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Enemies Hypothesis: A Review of the

Effect of Vegetational Diversity on

Predatory Insects and Parasitoids

by Edmund P. Russell

1989

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permission of the publisher. The original published version can be
found at the link below.

Russell, Edmund P. “Enemies Hypothesis: A Review of the Effect

of Vegetational Diversity on Predatory Insects and Parasitoids”
Environmental Entomology, Volume 18, Number 4, August 1989 , pp.
590-599(10)

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 Enemies Hypothesis: A Review of the Effect of Vegetational
Diversity on Predatory Insects and Parasitoids
EDMUND P. RUSSELL

Department of Biology, University of Michigan,

Ann Arbor, Michigan 48109

Environ. Entomol. 18(4): 5 9 0 - 5 9 9 (1989)

ABSTRACT The enemies hypothesis holds that predatory insects and parasitoids are more
effective at controlling populations of herbivores in diverse systems of vegetation than in
simple ones. Eighteen studies that tested the enemies hypothesis are reviewed. Of those
studies reporting mortality from prédation or parasitism, nine found higher mortality rates
in diverse systems; two found a lower mortality rate; and two found no difference. T h e
mechanisms that are thought to underlie the enemies hypothesis and directions for future
research are discussed. Evidence suggests that the enemies hypothesis and the resource
concentration hypothesis (which predicts that herbivores more easily find, stay in, and re-
produce in monocultures of host plants than in polycultures) are c o m p l e m e n t a r y mechanisms
in reducing numbers of herbivores in diverse agricultural systems.

K E Y WORDS Insecta, enemies hypothesis, resource concentration, predators

THEORIES ABOUT THE FACTORS that control the For the purposes of this paper, a diverse agri-
abundance of herbivorous insects have figured cultural system, or polyculture, is one in which two
prominently in the history of ecology, occasioning or more plant species grow simultaneously. A sim-
several of the discipline's seminal papers (Andre- ple system, or monoculture, consists of one plant
vvartha & Birch 1954, Hairston et al. 1960, Ehrlich species. Enemies are predatory arthropods or insect
& Raven 1964). Recently, particular attention has parasitoids. Victims are their prey or hosts. Gen-
been paid to the effect of vegetational diversity on eralists consume a variety of species. Specialists
phytophagous insects (Feeny 1976, Rhoades & Cates consume one or several related species.
1976, Scriber 1984) arid their natural enemies (Price
et al. 1980, Sheehan 1986). Agricultural systems,
where variables such as density and patch size can
Testing the Enemies Hypothesis
be controlled, have proved especially useful in test-
ing hypotheses about diversity and insects. Root's (1973) formulation of the enemies hy-
Studies have commonly, though not universally, pothesis makes one essential prediction: "predators
found that populations of herbivorous insects reach and parasites are more effective in [complex en-
higher levels in simple agroecosystems than in di- vironments than simple ones]" (114). That predic-
verse ones (reviewed by Andow 1983b, Risch et al. tion can be broken into two components: predators
1983, Altieri & Letourneau 1984, Vandermeer and parasites kill herbivores at higher rates in poly-
1989). Root (1973) proposed two possible expla- cultures than in monocultures, and the higher mor-
nations for this pattern. (1) The enemies hypothesis: tality rates in polycultures significantly reduce her-
Predators and parasites are more effective in di- bivore populations.
verse systems than in simple ones. (2) The resource Table 1 lists studies that explicitly test the ene-
concentration hypothesis: Specialist herbivores more mies hypothesis or that compare prédation or par-
easily find, stay in, and reproduce in simple systems asitism rates in agricultural monocultures and poly-
(monocultures) of their host plants. cultures. All controlled tests of the hypothesis that
This paper reviews the enemies hypothesis; the I found were done in agroecosystems. Some studies
resource concentration hypothesis has been re- measured only mortality rates; others also did cen-
viewed by Kareiva (1983) and Stanton (1983). In suses of herbivore populations. I did not include
the first part, I examine whether predators and studies that deduced enemy-caused mortality from
parasites inflict significantly higher mortality on inverse correlations between enemy and victim
insect herbivores in diverse than simple systems abundances, except for the studies in which the
and thereby reduce herbivore populations. I review author said he or she was testing the enemies hy-
the mechanisms proposed for greater predator and pothesis. Such correlations do not prove that ene-
parasite effectiveness in diverse systems and direc- mies caused the reductions in herbivore numbers.
tions for future research in the second section. In I included only studies that compared the effects
the last section, I discuss the relationship between of within-field diversification. Diversity on a larger
the enemies and resource concentration hypothe- scale is an important part of the enemies hypoth-
ses. esis, but to my knowledge controlled comparisons

