FORUM
Hypersen~itivity:
Mechanism
A Neglected Plant Resistance
Against Insect Herbivores
c.
Department
WILSON
FERNAKDESI
of Biological Sciences. Northern Arizona
Flagstaff. Arizona 86011
University
EnV1ron. Entomol. 19(5)- 1173-1182 (1990)
ABSTR.-\cr
Despite many examples of plants. hypersensitive reaction against pathogens,
there are exceedingly few examples of hypersensitive reactions having any importance against
insect nerbivores. However. such plant defense mechanisms may be widespread among more
sedenwy insect herbivores. The examples in which a hypersensitive reaction was elicited
agains: insect herbivores were against galling insects. bark beetles. adelgids. and siricids. The
intimate and sessile interactions during insects. egg and larval stages may have selected more
specilic and more complex d~fcnses. because of the greater and more varied opportunities
that t!:-e host plant has for regulating the lives of its intimate associates. Thus. it is argued
that t:r.e intimate association of these herbivores during egg and larval stages set the scenario
for t~ evolution of this plant defense mechanism. The dearth of accepted examples of
hypersensitive reaction against insect herbivores may not reflect its actual frequency
and
occurrence in nature. Further investigation
on plants. hvpersensitive reaction against insect
herbl'ores may shed light on the ecology and evolution of insect-host plant associations.
KEY
WORDS
lnsecta,
hypersensitive
reaction.
STUDIESOF PLA-'l RESlSTANCEto insects have been
centered on a wiàe spectrum of plant features, such
as secondary com!X>UDds(Rosenthal & Janzen 1979,
Green & Hedin 1986), nutritional
factors (Rodriguez 19i2, Wbite 1984), phenology (Feeny 1976,
Faeth et al. 1981i. age (Morgan et al. 1983, Kearsley & Whitham 1989). induced defense (Green &
Ryan 19i2. Rhoaàes 1979, Haukioja 1982. Baldwin
1988 ). abscission : Kahn & CorneII1983, F ernandes
& Whitham 1989), plant morphological
traits (pubescence [Levin 1973. Pillemer & Tingey 1976,
Woodman & Fernandes in press], tissue hardness
[Coley 1983], coior [Tingey 1981], shape [Rausher
19i81 size [Kogan 19i51 and presence or absence
of nectar-secreting glands [Wilson & Lee 1971J).
Verv few studies :nave. however, addressed the importance of a particular type of induced defense,
i.e., plant hyper!eDsitivity, as a source of plant resistance to inseCt herbivore attack.
Plant hypersemitivity
is a term primarily
used
by plant pathologists to describe a response to infection by pathogens as well as to many nonpathogenic stimuli :e.g.. Matta 1971, Misaghi 1982).
Since the beginmng of this century. hypersensitivity has been recognized as an important
defense
mechanism used by plants against pathogens (e.g.,
Ward 1902. Stakman 1915).
I Current
addr~
ICB/Univenidade
zonte. ~1G-BraziL
~ento
de Biologia
Federal de Minas
Gerais.
Geral. C.P. 2486.
30161
Belo Hori-
induced
defense.
insect
herbivory
The hypersensitive
reaction
encompasses alI
morphological and histological changes that. when
produced by an injurious agent. elicit the premature dying. or necrosis. of the infected tissue. as
well as inactivation and localization of the infectiousagent (Mfil1er 1959. Maclean et al. 1974. Agri~
1988). After reaching the plant.s surface. the pathogen must penetrate into the plant .s cells. After
penetration. a suitable nutritional site must be found
to guarantee successful establishment. In some ca25.
establishment may fail because of the rapid death
of the host.s tissues at the site of infection. It is not
the invaded cells. but the adjoining cells that die
(White & Baker 1954. Hirata 1956). There is a
positive correlation between the speed of reaction
and the degree of host resistance to microorganisms
(White & Baker 1954. Cóffey & Wilson 1983. Davidse et al. 1986). Hypersensitivity
is usually controlled by an individual
gene or. more rarely. by
a few genes. Flor (1955) showed that hypersensitivity to fungi is determined by two specific genes.
one in the host and the other in the pathogen. For
further explanation of the gene-for-gene relationship. see reviews by Flor (1971) and Barrett (1985).
Hypersensitive reaction is the primary event in
resistance to fungal parasites (Maclean et al. 1974.
Agrios 1988). This reaction by the host leads to a
disruption of nutrient supplies to the invading microorganism (Wong & Berryman
1977) and the
production of many toxic metabolites. such as phytoalexins (Bavlev & Mansfield 1982. Smith & Banks1986) resultiitg in the cessation of microorganism
0046-225X/90/1173-1182S02.00/0
(C) 1990 Entomological
Societv of A~ca
174
ENVIRONMENT
growth (Maclean e[ al. 1974, but see Johal & Rahe
19881. Furthermore. water ar'd oxygen also are
reduced. thus further decreasing the probabilities
of establishment and success for the .invading organism (Wong & Berryman 1977).
Despite numerous examples of the hypersensitive reaction against pathogens, there are exceedingly few examples of hypersensitive reactions having any importance
against insect herbivores.
Painter (1951 i concluded that hypersensitivity
was
not offered as an explanation for any insect-plant
relationships despite the possibility that it is involved as a response to insects with sucking mouthparts. Here 1 revíe\\. the literatiíre in which hypersensitivity
is reported
to be one of the
mechanisms by which plants respond to insect herbivores, and I trv to evaluate whv there are so few
examples of it i~ the insect and plant literature.
Some Biochemical and Physiological
Aspects of Hypersensitivity
Several metabolic changes are detected at the
time tissue necrosis appears. The respiration rate,
oxidase levels, peroxidase levels, and mitochondria
numbers ali increase during the hypersensitive reaction (Királ:-. 1980). In addition, levels of phenolic
and flavonoid compounds are increased (Loebenstein 19+2). However, because several biochemical
changes are detected simultaneously, it is difficult
to decide with certainty which one is the primary
event that causes cell and tissue necrosis and rapid
loss of water. The necrotic response is the result of
a disturbance of balance between oxidative and
reductive processes (Király 1980). The result is an
excessive oxidation of polyphenol compounds and
a breakdown of cellular and subcellular structures.
It is not known whether the excessive oxidation of
phenols by phenolases or perox~Qases is the cause
or consequence of breakdown in cellular structures
(Király 1980. Cruickshank 1980).
The local necrosis may be regarded as a consequence of a pronounced senescence effect (Farkas
1978). Nevertheless, necrosis development
and
spread can be decreased by induction of a high
rate of RNA and protein synthesis (i,e., by the
rejuvenation effect of cytokinin treatment and other manipulations) (Király 1980), Not surprisingly,
host plant tissues under the action of gall-forming
insects present a high rate of RN A and protein
synthesis (e,g.. Bronner 1977, Rohfritsch & Shorthouse 1982, Meyer 1987). I postulate that in addition to increa5ed nutritional quality and prevention of abscission (by rejuvenation),
gall formers
engineer the host plant tissue to produce metabolites that avoid or decrease the probability
of a
hypersensitive reaction by the plant.
