Reprinted from BioScience
The Influence
on
of
Arthropods
Ecosystems
T. R. Seastedt and D. A. Crossley, Jr.
Arthropod interactions with plants and microbes influence the amounts of living
and dead organic matter and transfers of nutrients in terrestrial ecosystems. Arthropods in the canopy have their greatest effect on mobile elements such as potassium,
whereas soil detritivores influence mineralization rates of less mobile elements
such as nitrogen, phosphorus, and calcium. Nominal (baseline) herbivory and detritivory combine to speed nutrient cycling and reduce standing crops of decaying
plant materials. (Accepted for publication 10 August 1983)
Arthropods are the most abundant
herbivores and detritivores in many terrestrial ecosystems. Research conducted
in the late 1960s and early 1970s (largely
in connection with the International Biological Program) documented the densities, diversities, standing crops, energetics, and nutrient contents of these
organisms in many North American biomes. The results indicated that the
amounts of mass, energy, and nutrients
in and flowing through arthropods were
much smaller than amounts measured
for plants and microbes (e.g., Dyer
1977). Perhaps for this reason, arthropods were often ignored in descriptive
and quantitative ecosystem models.
However, beginning in the mid 1970s
and continuing to date, a large number of
studies have indicated that arthropods
have a strong indirect influence over
plant productivity and nutrient cycling
processes (e.g., Crossley 1977, Dyer et
al. 1982, Kitchelletal. 1979, Krivolutsky
and Pokarzhevsky 1977, Mattson and
Addy 1975). Herbivores have attracted
considerable attention, and Mattson and
Addy (1975) argued that herbivores have
more influence on the ecosystem than do
detritivores. Herbivores act on living
plants, whereas detritivores act on nonliving detritus. The herbivore-plant interaction has more potential for both
positive and negative feedback loops
than the detritivore-detritus interaction.
Herbivores have a propensity for periodic population outbreaks. When these
outbreaks occur, the arthropods may
have a very different effect from that
which occurs in most years (Schowalter
Seastedt is with the Division of Biology, Kansas
State University, Manhattan, KS 66506, and Crossley is with the Department of Entomology and
Institute of Ecology, University of Georgia, Athens,
GA 30602. © 1984 American Institute of Biological
Sciences. All rights reserved.
March 1984
1981, Schowalter et al. 1981), and the
effects on ecosystems are markedly different from the usual. A large number of
litter and soil arthropods (often labeled
detritivores) feed primarily on fungi.
Fungivore-fungus interactions also result in positive and negative feedbacks
within the detritus food web.
Woodmansee (1978) and Kitchell et al.
(1979) provided numerous examples of
consumers translocating and transforming mass and elements of other ecosystem components thereby modifying nutrient transfers. We will discuss
terrestrial herbivore and detritivore (including fungivore) arthropods and suggest that there is a consistent pattern for
arthropod effects on ecosystems. At
nominal or baseline levels of consumption, arthropods speed nutrient cycling,
have only minor effects on plant productivity, and have a strong influence on
detritus standing crops. Elemental cycling appears directly correlated with the
amount of arthropod feeding activities,
whereas net primary productivity exhibits a curvilinear response to feeding activities. The plants may increase production in response to low-to-moderate
herbivory, but extensive herbivory can
reduce annual production (e.g., Dyer et
al. 1982, Hilbert et al. 1981, McNaughton 1983). Net primary productivity does
not vary greatly over the levels of consumption observed when there are no
outbreaks of herbivores.
Interactions between plants and herbivorus arthropods and between soil microflora and soil arthropods have, over
evolutionary time, influenced present
ecosystem structure. These influences
are not adequately depicted by discussing standing crops (g/m2) of biota or
fluxes (g/m2/yr) of mass or elements.