0046-225x/89/0590-0599$02.00/0 © 1989 Entomological Society of America

August 1 9 8 9 RUSSELL: ENEMIES HYPOTHESIS 591

Table 1. Tests of the enemies hypothesis in polyculture versus monoculture

Préda-
tion/ Enemy/
Researcher Victim stage Enemy Herbivore
para- Sampling method herbivore
examined abundance abundance
sitism ratio
rate

Altieri & Schmidt 1986 Higher Egg prédation Prédation on eggs on Higher Lower Higher
cards
Andow 1983a Same Egg, larval prédation Visual NA Varied NA
or parasitism
Andow 1983b NA NA Review Usually Usually Usually
higher lower higher
Andow & Risch 1985 Lower Egg prédation Prédation on eggs on Lower Higher Lower
cards (1 spp.)
Andow & Risch 1987 Lower Egg parasitism Parasitism on eggs on NA NA NA
cards
Bach 1980a NA NA Visual; pitfall; sticky Same Lower Higher
traps
Bach 1980b NA NA Visual Higher Lower Higher
Dempster 1969 Higher Larval prédation or Visual; pitfall Higher Lower Higher
parasitism"
Dempster & Coaker Higher Larval prédation Visual; pitfall Higher Lower Higher
1974
Hansen 1983 Higher Egg prédation Eggs on cards Higher'' Lower Higher 1
Leius 1967 Higher Egg, larval, pupal Collected all stages NA NA NA
parasitism from orchards
Letourneau 1987 Higher Egg parasitism Collected eggs Mixed'' Higher NA
Letourneau & Altieri Higher All stages: prédation Visual; cages Higher Lower Higher
1983
Risch 1981 Same Adult parasitism; egg Visual; eggs collected Same Lower Higher
prédation or para-
sitism
Risch et al. 1983 NA NA Review Usually Usually Usually
higher lower higher
Root 1973 NA Adult: neither Vacuum; bags Same Higher Higher
Ryan et al. 1980 Higher Egg, larval prédation Pitfall; visual Same Lower Higher
Speight & Lawton 1976 Higher Pupal prédation Pitfall; pupae on Higher NA NA
cards
Tukahirwa & Coaker Same Egg prédation Visual; pitfall; yellow Higher Lower Higher
1982 traps

" Prédation rate higher. No difference in parasitism rate.

'' Non-ant enemies significantly higher in polycultures all season. Early in the season, ants were more abundant in squash monoculture,
but that pattern reversed itself by the end of the season.
c Number of herbivores not reported. However, Risch's (1981) study on same plots at same time reported fewer beetle pests in

polycultures. Given that the number of enemies increased and the number of beetles, the major pests, decreased, the ratio of enemies
to herbivores must have been higher.
d More parasites were found in polycultures and in maize monoculture. Predators were unaffected by cropping pattern.

with monocultures of comparable size have not for slow-moving apterous larvae (Cain et al. 1985).
been made. Drawing the same conclusions about adult popu-
Most studies verify the prediction of the enemies lations is more difficult, because alates can move
hypothesis that enemies cause higher herbivore in and out of patches easily. The one manipulative
mortality in polycultures than in monocultures. study that controlled for such adult movement (Le-
Nine studies found higher mortality rates from pré- tourneau & Altieri 1983) found that predators ef-
dation or parasitism in diverse systems and two fectively controlled all life stages of herbivorous
found no difference. It is interesting that only 2 thrips. More manipulative studies are clearly need-
studies out of 13 found lower mortality in poly- ed.
cultures than in monocultures given predictions Three studies (Root 1973; Bach 1980a,b) and two
that predators (Risch et al. 1982) and parasitoids reviews (Andow 1983b, Risch et al. 1983) that tested
(Monteith 1960, Sheehan 1986) should display re- the enemies hypothesis by comparing insect abun-
duced searching efficiency in more dense or diverse dances in simple and diverse systems found little
systems. If this occurs for individual enemies, their or no evidence for the hypothesis, almost the op-
greater numbers in polycultures (Andow 1983b) posite result from the studies that measured mor-
may compensate. tality rates. Enemy abundances often correlate in-
Published studies generally support the second versely with victim abundances (Coaker 1965; Smith
part of the prediction, that enemies cause smaller 1969,1976; Speight & Lawton 1976; Mayse & Price
herbivore populations in polycultures, especially 1978; Andow & Risch 1985), but the correlation is
 vol. 18, no. 4
ENVIRONMENTAL E N T O M O L O G Y
592

