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Plant Defense Guilds

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DOI: 10.1126/science.193.4247.24 · Source: PubMed

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Plant Defense Guilds

Peter R. Atsatt; Dennis J. O' Dowd

Science, New Series, Vol. 193, No. 4247. (Jul. 2, 1976), pp. 24-29.

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 I should like to mention only gener-
alized pseudoasymmetric cases with
pseudoasymmetric axes and planes,
models of which are shown in Fig. 16.
Examples of stereoisomeric molecules
represented by these models have been
prepared by Gunter Helmchen (23) in
our laboratory (Figs. 17 and 18). It is
noteworthy that many bilateral orga-
nisms including men are examples of
planar pseudoasymmetry.
I have limited the discussion to three-
dimensional basic f i g ~ ~ r ewith
s four lig-
ands because they are typical for organic
stereochemistry. The same procedures
can be applied to produce catalogs based
on figures with five or more vertices. but
the multiplicity of models so obtained is
larger and therefore more d~fficultto deal
with in a brief lecture o r article.
The need for brevity also prevents me
from dealing with the manifold biochemi-
cal and biological aspects of molecular
chirality. Two of these must be men-
tioned, however briefly. The first is the
fact that, although most compounds in-
volved in filndamental life processes.
such as sugars and amino acids, are chir-
a1 and although the energy of both
enantiomers and the probability of their
formation in an achiral environment are
equal, only one enantiomer occurs in
nature; the enantiomers involved in life
processes are the same in men, animals.
plants. and microorganisms, independent
of their place and time on Earth. Many
hypotheses have been conceived about
this subject. which can be regarded as
one of the first problems of molecular
theology. One possible explanation is
that the creation of living matter was an
extremely improbable event. which oc-
curred only once.
The second aspect I would like to
touch, the maintenance of enantiomeric
purity, is less puzzling but nevertheless
still challenging to chemists. N a t ~ l r eis
the great master of stereospecificity
thanks to the ad hoc tools. the special
catalysts called enzymes. that she has
developed. The stereospecificity of en-
zymic reactions can be imitated by chem-
ists only in rare cases. The mystery of
enzymic activity and specificity will not
be elucidated without a knowledge of the
intricate stereochemical details of en-
zymic reactions. The protagonist in this
field is John Warcup Cornforth.
References
See Lord Kelvin,BalfimOreLectures (C. Clay
and Sons. London, 1904), pp. 436 and 619.
2. A . F.MGbius. Der Burvcentrischr Caicil, Ge-
~amfllelf' wrrhe (Leipzig. 1885). Bd. 1: F.
Klein. Elementrrrmuthemarik (Splinger. Berlin.
ed. 3, 192.5).~ d 1,.p. 3.
3. L . Pasteur, Ann. Chim. Phys. 24 (3) 442 (1848):
28. 56 (1848); 38, 437 (1853); Lecons sur In
Dissymrtrir Molrculuirr (Hachette. Paris,
1x61)
4 E.,'-A. Abbot. Flutlrrnd (Dover. New York.
ed. 6 , 1968).
5. A. Huxley, Durtlulus. Spring 1962, p. 279.
6. A. S. Couper, Compt. Rend. 46, 1157 (1858).
7. J . Wislicenus. Ber. Deutsch. Chem. Ges. 2, 620
(1869).
8. J. H. van't Hoff. Vorstel tot uithreiding der tegm-
woortlig in de schrikunde gebruikte structurgor-
mules in de ruimtr (Greven. Utrecht. 1874): Bull.
Soc. Chim. France 23 (2), 295 (1875): La chimie
dans I'Espacr (Bazendijk, Rotterdam. 1875).
9. J . A. Le Bel, Bull. Soc. Chim. France 22 (2). 337
(1874).
10. J . H. van't Hoff, Die Lrrgerung der Atome im
Ruume (Vieweg, Braunschweig, 1876). Anhang,
p. 46.
11. V. Meyer. Ber. Deutsch. Chem. Grs. 23. 567
(1890).
12. J. D. Dunitz, D. M. Hawley, D. MikloS. D. N.
J. White. Yu. Berlin. R. Marusid. V. Prelog, Heli..
Chim. Actu 54, 1709(1971).
13. R. S . Cahn. C. K. Ingold. V. Prelog, Experientia
12, 81 (1956); Angew,. Chrm. 78. 413 (1966);
An,qew. Chrm. In!. Ed. 5. 385 (1966).
14. See A. Feldman,J. Org. Chem. 24. 1556 (1954).
15. E . Fischer, Ber. Deutsch. Chem. Ges. 23. 2114
(1890): 24. 1836(18911: 27.3189(1894).
16. -.-, Aus meinem Leben '(Sp~inger,Ber-
lin, 1922), p. 134.
