AM. ZOOLOCIST, 8:Gl-69
(1968).
The Role of Soil Arthropods in Community Energetics
MANFRED D. ENCELMANN
Department of Natural Science, Michigan State University,
East Lansing, Michigan 4S823
SYNOPSIS. Though the primary development of principles of energetics was pioneered in
aquatic studies, considerable information has accrued from more recent investigations of terrestrial species. Studies of soil organisms—particularly arthropods—have given us some understanding of the applicability of principles of energetics to terrestrial communities. Data from
soil communities have yielded an annual energy budget for oribatid mites, ecological efficiencies
for two trophic levels, and a series of herbivore:carnivore ratios for a number of communities.
Energy-flow analyses of the problems of species abundance in community organization, the relationship of population production and maintenance, and the energy relationships of the soil to
above-ground communities have also been attempted. As data accumulate, however, the inadequacy of the Lindcman model becomes apparent, and there are prospects for change in this
conceptual scheme.
Much of the earliest work on energy
transfers in ecological systems was done in
fresh-water lakes, and investigations of this
nature culminated in the important theoretical formulations of Lindeman (1942).
Viewed in this historical perspective, it is
interesting to note that Bornebusch (1930)
investigated the metabolism of forest
arthropods more than 10 years before
Lindeman's paper appeared. Bornebusch,
a forest entomologist, was strongly influenced in his thinking by the contemporary
physiologist, Krogh, who emphasized that
the total metabolism of forest arthropods
was as important a consideration as knowledge of total numbers. At Krogh's urging,
Bornebusch studied soil animals of five different forest types, not only from the standpoint of composition and abundance of
species, but also in terms of their metabolic
activity. Although Bornebusch's work suffered from certain technical inadequacies,
it continues to provide an important baseline for contemporary research. In fact,
most of the studies in England and Europe
which can be considered "energetic" are
not patterned after Lindeman's model, but
follow the Bornebusch tradition of emphasizing respiratory metabolism (e.g., the
work of Macfadyen (1963) in England, and
Berthet (1963) in Belgium). There is, however, no reason why the soil community
cannot be considered in terms of Lindeman's views.
Let us look just for a moment at the
61
basic structure of the Lindeman system. In
Figure 1 the trophic level is represented by
the circular portion of the diagram. The
trophic level consists of the energy within
the bodies of the individual populations
assigned to the level. The populations form
a superstructure through which energy
flows. The trophic level is not stable, for
if its energy were cut off all the populations
would die and the trophic level would disappear. And if the energy flow were to be
resumed, a trophic level would reappear,
but it might well have an entirely different
species composition than before. In fact,
populations do not make up trophic levels.
Rather it is the energy that binds the elemental substances in the bodies of individuals. The mass of the body (i.e., carbon,
nitrogen, hydrogen, etc.) is not represented
at all in the Lindeman trophic level. This
point emphasizes the level of abstraction
with which we are dealing. The arrows in
Figure 1 indicate the flow of energy
through the trophic level, and \x represents
ingestion. Of the total ingested energy, a
portion enters the energy pool of the trophic level as assimilated energy, and another
portion is egested. If one eats a handful of
sawdust (with an energy content of about
5000 cals/g), it enters the digestive tract,
but in 48 ± hours it will be defecated as
sawdust and it will still contain 5000 cals/g
of energy. The sawdust never entered another trophic level in spite of the fact that
it was ingested. In other words, the lumen
62
MANFRED D.
TO DECOMPOSER
SYSTEM
HEAT LOST
TO SYSTEM
TO NEXT TROPHIC
LEVEL
FIG. 1. Diagram of a single trophic level of the
Lindeman system. Arrows indicate the direction of
energy flow through the level. The symbols
"Lambda," "D," and "R" are used in the manner
of Lindeman (1942).
of the intestine is simply a tunnel of the
external environment through the body as
far as energetics are concerned. The other
arrows in Figure 1 represent the different
pathways by which assimilated energy may
leave or be used in a given trophic level:
respiration, physiological death, and death
by predation. The simplest manner in
which to visualize a community is to imagine three trophic levels: primary producers
(plants), herbivores (plant eaters), and
carnivores (eaters of other animals). Actually, of course, the community is much
more complex.
Any useful model should not only accurately reflect nature, but also exhibit simplicity and order. The part of nature I
choose to consider is the soil system—a
portion of the ecosystem with several attributes useful in energy studies. One of the
ENGELMANN
most intriguing features of the soil fauna
is the enormous diversity of organisms,
many of them very poorly understood.
