Download STRAYER, DAVID On the limits to secondary production

Comment
Limnol. Oceanogr., 33(5), 1988, 1217-1220
0 1988, by the American Society of Limnology
and Oceanography,
1217
Inc.
On the limits to secondary production
In closing their important study of bacterial dynamics in Lake Michigan, Scavia
and Laird ( 198 7) compared annual bacterial
carbon demands to autotrophic production
and concluded that (p. 10 17) “bacterial carbon demand is met by autotrophic production only if little of the latter is lost by other
means.” The bases for this conclusion were
their measurements of primary production
and bacterial production (which showed that
bacterial production was 63% of primary
production), their assumption that bacterial
growth efficiency was about 60% (which
would then imply that bacterial carbon demand was slightly greater than primary production), and their statement that (p. 1030)
“bacterial demand must be lower than autotrophic production.”
This last statement
is not true, and reflects a widely overlooked
property of secondary production. In this
comment, I explore briefly the limits on secondary production (which includes the production of heterotrophic bacteria as well as
that of heterotrophic eucaryotes) and reanalyze the data of Scavia and Laird.
Although it is true that the summed respiration of consumers cannot exceed the organic inputs to an ecosystem, summed carbon demand (i.e. assimilation) and summed
production of consumers both may easily
exceed the organic inputs to the ecosystem.
This counterintuitive
situation arises because organic carbon is recycled (albeit inefficiently) by consumers. Consider an ecosystem that receives organic inputs of 100
g of C and which is populated by consumers
with a growth efficiency (i.e. production/assimilation) of 60% (Fig. 1). After all of the
inputs have been assimilated by consumers,
40 g of C is lost in respiration and 60 g
Acknowledgments
A contribution
to the program of the Institute of
Ecosystem Studies of The New York Botanical Garden.
I thank N. Caraco, J. Cole, S. Findlay, G. Likens,
G. McManus, M. Pace, B. Peierls, and D. Scavia for
helpful discussions.
remains to be reassimilated by consumers.
When this tissue is reassimilated, it supports a further secondary production of 36
g of C, which supports a subsequent secondary production of 2 1.6 g, and so on. By
the time the entire 100 g of C has been
respired, a total secondary production of 150
g will have occurred. The summed carbon
demand of these consumers will have been
150/0.6 = 250 g of C. Both secondary production and consumer carbon demand are
thus much greater than organic inputs in
this system.
More generally, the total secondary production (P) and consumer carbon demand
(D) of an ecosystem can be calculated by
knowing the magnitude of inputs (I) to and
losses (L, from the ecosystem of interest,
along with the growth efficiency (G) of the
consumers in the system. All organic matter
that enters an ecosystem and does not leave
it must be destroyed by respiration (R). Thus
R=I-L.
By definition
G=P
Combining
that
P+R’
these two relationships,
P= &$I
we find
- u
and
D=- I-L
1-G’
Note that G is expressed as a proportion,
rather than a percentage, Z includes both
autochthonous
production and allochthonous inputs, and L includes all nonrespiratory losses (e.g. burial, fluvial outflow). Although these equations refer to an ecosystem
in steady state, it is simple to add a storage
term to the equations if standing stocks of
organic matter in the system are changing.
Comment
1218
a
3 consumer
0
P=36
R=24+f-i
2 consumer
0 P=60
R=40ll
1 consumer
4
0 I=I00
Fig. 1. Schematic diagram of carbon flow through
a consumer community with a growth efficiency of 60%
that receives inputs (I) of 100 g of C. Numbers of
arrows show production (P) and respiration (R) associated with each cycle of assimilation, in units of g of
C (see text).
Several interesting points arise from an
analysis of the summed production and carbon demand of the consumer community
as a function of the retentiveness of the ecosystem and the growth efficiency of consumers (Fig. 2a, b). The conditions for secondary production to exceed organic inputs
are fairly stringent, but likely to be met in
some retentive ecosystems, such as large
lakes or the open ocean. Secondary production is large relative to organic inputs in
many ecosystems. As a consequence, the
food available to consumers (including bacteria) is not overwhelmingly
dominated by
plant material, but consists of a fairly even
mix of plant tissue and consumer tissue.