17. F. M. J a e ~ e r .Lectures on the Princinles o f
Symmetry r n d its Applicatio~ in all ~ r r f u r d
Sciences (Elsevier, Amsterdam, 1917).
18. G . Polya. Helv. Chim. Acta 19. 22 (1936); Actrr
Math. 68, 145 (1937).
19. J. K . Senior. J . Org. Chem. 1, 254 (1936); A. C.
Lunn and J . K . Senior, J . Phvs. Chem. 33. 1027
(1951).
20. E . Ruch. Accounts Chem. Res. 5. 49 (1972): A.
Mead, E. Ruch. A. Schonhofer, ~ h e b r dhim. .
Acta 29, 269 (1973).
21. V. Prelog and H . Gerlach, Heit'. Chim. Actrr 47,
2288 (1964).
22, A. Young, Proc. L O ~ ~~ ( ~ ~ h ~. 33 ( I ) , 97
I tSOC.
(1901).
23, V. Prelog and G. Helmchen, ffrlv. Chim. Actu
55,2581.2599.2612(1972).

have long noted the etfects of specific

Plant Defense Guilds
Many plants are functionally interdependent
with respect to their herbivores.
P e t e r R. A t s a t t a n d D e n n i s J. O ' D o w d
It is generally agreed that herbivores the chemistry. morphology. distribution.
exert strong selectional pressures on and abundance of alternative prey and
plant populations and that chemistry (in- nonprey as well. Only a few protective
cluding nutrition), morphology, and es- traits are lethal deterrents. whereas the
cape in time and space are the plant's majority function by influencing the feed-
primary means of defense ( 1 4 ) . Re- ing behavior of potential herbivores.
search on antiherbivore mechanisms has causing the animal to exclude certain
naturally focused on the individual's plants or plant parts from its optimal diet
own suite of protective characteristics. ( 5 ) . When traits are marginally protec-
T h ~ sa pproach generally neglects an im- tive. their deterrent value is highly condi-
portant facet. that the probability of a tional on a variety of stimuli produced by
other plants. The literatures of ecology.
plant being fed upon depends not only on
its inherent q~lalityand quantity, but on entomology, pathology, and agriculture
kinds of plants in reducing herbivory; in
this article we bring together these exam-
ples in developing the concept of
"guild" defense against herbivores. We
wish to emphasize the ways in which
plant associates can function as antiher-
bivore resources in ecological time and
discuss the possible selective value of
defense "guilds" through evolutionary
time.
The term guild has been used botani-
cally to describe groups of plants in some
way dependent on other plants, such as
the epiphytes, saprophytes, parasites. or
climbing vines. More recently the term
has been used in a broader sense to
characterize ecologically unified, func-
tional groups of organisms (6). Our usage
denotes individuals that are filnctionally
dependent or interdependent with re-
spect to their herbivores. and does not
necessarily imply spatial association. Al-
though close spatial relationships are of-
ten important, functional guild bound-
Dr. Atsatt is associate professor of biology in, and
acting chairman of, the Department of Ecology and
Evolutionary Biology. University of California, Ir-
vine 92717. Mr. O'Dowd is a graduate student in the
same department.

24 SCIENCE, VOL. 193


aries are in each case defined by herbi-
vore feeding behavior and dispersal ca-
pacity.
Guild members function as antiherbi-
vore resources in three major ways: (i) as
insectary plants that aid in the mainte-
nance of herbivore predators and para-
sites. (ii) as repellent plants, either direct-
ly or indirectly causing the herbivore to
fail to locate or reject its normal prey.
and (~ii)as attractant-decoy plants caus-
ing the herbivore to feed on alternative
prey. In most cases the chemical or phys-
ical influence of these plant associates
causes a lowered herbivore functional or
rived from a cactus patch o r a spiny
numerical response (or both) (7). Guilds
shrub is often readily apparent, whereas
of potentially alternate prey may have
the additional long-term effect of increas-
ing the functional l ~ f eof plant defense
genes. We find the last-mentioned hy-
pothesis part~cularlyinteresting and de-
vote most of our discussion to its explo-
ration.