There is an almost endless variety of creatures—many no bigger than a speck of dust
—living their clandestine lives among the
rotting leaves and twigs of the forest floor:
mites and collembolans, pseudoscorpions
and centipedes. These tiny creatures are
everywhere—just one stoop away in the
nearest clump of grass or bunch of moss;
in frozen winter earth, moist fall and
spring soils, or dry summer sod. Animals
can be obtained in great numbers from a
lawn or any mulched area almost any time
of the year (the poorest time is mid-summer). All that is necessary to bring them
forth is a goose-neck lamp and coffee can
(with a hole cut in the bottom and a screen
inserted) set over a beaker of water.
Twenty-four hours of heat from the lamp
will drive the animals from the soil into
the beaker. A few quick strokes of a camel's
hair brush will remove them to a salve jar
lined with moist cellucotton, paper towel,
or filter paper; and observations can be
made for hours or days. With proper feeding the animals will go through their life
cycles, and cultures can be kept for months
or even years.
Soil organisms are not only diverse, but
also represent every trophic level—producers, herbivores, carnivores, and parasites.
Populations are usually dense, and samples
can be relatively small. A soil sample 2"
in diameter from glacial soils of a Michigan
old-field have yielded as many as 450 individuals representing 13 species of oribatid
mites alone. From 35 samples, Hairston
and Byers (1954) counted a total of over
74,000 individuals of 177 different kinds
of soil arthropods taken from this same
old-field soil—an average of over 2000 individuals per sample. Soils over large areas
are fairly uniform, and to that degree, observations can be repeated. There is more
uniformity in species composition than in
numbers. The soil system lends itself to
manipulation. Clipping, fertilizing, shading, watering, and numerous other simple
treatments can be used to alter the conditions in soil, thus exposing the effects of
SOIL ARTHROPODS AND COMMUNITY ENERGY FLOW
63
TABLE 1. A list of the major groups of organisms found in soils.
Group
Bacteria
Auto trophic
Heterotrophic
Actdnomycetes
Fungi
Protozoa
Nematoda
Kotifera
Annelida
Arthropoda
Hexapoda
Coleoptera (mostly larval forms)
Collembola
Diptera (all larval forms)
Acaxina
Function and Food Source
Autotrophic; synthesis of carbon compounds.
Decay organisms; rapid decomposers.
Decay organisms; slow decomposers.
Decay organisms; rapid decomposers (one predator).
Herbivorous on certain bacteria or predaceous.
Feed on bacteria; predatory.
Feed on bacteriaFeed on dead plant material.
Predatory or mycophagous.
Feed on fungi (predatory on nematodes?).
Feed on bacteria and fungi; predatory.
Feed on fungi and bacteria; predatory.
laboratory approaches (Engelmann, 1961).
such alterations on soil populations.
Studies of the soil system are not, how- By applying these estimates to counts of
ever, without problems. The taxonomy of field populations, an energy-flow chart was
the U. S. soil arthropods is, in general, constructed (Fig. 2). These values were
seriously incomplete. Also, because the ani- estimated for animals found in an area one
mals may be extremely small, technical meter square and 12.5 cm deep. As can be
problems arise when equipment must be seen, 75% of the ingested energy is egested,
miniaturized and/or sensitized to deal with and of the 25% assimilated 95% is dissipated in respiration. Because the figures
such species.
The major groups of soil organisms are for each arrow were obtained separately,
summarized in Table 1. Many groups the total energy budget does not balance
which are present in the soils are not rep exactly. There is a 5% deficit in the inresented in this table. Any one of three gestion-assimilation portion of the diagram
reasons may account for this situation: (1) and a 16% surplus in the figures for methe animals are a minor component in the tabolism.
One of the major concepts of the Lindesoil (e.g., algae, centipedes, millipedes,
pseudoscorpions, moles); (2) the animals
may burrow in the soil, but feed primarily
upon components of the above-ground community {e.g., ants, shrews, foxes, etc.); or
AS9IMILATE0
Z.OSBcall.
(3) the animals, although abundant, may
not yet be recognized as members of the
soil community {e.g., harvestmen, robins).
STANDING CROP
^RESPIRATION
27Ocal>.
" * 1.965 coll.
This paper is concerned with the soil arthropods, which are second only to the
nematodes in abundance in the soil. What
ESESTED
EGO
ADULT
7,686 colt. MORTALITY
MORTALITY
have soil arthropods contributed to our
270cal>.