not a sure index of mortality rates. Mortality rates exported in the monoculture than in the polycul-
can vary between treatments with equal enemy ture. Bach et al (19H2) found no difference in
densities (Ryan et al. 1980), or be equal despite species numbers in secondars succession near and
differences in enemy density (Tukahirwa & Coaker far from tropical rainforest after a few sweeps.
1982). Mortality during egg and larval stages is Further sampling fourni the numlx-r of herbivorous
significant (Price 1984) but often unmeasured. species the same in Itollt habitats, but the number
of entomophagous species increased with distance
I found only two experiments that manipulated
from the forest
enemy density. Letourneau & Altieri (1983) used
cages and Tukahirwa & Coaker (1982) erected bar- The studies finding a |x>sitive correlation be-
riers of bituminized felt to exclude ground-dwell- tween vegetational diversity and the number of
ing carabids. We need more such manipulations, herbivorous species were done in temperate re-
despite their disadvantages in changing microcli- gions, whereas those finding other patterns were
mates (DeBach et al. 1976) and in limiting move- done in the tropics Further studies are needed
ment by victims and enemies. Barriers to ground- before we can conclude whether the differences
dwelling predators (Tukahirwa & Coaker 1982) do are due to the regions studied or to the sampling
not prevent immigration by alate enemies, which methods.
may have contributed to equalizing prédation rates "As a result, relatively stable papulations of
in that study. generalized predators anil /m ra.il tes ran persist In
Another striking pattern in Table 1 is that the these habitats because they can exploit the wide
predator/herbivore ratios rise in all but one of the variety of herbivores which heroine mailable at
polycultures. What are the implications of this different times or In différent rnicrolwbitats" (114).
change? We might predict more search movement Do generalist enemy populations fluctuate less in
by enemies, more enemy emigration, or higher diverse than in simple systems'-' A subjective in-
enemy effectiveness. I found no studies that test spection of graphs in the studies listed in Table 1
predictions based on this ratio. revealed no clear or consistent differences. I'erfecto
et al. (1986) did the only study of enemy movement
patterns, which would largely determine popula-
tiori fluctuations. They found no consistent response
Mechanisms Underpinning the to plant diversity, but carabids did stay longer in
Enemies Hypothesis plots with ground cover W e need more studies of
Root (1973) presents five reasons why enemies the specific factors to which enemies respond in
should control populations of herbivores more ef- polycultures, In-cause "diversity" is actually a
fectively in polycultures than in monocultures. shorthand description of a immlxT of factors that
"A greater diversity of prey/host [victim ] species change in intercrops, including nuinlxT of secies,
and microhabitats is available within complex en- density, architecture, moisture, and wind patterns.
vironments, such as most natural, compound com- Does increasing the diversity of prey sixvies re-
munities" (114). Several studies have found a cor- sult in populations of predators jx-rsisting longer?
relation between the diversity of plant species and Many ecologists have argued that increasing di-
the diversity of herbivorous insects. This relation- versity leads to greater stability for communities
ship has been reported for Homoptera (Murdoch in general (Odum 195-3. MacArtlmr 1955, Elton
et al. 1972); for Hemiptera, Homoptera, and Thy- 1958, Margalef 1968. Armstrong 1982) and for ag-
sanoptera (Brown & Southwood 1983); and for ricultural systems in particular (Pimentel 1961, van
communities of herbivores in agricultural fields Emden In Williams 197-1. Murdoch 1975). The doc-
(Mayse & Price 1978). A review by Lawton & trine came under question when May (1973) and
Strong (1981) concluded that this pattern holds for others (reviewed in Ma> (1976)) showed that in-
insect communities in general. creased diversity leads to decreased stability in some
However, none of these studies mentions how mathematical models. Definitions of stability (Pimm
the investigators determined appropriate sampling 1984) and assumptions (reviewed by Begon et al.
effort, a crucial methodological question. In any 1986) often determine whether a model is stable.
community, we expect the number of sampled For example, Vandermeer (personal communica-
species to rise with sampling effort, reaching an tion) has found that increased diversity theoreti-
asymptote at the total number of species. Risch cally results in increased species jx-rsistence when
(1979) found higher species diversity in a tropical indirect interactions (Vandermeer 1980, Vander-
diculture than in monoculture, but an increase in meer el al. 1985) are taken into account.
parasitic Hymenoptera, not herbivores, accounted
Indirect interactions may prove more significant
for the difference. In fact, the number of herbiv-
than previously realized Price el al (1980) noted
orous species was lower in the diculture. More im-
that plants and enemies function as indirect mu-
portantly, Risch noted that the species-sweep curve
tualists, because plants "provide" victims for the
did not level after 600 sweeps. Risch used the for-
enemies, and enemies presumably help the plants
mula developed by Stout & Vandermeer (1975) to
estimate the number of species in the community by eliminating herbivores. Similarly, herbivores and
The pattern reversed itself, with more total species enemies on the fourth trophic level should be con-
sidered mutualistic. Parasites and predators can kill