Insectary Plants
Floral and extrafloral nectaries pro-
vide an important alternative energy
source for herbivore predators and para-
sites. When nectar production by neigh-
boring (insectary) plants is synchronized
with egg laying by herbivore predators
and parasites, the efficiency of these in-
sects may be significantly higher. caus-
ing a lowered herbivore numerical re-
sponse. Parasitization of tent caterpillar
pupae in trees growing near nectar-pro-
ducing plants can be 18 times greater
than in trees lacking associated nectar
sources (8).Species of Pltuceliu grown in
orchards greatly increase the para-
sitization of l-'rospaltella perrziciosi by its
parasite Aphytis proclia (9). Chuma-
kova's data also show that the efficiency
of tachmid and ichneumon~dparasites is
substantially higher in cabbage fields
when they are grown near flowering um-
belliferous plants. Allen and Smith (10)
report that parasitization of the alfalfa
caterpillar by Apantelrs ~neditugirzis is
far greater where adjacent weeds are in
bloom than where they are absent. Simi-
larly, more beneficial insects can be
found in cotton growing immediately ad-
jacent to sorghum than in cotton growing
without sorghum (11).
Insectary plants also function as nur-
sery plants by supporting alternate hosts
for predators and parasites (12) Mucro-
centrus ancylivoru~is an effective para-
site against the oriental fruit moth in
southern New Jersey, where straw-
berries are frequently grown near peach
orchards and support alternate hosts for
2 JULY 1976
Estimated cover of buttercup i%) capacity of herbivores and their preda-
50 40
, ---. 30 20
, , 'P
O- , - tors o r parasites warns against the ex-
pectation that defense guild members
will always occur in close spatial proxim-
ity.
Repellent Plants
Repellent neighbors primarily lower
herbivore functional response via spines,
toxins, odors, and shade, causing the
o .A--l-- l
0 20 40 60 80 100 herbivore to reject or fail to locate its
Buttercup removed (%) normal prey. The physical protection de-
Fig. 1. Selective grazing by cattle of Agrostis
and Fesfuco in the presence of differing
densities of the b~~ttercupRnn~tnculus
hulbosus interference by a chemically repellent
[Data from (15)] neighbor is not s o obvious. In one such
case, Phillips and Pfeiffer (15) have
shown that forage grasses such as Agros-
the overwintering of the parasite (13). An tis and F t ~ ~ t u cgaina considerable protec-
outstanding example of a single para- tion from cattle when associated with the
sitoid species functioning on two sepa- noxious buttercup Run~rnc~4l~rs b~rlbosus.
rate leafhopper hosts on two separate This species contains the lactone ra-
plant genera has been described (14). In nunculin (16), a powerfi~lirritant of skin
central and northern California the wild and mucous membranes. Our plot of
grape. Vitis californicu, is attacked by their data (Fig. I ) shows the general cor-
the grape leafhopper m t h r o n e u r a t ~ l r - relation between decreasing buttercup
gunt~rlu.The egg parasite Anrrgrus rpos density and increased intensity of graz-
is particularly effective in controlling the ing. A similar but ~~nquantified example
grape leafhopper, but must have an alter- is found in southern Arizona rangelands,
nate host (the leafhopper Dikrella cru- where the presence of poisonous bur-
entata). which occurs on wild black- roweed (Haplopappu~trrzuisrctus) con-
berries (Rubus ursirzus). Wild grape and veys considerable protection to its asso-
blackberries grow in the same riparian ciated perennial grasses (17). In other
habitat and are often intertwined. Early cases of increased resistance in rnixed
each year, usually in February, the Dir- species stands. the specific cause is un-
krellu females are stimulated to oviposit known. Two closely related species of
by the rapid flush of new blackberry Trifoliurn, T. repens (white clover) and
leaves. The parasitoids quickly respond T. fragijeru~n, are commonly found as
and their numbers increase enormously, wholly intermingled swards in lowland
reaching their peak in late March. The and riverside grasslands in Britain.
outpouring of adult Arzagrus from black- When plots of these species were grown
berry thickets coincides effectively with as pure stands and as m i x t ~ ~ r at e s Oxford
the first appearance of grape leaves and (IS), white clover was ignored by hares,
the initial deposition of eggs by over- which, however, completely defoliated
wintering grape leafhoppers. The phenol- the plots of T. fragifrrurn. In mixed
ogy may be accelerated or delayed de- stands T. frugijeruln was ignored by the
pending on temperature, but the same hares and the species persisted together.
factors that govern the appearance of Similarly. the grass grub C o ~ t r l y t r uzea-
new blackberry growth also seem to in- lundica and the porina caterpillar dam-
fluence the time of appearance of the age white clover in pure stands, but sus-
grape leaves and the first oviposition by ceptibility is decreased in stands mixed
Erythrorzrura. Selection may have fa- with perennial ryegrass (19).
vored grape plants with a delayed leaf The well-documented principle of
production synchronized with the avail- warning coloration for visually orienting
ability of egg parasites "cultured" on predators predicts the operation of warn-
blackberries. ing odor for chemotactically orienting
Although grape plants derive maxi- herbivores. Levin (3) advances the hy-
mum protection by growing adjacent to pothesis that volatile components of tri-
o r intermixed with blackberries, dis- chome exudates serve the plant as an
persal of Arzagrus individuals produced outer line of defense by advertising the
early in the spring provides efective con- presence of substances that insects
trol of the grape leafhopper at least 4 would find repellent should they sample
miles from blackberries. The dispersal the host. Volatile chemical deterrents
 Egg masses Attractant-Decoy Plants
captured (%)
Solanum tuberosum 50 3
We now consider plants that can po-
/,-
tentially serve as alternative prey and
examine how feeding and oviposition be-
havior is influenced by relative quality.