!6Ocol«.
knowledge of community energetics?
First, we have been able to make some
estimates of the total productivity of some 7.686 (-2.058 = 9.744 <504CALS. UNACCOUNTED FOR)
soil arthropods. Using the Oribatei (an 1.965 + 270+160 = 2395 (337 CALS. OVERESTI MATEID)
2. Annual energy balance sheet for the oribaabundant group of mites found in most FIG.
tid mites found in the soils of an old-field in southsoils), I estimated ingestion, egestion, res- eastern Michigan. Original data from Engelmann
piration, and reproduction, using several (1961).
T
64
MANFRED D.
ENCELMANN
TABLE 2. Average nurtibers of individuals, Viomaxs, and
respiration of the soil arthropods found
in a. Michigan old-field. Values pertain to volume 1 m2 and 20.J cm deep. (Data from Engelmann,
1961).
Category
ACARINA
Parasitoid
Oribatid
Sarcoptoid
Trombidoid
Eupodoid
Pauropoda
Symphyla
Protura
INSECTA
Japygida
Podurid
EiLtomobrjdd
Srninthurid
Average
Number
Biomass (nig)
Standing Crop
(cal)
Respi ration
(cal)
Pood Habits
12414.8
87582.6
4721.8
] 797.8
9191.0
20396.4
2543.0
236.4
679.9
51.3
662.1
9.330
28.596
3.406
1.722
3.282
5.204
1.974
0.042
0.244
0.418
2.387
46.650
142.980
17.330
8.610
16.310
26.025
9.870
0.210
1.220
2.090
11.935
354.37
115.96
138.66
53.33
136.42
233.32
67.06
2.57
10.73
11.52
60.53
Cam.
Herb.
Herb.
Cam.
Herb.
Herb.?
Cam.
Cam.?
Herb.
Herb.
Herb.
388.5
7764.2
243.2
175.7
13.472
7.534
2.095
0.121
67.365
37.670
10.475
0.605
298.78
274.81
53.60
3.64
Herb.
Herb.
Herb.
1
TABLE 3. Estimated ecological efficiencies of the soil herbivores of <j Michigan old-field. (Data
from Engelmann, 1961).
Assimilation (%)
Carnivores
32
25
14
Herbivores
32
25
14
32
25
14
32
25
14
Without
Japex
18.9
15.4
9.6
23.0
18.9
12.0
32.9
28.1
18.9
man model is the efficiency of transfer from
one trophic level to another; sometimes
called Ecological Efficiency (EE). For soil
arthropods this can be given as:
EE =
cals invested by carnivores
X 100.
cals ingested by herbivores
The above formulation essentially asks
"How effectively do the members of one
trophic level use the members of another?"
Applying the information gained from
populations of oribatid mites, energy estimates were made for the more extensive
field data of Hairston and Byers (1954).
These data are summarized in Table 2.
The figures were used to estimate ecological efficiency. Two uncertainties arose in
these last calculations. What is the effi-
Ecological efficiency (%)
Japex
Japex
Carnivorous
Herbivorous
27.5
22.9
14.7
32.7
27.5
18.1
45.4
39.4
27.5
16.9
13.7
8.5
20.7
16.9
10.6
30.1
25.5
16.9
ciency of assimilation by animals in the
field? An assimilation of 32% represents a
starvation regime, while 14% represents a
surfeit. The second uncertainty lay in the
food habits of the thysanuran, Japex, which
may be carnivorous or herbivorous. Because of these problems I have calculated a
spectrum of possible efficiencies, rather than
a single estimate, and this range of values
is given in Table 3. The array of ecological efficiencies ranges from 8.5% to 45.4%,
depending on the assumptions adopted,
but most of them lie between 14 and 28%.
These efficiencies fall within the range of
values found for various aquatic communities and support the applicability of the
Lindeman system to terrestrial as well as
aquatic communities.
65
SOIL ARTHROPODS AND COMMUNITY ENERGY FLOW
TABLE 4. The comparison of percent or rani; of annual calorie dissipation, and predator:hcrbivorc ratio of
different trophic groups found in nine natural communities on the British Isles and the European Continent. (Data from Macfadyen, 1963).