Peng & Miles (1988a,b. and references therein)
experimentally
showed that the sap-feeding rose
aphid. MaCTosiphum Tosae L., manipulates its host
plant .s chemical defenses. The phenol-oxidizing
enzyme found in the aphids. salivary glands and
AL
ENTOMOLOGY
Vol. 19. no.5
secretions showed a capacity to oxidize the o-diphenols present on the buds of its host plant (Miles
& Peng 1989). Removal of the aphids from treatment plants resulted in significantly elevated catechin levels. These studies illustrate the abilitv of a
sap-feeding insect to inter.vene in the host plant.s
defense mechanism, making plants more acceptable to the insect. A mucus of an unknown chemical
nature that is injected by siricid woodwasps during
oviposition reduces the host plant.s hypersensitive
reaction against the larval feeding stages of the
wasp and its symbiotic fungus (Madden 1988). In
another case. a mucous substance injected by siricid
female woodwasps during oviposition reduces the
host plant.s hypersensitive reaction against their
offspring (Madden 1988). However, more studies
are necessarv to evaluate insect herbivore.s abilitv
to manipulate localized reactions of host plants suc'cessfullv.
The hypersensitive response of plants to injury
and the consequent development of necrotic tissue
is prevented by high temperatures (37°C [98.6°F])
(Deverall1977, Király 1980). This is consistent with
tne observations by Fernandes & Price (1988, in
press) that gall-forming
insects are more speciesrich in xeric and hot, nutrient-poor,
areas than in
mesic and.cooler, nutrient-rich
areas. Fernandes &
Price \in press) argued that galling insects survive
better on en..ironmentally
stressed plants than on
healthy plants. Environmentally,
stressed coniferous trees were also more susceptible to bark beetle
attacks (e.g., Wong & Berryman
1977; Raffa &
Berryman 1982, 1983, 1987; Christiansen et al.
1987).
The hypersensitive reactions of trees are less effective under stress conditions (Puritch & Mullick
19'i5, Christiansen et al. 1987). For instance, water
stress greatly affected the necrophylactic
periderm
formation in Abies grandis and consequent increased susceptibility of trees to insect herbivores
(Puritch & Mullick 1975). The synthesis of defensive chemicals is an energy-expensive process (e.g.,
Feenv 19'i6, Rhoades 1979); hence the success of
eliciting a h)1>ersensitive reaction must be dependent on current availability
of energy (see Berryman 1988). Physiologically
healthy plants have
more energy (Miller & Berryman 1985), and perhaps better mechanisms for responding to their
herbivores than plants in poor physiological condition lsee a1SoBernard-Dagan
1988, Cheniclet et
al. 1988, Tuomi et al. 1988). There is an obvious
need for cooperative endeavors between plant pathologists, plant physiologists, and entomologists.
Onlv a multidisciplinarvapproach
can unravel the
fact:s that lead to an understanding of the processes
and mechanisms involved in the interaction between plants and their concealed or sedentary insect herbivores (or both). This approach taken in
bark beetle-host plant-fungus
systems led to an
enormous understanding of the patterns and proximate and ultimate mechanisms involved in the
svstems.
October 1990
FERNANDES:
HyPERSE."SITIVE
REACTIONS
Hypersensitivity
Response
Against lnsect Herbivore§
Plants present a large spectrum of resistance
mechanisms against insect herbivores. The defense
mechanism used is largely dependent upon many
factors. but primarily
the physiological status of
the plant. timing of attack. damage levei. type of
tissue removed. and intimacy of the relationship
between plant and herbivore. Thus. lnseCt herbivores can be classifjed according to the kind and
amount of injury they inflict on their host plants.
Mattson et al. (1988a) classifjed phytophagous insects into two major groups, free-feeding and attached-embedded
insects. Based on the potential
effect on host growth and reproduction. ~Iattson
et al. (1988a) ranked phytophagous insects into 13
feeding guilds. They argued that gall formers pose
the least threat to their host plant .s growth and
reproduction, whereas phloem. cambium. sapwood
borers have the greatest potentia] effect (but see
Fernandes 198i). However. gallers and bark beet]es may influence p]ant defense mechan1Sms in
similar ways.
Price (1980) argued that the host.s spectrum of
defense responses to parasites is dictated by the
intimacv of the association Isee aJsoHarris-& Frederiksen i984). Mattson et a]. (1988al state that with
the most intimate associations. alllife stages occur
within p]ant tissue, such as some bark beet]es and
galling insects. The least intimate association wou]d
then be those of herbivorous insects that feed externa]]y on their host p]ants. Mattson et al. (1988a)
suggested that intimate interactions may select more
specifjc and more complex defenses because of the
greater and more varied opportunities t:i1at the host
plant has to regulate the lives of its intimate associates. This hypothesis is supported by the fact
that embedded and phytophagous insects with
strongly limited movement are more host specifjc
than free-feeding insects (see Haak & Slansky 1987 ;
Mattson et al. 1988a.b). and by Maddox & Root.s
(1987) fjndings that heritab]e differences among
c]ones of Solidago altissima for resistance to galling
insects were larger than for other kinds of phytophagous insects.
In ]ine with Mattson and his assocÍates. arguments. I present examp]es where pJants respond
simi]arly to both ga]]-forming insects. bark beet]es.
adelgids. and woodwasp attack. I h)1>0thesize that
the intimacv of the association. the feeding behavior. damage' type. and type of plant tissue ;emoved
set the stage for hypersensitive reactioD.
Hypersensitive
ReactioD Against Galling Insects. The fjrst recorded case of a hypersensitive
reaction by a plant against an insect herbivore may
have been that of grapes and their Phylloura ga]]er. Bõtner & Schi]der (1934) observed that resistant
Vitis spp. were hypersensitive to P. oostatrix (Fitch).
a leaf-ga]]ing insect. Resistant plants reacted to the
attack of P. vastatrix with locall\" limited necrosis.
As a result, ga]]s did not develo"p arouod the site
AGAINST
HERBIVORES
1175
of induction. The induction sites were shut off bv
an inner wound periderm from the remaining ti;sue. The necrotic tissues were'later abscised (Miiller
1959).
The eastern spruce gall aphid. Adelges abietis
L., induces pineapple-like galls on Picea excelsa L.
(Rohfritsch
1981). Both susceptible and resistant
spruce trees were attacked by A. abietis. However.
a hypersensitiv~ reaction is elicited by resistant trees
during the first stages Qfgall initiation (Thalenhorst
19i2, Rohfritsch 1981 ). The greater hypersensitivity of the attacked cells leads to cell collapse by
plasmolysis. necrosis. and accumulation of phenolic
substances (Tjia & Houston 1975; Rohfritsch 1981.
1988). The insect that is now surrounded by the
necrotic cells has its access to soluble proteins ter-minated. Rohfritsch (1988) argued that a ..kind oi
hypersensitive reaction.. is the primary mechanism
bv which P. excelsa trees respond to the attacks of
their galling insects.
Hypersensitive reactions also have been reported
for EuTosta solidaginis (Fitch,. a tephritidstem
galler on Solidago altissima L. Seventy-three percent of EuTosta larval mortality was due to a hypersensitive reaction by the plant (Anderson et al.
1989). Field and laboratory experiments have shown
that plant genotypes that grow faster are preferred
by the ovipositing female, and that these ramets
are more reactive to the insect larval stimuli for
gall formation
(Weis & Abrahamson 1985). Anderson et al. (1989) showed that adult females preferred susceptible ramets over resistant ramets in
laboratory trials, thus suggesting that females have
discriminatory
abilities. Female choice had strong
effect on larval survivorship because larvae survived better in susceptible plants than in resistant
plants. In susceptible plants. 100 and 97% of the
larvae developing in leaf buds and meristem, respectively, survived. However. only 6i a!!d 35% of
the larvae developing in leaf buds and meristem.
respectively. of resistant plants survived.