Because secondary production can be calculated from a knowledge of organic inputs
and losses from the ecosystem and the
growth efficiency of consumers, this estimate of secondary production can be used
as a rough check on the adequacy of direct
estimates of secondary production (e.g. Table 1). However, in doing so it is important
to keep in mind that consumer growth efficiencies can vary widely (e.g. Humphreys
1979; Schroeder 198 1) and are not always
known accurately. Conversely, if one has
good direct estimates of secondary production, one can back-calculate the effective
C
c
Retentiveness
P/O)
Fig. 2. Some energetic properties of the consumer
community as a function of consumer growth efficiency
(G) and retentiveness [(inputs - nonrespiratory
losses)/inputs] of the ecosystem: a- secondary production
(expressed as a percentage of organic inputs); b-consumer carbon demand (expressed as a percentage of
organic inputs); c-minimum
number of cycles of assimilation by consumers.
growth efficiency
munity.
of the consumer
com-
P
C=
”
(I - L + P) For example, the growth efficiency implied
Comment
Table 1. Secondary production in Mirror Lake, New
Hampshire. Data from Jordan et al. (1985), modified
by Strayer and Likens (1986).
Secondary
production
(g C m-* yr-‘)
Direct estimate
Pelagic bacteria
Benthic bacteria
Metazoan plankton
Metazoan benthos
Fish
Total direct estimate
6
10.5
2.5
6
0.2
25.2
Indirect estimate
Organic inputs
Nonrespiratory
losses
Assumed growth efficiency
Summed secondary production
60
24.9
0.5*
35
* From Humphreys
1979, Schroeder
1219
Table 2. Partial organic carbon budgets for nearshore Lake Michigan: annual- the entire nearshore
ecosystem on an annual basis; summer-the
epilimnion in summer. Based on data from Fahnenstiel and
Scavia (1987) Scavia and Fahnenstiel(l987)
and Scavia and Laird (1987).
Annual
198 1, and Jordan
1985.
by the data from Mirror Lake (Table 1) is
4 1% (only a very approximate estimate in
this case due to uncertainties in measuring
benthic production).
Before moving on to the data from Lake
Michigan, it may be useful to introduce one
more parameter that is implicit in this analysis: the minimum number of cycles of assimilation by consumers needed to destroy
the organic matter that was brought into or
produced autotrophically
in the ecosystem.
The amount of organic matter that remains
in an ecosystem after n cycles of assimilation is ZGn, assuming that all organic inputs
are available to consumers. This term must
equal the nonrespiratory
losses from the
ecosystem. As a result,
If some organic inputs are unavailable to
consumers (e.g. if they are exported before
they can be used), then the actual number
of cycles of assimilation will be >n. Note
that n is not the same as the average number
of cycles made by an atom of organic carbon
as it passes through the ecosystem, because
less and less carbon participates in each succeeding cycle of assimilation.
The distribution of n as a function of consumer growth
efficiency and ecosystem retentiveness is
shown in Fig. 2c.
Considering first the annual carbon budget of the entire nearshore ecosystem of Lake
Michigan, my reanalysis of the data of Sca-
Summer
(g C mm2 yr-‘)
Inputs
Nonrespiratory
losses
Growth efficiency
Summed secondary production
Pelagic bacterial production
Carbon demand by all consumers
Carbon demand by pelagic
bacteria
Minimum cycles of assimilation
232
8
0.6
336
142
560
29.4
9.4
0.6
30.1
26.3
50.1
224
6.6
43.8
2.2
via and Laird (Table 2) supports the following conclusions. Secondary production of
consumers in Lake Michigan
is higher
(1.45 x ) than organic inputs. Even if one
assumes that the eucaryotic consumers have
a lower growth efficiency than the bacterial
consumers, pelagic bacterial production accounts for roughly half of the secondary production in the lake. The fact that most or
all of the primary production passes through
the pelagic bacteria does not imply that other consumers are unimportant.
Carbon
available for assimilation by consumers in
Lake Michigan is much greater (2.4 X) than
organic inputs to the lake and much more
than adequate to support the bacterial demands calculated by Scavia and Laird. There
is considerable reassimilation
of organic
carbon in Lake Michigan: at least six to seven cycles of assimilation by consumers must
take place to respire the necessary 224 g C
m-2 yr- l, assuming a 60% growth efficiency. Table 2 also includes a partial carbon
budget for the epilimnion in summer, a season for which Scavia and Laird reported the
apparently problematic situation of bacterial production being equal to primary production. My reanalysis shows, however, that
there are ample inputs of organic carbon to
support contemporaneous bacterial production, even in this situation. Thus, budgetary
considerations
provide weak evidence at
best for “temporal disequilibrium”
in Lake
Michigan.