2
1
Community
4
Oak
Mull
3
Grass- Limestone Juncus
Moor
land
Grass
8
Herbivore rank
Herbivore %
22.29
Large decomposer
4
rank
L. decomposer % 27.36
Small decomposer
4
rank
S. decomposer % 39.32
Predator rank
6
10.95
Predator %
Rank total
1
Kcal/yr
Carnivore:herbivore
Ratio
0.1232
5
Beech
BH
6
Beech
Mull
7
Beech
Mull
8
Spruce
Mull
9
Spruce
BH
3
31.77
4
30.85
9
20.36
6
27.25
32.08
5
28.36
1
32.91
8
1.21
2
33.49
5
8.42
3
31.24
6
3.46
7
3.3
9
0.54
1
64.18
6
29.87
2
46.06
8
23.92
3
45.41
1.38
8
2.85
7
5.79
3
25.15
5
17.58
4
19.05
2
4
7
9
5
3
8
6
0.0140
0.0293
0.0614
0.3360
0.2133
0.2353
0.4675
0.5981
7
25.65
1
55.54
9
17.38
9
When we consider the uniformity of energy flow through communities, the data
from soil arthropods prove more perplexing. Because nearly 80-90% of an animal's
assimilated energy is normally respired, it
is not surprising that early attempts to compare different communities relied upon
measurements of metabolism. Macfadyen
(1963) analyzed the animals found in the
soil of several different communities in
England and Europe. I have re-analyzed
these data and estimated the calories consumed by each trophic group (Table 4).
Then I have calculated the respiration of
herbivores and carnivores as fractions of
the total community respiration (Engelmann, 1966, p. 94). If there is functional
uniformity in communities, the ratio of
calories processed by the carnivores versus
the herbivores should be about the same
for all communities. As can be seen from
Table 4, the data on soil arthropods do not
support that hypothesis (the ratios vary
from 0.01 to 0.59). The only trophic level
which made up a relatively constant percentage for all nine communities was the
Herbivore level (20-33%). The implications of these data are not yet clear.
In reviewing the productivity of animals
in natural communities (Engelmann, 1966),
I developed an empirical relationship relating net productivity to respiration (sec
5
36.48
2
31.86
7
29.12
1
37.43
Table 5 and Fig. 3). The relationship for
.1
i
X
/
2
-
LOG Y « 2 .59 + 1.75 LOG X
Va
5
0
U
Z
<
1
/
14
0
/
t
8
X
.•
2/
/
/o
/
f
.8
/
/
o
/9
1
4°
o
/
X
/ LOG V • 62* .86LOGX
X
/
.J
.
i/
1
i
t
1
t
I
i
.
*
i
i
LOG NET PRODUCTIVITY
FIG. 3. Relationship between maintenance metabolism and net productivity. Open circles represent data from homeotherms, the "X's" data from
heterotherms. The regression for the heterotherms
(the solid line) is significant at the 5% level. Hased
on Engelmann (1966^.
66
MANFRED D. ENGELMANN
heterothermic animals represented by the
solid line is significant. The significance
of the dotted line—pertaining to homeotherms—has not yet been established. Most
of the points relating to heterotherms are
based on populations of a single species.
However, point #9 represents the 0.43
Kcal/m2/yr combined production of 22
species of oribatid mites in an old-field. If
the relationship of maintenance metabolism to net production implied by the regression equation is meaningful, the aggregate production of 22 species should be calculable in terms of the estimated metabolism of the individual populations. This
procedure is illustrated in Table 6. The
o
en
3 §
-^ to~ S o
6 0 0 3 0
•» r-l*. „ iH
- ^^^J ^ J « ffl
s - a - a i S^ "^ 'O fi 7a 3_o3s^- ^O o
'S
0) S
K
t/1 CO tO
c;
n
CJ C3
pr-
^ ^ i—i
Co ^— ^-<
5 2 3 2{r;tc
CJ 0) O S
OOOaiO
TABLE 6. Net reproduction of oribatid mites calculated from the formula for maintenance-net reproduction. (Respiratory data from Engelmann, 1961.)
CO
to
s
J
•S
Species
Number*
•££§
Si**
3 £.2
(M
4.
1
101
102
103
108a
108c
108d
108c
109
•3 5 S
no
111
CJ^COIOHOMHH
^OriOW
Cl C
O
tM
(M
113
114
115
117
120
C\J IO T
o
00
to <
COJDC
•*o<onioi
O IO o i »O IO O CO •
C i CO CM 1 ^ (M
CO r
OJ
CM
CO IO » ; CO IC>
CO 1 ^ t o CO IO
to
M
121
126
128
TOTAL
O O CD O
e
rCl
8
fe o s *a
< IS
Species Name
Net
Productivity
in cal/m 2 /yr
Tectocepheus velatus
Scheloribates pallididvs
Camisia sp.