Another case that is currently under investigation \unpublished
data) is the hypersensitive reaction of the shrub ChTysothamnus nauseosus
(Palias) Britt. to a Rhopalomyia cecidomyiid stem
gall former. On resistant plants, h~1Jersensitive reactions develop after the larvae hatch and start
feeding on plant tissue. Necrotic tissue develops
concentrically
around the feeding site stopping
water and food supply to the lan.a. These galls do
not achieve normal size and do not fully develop
the trichome layer that covers the gall chamber.
Preliminary
data indicate that hypersensitivity
is
the main mortality
factor for this gall former in
humid habitats.The feeding activity of a mite species, ETiophyes
cladophthiTus
Nal., induces a h~1Jersensitive reaction on its solanaceous host plant. It perforates
the wall of epiderriial cells of its host. Solanum
dulcamaTa L.. causing cone-shaped feeding punctures (WestphaI1980.
Westphal et al. 1981). Callose was detected near the puncture after 20 min
1176
E~VIRONMENTAL
ENTOMOLOGY
Vol. 19. no.5
of the life cvcle, the insect is anchored to the tree
and the injured cel15 were transformed into nutriby the feeding sty.lets that are inserted in the bark
tive ce115.Cel15 near the feeding 5ite5 on 5U5ceptible
(Greenbank 1970). Abies spp. respond to their adel-plan.t5 become nutritive ce115.w~ereas on re5i5tant
gid herbivore with the formation of "rotholz,"
or
plant5 they become necrotic. This hyper5en5itive
re5pon5e wa5 detectable on injured epidermal cel15 redwood, in the xvlem tissues \see Balch 1952. Hain
1988). Rotholz f~rmation appears to be a continafter 10 min and led to 5evere necr05is of 5urrounduation of the host hypersensitive response to the
ing ti55ue5 after 1 h. Polyphenolic compound5 were
invading adelgids. The first fir response to the indetected in the necrotic region after 4 h. Water
jury is the formation of a secondary periderm, the
1055at the contact 5ite between h05t and para5ite
necrophylactie-periderm.
internal to the wound
may have been the triggering mechani5m to the
(Mullick & Jen~en 1973a.b; Mullick 19ii). which
hyper5en5itive reaction (We5tphal et al. 1981. 5ee
isolates the necrotic cells of the hypersensitive real5o Abawi et al. 1977. Sigee & Epton 1976). After
action from the healthv. unaffected cells (Hain
the mite had perforated a cell, its vacuolar pH
1988). A layer of impe~ious tissue precedes forincrea5ed in 5U5ceptible andre5istant plant5 (We5tmation of the necrophylactic
periderm (Mullick
phal 1982). However. the reaction wa5 fa5ter in
1975). However. in susceptible hosts. the formation
5U5ceptible h05t5 than in re5i5tant h05t5. which reof the impervious layer is inhibited or delayed; or
5ulted in the collap5e and death of injured cel15 in
both. Mullick & Jensen ( 19i6) found that the rates
the latter.
of the development of this tissue were consistently
Hypersensitive Reactions ~st
Bark Beetles.
faster on resistant hosts than on susceptible ones.
Hyper5en5itivity
i5 a mechanism whereby conifThe more effective response of European firs to
erou5 plant5 re5i5t bark beetle attack (e.g., Berrythe balsam woolly adelgids compared with Amerman 1969. 1972; Berrvman & A5hraf 1970; Raffa
ican firs is due to a faster hypersensitive reaction
& Berrvman 1982. 1987; Christiansen et al. 1987),that kills or inhibits feeding of the insect herbivore
The ~etle5 that 5urvive the limited flU5h of primarv re5in are faced with the tree.s second line of
(Hain 1988).
defe'n5e-hyper5ensitive
reaction in the ti5sues surHypersensitive
Response Against W'oodwasps,
Growth of woodwasps lan.ae of the geniis Sirex is
rounding the beetle.s galler~'. The cel155urrounding
drastically impaired on host plants that elicit a hythe attacked site degenerate. and terpenes. pol~,persensitive response. Hosts belong to-the genera
phenol5, and other toxic or inhibitory compQunds
Pinus, Abies, Picea, Larix. Pseudotsuga, and Auare relea5ed (Miller et al. 1986. Christian5en et al.
ricaria (Morgan 1968, ~1adden 1988). Woodwasps
1987). As a re5ult, both beetle and pathogenic funare attracted to physiologica1ly stressed trees (Madgu5 inoculated by the beetle are sealed in a le5ion
den 1977, 1988). During oviposition, the female
of dead. re5in-impregnated
tissue (Wong & Berinjeets a mucus of unknown chemical nature and
ryman 1977. Raffa & Berryman 1987). The nespecies-specific symbiotic fungal spores into the host
crotic area al50 is impregnated \\ith re5inou5 and
plant tissue. The mucus alters the water balance of
phenolic compounds that prevent construction of
plant needles causing tissue desiccation and colbeetle gallery, fungal proliferation. and beetle egg
lapse of the phloem elements (Fong & Crowden
and larval 5urvival (Russel & Berryman 1976, Raffa
1973) and resu1ting in inhibition of translocation
et al. 1985, Christiansen et al. 1987). Hypersensitive
(Madden 1988). The combination of these proreaction appears to be the most important defen5e
cesses, plus plant tissue laceration during woodmechanism in lodgepole pine and Norway 5pruce
wasp oviposition favors fungus establishment and
against bark beetle attack (see Raffa & Berryman
growth. Host resistance to Sirex and its symbiotic
1982, Christiansen & Horntvedt 1983). The coniffungus is primarily due to a hypersensitive reaction
erou5 tree bark-beetle fungus ~"stem is the mo5t
by the invaded host plant \e.g., Coutts & Dolezal
well-5tudied example of plant h,.-per5en5itive re1966; Coutts 1969a,b). Polyphenols are produced
action involving herbivorous insects (for additional
as a specific response to the woodwasp symbiont
reference5 5ee Chri5tiansen et~.
1987, Raffa &
fungus (Coutts & Dolezall966, Hillis & Inoue 1968).
Berrvman 1987, Berrvman & Ferrell1988,
Chri5The mucus plays a major role in inhibiting
transtian5'en & Bakke 1988, Flamm et al. 1988, Raffa
location
of
photosynthatea
precursor
to
polyphe1988).
no1 synthesis (Madden 1988). Water-stressed trees
Hypersensitive
Reactions
Against
Balsam
are the most susceptible hosts to woodwasps. In
Woolly
Adelgids. Hypersensitive reaction5 sucwater-stressed hosts, photosynthesis and transpicessfully reduce the effect caused by bal5am woolly
ration decline, thus impairing host hypersensitive
adelgids on fir trees. North .-\.rnerican fir5, comreactions against the invading fungus (see Madden
pared with European fir trees, experience extensive
crown dieback, or tree death. or both, as the result
1988).
of attack by Adelgis piceae (Ratzeburg};On hatching, the fir5t-instar nymphs wander on the tree
DÍ6eu§8ion
before 5ettling on selected feeàing sites within the
Hypersensitivity
is an important
mechanism
tree crown or on steffi$. This brief crawler stage i5
wherebv
plants resPOnd to insect herbivores.
Ali
the only motile stage. Throughout the remainder
L
October 1990
FERNANDES:
HyPERSENSITIVE
REACTIOr.;S AGAINST HERBIVORES
the cases in \vhich hypersensitivity
was found to
be a mechan1Sm operating against insect herbivores
were for galiers, bark beetles, adelgids, and woodwasps. However, plants' hypersensitive
reactions
may be common against other phytophagous insects particularly less mobile insects during their
feeding stages. such as coccids, psyllids, and galling
sawflies. The intimacy of the association posed by
the h~rbivorous feeding habit and quality of the
tissue remo\.ed ma\, have set the scenario for the
development and évolution of this plant defense
mechanism. Adoptmg an ..optimal defense view,.'