i
August 1989 R U S S E L L : E N E M I E S HYPOTHESIS 593

a significant number of natural enemies (Spencer not mature unless the female feeds on pollen (Bom-
1926; van Emden 1965, 1966; Iperti 1966; Kirk bosch 1966). Different species of pollen affect fe-
1974), but their effect in the field has seldom been cundity and longevity differently (Leius 1963), so
assessed (Doutt et al. 1976, Orr & Boethel 1986). access to a diversity of plant species might well
If diverse systems attract greater numbers of ene- prove advantageous to enemies. Nectar and pollen
mies on the fourth as well as third trophic level, appear to be important in keeping parasites (Leius
the effect of the third trophic level on herbivores 1963, Shahjahan 1974, Hansen 1983) and predators
mav be reduced. (Smith 1966, Bentley 1977) in certain vegetation.
"Specialized predators and parasites are less This often leads to higher herbivore mortality (Leius
likely to fluctuate widely because the refuge pro- 1963, van Emden 1965, Shahjahan 1974, Tilman
vided by a complex environment enables their 1978, Barton 1986).
prey/host species to escape widespread annihi- Discussion of the availability of alternative vic-
lation" (114). The generalization that refuges pre- tims, nectar, and pollen raises questions about the
vent annihilations and thus "stabilize" predator- scale on which enemies operate. Flaherty (1969)
prey interactions grew out of laboratory studies found that weeds growing within a field harbored
(Huffaker 1958, Pimentel et al. 1963, Luckenbill alternative prey for predatory phytoseiids, which
1974, Glesener 1978). Unstable community models led to more effective control of Willamette mites,
can achieve global stability by adding a migration Eotetranychus willamettei Ewing, in weedy than
component (Levins & Culver 1971, MacArthur weedless fields. Perrin (1975) argued that nettles
1972, Vandermeer 1973, Horn & Levin 1974, Slat- growing next to fields support alternative victims
kin 1974, Hassell 1978). for enemies, including entomophagous fungi. Ene-
Few field tests of the role of refuges in population mies can colonize cultivated fields from unculti-
dynamics have been done. Reeve & Murdoch (1986) vated land near fields (van Emden 1962, Galecka
found that effective control of the California red 1966). Parasitization rates on sugar cane weevils
scale had been achieved by a parasitoid because increased within 200 ft of nectar sources in field
the scale was able to find a spatial refuge in the margins in Hawaii (Topham & Beardsley 1975).
interior of trees, thus preventing extinction of both Bombosch (1966) inferred from population mea-
species. In Australia, Myers et al. (1981) found that surements that syrphids move in a constant pattern
refuges are important in continued control of the from woodland edges to distant sugar beet and
prickly pear cactus by enemies. Kareiva (1985,1987) potato fields to roadsides and weedy ditchbanks
found that vegetational patchiness leads to in- over an area of 10 km2. Doutt & Nakata (1973)
creased outbreaks of aphid populations in the field, found that control of leafhoppers declined in vine-
apparently by interfering with searching and ag- yards more than 6 km from Rubus bushes, which
gregation behavior of predatory coccinellids. The support an essential alternative host.
experiment did not run long enough to draw con- All of these studies show that vegetational di-
clusions about persistence of the system. versity benefits enemy populations, but what is the
Classical biological control theory has focused on appropriate scale for the enemies hypothesis? Such
specialist enemies and how to keep them from questions assume great significance in experimen-
eliminating themselves along with their prey tal tests, which rarely are done on plots 6 km wide.
(DeBach 1974, Huffaker & Messenger 1976). The Highly mobile species with diverse requirements
same concern has not traditionally been voiced for probably benefit from diversity over a large area,
generalist predators, but questions have been raised whereas less mobile enemies with fewer needs
about the assumption that specialists more often probably operate on a smaller scale. The explicit
drive themselves to extinction than do generalists. tests of the enemies hypothesis (Table 1) have gen-
Introduced predators (which tend to generalize) erally used test plots 10 or 15 m on a side, usually
and parasites (which tend to specialize) have been located within 10 m of each other. This has at least
found to establish themselves at the same rate (Hall two important implications.
& Ehler 1979). More importantly, a review by Mur- First, enemies may regard the sum of the test
doch et al. (1985) of successful biological control plots as one large polyculture, moving freely be-
programs found that local annihilation of prey did tween individual monocultures and polycultures.
not threaten long-term control. Altieri & Whitcomb (1980) found that predatory
"(D)iverse habitats offer many important req- communities did not differ between monocultures
uisites for adult parasitoids and predators, such and polycultures when test plots were located 8 m
as nectar and pollen sources, that are not available from each other. In contrast, they found signifi-
in a monoculture" (114). Many monocultures do cantly more predators in polycultures when test
produce nectar and pollen, but more kinds of pol- plots were 50 m from each other. Finding the same
len generally are available, and at more times in enemy abundance or herbivore mortality between
the season, in polycultures. Eating nectar and pol- treatments might mean a lack of evidence for the
len increases predator and parasite longevity and enemies hypothesis, or it might mean that the test
fecundity (Leius 1963, Bombosch 1966, Hodek plots are too close together. Small, juxtaposed plots
1966, Shahjahan 1974, Syme 1975, Hagen et al. constitute a conservative design, because their
1976, Vinson 1981). Indeed, syrphid ovarioles do proximity tends to reduce differences between plots.
 ENVIRONMENTAL ENTOMOLOGY v ° l - 18, no. 4
594