Each food plant has an absolute q~lality
Fig. 2. Growth response of defined by its chemical, morphological,
the Colorado potato beetle temporal, spatial, and numerical effects
on six Solanaceous species.
43,0 contrasted with the percen- on herbivore fitness. but also has a rela-
tage of egg masses captured tive quality that is a function of its abun-
by these plants in the pres- dance and its chemical, morphological,
ence of equal amounts of the temporal. and spatial distance (quality
normal host, Solonr*m t u b ~ r -
osrtm. [Modified from Hsiao distance) from other known prey. Attrac-
and Fraenkel(33)l tant plants and decoy plants represent
0 0
the two extremes in this spectrum of
relative quality. Both draw off herbi-
vores and dilute their impact, but have
opposite effects on herbivore fitness.
Many attracting plants are not what
24 48 72 they advertise, and function as decoys.
Time (hours) causing mortality o r reduced fecundity
because of the presence of toxins or
because of the absence, deficiency, or
may also modify feeding behavior on parasitism by Brssa hrrrveyi of the larch imbalance of certain nutritional materi-
neighboring plants by acting as a general sawfly Pristiphoru rrichsonii in different als. Although some animals select food
repellent o r by the masking and antago- sections of its food tree were primarily primarily in a negative way and eat ev-
nism of feeding cues. Significant data on due to the masking effect of the odors erything not containing deterrent chem-
repellent-interference have been mar- from shrubs beneath the Lari,~luricinn icals ( 1 , 3 1 ) , the presence of feeding ex-
shalled through st~ldies of plant-insect trees and by the close proximity of Picpa citants may be the stimulus for oviposi-
associations in simple and diverse com- glu~icuand other species of trees. tion "mistakes" that lead to larval death
munities (20, 21). These investigations The shade produced by plant canopies in many specialized insects (32). Herbi-
and others (22) establish the pattern that can also be an effective herbivore deter- vores dependent on specific oviposition
plants grown in rnonocult~~re may suffer rent (26). At the time of its introduction o r feeding cues are susceptible to the
a higher herbivore load than conspecifics into North America, the Klamath weed presence of similar stimuli in associated
grown in floristically diverse habitats. Hypericuin prrforutmm grew best on species of variable nutritional value, as
Field experiments by Tahvanainen and open, sunny, well-drained slopes. and illustrated by the study of Hsiao and
Root (21) suggest that the presence of grew poorly in the shade. In a biological Fraenkel (33) on host selection and
nonhost plants interferes with herbivore control effort, two leaf-eating beetles growth response of the Colorado potato
orientation and host utilization. On the (Chrysoliilrr yurrtdrigrininu and C , hyper- beetle, Leptinotarsrr tdecemliileata (Fig.
basis of the hypothesis that some plants icu) were introduced into Californic'i from 2 ) . In the presence of equal amounts of
produce repellent or masking chemical France and England. The beetles prefer the normal host, Solan~im t~iberosum,
stimuli, choice experiments were used to to lay their eggs in sunny areas, and species from several genera in the Sola-
test the influence of nonhost plants on consequently the weed was eliminated naceae each capture a large proportion
the feeding behavior of a specialized best from open habitats. Klamath weed of the available egg masses. Growth re-
herbivore. Phyllotrcttr c.rlic(ferrre. In all now occurs more frequently under trees sponse, and presumably fecundity, dif-
cases, collard (Brassicz olerucea var. than in sunny areas (27). The crucifer fers markedly, with one of the most le-
uc.c.phol(r) that was kept alone was pre- Dentarirr diphj'llrr is apparently protected thal decoy plants (Solun~im nigruin)
ferred over collard associated with the from at least three flea beetles by grow- drawing the highest percent of egg
nonhost test leaves (tomato and Ain- ing in shady woodland habitats (28). masses. These data and others (34) sug-
hrocia urtemi~irfoliu).The experiment in- Herbivore pressure may also confine the gest that coexisting toxic and nontoxic
dicated that interference was effective on hemiparasitic plant Prciic~ilaris liens[- plants with similar attractant chemistry
the olfactory level and possibly was due j/oru largely to growth in the shade of represent a selectional paradox for
to direct repulsion rather than merely to oak trees (29). Larvae of the nymphaline would-be host-specific herbivores. In ag-
feeding inhibition. Root (23) concluded butterfly Euphj'tdryas editha feed on this ricultural systems, the proper manage-
from these studies that ecosystems in plant, but ovipositing females at Jasper ment of decoy plants might produce ef-
which plant species are intermingled pos- Ridge do not fly into the shade, even on fective control of some crop pests. The
sess an "associational resistance" to cer- hot days (30). This flight behavior tends a r g ~ ~ m e nthat t similar ovipositional and
tain types of herbivores. to keep them out of contact with Prci- feeding "mistakes" would not be ex-
The principle of odor masking is fur- icmlrrris, although they f r e q ~ ~ e n t l yfly pected in nat~lralcoevolved systems ne-
ther supported by the fact that host- within 3 to 4 meters of large stands of the glects the occurrence of rapid changes in
finding by the parasites of herbivores plant. Shade is, of course, produced by a plant quality. We discuss later a variety
often depends on cues produced by both variety of abiotic objects, but in many of factors that produce such variability.