Berryman ( 1988) proposed that defensive traits are
selected to optimize plant fitness in the face of
different herbivore attack patterns and life history
strategies\seealsoRaffa & Berryman 1987). Hence,
different plant defense strategies should be expected against the different insect herbivore guilds.
Other plant defense mechanisms should be expected for free-feeding insect herbivores. It would
be detrimental to a plant to be hypersensitive to
free-feeding herbivores, because free feeders can
move about and among plants. The immediate consequence of this strategy \vould be a cork tree! The
apparent lack of substantial evidence for significant
genetic variation among plants resistant to most
free-feedin2 leaf herbivores is corroborative of this
view (e.g., ~ Maddox & Root 1987, and revie\"
by Mattson et al. 1988a). Conversely, differential
pl~pt resistance to sap-feeding, gall-forming,
and
bark beetle insects are very common in the literature (e.g., Edmunds & Alstad 1981; Wilson &
Moore 1986; Mattson et al. 1988a,b; Rohfritsch
1988).
Hypersensitive reactions of plants ultirnately may
have inHuenced the distribution of movement-constrained insect herbivores. The sessile habit is complete in galling insects because they can not leave
their galls once formed, but leafminers, stem borers, and bark beetles can still move with some freedom inside their host or even leave it (e.g., Gross
& Price 1988). Hence, leafminers and stem borers
can avoid or select feeding areas inside the host.
Several gallers develop from eggs laid inside their
host plants, and thus cannot choose where to induce
the gall. However. the females must have evolved
behaviors to avoid laying eggs in plant parts where
necrosis is more likely to happen. DeClerck
&
Steeves (1988) reported that the cecidomyiid
CYstiphora sonchi (Bremi) lays its eggs through the
stomata of its host plant, Sonchus arvensis L., thus
avoiding injury to the host and a possible hypersensitive reaction against the egg. Furthermore,
larval behaviors may have evolved to elicit rejuvenation of tissue that guarantees a highly nutritious diet and at the same time prevents necrosis.
For example, galling aphids and psyllids penetrate
the tissues of food plants intercellularly
and feed
primarily on phloem sap, thus bypassing the contents of parenchymal cells en route (Campbell et
al. 1986. Raman 1987). These behaviors corrobo-
1177
rate the view that more specifjc insects such as
gallers. bark beetles. and sap-feeders can avoid
feeding on plant tissues where hypersensitive responses are likery to occur.
More studies on plants. hypersensitive reactions
to herbivores are needed. Closer observations should
be made during the herbivore.s oviposition period
to verify site selection and host response to egg
laying and injury. Because microorganisms may be
associated with insect gall formation (e.g., Cornell
1983. Price et al. 198i), we must verifv if the hvpersensitive reaction is directed to the. insect hérbivore or to the associated microorganisms, as seen
in the bark beetle svstems, as well as in the siricidfungus systems. Ind.eed much of plant defense may
be adapted to the symbiont microbes rather than
the insect herbivore. For instance, Jones et al.
(1981a.b) showed that allelochemical
defenses of
baldcypress inhibited
silkworm
enteric microorganisrns by altering the physiological state of the
silkworm .s gut. The loss of the microbial nutritional
contribution caused silkworm larval growth inhibition. ~tany other examples exist (e.g., Hedin et
al. 19i5. Martin 198i), indicating
that this phenomenon may be widespread. Insect herbivoremicrobe mutualisms are widespread in nature and
influence the success and radiation of marn' insect
orders. such as Isoptera and bark beetles (Breznak
19i5,.Jones 1984, Price 1984. CampbeII1989).
Microorganisms contact with plants happened much
earlier in evolutionary time than contacts between
insects and plants (e.g., Atsatt 1988). Thus, it is
possible that many plant defenses, such as hypersensitivity reaction, and perhaps phenolic compounds, are responses directed to symbiont rnicroorganisms rather than the herbivore.
Phenolic
compounds are very widespread and an important
plant response against microorganism
invasion
(Matta 19i1, Misaghi 1982). Recent studies have
also shown that many defense mutualisms have
evolved between plants and endophytes (e.g., Carro111988, Clay 1988). The pursuing of studies on
these phenomena may broaden our limited, twodimensional (herbivore-host
plant) view of herbivore-plant relationships.
A theory for plant defensive responses on a cellular levei was developed by Berryman (1988) (see
also Bernard-Dagan
1988, Cheniclet et al. 1988,
Lieutier & Berryman
1988a,b). In this theof)..
parenchyma cells react to alI kinds of injuries in a
similar way (see Hadwiger & Beckman 1980, Hadwiger et al. 1981, Lieutier
& Berryman 1988b).
Plant cell wall polysaccharide
fragments are released by mechanical damage or by the action of
enzymes secreted either by the host plant or herbivore during herbivore feeding (Darvill & Albersheim 1984). The release of these fragments triggers
the attacked host plant to produce some defensive
chemicals. The chemicals produced would be contained ",ithin vacuoles and nonliving plant tissues
or transported via the conducting tissue and would
ENVIRONME!-.IAL
1178
activate celis remote from the point of injury (Berryman 1985). thus causinga systemic reaction ob
served in some plants (e.g., Edwards & Wratten
1983. Kúc 1983). This type of résponse is elicited
by enàogenous or endoelicitors that are products
of the plant itself (Berryman 1988). Exogenous or
exoelicitors lenzymes or toxins secreted by the invading organism or fragments of their extemal skin
releaseà by the action of plant enzymes) would
give rise to a different plant response (see Ryan
1984. ~1iller et al. 1986. Berrvman 1988). In this
case. host parenchyma cells become hyperactive.
thus producing large quantities of defensive chemicals that are synthesized in an apparently uncontrolled manner. The defensive substances or their
precursors and cell fragments are released into the
conàucting plant tissues blocking the penetration
of the pathogen and extending the reaction zone
(Be~man
1988). Hyperactivity
will cease as soon
as the invasion is contained.
?\'evertheless. our knowledge about the biochemical anà cellular bases for the hypersensitive response to phytophagous insects is still fragmentar).
and rudimentary. There is an increased need for
more focused studies on this plant resistance mechanism as more examples of its widespread occurrence are discovered. It is true that well-documented cases of the hypersensitive reactlon against
insect herbivores are rare. However, a phenomenon mav lack documentation for reasons other than
the sca~cih. of its occurrence. For instance, studies
of host'resistance could have missed hypersensitivity as a mechanism because of the way in which
studies were done. In addition, a phenomenon also
may appear rare due to rigid standards posed by
the scientific community
for its identification
and
verification. Thus, the dearth of accepted hypersensitive reaction examples against insect herbivores may not reflect its actual frequency and occurrence in nature. Further investigation on plants.
hypersensitive reaction against herbivorous insects
may shed light in many other areas of ecology and
evolution- and perhaps bridge our fragmentar)'
knowledge of many fields in biology.
Acknowledgment
I thank T. G. Whitham.
P. W. Price, S. Suter, K. C.
Larson. O. Rohfritsclr,
E. Westphal. J. States. R. Declerck-Floate. M. J. C. Kearsley, a special anonymous
reviewer .and two other anonymous reviewers for their
enthUSIasm and helpful comments on early drafts of this
manuscript. I also acknowledge
a scholarship provided
by the Conselho Nacional de Ciência e Tecnologia in
Brazil :CXPq. process #200.747/84-3-Z0).
and the facilities Dro\ided bv Northern Arizona University.