These recalculations change the picture of
the pelagic ecosystem of Lake Michigan from
one in which autotrophic carbon is barely
Comment
1220
sufficient to meet bacterial needs (let alone
the needs of other consumers) to one in
which bacterial needs are very much less
than available carbon, thereby solving the
budgetary problems discussed in the closing
paragraphs of Scavia and Laird’s paper.
Similarly, an explicit consideration of the
recycling of organic carbon by consumers
may help to explain apparently excessive
demands of consumers in other ecosystems,
especially retentive systems such as the open
ocean.
David Strayer
Institute of Ecosystem Studies
The New York Botanical Garden
Box AB
Millbrook
12545
References
FAHNJZNSTIEL,G. L., AND D. SCAVIA. 1987. Dynamics
of Lake Michigan phytoplankton:
Primary pro-
Limnol.
Oceanogr., 33(5), 1988, 1220-1224
0 1988, by the American
Society of Limnology
and Oceanography,
duction and growth. Can. J. Fish. Aquat. Sci. 44:
499-508.
HUMPHREYS, W. F. 1979. Production
in animal populations. J. Anim.
and respiration
Ecol. 48: 427-
453.
JORDAN, M. J. 1985. Bacteria, p. 246-250. In G. E.
Likens [ed.], An ecosystem approach to aquatic
ecology: Mirror Lake and its environment. Springer.
-,G.
E. LIKENS,AND B.J. PETERSON. 1985. Organic carbon budget, p. 292-30 1. In G. E. Likens
[ed.], An ecosystem approach to aquatic ecology:
Mirror Lake and its environment.
Springer.
SCAVIA, D., ANDG. L. FAHNENSTIEL. 1987. Dynamics
of Lake Michigan phytoplankton:
Mechanisms
controlling
epilimnetic
communities.
J. Great
Lakes Res. 13: 103-120.
AND G. A. LAIRD. 1987. Bacterioplankton
in
Lai<e Michigan: Dynamics, controls, and significance to carbon flux. Limnol. Oceanogr. 32: 10 171033.
SCHROEDER, L. A. 198 1. Consumer growth efficiencies: Their limits and relationships to ecological
energetics. J. Theor. Biol. 93: 805-828.
STRAYER, D., AND G. E. LIKENS.
1986. An energy
budget for the zoobenthos of Mirror Lake, New
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Inc.
On the role of bacteria in secondary production
Our recent work on the role of heterotrophic bacterioplankton
in Lake Michigan
(Scavia et al. 1986; Scavia and Laird 1987)
has led to the assertion that bacterial secondary production is high relative to autotrophic primary production.
We found
that annual areal bacterial carbon demand
was about equal to that supplied through
phytoplankton
net production; in the summer epilimnion, however, that demand was
much greater than contemporary
phytoplankton supply. We concluded our second
paper with two uncomfortable
observations. First, because bacterial carbon demand was approximately
equal to organic
carbon supply, carbon demand by consumers, other than bacteria, could not be
met by phytoplankton
production (or the
Acknowledgments
GLERL Contribution
622.
I thank H. Ducklow, G. Fahnenstiel, G. Laird, and
H. Vanderploeg for reading an earlier draft of this
manuscript.
estimates of phytoplankton and/or bacterial
production were wrong). Second, bacterial
carbon demand that was greater than phytoplankton supply in the summer epilimnion suggested a temporal disequilibrium,
where bacterial summer demand is met partially by winter and spring algal production.
Strayer’s ( 1988) reanalysis of our data sheds
important light on the commonly assumed
restriction that secondary consumption must
be equal to or less than primary production.
He demonstrates that because organic carbon can cycle within the food web, this restriction is false. I agree with his reassessment and recognize that, because of this
relaxed and more appropriate limit to secondary production, our first uncomfortable
observation is more acceptable.
This reanalysis is important
because
highly retentive, autotrophically driven Lake
Michigan certainly supports a rich and productive array of secondary consumers in addition to bacteria. It is also important for
other large systems. Recent reports of very