,b
2a,b
3a,b
4a,b
5a,b
35
PRODUCTIVITY
from different
-1
Cal g
(dry wt)
3,863+193
4,192?68
4,060+153
4,135+110
3,820+137
fecal
sets of microcosms
Ash Total-r
(X) (mg g
74
68
82
79
67
117
123
119
111
120
1
Total-f
(ws f3 1
38
45
41
44
42
4a, b and 5a, b should have had an even
grcatcr cffcct than 3a, b. This was not the
cast (see Fig. 2). Thus, the enhancement
of net primary productivity in cxperimcntal
microcosms la, b, 2a, b, and 3a, b by low
to intermediate
intensities
of herbivore
grazing must have been largely independent
of nutrient rcgcneration rates and was prcsumably due to reduction of the standing
crop of primary producers.
Two possible sources of error in experi,mcntal design might affect this conclusion.
The first is that if nutrients arc rcgcncrated
by the rcleasc of soluble organic material
as well as by the production of fecal pellets,
my measurements of nutrient regeneration
were incomplete. If the rclcase rate of soluble organic material by Notropis is directly
rclatcd to the rate of fecal pcllct production,
the conclusion would remain unaffected.
If the relationship between thcsc two variables is markedly nonlinear or inverse, the
conclusion
could bc erroneous because
soluble release products might have stimulated net primary productivity in the microcosms. The fact that removal by grazing
was greater than rcplaccmcnt rates in 4a, b
and 5a, b argues against this.
Another possible source of error is that
bacterial colonization of the fecal pellets
could have increased both their nutrient
and caloric contents leading to an overestimation of regeneration rates brought about
by hcrbivorc grazing. Bacterial colonization
of detritus has been shown to alter the nutrient composition of the particles in estuarine ccosystcms (Odum and de la Cruz
1967), and the same phenomenon could
have occurred during these experiments.
However, if the assumption that bacterial
colonization of fecal material is directly re-
36
DAVID
latcd to fecal pellet production is valid, my
basic conclusions remain unchanged since
nutrient rcgcneration rates would be even
grcatcr in those microcosms which were
chronically overgrazed.
In the examination of production-consumption relationships, it is important that
the dynamic nature of the interaction bc
recognized. To paraphrase Slobodkin (1964),
a consumer population must cxercisc prudcncc in the exploitation
of a producer
population.
A large amount of litcraturc
indicates that a maximum sustainable yield
is often obtained by a consumer population
only by a reduction in its exploitation of a
food source. For example, optimal fisheries
yields often require reduced exploitation
rates and fishing intensities, particularly
dircctcd toward juvenile recruits (Bcverton 1953; nicker 1954a, b; Dickic and McCracken 1955). Producer populations, in
turn, may compensate for modcratc exploitation by a consumer population by inSlobodkin
( 1951,
crcascd productivity.
1960) and Slobodkin and Richman (1956)
conclude that the most apparent effects of
removal of newborn animals from a population of Daphnia pulicaria arc compcnsatory increases in growth rate and fecundity of the remaining population.
Watt
(1955) found that all indices of productivity
increased with increasing rates of exploitation of Trilohium confususm populations
and then dccreascd after a certain cxploitation threshold (optimum yield) was surpassed. Within certain limits, incrcascs in
net primary productivity in the microcosms
used in this investigation
suggest similar
compensatory mechanisms by primary producers to herbivore grazing.
It is interesting
that the bell-shaped
curve of herbivore biomass vs. net primary
productivity
diffcrenccs bctwccn cxpcrimental and control microcosms ( Fig. 2) approximatcs the first derivative of Pearl’s
(1930) model of population growth. Rcduction of’ producer standing crops by
grazing appears to initiate an increase in
turnover rates shown by increases in net primary productivity,
a response independent
of increased rates of nutrient regeneration.
C.
COOPER
Grazing intcnsitics that result in the rcduction of producer standing crops below K/2
in the Pearl model would thus be described
as overgrazing. The reductions in net primary productivity
at higher grazing intcnsities suggest that overgrazing occurred in
experimental microcosms 4a, b and 5a, b.
The range of herbivore population dcnsitics
in the experimental microcosms was well
within the observed ranges in natural stock
populations,
This suggests that undcrgrazing, optimal exploitation,
and ovcrgrazing may be frequent and concurrent
interactions in microhabitats of a balanced
aquatic ecosystem.