References
Cited
Abawi. G. S.. D. C. Crosier & A. C. Cobb. 1977.
Pod
fleck.ing of snap beans caused by Alternaria alternata.
Plant Di.s. Rep. 61: 901-905.
ENTOMOLOGY
Vol. 19. no.5
Agríos. G. N. 1988.
Plant pathology, 3rd ed- Academic. New YorkAndenon. S. S.. K. D. McCrea, W. G. Abrahamson &
L. M. Hartzel.
1989.
Host choice by the ball gaJl.
maker Eurosta solidaginis
(Diptera:
Tephritidae
Ecology 70- 1048-1054.
Ataatt. P. R. 1988.
Are vascular plants "inside-out-.
lichens? Ecology 69: 17-23Balch. R. E. 1952.
Studies on the balsam wooly aphid.
Adelgis piceae (Ratz.) (Homoptera:
Phylloxeriàae;
and its effects on balsam fir. Abies balsamea (L-) ~Iill.
Canadian Department
of Agriculture Publication 5õ:'.
Fredericton.
New Brunswick.
Baldwin, I. T. 1988.
Short.term
damage-induced mcreases in tobacco alkaloids protect plants. Oecologia
(Berl_) 75: 36i-370.
Barrett, J. 1985.
The gene-for-gene
hypothesis: par.
able or paradigm. pp. 215-225. In D. Rollinson & R.
~1. Anderson [eds.J, Ecology and genetics of hostparasite interactions.
Academic. London.
Bayley,J:-A.
& J. W. Mansfield.
1982.
PhytoalexinsWiley, New York.
Bemard-Dagan.
C. 1988.
Seasonal variations in energy sources and biosynthesis of terpenes in maritime
pine. pp. 93-116. In W- J- Mattson. J- Levieux & C
Bernard-Dagan
(eds.), Mechanisms of woody p!ant
defenses against insects: search for pattern. Springer\.erlag, New York.
Berryman, A. A. 1969.
Responses of Abies grandis to
attack by Scolytus ventralis (Coleoptera
,colytidae,
Can. Entomol. 101: 1033-1041.
1972. Resistance of conifers to invasion bv bark beetlefungus associations. BioScience 22: 59S:.OO2.
1988. Towards a unified theory of plant defense. pp
39-55. In W. J. Mattson, J. Levieux & C. BernardDagan [eds.J, Mechanisms
of woody plant defe~
against insects: search for pattern. Springer-Verlag,
New York.
Berrvman, A. A. & M. Ashraf.
1970.
Effects of Ahie:3
iandis
resin on the attack behavior and brood survival of Scolytus ventralis
(Coleoptera: ScolytidaelCan. Entomol. 102: 1229-1236Berryman. A. A. & G. T. Ferrell.
1988.
The fir engraver beetle in western states, pp. 555-57i. In A. ABerryman [ed.J, Dynamics
of forest insect populations: patterns. causes, implications.
Plenum, ~~York.
Bõmer, C. & F. A. Schilder.
1934.
Beitrãge zur Ziichtung reblaus- und mehltaufester
Reben. Mitt. BioL
Zentralanstalt (Reichsanstalt. ) Land- Forstwirtsch. 49
Breznak. J. A. 1975.
Symbiotic relationships between
termites and their intestinal microbiota. Symp. Soc.
Exp. Biol. 29: 559-580.
Bronner. R.
1977.
Contribution
à r étude histochimique des tissus nourriciers des zoocécidies. Marcellia
40: 1-34.
Campbell. B. C. 1989.
On the role of microbial ~'Inbiosis in herbivorous
insects. pp. 1-43. In E. A. Bernays[ed.J, lnsect-plant
interactions. vol. I. CRC. &x:a
Raton, FIa.
Campbell. B. C.. K. C. Jones & D. L. Dreyer.
1986.
Discriminative
behavioral responses of aphids to various plant matrix polysaccharides. EntomoL Exp. Appi
41: 17-24.
Carroll. G. 1988.
Fungal endophytes in stems and
leaves: from latent pathogen to mutuaJistic symbiont.
Ecology 69: 2-9Cheniclet. C.. C. Bernard.Dagan
& G. Pauly.
1988.
'i
~
-L--
October 1990
FERNANDES:
HyPERSE~SITIVE
REACTIONS
Terpene biosynthesis under pathoiogical conditions,
pp. 11i-130. In W J. Mattson, J. Levieux & C. Bernard-Dagan
[eds.J, Mechanisms oi woody plant defenses against insects: search .for pa\tern. SpringerVerlag, New York.
Christiansen.
E. & A. Bakke.
1988. The spruce bark
beetle of Eurasia, pp. 4i9-503. In A. A. Berryman
[ed.J, Dynamics of forest insect populations: patterns,
causes, implications.
Plenum, ~e\\. York.
Christiansen.
E. & R. Homtvedl.
1983.
Combined
Ips ICeTatoC!/stis attack on ~orwa\" spruce, and defensive mechanisms of the trees. z. ,-\nge\\" Entomol.
96.110-118.
Christiansen.
E.. R. H. ~.aring & A. A. Berryman.
1987.
Resistance of_conifers to bark beetle attack
searching for general relationshlps. For. Ecol. Manage. 22: 89-106.
Clay. K.
1988.
Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology
69: 10-16.
Coffev. M. D. & U. E. Wilson.
1983.
An structural
st~dy of the late-blight fungus Ph!ltophthoTa infestans and its interaction with the foliage of two potato
cultivars possessing different levels of general (field)
resistance. Call. J. Bot. 61: 2669-2685.
Coley. P. D. 1983.
Herbivory and defensi\"e characteristics of tree species in a lowland tropical forest.
Ecol. Mollogr. 53: 209-233
Corne11. H. v.
1983.
The seconàar\" chemistry and
complex morphology of galls fonned by the-cynipinae (Hymenopteral:
why and ho\\"? Am. ~Iidl. Nat.
110: 225-234.
COU"s. M. P. 1969a. The mechanism of pathogenicity
of SiTex noctilio on Pinus Tadiata, I. The effects of
the symbiotic fungus Am!/lostereum
sp. (Thelophoraceae). Aust. J, Biol. Sci. 22: 915-924.
1969b.
The mechanism of pathogenicity of SiTex noctilio on Pinus Tadiata. II. Effects of s. noctilio mucus. Aust. J. Biol. Sci. 22: 1153-1161.
COU"s. M. P. & J. E. Dolezal.
1966. Polyphenols and
resin in the resistance mechanism of Pinus Tadiata
attacked by the woodwasp. SiTex noctilio. and its
associated fungus. Leaf1et of the Commonwealth
Forestry and Timber Bureau 101: 10-19, Canberra, Australia.
Cruiekshank.
1. A. M. 1980.
Defenses triggered by
the invader: chemical defenses, pp. 24i-267.
In J.
Horsfall & E, B. Cowling [eds.]. Plant diseases, vol.
". Academic, New York.
Darvi1l. A. G. & P. Albersheim.
1984.
Phvtoalexins
and their elicitors: a defense against microbial infection in plants, Annu. Rev. Plant Physiol. 35: 243-275
Davidse. L. C.. M. Boekeloo & A. J. ~I. van Eggermond.
1986.
Elicitation
and suppression of necrosis in potato leaves by culture filtrate components of Ph!/tophthoTa infestans, pp. 205-206. In J. Bailey [ed.J,
Biology and molecular biology of plant-pathogen
interactions. Springer- Verlag. Berlin.