Oppia nova
Cultroribula sp. (divergens)
Suctobelba
Oppia minutissima
lihysotriiia ardua
Peloribates curtipilus
Allogalumna alaium
Adult Oppidae
Trhypochthonius sp. {tectorum)
Belba sp.
Thyrisoma ovata
Liochthonvus perpusillus and
Brachychthonius jugatus
Zygoribatula rostrata
Tarsonomid
Tarsonomid
86.0
39.3
25.0t
32.4
9.5
4.4
0.6
28.1
27.4
17.5
1.1
69.5
0.5
14.5
17.2t
27.6
13.5t
14.31
428.4
* System of identification used by Engelmann
(1961).
t Assumed 1/3 population productive.
resulting total (0.428 Kcal/m2/yr) is almost
identical to the independently derived estimate of 0.430 Kcal. I will not make too
much of the apparently remarkable accord
because the agreement could be somewhat
fortuitous. However, I do believe that the
equation can give first approximations on
fee the productivity of populations.
Energetics studies also shed light on other
questions relating to community organization, e.g., the problem of relative abun-
67
SOIL ARTHROPODS AND COMMUNITY ENERGY FLOW
100
x-OBSERVED
— PREDICTED
x x
10
NUMBER OF
INDIVIDUALS
0.1 •
*x
I
5
10 15 20 25
INTERVAL
some functional measure (rather than simply numerical abundance) may be a more
meaningful way to consider community organization. Figure 5 shows total respiration of old-field mites plotted against the
prediction of the model. Although there
are still appreciable disparities, the general
agreement seems improved.
Finally, studies on soil systems have given
us a different view of the trophic-dynamic
organization of the old-field community
(Fig. 6). In addition to the above-ground
levels, there are at least three soil levels
which are dependent upon the energy falling to the soil in the form of dead bodies
and feces. The soil trophic levels act more
or less as does the Krebs cycle, eventually
respiring all energy and dissipating it as
heat. This concept is particularly pleasing,
because it leaves no calories "sitting
around" to be accounted for in some undefined population or trophic level.
These are the facts and concepts contributed by studies on soil arthropods, but
1000
FIG. 4. Comparison of species abundance of oribatid mites from the soil of an old-field with the
"broken-stick" model. From Engelmann (1961).
dance of species (see Hairston, 1959; Whittaker, 1965). Several mathematical models
have been developed—mostly empirical and
with no clear biological basis. However,
MacArthur (1957) proposed three hypotheses with an underlying biological rationale.
These models differed in the manner in
which the environment was assumed to be
partitioned among its occupants. One of
these models, which visualized the environment as being subdivided into a number
of contiguous but non-overlapping niches,
has been tested with data from many kinds
of animals (see King, 1964, for a review).
In general, it has been found that the
model underestimates the abundance of the
most common species and overestimates the
abundance of rare species. The problem is
well illustrated by Figure 4, in which the
estimated relative abundance of old-field
mites is compared with predictions of the
model. The point of this discussion is that
x -OBSERVED
--PREDICTED
RESPIRATION
CALORIES
5
10 15 2025
INTERVAL
FIG. 5. Comparison of species abundance of mites
as represented by respired calories with the MacAuhur "broken-stick" model. From Engelmann
(I'JCl).
68
MANFRED D.
RADIANT ENERGY
FROM THE SUN
ENGEUMANN
time. Currently, the discipline of energetics is undergoing a change. Investigators are becoming disenchanted with the
concept of the trophic level. How does one
cope with the omnivore, or with the holometabolous insect whose larvae feed differently from the adults? How can one
enumerate all of the populations in a given
trophic level? These questions and others
call for innovations in the Lindeman model
as it is now conceived. I believe that these
changes will be more accurate descriptively, will be more mathematically elegant,
and will provide more precise direction to
research on function and organization of
the community.
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HEAT AND RADIATION
TO OUTER SPACE
FIG 6. A schematic representation of the energy
flowing through the various above-ground and soil
trophic levels of an old-field in Michigan. Fiom
Engelmann (1961).
we must recognize that these ideas are not
necessarily immutable. In energetics as in
all endeavors of science, the facts hang on
beautifully contrived constructs which we
call models and theories. Too often we
think of the theories and models as facts,
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the human mind. Although theories and
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for research, these constructs of. the human
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