the herbivore larvae and by their food habitats plant foliage is the only available Plant attractiveness is often relative
plants (24). Monteith (25) demonstrated source of this potential herbivore deter- and changes with the availability of other
that the differences in the percentage of rent. choices. The amount of bracken fern
SCIENCE, VOL. 193
 eaten by cattle is a function o f the rela-
tive palatability o f neighboring plants
(35). In pastures where highly palatable
species are available, bracken fern is
rarely grazed (20 grams per head daily),
while in pastures with moderately palat-
able species available cattle consume up
t o 200 g per head each day. Bracken
consumption jumps to 2 kg per head per
day in pastures with many unpalatable
species. Neighbor-controlled relative
preference is equally operative within
polymorphic populations. In the pres-
ence o f alternative prey, the slug Agric~li-
max rc~titmlrrtm \ rejects strongly cy-
anogenic Lotus cornic u l a t ~ rindividuals,
~ fungus. Sooner o r later the fungus responds
but readily consumes this chemical
morph in the absence o f the preferred
intermediate and acyanogenic phenotype
(361.
Attractant plants filnction as sinks for
insect herbivores and may permit a less
preferred species, race, morph, or age-
class to exist at high absolute abundance
or to escape during a critically suscep-
tible growth stage. In agricultural sys-
tems, the lygus bug attacks both cotton
and alfalfa, but shows a decided prefer-
ence for alfalfa. Stern rt ul. (37) inter-
planted 160 acres ( I hectare = 2.47
acres) o f cotton with strips o f alfalfa
totaling 8 acres. In June, July, and Au-
gust the average number o f Lygrn5 adults
per 50 sweeps was 100. 96, and 198 per
month in the alfalfa strips. and only 2
per month in the cotton. Cotton is nor-
mally sprayed for L y g u ~ when den-
sities reach 10 to 15 adults per 50
sweeps; and in the absence o f alfalfa, as
many as four chemical treatments o f cot-
ton may be required during the season.
Changes in the relative abundance o f
prey did not alter preference; when an
adjacent 160-acre field o f alfalfa was
cut. the number o f adults in the neigh-
boring alfalfa strips increased from 198
to 439 immediately after cutting. At the
same time, adult Lyglrs bugs in the inter-
plant cotton only increased from two to
four per 50 sweeps. In a similar case
(38), the sorghum shoot fly damages
exotic and Indian varieties o f sorghum
equally when there is no choice for ovi-
position, but manifests a strong prefer-
ence for exotic varieties in a choice situ-
ation. Counts o f eggs per plant averaged
7.3 on the exotic variety as compared
with a range from I .4 to 2.5 on four In-
dian varieties. Attractant plants are thus
at a selective disadvantage and would
tend to maintain this status in regimented
agricultural systems. The reverse may
be true in natural ecosystems, where a
variety o f perturbations and natural
cycles alter the relative attractiveness
o f alternative prey.
2 JULY 1976
Gene Conservation Guilds
In the adaptation-counteradaptation
view o f plant-herbivore coevolution
it is assumed that plant gene pools are
sufficiently diverse and that recombi-
nation is sufficiently effective to meet
most new herbivore breakthroughs. Pa-
thologists seeking t o control plant dis-
ease in agricultural systems have in the
past made analogous assumptions, as
V a n der Plank (39) humorously de-
scribes:
The plant breeder incorporates into a new
wheat variety a gene for resistance to a rust
with a gene or genes that allow it to attack
the new variety. The breeder then adds more
genes, the fungus overcomes them, etc. T o
ensure a continuous supply of genes for de-
fense the breeder establishes an international
wheat collection to discover all available
genes in Trificrrm,and to make doubly sure he
is missing nothing, he draws on Argilops
and Agropyron as well. If only he can find
enough defense genes to match every one
the fungus can throw into the battle, and then
have one to spare when the fungus has ex-
hausted itself, the battle will go to the breed-
er. Victory, in this view, goes in the end to the
side with the remaining gene.