DeClerck.
R. A. & T. A. Stee.es.
1988.
Oviposition
of the gall midge, C!/stiphora sonchi (Bremi) (Diptera: Cecidomviidae)
via the stomata of perennial
sowthistle (Son:chus aTvensis L, ). Can. EntomoL 120:
189-193.
De"era11. B. J. 1977.
Defense mechanisms of plants.
Cambridge,
Cambridge.
Edmunds. G. F. & D. N. A1stad. 1981.
Response of
black pineleaf scales to host plant \"ariability, pp. 2938. In R. F. Denno & H. Dingie [eds.]. 1nsect life
L-
AGAINST
HERBIVORES
1179
history patterns: habitat anà geographic variation.
Springer, New York.
Edwards. P. J. & D. W.ratten.
1983. \\-.ound induced
defenses in plants and their consequences for patterns
of iIisect grazing. Oecologia í Berl. ) 59: 88-93.
Faeth. S. H.. S. Mopper & D. 5imberloff.
1981.
Abundances and diverslty of leai-mining
insects on
three oak host species: effects oi host-plant phenology
and nitrogen content of leaves. Oikos 37: 238-251.
Farkas. G. L. '978.
Senescence and plant disease. pp.
391-412. ln J. Horsf~
& E. B. Cowling [eds.]. Plant
diseases, vol. III; Academic. :'\e\\ York.
Feeny. P. P. 1976.
Plant apparencv and chemical
defense. Recent Adv. Ph\'tochem. 10: 1-40.
Fernandes.
G. ,,!.
1987.
Gall forming insects: their
economic importance and control. Rev. Bras. Entomol. 31: 379-398.
Fernandes. G. W. & P. "'. Price. 1988. Biogeograph-ical
gradients in galling species richness. tests of hy:potheses. Oecologia (Berl ) í6: 161-167.
In press. Comparisons of tropical and temperate galling species richness. the role oi environmental
harshness and plant nutrmonal status. ln P. w. Price et al.
[eds.], Plant-animal interactions. evolutionary e-cology
iritropical
and temperate regions. Wiley, New York.
Fernandes. G. W. & T. G. Wbitham.
1989.
Selective
fruit abscission by Jumperus manospeTma as an induced defense against predators .-\m. ~1idl. Nat. 121
389-392.
Flamm. R. O.. R. :\:. Coulson & T. L. Pavne.
1988.
The southern pine beetle, pp. 5S1-553. in A. A. Berryman [ed.]. Dynamics of forest insect populations.
patterns. causes, implications. Plenum, Ne\V York.
Flor. H. H. 1955. Host-parasite interaction in flax rust:
its genetics and other implications.
Phytopathology
45: 680-685.
1971.
Current status of the gene-for-gene
concept.
Annu. Rev. Phytopathol. 9: 275-296.
Fong. L. K. & R. K. Crowden.
1973.
Physiological
effects of mucus from the woodwasp SiTe% noctilio
F. on the foliage of Pinus Tadiata D. Don. Aust. J.
Biol. Sci. 26: 365-378.
GJ"een. M. B. & P. A. Hedin.
1986. Naturalresistance
of plants: roles of allelochemicai5. ACS Symposium
Series. American Chemical Societ)., Washington, D.C.
Green, T. R. & C. A. Rvau.
1972.
\\-.ound-induced
proteinase inhibitor in.plant lea\,es: a possible defense
mechanism against insects. Science 175: 776-777.
Greenbank.
D. 0. 1970. Climate and the ecology of
the balsam woolly aphid. Can. Entomol. 102: 546578.
Gross. P. & P. W. Price.
1988.
Plant influences on
parasitism
of two
miners: a test of enemv-free
space. Ecology
69: leaf
1506-1516.
.
Haak. R. A. & F. Slansky, Jr. 1987. Nutritional
ecology of wood-feeding
Coleoptera. Lepidoptera,
and
Hymenoptera,
pp. 449-486. ln F. Slansky, Jr. & J. G.
Rodriguez [ eds. ]. N utritional ecoicgv of insects, mites,
spiders, and related invertebrates. Wiley, New York.
Hadwiger.
L. A. & J. M. Beckman.
1980,
Chitosan
as a component of pea-Fusanum
solani interactions.
Plant Physiol. 66: 205-211.
Hadwiger. L. A.. J. M. BeckmaD & ~I. J. Adams.
1981.
Localization
of funga1 components in the pea-Fusarium interactionâetected
immunochemicallv
with
anti-chitosan
and anti-fungal cell wall antisera: Plant
Physiol. 67: 170-175.
Hain. F. P. 1988. The balsam ".oolly adelgid in North
1180
E~"VIRONMENTAL
ENTOMOLOGY
Vol. 19. no.5
America. pp. 8i-109. In A. .~ Be~"Inan [ed.]. Dynamics of forest msect populatlons patterns. causes,
implications.
Plenum. ~ew York.
Harris. M. K. & R. A. Fred~rikseD.
1984. Concepts
and methods regarding host piant re51Stan~_to arthropods and pathogens. .-\nnu. Rev. Phytopathol. 22:
247-272.
Haukioja.
E. 1982.
Inducible deienses of white birch
to a geometric defoliator. E1"mta aurumnata.
pp.
199-203. In Proceedings of the 5th lnternational
Symposium
on Insect-Plant
Relatlonships.
Pudoc,
pp. 313-319. In W J. Mattson, J. Levieux & C. Bernard-Dagan
[eds.1 MechanlSms of woody plant defenses against insects: search for pattern. SpringerVerlag, New York.
Loeben8'ein.
G. 1972.
Localization and induced resistance in virus-infected
plants. Annu. Rev. Phytopathol. 10: 1íí-206.
M8cle8n. D. J.. j. .~. S8rgent. I. C. Tommerup
& D. S.
Ingram.
1974.
Hypersensitivity
as the primary
event
in resistance
to fungal parasites. Nature 249.
186-187.
-
\\-.ageningen.
H~din. P. A.. O. H. Lindig. P. P. Sikoro_ki
& M.
W.yatt.
1978.
Suppressants of gut Dacteria in the
boll weevil from the cotton "pIãnt. J Econ. Entomol..
i1; 394-396.
Hi"is.
W. E. & T. Inou~.
1968.
The formation
of
polyphenols in trees. 1\.. The poJ~"phenols found in
Pinus radiata after SiTe% attack. Ph~1opathology 7;
13-22.
Hirata. K.
1956.
Some obsen.ations on the relation
between penetration
hypha and haustorium of the
barle~. mildew (Er!/siphe gramlnis I and the host cell.
11. On the collapse of mesoph~-lj ceils of the barley
leaves attacked by the mildew. .-\nn. Phytopathol.
Soc. Jpn. 21; 23-28.
Johal. G. S. & J. E. Rahe. 1988. Gl~"phosate, hypersensitivity and phytoalexin accumuiation in the incompatible
bean anthracnose host-parasite interaction. Phvsiol. Moi. Plant Pathol. 31; 167-281.
Jones. C. G. 1984.
~licroorganisms
as mediators of
plant resource exploitation b~. insect herbivores-. pp.
53-99. In P. W Price, C. ~. Slobodcbikoff
& W. S.
Gaud [eds.], A new ecolog~.; noveJ approaches to interactive systems. Wiley, New York.
Jon~5. C. G.. J. R. Aldrieh & M. 5. Blum.
1981a.