There are energy costs associated with
the production of antiherbivore or antifungivore defenses, and even in the absence of consumers some energy is allocated to these chemicals (e.g., Schultz
and Baldwin 1982). This baseline commitment to defense represents energy
that cannot be used in the production of
tissues used for nutrient uptake or carbon fixation. Janzen (1979, 1983) believes that this energy cost is very large
and cannot be measured using traditional
control versus defoliation-type experiments. Our interests, however, are directed at the effects of arthropods on
ecosystem phenomena over relatively
short periods of time (years or decades),
and these effects can be described in
terms of mass or nutrient transfers. We
have just scratched the surface, but it is
an interesting and measurable surface.
THE COUPLED ECOSYSTEM
A simplified nutrient cycling model
emphasizing consumers and their regulation of nutrient transfers is illustrated in
Figure 1. Litter microbes and detritivore
arthropods are "downstream" from the
canopy and roots and are potentially
responsive to energy inputs resulting
from plant-herbivore activities (e.g.,
Swank et al. 1981). Conversely, the activities of the detritivore food web influence the mineralization of organic matter, and detritivores are therefore
"upstream" from plant roots and mycorrhizae. A change in the feeding activities
of either herbivore or detritivore groups
can therefore influence the entire system. The amounts of mass or nutrients
represented by and directly flowing
through arthropod components are usually small, as is the component containing arthropod remains (Seastedt and
Tate 1981). The standing crop of arthropod feces has not been quantified in any
terrestrial ecosystem; however, this
component is much larger than any of
those mentioned previously. The standing crop of fecal pellets from macroarthropod detritivores such as millipedes
may locally exceed annual litterfall inputs (Webb 1977). Fecal pellets of mi157
Figure 1. A simplified conceptual model of elemental cycling in a terrestrial ecosystem
emphasizing the presence and activities of arthropod consumers. Indirect regulation of
elemental movements by arthropods is indicated by the hourglass-shaped valves on these
flows. Virtually all fluxes within ecosystems are known or believed to respond to varying levels of
arthropod activity.
croarthropods (mostly mites and collembolans) are often abundant in samples of
humidified litter and decaying wood and
represent a major fraction of what is
commonly referred to as humus. These
pellets form aggregates that may decay
slowly and represent a large reservoir of
organic matter and nutrients in soil (Anderson and Ineson 1983). However, we
believe that the indirect effects of arthropods are more important to ecosystem
nutrient cycles and amounts of living and
dead phytomass than are the direct effects of arthropod consumption, egestion, and excretion, and our subsequent
discussion evaluates these indirect
effects.
CANOPY ARTHROPODS
Canopy arthropods, feeding on the
green foliage of the forest, grassland, or
desert, convert foliage into insect bodies
and frass. Their feeding produces early
litterfall and enhanced leaching losses
(Kimmins 1972, Reichle et al. 1973,
Schowalter et al. 1981). The effect on
leaching losses appears to be the most
important. Living tissue injured by herbivores leaches more organic and inorganic compounds than does healthy, undamaged tissue (Tukey 1970). Living
plants are nutrient pumps, and damaged
pumps may lose more material than that
represented by the pump itself. This effect is particularly evident during severe
defoliation by insects (Kimmins 1972,
Nilsson 1978); however, low levels of
herbivory can also greatly affect foliar
158
absorption and leaching of certain elements (Table 1). Leaching losses from
foliage during the growing season appear
most pronounced for mobile elements
transported through plant tissues as simple ions. Seasonal losses of potassium by
foliar leaching may be increased by over
100% due to a modest increase in herbivory, and foliage can be converted from
a net sink of sulfate-sulfur (accumulated
from atmospheric inputs) to a net source
of sulfate-sulfur for the soil system (Table 1). Inorganic forms of nitrogen seem
less prone to leaching from lightly damaged tissue, perhaps because phylloplane microbes absorb the ions before
these can reach the soil (e.g., Carroll
1980). Phosphorus cycling is also probably increased by nominal herbivory,
even though leaching losses of inorganic
forms of this element from moderately
grazed foliage are negligible. Phosphorus
concentrations in forest foliage exhibit
strong peaks during bud break (Day and
Monk 1977), and the concentrations of
phosphorus in this young foliage can be
reduced by herbivory (Seastedt et al.