This notion o f "winning the arms race"
has proved ~lnrealisticin agricultural sys-
tems and is equally invalid in nat~lral
ecosystems. Decades o f experience with
crop protection have led to the general
conclusion that actions delaying the de-
mise o f existing defenses are often more
beneficial than an endless search for new
weaponry (40).T h e most interesting pre-
diction arising from our consideration o f
defense guilds is that gene conservation
should also play an integral role in the
defensive posture o f natural populations.
I f gene conservation is a principal fac-
tor in successfi~l long-term defense
against herbivores, selection should fa-
vor individuals living in environments
that effectively "cultivate" herbivore
susceptibility. Susceptibility can best be
maintained through host nonuniformity
that disrupts evolutionary tracking or
specialization by herbivores. Individuals
occurring within feeding environments
(guilds) that provide acceptable options
o f similar but distinctive quality should
have greater fitness than those in feeding
environments offeringlittle or no choice.
The requisite variability in plant quality
may be generated within populations via
age-class differences, genetic polymor-
p h i s m ~ ,and variable growth conditions,
or by guild formation between popu-
lations, races, closely related species,
and ~lnrelatedbut chemically similar spe-
cies.
Herbivore susceptibility may be en-
hanced either by selection against viru-
lent individuals, or by decreasing the
exposure frequency o f susceptible geno-
types. T h e latter event takes advantage
o f herbivore behavioral sensitivity to
variable food quality. Georghiou (41) ar-
gues that selection for behavioristic re-
sistance to pesticides (the ability to de-
tect, escape t o nontreated areas, and
survive) operates in favor o f individuals
with physiological susceptibility t o the
pesticide. I f the "irritated" insects do
not have an escape opportunity (alter-
nate nontoxic areas), selection will favor
physiological resistance. Analogously, i f
herbivores are "irritated" by their food
but have no feeding alternatives, selec-
tion will favor physiological resistance.
The second model o f direct selection
against "virulent" genotypes requires
temporal cycling o f the herbivore popu-
lation between resistant and nonresist-
ant hosts. It also assumes that herbivore
races with the "virulence" necessary to
counter a particular resistance gene are
less fit to compete successfully on host
types without this gene. Evidence for
loss o f fitness by organisms carrying un-
necessary virulence is well documented
(42), particularly for plant pathogens.
V a n der Plank (39) contrasts the ability
o f the stem rust P~icciniugrurninis to
overcome resistant wheat under condi-
tions approaching monoculture, with its
inability to do so with alternating ex-
posure to nonresistant varieties. In
North America, P. gruoninis cycles be-
tween spring wheat, which is protected
by the resistance gene S1.6, and winter
wheat, substantially without the Sr,
gene. P. grrrminis spends about 2 months
o f the year in varieties with the Sr, gene
and the remaining 10 months o f the year
in varieties without this gene. Races o f
P. graminis able to attack varieties with
the gene S1.6 have been present in North
America for many years, but spring
wheat continues to remain relatively free
from attack. V a n der Plank calculates
that, during the 10 months or 30 genera-
tions P. graminis is on winter wheat, the
relative abundance o f races with the nec-
essary virulence to attack spring wheat
drop to 2.6 x o f its initial value.
Puc,c.inia grrrlninis is completely ca-
pable o f flourishing on the genotype Sr,.
This genotype (variety Eureka) was re-
leased in Australia in the late 1930's and
soon became widely grown in Queens-
land and northern N e w South Wales.
The rust utilized grasses and self-sown
wheat as alternate hosts when it was not
in the planted wheat fields. As the Eu-
reka variety increased in popularity, the
self-sown wheat also became largely o f
the same genotype. Without relaxation
o f selection for resistance, the Eu-
reka variety was quickly destroyed. Van
der Plank emphasizes that, although
there is no substitute for strong genetic
resistance, it is a common misconception
that a resistance gene is a resistance gene
per se, wherever it may be.