2-furaldehyde
from baldc~.press: a c~ical
rationale
for demise of the Georgiasilkworm
industry. J. Chem.
Ecol. 7: 89-101.
1981b.
Baldcypress allelochemics and the inhibition
of silkworm enteric microorg~niom"
some ecological
considerations. J. Chem. Ecol i: 1m-114.
Kahn. D. M. & H. V. Cornell.
1983. Earlv leaf abscission and folivores: comments and considerations.
Am. Nat. 122; 428-432.
Keanlev.
M. J. c. & T. G. Whitham.
1989.
Developm~ntal changes in resistance to berbivory:
implications for individuals and populatwns. Ecology 70.
422-434.
Király.
Z. 1980.
Defenses tnggered by the invader.
hypersensitivity,
pp. 201-225. !-:LJ Horsfall & E. B.
Cowling [eds.1 Plant diseases, ~.ol \.. .-\cademic. New
York.
Kogan. M. 1975. Plant resistance in ~
management,
pp. 103-146. In R. L. Metcalf & \,. Luckmann [eds.].
lntroduction
to insect pest manag~t.
Wiley. New
York.
Kúe. J. 1983.
Induced systemic res1stance in plants
to disease caused by fungi and bact~.
pp. 191-219.
In J. A. Bailey & B. J. Deverall [eàs.~ The dynamics
of host defense. Academic. ~e~. Ym-k.
Levin. D. A. 1973.
The role of tríchomes in plant
defense. Q. Rev. Biol. 48; 3-15.
Li~uti~r.
F. & A. A. Bernman.
1988a.
Preliminarv
histological investigatio~
of the deíense reactions o'f
three pines to CeTatoçljst\$ cla[;Íge7"a and two chemical elicitors. Can. J. For. Res. 15; l243-1247.
1988b.
Elicitation
of defensJve reactions in conifers.
M8dden. J. L. 1977.
Phvsiological reactions of Pinus
radiata to attack by wood~.asp Sirex noctilio F. (Hymenoptera: Siricidae). BulI. Entomol. Res. 67: 405426.
1988.
Sirex in Australasia. pp. 407-429. In A. A. Berryman [ed.1 Dynamics of forest insect populations:
patterns, causes. implications.
Plenum, New York-:
M8ddox. G. D. & R. B. ROOl. 1987.
Resistance to 16
diverse species of herbivorous insects within a population of goldenrod.
Solidago altissima:
generic
variation and heritabilit~.. Oecologia (Berl. ) 72: 8-14
Maltais. J. B. & J. L. Aucl8ir.
1957.
Factors in resistance of peas to the pea aphid. Ac!/rthosiphon
pisum
(Harr. ) (Homoptera:
Aphididae). I. The sugar-nitrogen ratio. Can. Entomol. 89: 365-370.
M8rtin. M. M. 1987.
lnvertebrate-microbial
interactions: ingested fungal enzymes in arthropod biology.
Cornell Universitv Press. 1thaca. N. Y.
Matta. A. 1971.
Microbial penetration and immunization of uncongenial host plants. An~~. Rev. Phytopathol. 9: 38í-410.
Matt8on. W. J.. R. K. Lawrence. R. A. Haak. D. A.
Herm8 & P-J. Charles. 1988a. Defensive strategies
of woody plants against different insect-feeding guilds
in relation to plant ecological strategies and intimacy
of-association with insects, pp. 3-38. In W. J. Mattson,
J. Levieux & C. Bemard-Dagan
[eds.1 Mechanisms
of woody plant defenses against insects: search for
pattern. Springer-Verlag.
New York.
Matt80n. W. J.. J. Leyjeux & C. Bernard-Dag8n
[eda.].
1988b.
Mechanisms of woody plant defenses against
insects: search for pattem. Springer- Verlag, New York.
Meyer, J. 1987.
Plant galls and gall inducers. Gebriicler Borntraeger, Berlin.
Miller. R. A. & A. A. Berryman.
1985.
Energetics of
conifer defense against bark beetles and associated
fungi, pp. 12-23. In L Safranyk [ed.J, The role t'f
the host in the population dynamics of forest insects.
Canadian Forest Service- Victoria, B.C.
Miller.
R. A., A. A. Berryman & C. A. Ryan.
1986.
Biotic elicitors of defense reactions in lodgepole pine.
Phytochemistry
25: 611-612.
Mile8. P. W. & z. Peng. 1989. Studies on the salivary
physiology
of plant bugs: detoxification
of phytochemicals by the salivary peroxidase of aphids. J.
Insect PhysioL 11: 865-872.
Misaghi. I. J.. 1982.
Physiology and biochemistry
of
plant-pathogen
interactions. Plenum, New York.
Morgan. D. L.. G. w. Frankie & M. J. Gaylor.
1983.
An evaluation of the gall-forming capacity of live oak
in response to the c~.nipid wasp, Disholcaspis cinerosa, in Texas. J. Kans. Entomol. Soc. 56: 100-108.
Morgan. F. D. 1968.
Bionomics of Siricidae. Annu.
Rev. Entomol. 13: 239-256.
Miiller.
K, O. 1959.
Hypersensitivity.
pp. 469-519.
In J. Horsfall & A. E. Dimond [eds.1 Plant pathology.
Academic. New York-
October
1990
FERNANDES:
HyPERSENSITI\'E
REACTIO!.;S AGAINST
~ullick.
D. B. 1975.
A new tissue essential to necrophyiact1c periderm formation
in the bark of four
conifers. Can. J. Bot. 53: 2443-2457"
Mullick. D. B. 1977.
The non-specific nature of defense m Dark and wood during wounding insect and
pathogen attack. Recent Adv. Phytochem.
2: 395441.
'lullick.
D. B. & G. D. Jensen.
1973a.
Crvofixation
reveals urnqueness of reddish-purple
seq~ent peri.:;.:rm anà equivalence between brown first and brown
sequent periderms of three conifers" Can. J. Bot. 51
135-14'3
1973b.
~ew concepts and terminology
of coniferous
periderms. necrophylactic
and exophylactic
periderms" Can. J. Bot. 51: 1459-1470.
1976.
Rates of non-suberized
impervious
tissue development after wounding
at djfferent
times of the
year m three conifer species, Can. J, Bot. 54: 881891.
Painter. R. H. 1951.
1nsect resistance in crop plants,
\Iacmillan.
~ew York,
Peng. z. & P. w. 'liles.
1988a.
Studies on the salivar}"
ph:-.sioiogy of plant bugs: function
of the catechol
oxidase of the rose aphid" J, 1nsect Physiol. 34: 10271033"
1988b. .-\cceptability of catechin and its oxidative condensatlon products to the rose aphid. f.,lacTosiphum
Tosae" Entornol" Exp. Appl" 34: 255-256,
PiIlemer. E. A. & W. M. Tinge:-'.
1976.
Hooked trichornes a physical p~lant barrier to a major agricultural pest" Science 193. 482-484,
Price. P. ~.. 1980. .Evolutionary
biology of parasites"
--Princeton
L'niversity Press. Princeton, N.J,
1984. 1nsect ecolog}.. 2nd ed. Wiley. New York.
Price. P.
G. w. Fernandes & G. L. Wariog.
1987.
Adaptive nature of insect galls. Environ.
Entomol.
16: 15-24"
Pmitcb. G. S. & D. B. Mul1ick.
1975.
Effect of water
stress on the rate of non-suberized
impervious tissue
formation following wounding
in Abies gTandis. J,
Exp. Bot. 26: 903-910.