1983). This phosphorus is later replaced,
probably due to increased phosphorus
absorption by roots (Chapin 1980, Chapin and Slack 1979).
Wood and foliage production in forests
is largely unaffected in ecological time by
nominal herbivory (Rafes 1970). Under
these conditions plants do not markedly
alter their carbon allocation strategies,
i.e., new leaves are not produced to
replace those lightly damaged by herbivores. Thus, the amount of easily degraded tissue returned to the forest floor
via early leaf drop, insect orts, and insect
frass is not much larger than that amount
directly consumed by insects (Seastedt
et al. 1983). In contrast, extensive herbivory (consumption of entire leaves
and/or removal of a large fraction of the
canopy) often results in replacement of
foliage. Plants shift their carbon allocation strategies, resulting in more annual
foliage production and less wood production (Morrow and LaMarch 1978,
Nilsson 1978, Swank et al. 1981). Nutrient elements (K, Ca, N, P) are relocated
in new foliage. The net result is a larger
input of foliar litter and frass to the forest
floor. Foliage and frass of herbivores
decomposes more rapidly than wood,
and more nutrients are available for plant
uptake. Cycling of nutrients thus increases with defoliation. This fertilization effect may be partially responsible
for an increase in net primary productivity in years following defoliation (Mattson and Addy 1975, Swank et al. 1981).
There may be an increased export or loss
of some elements from the soil. Swank et
al. (1981) documented increased nitrate
nitrogen concentrations in streamwater
following defoliation by a caterpiller, the
fall cankerworm, in Southeastern forests. No other elements were reported to
Table 1. Net throughfall (canopy leachates minus bulk precipitation inputs) from trees
experiencing different amounts of herbivory, May through August 1980.
Species
Herbivory rate
(% leaf area
removed)*
kg/ha
K
SO4-S
N03-N
NH4-N
Organic N
P04-P
Black locust
Black locust
Red maple
Red maple
10.5
1.7
4.4
1.3
9.75
5.72
2.21
0.81
0.26
-0.40
0.19
-0.11
-0.49
-0.47
-0.61
-0.54
-0.26
-0.36
-0.71
-0.74
0.60
0.50
0.51
0.39
0.013
0.011
0.001
0.001
'Based on an average of 40 leaves or 100 leaflets from each of six trees obtained in August. Herbivory was
artificially reduced by insecticide application. Elemental amounts are based on collections made beneath each
tree. Negative values indicate uptake of ions from bulk precipitation; positive valves indicate net leaching
losses from foliage. Estimates for red maple are adjusted for different foliar biomass between treatments (from
Seastedt et al. 1983).
BioScience Vol. 34 No. 3
Table 2. Changes in standing crops of detritus in relation to changes in decomposition microbial biomass or nutrient concentrarates (based on the model: standing crop = inputs/decomposition constant (k); Olson tions, then net mineralization occurs.
1963).