Many insect populations use several
hosts of variable quality but, over a peri-
od of time. they may be exposed to
additions, deletions, and changes in the
proportion of each type of host. For
example, from a population sample of
the African Queen butterfly, Durzuus
chrysippus, collected in Ghana, Brower
and his associates (43) concluded that 6
percent of the caterpillars fed on Calotro-
pis proceru, 10 percent on Perg~ilrrria
ciaemia, and 84 percent on Lc~ptuderzia
hrrstrrtrr, three species of the Asclepia-
daceae with markedly differing cardeno-
lide concentrations. At a series of sites in
Colorado, larvae of the Rower-feeding
lycaenid butterfly Gluucop.syc.he lyg-
cirrmus feed on a suite of perennial herba-
ceous legumes: four Lrnpirz~4s species,
Thrrlnopsis ~nontanrr, and Vicia ameri-
calla (44). Oviposition choice among the
lupine species is related to pubescence;
when G. lygdu~nushas a choice, it lays
eggs preferentially on the inflorescences
of the least hairy Lupirzrns present. Dol-
inger and co-workers (45) have shown
that three of the Lupinus species have
distinctly different alkaloidal patterns,
"low," "high variable." and "high con-
stant." They hypothesized that within-
population variability in alkaloids is an
antispecialist chemical defense mechan-
ism which may impede selection for pest
strains capable of detoxifying these com-
pounds. They suggest that plant popu-
lation variability may be maintained by
frequency-dependent selection, since, as
an alkaloidal type becomes most com-
mon, it will also, after several butterfly
generations, become the most suscep-
tible to predation. Their view of the sig-
nificance of intrapopulation variability is
analogous to our concept of gene con-
servation guilds, and frequency-depen-
dent selection is one mechanism, among
others, that could force herbivore cy-
cling between guild members. whether
they be intra- or interspecific associates.
Herbivores exhibiting a flexible search
image influenced by learning have the
ability to switch prey, that is, to concen-
trate their attacks disproportionately on
a new prey type (46). Conditions that
favor switching behavior in general pred-
ators may include (i) prey that are patchy
in distribution in both space and time
with respect to the search range of the
predator, (ii) mobile searching behavior
in the predator, and (iii) use of sensory
detection systems that work at a dis-
28
tance. Although clear cases of switching
remain to be observed, many herbivore-
plant systems satisfy these general condi-
tions. The checkerspot butterfly. Eu-
phydryu.~ c~tditha,from Gardisk Lake.
California, will oviposit on either Pen-
JtcJmorz heterodoxus or Cu~tillqjunrrrzu if
no choice exists, but in the presence of
C. narzu the insect must reach a high
state of oviposition motivation before P.
hc~tc~rocic~xrnsbecomes an acceptable al-
ternative. Singer (30) suggests that the
probability of this state being reached
would depend on the relative densities of
both species, and on their distribution
relative to that of E. editifrr females. In
pop~llationswhere adult nectar sources,
oviposition plants, and larval food plants
are all abundant and share similar distri-
butions in space, oviposition motivation
would only rarely rise to the point at
which secondarily preferred oviposition
plants are accepted. In contrast, when
nectar sources are dispersed and favored
oviposition plants are less abundant, the
frequency of oviposition on secondarily
preferred plants should increase (30). Ac-
cordingly, a chemotactically preferred
host such as C . nunu should increase its
fitness by growth at low frequency, inter-
mixed with an acceptable alternative
host, and away from potential nectar
sources.
Events that induce or force changes in
herbivore feeding behavior are poorly
understood. The availability of preferred
prey can be altered by changes in the
physical environment, by herbivore com-
petitors (47). by interplant competition
that may result in cycles of alternating
high and low pop~llationdensities (48)
and by repellent neighbors. The in-
troduction or immigration of new plant
species and races can cause temporal
host diversion of some phytophages (37,
38, 49). In sit^^ changes in plant quality
are facilitated by "open" recombination
systems (4,50) and by the fact that many
defense compounds also have important
metabolic functions and respond to stim-
uli other than predation (51). More rapid
and less predictable phenotypic changes
in secondary chemistry are caused by
diverse environmental factors such as
photoperiod, season. temperature.
drought, nutrient availability and ul-
traviolet light (51. 52). Mattson and Ad-
dy (53) emphasize the sensitivity of for-
est insects to changes in plant quality
and conclude that factors such as plant
age, stressful climatic conditions, low
fertility of the site, and bottlenecks in the
flow of certain nutrients interact to cause
significant increases in host quality and
decreases in host resistance. A dramatic
example is found in Australian grass-
lands where levels of tryptamine alka-
loids in the grass Phrrluris tuhrrosrr rise
with increasing temperature, light in-
tensity, and nitrate nitrogen, converting
this palatable food plant into a toxic
decoy plant that causes neurological dis-
orders and sudden death in sheep (54).
Even this environmentally mediated
change is neighbor-related; pastures on
which sudden deaths occur are in-
variably those on which nitrogen-fixing
clover has been -grown for some years.