Rda. K. f. 1988. The mountain pine beetle in westem North America, pp. 505-530. ln A. A. Berryman
[ed.J, Dynamics of forest insect populations: patterns.
causes. imphcations. Plenum. New York.
Rda. K. f. & A. A. BerrymaD.
1982.
Physiological
differences between lodgepole pines resistant and susceptibie to the rnountain pine beetle and associated
rnicroor2anisms. Environ. Entomol. 11: 486-492.
1983. phvsiological aspects of lodgepole pine wound
responses to a fungal symbiont of the mountain pine
beetle. DendToctonus pondeTosae (Coleoptera: Scolytidael" Can. Entomol. 115: 723-734.
1987.
1nteracting selective pressures in conifer-bark
beetle systems: a basis for reciprocal adaptations? Am"
Nat. 129: 234-262.
Rda. K. f.. A. A. Berryman.
J. Simasko. W. Teal &
B. L. ..-ong.
1985.
Effects of grand fir monoterpenes on the fir engraver. Scolytus ventTalis (Coleoptera: Scotylidae). and its symbiotic
fungus" Envlron. Entomol. 14: 552-556,
RamaD. A. 1987. On the cecidogenesis and nutritive
tissues of the leaf galls of GaTuga pinnata Roxburgh
(Burseraceael induced by PhacopteTon lentiginosum
Buckton (Pauropsyllinae:
Psyllidae:
Homoptera),
Phytopnaga 1: 141-159.
Rausber. 'I. D. 1978.
Search image for leaf shape in
a butterfiv. Science 200: 1071-1073.
L
HERBIVORES
1181
Rhoades. D. F.
1979.
Evolution
of plant chemical
defense against herbivores.
pp. 4-54. In G. A. R()-senthal
& D. H. Janzen [eds.], Herbivores: their interactions with secondary plant compounds. Academic, ?;ew York.
Rodriguez. J. G. 1972.
lnsect and mite nutrition: slgnificance and implications
in ecology and pest management. North-Holland,
Amsterdam, The ?\etnerlands.
Rohfritsch.O.
1981.
A ..defense" mechanism of Picea
excelsa L. against the gall former CheTmes abieti.s L,
(Homoptera, Adelgidae). Z. Angew. Entomol. 92: 1~
26.
1988.
A resistance response of Picea exceLsa to the
aphid, AdeLgis abietis (Homoptera:
Aphidoideal. pp
253-266. In W. J. Mattson, J. Levieux & C. BemardDagan [eds.], Mechanisms of woody plant defenses
agamst insects: search for pattern. Springer- Verlag,
New York.
Rohfritsch. 0. & J. D. Shorthouse.
1982. lnsect galli.
pp. 132-151. In G. Kahl & J. S. Schell [eds.], Mol~ular
biology of plant tumors. Academic, New York.
Rosenthal. G. A. & D. H. Janzen.
1979.
Herbivores
their interactions
with secondary plant metabolites
Academic, New York.
Russell. C. E. & A, A. Berrvman.
1976.
Host r~tance to the fir engraver b"eetle. I. Monoterpene composition of Abies gTandis pitch blisters and íungusinfected wounds. Can.L
Bot. 54: 14-18.
Ryan. C. A. 1984.
Defense responses of-plants. pp
3i5-386. In D. S. P. Verma & T. Hohn [eds.~ Genes
involved in microbe-plant
interactions. -Springer- Verlag, New York.
S~ee. D. C. & H. A, S. Epton.
1976.
Ultrastructural
changes in resistant and susceptible varieties of PhaseoLus vuLgaris following
artificial
inoculation with
P$eudomonas phaseoLicola. Physiol. Plant PathoL 9:
1-8.
Smith. D. A. & S. w. Banks.
1986.
Biosvnthesis, elicitation and biological activity of isoflav'onoid phytoalexins. Phytochemistry
25: 979-995.
Stakman. E. C. 1915.
Relation between Puccinla graminlS and plant highly resistant to its attack. J. .-\gric
Res. 4: 193-200.
Tbalenhorst.
W.
1972.
Zur frage der Resistenz der
Fichte gegen die Gallenlaus Sacchiphantes abieti.s
(L.). Z. Angew. Entomol. 71: 225-249.
TÍD8ey. W. M.
1981.
The environmental
control of
insects using plant resistance, pp. 175-19i. In D. Pimentel [ed.], CRC handbook of pest management in
agriculture, vol. I. CRC, Boca Raton, FIa.
Tjia. B. & D. B. Hou8ton.
1975.
Phenolic constituents
of Norway spruce resistant or susceptible to the eastern spruce gall aphid. For. Sci. 21: 180-184.
Taomi. J.. P. Niemelã. F. S. Chapin. 1lI. J. P. Bryant
& S. Sirén.
1988.
Defensive responses of trees in
relation to their carbon/nutrient
balance, pp. 57-i2.
In W. J. Mattson, J. Levieux & C. Bernard-Dagan
[eds.], Mechanisms of woody plant defenses against
insects: search for pattern. Springer-Verlag,
New York.
W8rd. H. M. 1902.
On the relations between host and
parasite in the bromes and their brown rust, Puccinia
dlSpeTsa (Erikss. ). Ann. Bot. 16: 233-315.
Wei8. A. E. & W. G. Abrahamson.
1985.
Potential
selective pressures by parasitoids on a plant-herbivore
interaction. Ecology 66: 1261-1269.
Westphal. E. 1980.
Responses of several Solanaceae
1182
ENVIRONME~IAL
to attack by a gall mite, Eriophyes cladophthiTUS Nal.
Plant Dis. 64: 406-409.
1982. Modification
du pH vacuolaire des ce11ules épidermiques foliaires de SolantJm dtJlcamaTa soumlseS
á I.action d'un acarien cécidogene. Can. J. Bot. 60
2882-2888.
Westphal. W ..R. Bronner & M. Le Rei. 1981. Changes
in leaves of susceptible and resistant Solanum dulcamaTa infested by the ga11 mite ETiophyes cladophthiTtJS (Acarina. Eriophyoidea).
Can. J. Bot. 59
875-882.
While. :'i. H. & E. P. Baker.
1954.
Host pathogen
reJations in powdery mildew of barley. I. Histolog:of tissue reactions. Phytopathology
44: 657-662.
~nile. T. C. R. 1984.
Thé abundance of invertebrate
herbivores in relation to the availabilityof
nitrogen
in stressed food plants. Oecologia (Berl. ) 63: 90-105
Wil5on. F. D. & J. A. Lee. 1971.
Genetic relationship
ENTOMOLOGY
Vol. 19. no.5
between tobacco budworm feeding res~nse and glanà
number m cottOI' seedlings. Crop Sci. 1 419-421
Wi18on. L. F. & L. M. Moore.
1986.
Preferences íor
some nursery-grown
hybrid Populus trees by the
s~tted
poplar aphid and its suppression by insecti.
cidal soaps (Homoptera:
AphididaeJ. Gr. Lakes Entomol.' 19: 21-26.
Wong. B. L. & A. A. Berryman.
1977. Host resistance
to the fir engraver beetle. 3. Lesion development and
containment
of infection by resistant Abies gTandis
inoculated with TTichospoTium sfjmbiotlCUm. Can. J
Bot. 55: 2358-2365.
Woodman.
R. L. & G. W. Fernandes.
In pre8s. Dif.
ferential mechanical defense: herbivor}.. eva~traru.
piration. and leaf-hairs. Oikos.
Received fOT publication
28 MaTch 1990.
27 OCtObeT 1989; accepted
!
ii)
I
i
~-
L-