Conversely, if microbial biomass or nutrient concentrations increase at a more
Decomposition rate*
rapid rate than the rate at which mass is
lost, net immobilization occurs. We have
Standing crop (input = 1 unit)
With fauna
Without fauna
observed both of these effects in field
experiments (Seastedt and Crossley
(%/yr) (k/yr) (%/yr) (k/yr) With fauna Without fauna Difference (units/area) 1980, 1983). The average result of replicated experiments suggests that arthro100.0
0.8 -0.008
124.50
24.50
1
-0.010
pod activities usually result in a net
-0.041
19.50
4
24.50
5.00
-0.051
5
mineralization of foliar litter nutrients
9.49
-0.083
11.99
2.50
8
10
-0.105
-0.174
4.48
5.74
1.26
20
-0.223 16
(Table 3). For nutrient-poor, recalcitrant
-0.386
1.96
2.59
0.63
40
-0.511 32
materials such as decaying wood, immo-1.022
0.62
0.98
0.36
80
-1.609 64
bilization of mineral elements resulting
'Decomposition rates (%/yr) in the absence of fauna are hypothesized to be 20% less than litter with fauna. from faunal-microbial interactions may
dominate for many years. However, Anexhibit significantly increased concen- important in terms of the relative differ- derson and Ineson (1983) found that artrations in streamwater. However, be- ences in amounts of this material remain- thropod feeding can result in inorganic
nitrogen release from substrates with
cause an ionic balance must exist in ing, are of lesser consequence.
streamwater, minor increases in the catAnalysis of the effects of arthropods high carbon-to-nitrogen ratios.
The mineralization rates of different
ion concentrations of the stream must on mineralization rates of elements in
have occurred. No increases in nitrate detritus is more complicated. Bacterial elements are not equally affected by denitrogen export were found with a defoli- and fungal activities largely determine tritivore arthropods. Field studies have
ation by another caterpiller, the saddle the rates at which organic materials are indicated that phosphorus and nitrogen
prominent, in watershed ecosystems in converted to inorganic forms. Thus, de- are often more affected by fauna than are
Northeastern forests, where baseline tritivore-microbial interactions are of such elements as potassium, calcium,
concentrations of nitrate nitrogen are primary concern when assessing faunal and magnesium (Table 3 and Seastedt
relatively high (Bormann and Likens impacts on the nutrient dynamics of lit- 1984). Ineson et al. (1982) and Anderson
ter. Certain densities of arthropods may et al. (1983) reported that the presence of
1979).
stimulate or depress microbial respira- fauna in litter resulted in relatively large
tion rates (Hanlon and Anderson 1979, increases in nitrogen mineralization rates
ARTHROPOD DETRITIVORES
1980), and we assume that total microbi- and moderate or no increases in the
The standing crop of decaying plant al immobilization and mineralization leaching losses of other elements.
materials found in most temperate eco- rates are similarly affected. Measuresystems is usually much larger than the ments of nutrient concentrations in litter COMPARISONS OF HERBIVORE AND
standing crop of any other biotic com- in the presence and absence of arthro- DETRITIVORE IMPACTS
ponent (e.g., Reiners 1973). Over 90% of pods show that the arthropods usually
net primary production is usually con- increase the nutrient concentrations of
Low-level herbivory by canopy arverted directly to detritus (Wiegert and the substrate (Seastedt 1984). Hence, thropods speeds the rate of nutrient cyEvans 1967). Accordingly, detritivore while arthropods speed decomposition cling in terrestrial ecosystems while havfood webs have greater biomass than rates, they concurrently enhance the nu- ing little impact on plant standing crops
herbivore food webs (Heal and MacLean trient concentrations of the litter-mi- and production. Arthropod detritivores
1975). Few studies have measured the crobe system. The sum of these oppos- speed the rate of nutrient flux through
effects of arthropods on the standing ing effects determines the net arthropod soil, but they also have a marked impact
crops of detritus directly, but these im- effect on nutrient loss from decaying on the standing crops of their food repacts can be assessed from studies of plant materials. If, for example, arthro- source. Plants respond to moderate
arthropod effects on litter decay rates. pods greatly enhance the rate of decom- losses due to herbivory by increasing the
Arthropods speed decay to anywhere position but only moderately increase photosynthetic activity of remaining fobetween 0% and 100% of the rates observed in the absence of arthropods Table 3. Arthropod effects on mass, nitrogen, phosphorus, and potassium loss from
(Swift et al. 1979, Vossbrinck et al. 1979, dogwood foliage litter and hypothesized effects on standing crops.*
Witkamp and Crossley 1966). Assuming
Loss (%/yr)
a negative exponential decay pattern for
Standing crop (kg/ha)
detritus (Olson 1963, Wieder and Lang
With fauna Without % Difference With fauna Without % Difference
1982), the effects of a modest (20%)
increase in decay rates attributable to
56
50
12.0
183
217
-18.6
arthropod feeding activities translates Mass
Nitrogen*
32
38
15.8
3.96
4.77
-20.4
into a 24-58% reduction in standing Phosphorus
31
24
22.6
0.36
0.50
-38.9
crops (Table 2). In absolute amounts, Potassium*
76
72
5.2
1.21
1.27
-5.0
arthropod feeding is most important in
reducing standing crops of recalcitrant 'Data are from three, one-year studies conducted in the southern Appalachians (Cromack 1973 and
unpublished data, Seastedt and Crossley 1980, 1983). Standing crop estimates are calculated as in Table 2.