A growing number of investigators
(23, 55, 56) have argued that diver-
sity per se does not increase stability in
plant-herbivore systems. The concept of
gene conservation guilds supports the
alternative idea that "a little powerful
diversity" of the right kind (55) is a key
component of stability. Validation of the
gene conservation hypothesis will re-
quire long-term genetic and demographic
studies of herbivore feeding patterns and
greater awareness of the food quality
variability achieved by abiotic environ-
mental factors, by population poly-
morphism, and by the association of
races, closely related species, and chem-
ically similar, unrelated species. The
common phenomenon of cohabitation by
closely related, theoretically competitive
plant species can be viewed with new
perspective under this model. Gene flow
may also be viewed as an important
means of retaining functional quality dis-
tance between species of diverging sec-
ondary chemistry. Sterile hybrids, often
seen as energetically superfluous, may
function as attractant-decoy plants that
contribute significantly to the cultivation
of herbivore susceptibility.
Summary
Optimal plant defense should incorpo-
rate any mechanisms that influence the
feeding behavior of potential pests.
From a diverse collection of examples
suggesting that the defense of a plant
may be improved in the company of
specific neighbors, we discuss a frame-
work of operational mechanisms that
begin to clarify some aspects of the re-
cognized influence of species diversity on
herbivory. Neighbors serve as insectary
plants for herbivore predators and para-
sites, and influence herbivore f e e d ~ n gbe-
havior by repelling, masking, attracting.
and decoying. Insectary plants lower the
numerical response of herbivores by in-
creasing the efficiency of their predators
and parasites. Repellent plants primarily
lower functional response by causing the
predator to fail to locate or reject its
normal prey. Attractant-decoy plants
SCIENCE, VOL. 193
dilute herbivore impact by drawing off
herbivores, either increasing or decreas-
ing their numerical and functional re-
sponse (or either).
The concept of gene conservation
guilds adds diversionary and delaying
tactics to the adaptation-counteradapta-
tion view of plant-herbivore coevolution.
The useful life of a given gene for re-
sistance may best be extended by mech-
anisms that disrupt genetic tracking
(specialization) by herbivores. Some
plants may remain inedible not because
their chemistry or morphology represents
an evolutionary impasse. but because they
live in an environment that provides
acceptable options of variable quality.
Feeding environments that provide little
or no choice promote specialization by
forcing physiological adaptation. Con-
versely, the evolutionary momentum of
specializing herbivores may be lowered
by enhancing their susceptibility, either
by selection against virulent individuals.
45. P. M. Dolinger, P. R. Ehrlich, W. L . Fitch, D.
E. Breedlove, ibid. 13, 191 (1973).
or by decreasing the exposure frequency
46. H. Cornell.Am. Nat. 110. 317(1976).
of susceptible genotypes. The latter
47. C . E . Atwood, Proc. ~ n t o m o l . ' ~ o c . ' ~97,
mechanism of conserving susceptible
individuals takes advantage of herbivore
behavioral sensitivity to variable plant
quality. Direct selection against virulent
genotypes requires temporal cycling of
the herbivore population between resist-
ant and nonresistant hosts. Both events
may occur within defense guilds that
provide acceptable feeding options of
similar but distinctive quality
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Plant Defense Guilds
Peter R. Atsatt; Dennis J. O' Dowd
Science, New Series, Vol. 193, No. 4247. (Jul. 2, 1976), pp. 24-29.
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32
Chemical Factors Determining the Choice of Food Plants by Papilio Larvae
V. G. Dethier
The American Naturalist, Vol. 75, No. 756. (Jan. - Feb., 1941), pp. 61-73.
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41
The Evolution of Resistance to Pesticides
George P. Georghiou
Annual Review of Ecology and Systematics, Vol. 3. (1972), pp. 133-168.
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46
Search Strategies and the Adaptive Significance of Switching in Some General Predators
Howard Cornell
The American Naturalist, Vol. 110, No. 972. (Mar. - Apr., 1976), pp. 317-320.
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48
The Comparative Biology of Closely Related Species Living in the Same Area. VII.
Interference Between Individuals in Pure and Mixed Populations of Papaver Species
John L. Harper; I. H. McNaughton
New Phytologist, Vol. 61, No. 2. (Jul., 1962), pp. 175-188.
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49
Rapid Asymptotic Species Accumulation in Phytophagous Insect Communities: The Pests of
Cacao
Donald R. Strong, Jr.
Science, New Series, Vol. 185, No. 4156. (Sep. 20, 1974), pp. 1064-1066.
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50
Pest Pressure and Recombination Systems in Plants
Donald A. Levin
The American Naturalist, Vol. 109, No. 968. (Jul. - Aug., 1975), pp. 437-451.
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53
Phytophagous Insects as Regulators of Forest Primary Production
William J. Mattson; Norton D. Addy
Science, New Series, Vol. 190, No. 4214. (Nov. 7, 1975), pp. 515-522.
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