REFERENCES
Anpo~T, W.
1966. Microcosm studies on cstuarine waters.
1. J. Water Pollut. Contr. Fed.
38: 258-270.
BEVERT~N, R. J. II.
1953. Some observations on
the principles of fishery regulation.
J. Cons.,
Cons. Perm. Int. Explor. Mer 19: 56-68.
DE A~IEZAGA, E., C. R. GOLDMAN, AND E. A.
STULL. 1972. Primary productivity
and rate
of change of biomass of various species of phytoplankton
in Castle Lake, California.
Int.
Ver. Theor. Angcw. Limnol.
Vcrh. 18: in
press,
DICKIE, L. M., AND F. D. MCCRACKEN.
1955.
Isoplcth diagrams to predict equilibrium
yields
of a small flounder fishery. J. Fish. Rcs. Bd.
Can. 12: 187-209.
HARGIXAVE, B. T. 19,70. The cffcct of a dcpositfeeding
amphipod
on the metabolism
of
benthic microflora.
Limnol.
Oceanogr.
15 :
21-30.
JOIIANNES, R. E. 1968. Nutrient
regeneration
In M. R.
in lakes and oceans, p. 203-213.
Droop and E. J. F. Wood [cds.], Advances in
microbiology
of the sea. Academic.
MC~TIRE, C. D., R. L. GARRISON, II. K. PIIINNEY,
1964. Primary producAND C. E. WARREN.
tion in laboratory streams. Limnol. Oceanogr.
7 : 396-413.
ODUM, E. P., AND A. DE LA CRUZ. 1967. Particulate
organic detritus
in a Georgia salt
marsh-estuarine
ecosystem, p. 383-388.
In
G. II. Lauff
[ea.], Estuaries.
Amer. Ass.
Advan. Sci. Publ. 83.
in flowODUM, 11. T. 1956. Primary production
ing waters.
Limnol.
Oceanogr. 1: 102-117.
---,
AND c. hf. IIOSKIN.
1957. Metabolism
of a laboratory
stream microcosm.
Publ. Inst.
Mar. Sci. (Texas) 4( 2): 115-133.
PAINE, R. T., AND R. I,. VADAS. 1969. The effccts of grazing
L,
._ by_ sea urchins Strong!llocerz-
ENHANCEMENT
OF
NET
trotus
spp. on benthic
algal populations.
Limnol. Oceanogr. 14: 710-719.
RICKER, W. E. 1954a. Effects of compensatory
mortality
on populations.
J, Wildl. Manage.
18: 45-51.
-*
1954b.
Stock and recruitment.
J. Fish.
Rcs. Bd. Can. 11: 559-623.
PEARL, R.
1930.
The biology
of population
growth.
Knopf. 260 p.
study of
SLOIIODKJN, L. 13. 1951. A laboratory
the effect of removal of newborn animals from
a population,
Proc. Nat. Acad. Sci. U.S. 43:
780-782.
-.
1960. Ecological
cncrgy
relationships
at the population
level.
Amer. Natur. 94:
213-236.
-.
1964. Growth and regulation of animal
Halt,
Rinehart
and Winston.
populations.
184 p.
1’RIMAltY
PRODUCTIVITY
37
-,
AND S. RICHMAN.
1956. The effect of
removal of fixed percentages of the newborn
on size and variability
in populations
of
Dnphniu
pulicnria.
Limnol.
Oceanogr.
1:
209-237.
SM~II,
J. II:. [ED.].
1968. “Torrey
Canyon”:
Pollution
and marinc lift.
Cambridge
Univ.
196 p.
STRICKLAND, J. l3. II., AND T. R. PARSONS. 1968.
A practical
handbook
of seawater analysis.
Bull. Fish. Res. Bd. Can. 167. 311 p.
WATT, K. E. I?. 1955. Studies on population
productivity.
1. Ecol. Monogr. 25: 269-290.
1968. Carbohydrate
reserves of
WELCH, T. c.
sancl recdgrass under clifferent
grazing intcnsitics. J. Range Manage. 21( 4) : 216-220.
Submitted:
Accepted:
13 December 1971
25 August 1972