Many authors have concluded that predators stay

Second, a "fine-grained" field to one enemy (e.g.,
in a habitat until the food supply drops below the
a specialist parasitoid that spends a great deal of
level needed to maintain them (Perrin 1975 Frazer
time flying) might appear more "coarse-grained
to another enemy (e.g., a sit-and-wait predator). & Gilbert 1976, Wheeler 1977, Hassell & South-
Van Emden (1965) found exactly this pattern when wood 1978, Baumgartner et al. 1981, Best et al
he charted prédation and parasitism rates in dif- 1981, Horn 1981, Ives 1981). The finer the scale
ferent parts of a 1.75-acre monoculture surrounded of diversity, the more likely enemies will be near
by diverse vegetation. Parasitism rates remained the place they are needed. If enemies live in weeds
virtually constant over the whole field, but pré- surrounding a field, their functional response will
dation rates were significantly higher near the edges. likely not prove so fast or effective as when weeds
Enemies operate on different spatial scales even grow in the field itself. This would probably be less
within the same system. of a problem for species that seem to switch habitats
"Thus incipient outbreaks of herbivores are when they can get a higher return in another patch
checked early by the functional response of ene- (Skuhravy & Novak 1966, Burleigh et al. 1973, Ives
mies whose numbers have been maintained by the 1981).
diverse resources available in complex environ- Are enemy populations maintained at higher
ments" (114). The biological control literature in- levels in polycultures, thus making the functional
dicates that predators and parasites can control pest response effective? Andow's (1983b) review shows
populations by their functional or numerical re- that enemies usually do maintain higher popula-
sponse to pest populations (reviewed in DeBach tions in polycultures than in monocultures.
1974, Huffaker & Messenger 1976, Hall etal. 1980).
Generalist enemies do exploit different victims at
different times (Evenhuis 1966, Hodek 1966, Fla-
Relationship Between the Enemies
herty 1969, Burleigh et al. 1973, Doutt & Nakata
Hypothesis and the Resource
1973, Hagen et al. 1976, Mayse & Price 1978, Car-
Concentration Hypothesis
roll & Hoyt 1986). Murdoch (1969, 1973) and Mur-
doch & Marks (1972) found that insect predators Root (1973) described the enemies hypothesis as
demonstrate the predicted Type 3 functional re- "one of the hypotheses most frequently offered to
sponse and control population outbreaks. However, explain smaller herbivore populations in complex
switching occurs when predators possess only a weak environments" (114). Root proposed an alternative
preference for one prey over the other. We do not hypothesis, the resource concentration hypothesis,
know whether generalist enemies require a diver- which stimulated a number of excellent studies
sity of prey, nor whether they become functional (Cromartie 1975; Bach 1980a,l>, 1984, 1986; Risch
specialists in the field (Fox & Morrow 1981). We 1980, 1981; Kareiva 1982). "Plant apparency"
need more research on the behavior of individual (Feeny 1976, Rhoades & Gates 1976) and "asso-
arthropod enemies, especially in the field, to de- ciational resistance" (Tahvanainen & Root 1972;
termine when and why they switch their choice of Altieri & Letourneau 1982, 1984) are other terms
victim species. emphasizing the importance of plant spatial pat-
Foraging theory might provide a useful frame- terns for herbivore movement and reproduction.
work to explore these issues (reviewed by Hassell The resource concentration and enemies hy-
& Southwood 1978, Stephens & Krebs 1986). The potheses are neither exhaustive nor mutually exclu-
results of the few studies on arthropod foraging are sive (Sheehan 1986). In the first part of this review,
sometimes consistent with predictions from for- I showed that enemies often inflict significantly