materials such as woody litter. Effects An annual input of 150 kg/ha of dogwood foliage containing 1.24% N, 0.09% P, and L.10% K is assumed.
on rapidly decaying substrates, although ^Based on only two, one-year studies.
March 1984
159
liage and increasing the uptake of nutrients by roots (Chapin 1980, Chapin and
Slack 1979, Hilbert et al. 1981, McNaughton 1979, 1983). Without an appropriate plant response, increased rates
of nutrient cycling would not occur.
However, herbivores may directly stimulate plant vegetative growth (e.g., Dyer
et al. 1982). Fungivore-fungi interactions
parallel those of herbivore-plant interactions, but the net effect of detritivore and
fungivore arthropod feeding is a reduction of detritus standing crops.
We suggest that herbivores and detritivores complement each other in the nutrients most affected by their feeding
activities. The more mobile elements are
affected by herbivores, since they are
most likely to be leached from damaged
tissue. These mobile elements readily
leach from decaying plant materials and
are turned over rapidly by microbes.
Detritus does not replace elements lost
by leaching, and detritivores are therefore relatively unimportant in affecting
the fluxes of these elements. Conversely, elements commonly occurring as
structural components or in complex organic molecules of plant tissues are less
affected by low levels of canopy arthropod herbivory. Microbial mineralization
processes, stimulated by detritivore
feeding, are critical for rapid recycling of
these elements. Our studies have indicated that potassium cycling is most strongly affected by herbivory (Table 1),
whereas nitrogen and phosphorus are
perhaps the two macronutrients most
affected by detritivore feeding (Table 3).
Calcium also accumulates in fungal hyphae and associated arthropods (millipedes and oribatid mites). In this case
arthropods constitute a modest elemental
sink as well as affect cycling rates (Cromack et al. 1977, Gist and Crossley 1975).
To summarize, arthropods clearly influence the amounts of living and dead
organic matter and nutrient transfers in
terrestrial ecosystems. The extent of this
influence has yet to be properly quantified but undoubtedly exceeds values calculated from measurements of feeding
rates alone. Although canopy arthropods
may occasionally have a large influence
due to outbreaks of defoliators, detritivore arthropods, on the average, probably have a greater impact on the cycling
rates of most elements due to larger
numbers and biomass of the detritivore
food web. Plant and microbial responses
to arthropods (i.e., the indirect effects of
feeding) are responsible for most of the
observed increases in nutrient cycling
rates.
160
of the World: Analysis of Grasslands and
their Uses. Cambridge University Press,
This work was supported in part by
London.
the National Science Foundation (DEB- Dyer, M. I., J. K. Detling, D. C. Coleman,
8012093) and the US Department of Enand D. W. Hilbert. 1982. Roles of herbivores in grasslands. Pages 255-295 in J.
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model of mineral cycling for an arthropod
an anonymous reviewer provided
foodweb in a Southeastern hardwood forest
thoughtful criticisms on the manuscript.
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