aging theory (e.g., Charnov 1976) and sometimes higher mortality on insects in polycultures than in
not (e.g., Eveleigh & Chant 1982a-c). Energy is monocultures, whereas studies of the resource con-
commonly used as currency in foraging models, centration hypothesis (cited above) found that
but herbivores often sequester secondary chemicals movement patterns play a significant role in de-
of their host plants (Duffey 1980), so toxicity is an termining specialist insect population patterns. The
important variable that is not reflected in caloric enemies and resource concentration hypotheses are
content. complementary, not competing, mechanisms.
Little quantitative work has been done on pre- Field studies confirm that the two mechanisms
dicting arthropod habitat choice based on costs and can function simultaneously. Dempster & Coaker
benefits of different habitats. The work of Werner (1974) found that enemies reduced the populations
& Mittelbach (1981) and Werner et al. (1983a,b) of some pests, while movement patterns reduced
with sunfish indicates that such approaches might the populations of others. The caterpillar Pieris
yield useful results. A few studies have attempted rapae (L.) lays eggs at tin; same rate in monocul-
to quantify the importance of various environ- tures and polycultures, but ground beetles and har-
mental variables such as nectar, pollen, and prey vest spiders prey on larvae; in the polyculture at a
availability (Hansen 1983, Andow & Risch 1985). significantly higher rate, verifying the enemies hy-
More are needed. pothesis. But cabbage aphids, Brevicoryne brassica
Most work on habitat shifts has focused on how (L.), and Erioischia brassicae (Bouche) immigrated
well shifts correlate with changes in prey density. at a significantly lower rate in the intercrop, ver-
August 1 9 8 9 RUSSELL: ENEMIES HYPOTHESIS 595

ifying the resource concentration hypothesis. Like- management should not be whether one or the
wise, Ryan et al. (1980) found both mechanisms at other is at work, but how to enhance both to achieve
work in the same place, but on one species. E. maximum control. The next step for the enemies
brassicae lay fewer eggs in polycultures than mono- hypothesis will be to move beyond qualitative stud-
cultures, but predators reduce their numbers even ies and into quantitative ones. We need to predict
more by preying at a higher rate in the polycul- and test the relative importance of various factors
tures. that control enemy effectiveness and response to
Comparisons of the enemies and resource con- vegetational patterns. That should allow us to move
centration hypotheses echo the longstanding de- into a more predictive theory of enemy activity in
bate over the factors that control populations diverse systems.
(Nicholson 1933, Andrewartha & Birch 1954, Ilair-
ston et al. 1960, Ehrlich & Birch 1967, Murdoch
Acknowledgment
1975). Are herbivores limited by the trophic level
below, the trophic level above, or by abiotic fac- I thank Catherine Bach, Deborah Goldberg, Ivette
tors? It eventually became clear that different fac- Perfecto, Brian Stockhoff, John Vandermeer, and an
tors operate at different times and in different places anonymous reviewer for helpful comments on an earlier
draft of this manuscript. David Andow and Deborah
(Begon et al. 1986). Similarly, I predict that a single
Letourneau kindly provided reprints and preprints. This
factor will not be found that explains why herbi- work was supported by a University of Michigan Regents
vores are often less abundant in diverse than simple Fellowship.
systems. In agroecosystems, the challenges are to
enhance the effect of each mechanism to control
pests by developing quantitative, mechanistic ap- References Cited
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N.Y.
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able, but need more testing. W e do not know for versified agroecosystems: relations between a cocci-
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