Antixenosis: The Effect of Plant Resistance on Insect Behavior

Abstract	

Insect damages to food and fiber crops cost farmers and consumers millions of dollars each year.  Many 
insect control strategies have been employed during this current century.  The use of resistant varieties is 
one of the most effective tools for reducing insect damage.  There are three  well known  mechanisms of 
plant defense to insect damage: Antixenosis, Antibiosis and Tolerance.  The Antixenosis describes the 
inability of a plant to serve as a  host to insect herbivore. It has a particularity of modifying insect behavior 
once in contact with the plant host, without effect on  metabolism of both plant and insect.   There are 
several modes of resistance used by plant to deter insects.  These  modes were categorized as chemical and  
morphological plant defenses.  In here, the review  article will discuss these two defense pathways but 
with  a special emphasis on morphological plant surface characteristic associated to plant resistance.  As 
examples of theses characteristics, plants present special epidermal characters (glandular trichomes,  
hairs...),  layers of surface waxes which prevent insects from feeding on them.  Resistance to oviposition  
may come from  plant characteristics that either fail to provide appropriate oviposition-inducing stimuli or 
to provide oviposition-inhibiting stimuli.  The review article will be enriched by a series of plant responses 
to insect dietetics.  The defense role of glandular trichome of certain number of plants against herbivorous 
insects has recently become an area of intense research at applied and academic levels.  Plant characteristics 
have been recognized for years as important resistance factors. The chemical inhibition of feeding can be 
through plant emition of allelochemicals such as repellents, deterrents or inhibitors. Each type of chemical 
defense engages the plant to different mechanisms to disturb  insect behavior.  The last part of this article 
will include a thought on the place  of this type of resistance in recent plant protection  movement.

	Introduction

Plant and insects have a long time coexisted relationship.  Harmful insects were suppressed by either other 
insects or toxic or by plant defense mechanisms, to create a balance between the insect pest population and 
host, and to avoid  serious crop losses. One of the modern way of reducing insect damage is to implement 
a popular known concept as integrated pest management IPM.  This approach uses a combination of host 
plant resistance, cultural, biological and chemical control methods.  Among all, host plant resistance is one 
of the most effective tools for reducing insect damage.

Each plant species has a unique set or collection of defense traits ranging from morphological to 
phytochemical parameters that have behavioral and physiological ramification for a potential herbivore 
consumer.  Insects that feed on plant known as phytophagous insects should be capable to locate the most 
suitable nutritional substrates in plant.  These behavioral patterns of insects can be affected by antixenotic 
mechanisms which involving physical and biochemical factors of respective host plants.

Antixenosis is host plant mechanism which  include morphological, physical or structural qualities that 
interfere with insect behavioral such as mating, oviposition feeding and feeding ingestion.  As a resistance 
mechanism, Antixenosis act as structure barriers which affect the insect behavior in selecting their hosts.  
The first plant organs contacted during the preliminary stages of host accept are surface hairs or trichomes.

Trichomes:

Trichomes are epidermal appendages of diverse forms and structures, such as non glandular hairs, scales, 
or pelts hairs.  Trichomes affect the insect behavior by providing a barrier that prevents small arthropods 
from landing on the plant surface and prevent movement and feeding (Goertzen and Small, 1993).  These 
trichomes limit the access of hopper feeding stylet to plant tissues and interfere with hopper attachment to 
plant.  Trichome-based Antixenosis exists in many cultivars such as  cotton cultivars that are resistant to 
the sweetpotato whitefly, Bemisia tabaci and leafhopper of the genus Empoasca (Butler et al. 1991).   
Yencho and Tingey (1994)  provided an evidence of the effect of the trichomes of the wild Bolivian potato 
on the feeding behavior of Colorado potato beetle  leptinotarsa decemlineata.  However, this was not the 
first evidence from the wild potato to herbivorous.  In 1986 Lapointe and Tingey, observed similar feeding 
behavior of the green peach aphid, Myzus persica on the wild potato, Solanum neocardenasii.  Moreover, 
there are several of examples of the effects of trichomes on some insects and are presented in Table 1. 
Tingey and Laubengayer (1986) showed that removing the pubescence resulted in increase of feeding by 
the potato leaf hopper.  Likewise, leaf pubescence also contributes to the feeding Antixenosis of some 
cultivars of soybean to the cabbage looper, Trichoplusia (Khan et. al., 1986)

The densities of trichomes on the buds and leave surface of some cultivars also deter feeding and some 
times oviposition.  Kamel (1965) determined that cotton cultivars with increased trichomes density on 
lower leaf surface, were more resistant to cotton leaf worm, Spodoptera littoralis.  Density of Gossypium 
spp. Cotton trichomes affects both leaf hopper and  whitefly preference in feeding. Butler et al. (1991)  
found that leaf hopper population declined while whiteflies population increased as the number of 
trichomes increased.  However, when the trichomes densities are 70 / 13.7 mm2 of leaf surface both 
whitefly and leafhopper population declined (Butler et al., 1991).  The pubescent cotton promotes 
population growth of the cotton fleahopper, Pseudatomoscelis seriatus and tobacco budworm, Heliotis 
virescens (Lukefahr et al., 1971).  

Table 1.  Insects affected by resistant crop plant cultivars possessing leaf and stem trichomes.
_________________________________________________________________________________
Crop			Trichome
Plant			Type			Insect Affected		Reference
________________________________________________________________________________
Alfalfa 		Simple 		Potato leafhopper		Shade et al. 1979
Glandular		Alfalfa weevil			Danielson et al. 1987
Alfalfa seed chalcid		Brewer et al. 1983
Spotted alfalfa aphid		Ferguson et al. 1982
Pea aphid			Shade and Kitch 1983
Alfalfa blotch leaf miner	MacLean and Byers 1983

Cotton			Simple		Empoasca Fasciaatus	Reed 1974
Boll weevil			Wessling 1958
Cotton leafworm		Kamel 1965
Tarnished plant bug		MeredithandScuster 1979
Lygus hesperus		Benedict et al. 1983
Whitefly and leafhopper	Butler et al. 1991
Cowpea		Simple		Legume pod borer		Oghiakhe et al. 1992

Poinsettia		Simple		Whitefly			Bilderback and Mattson 1977
						
Potato			Simple		Potao leafhopper		Taylor 1956
Glandular		Green peach aphid		Lapointeand Tingey 1986
Glandular		Colorado Potato beetle	Graig and Tingey 1994

Sorghum		Simple		Sorghum shoot fly		Maiti and Gibson 1983

Soybean		Simple		Agromyzid bean flies		Chiang and Norris 1983
Cabbage looper		Khan et al. 1986
Potao leafhopper 		Lee 1983
Strawberry		Simple		Black vine weevil		Doss et al. 1987

Sugarcane		Simple		Scirpophaga nivella		Verma and Mathur 1950

Sunflower		Glandular		Sunflower moth		Rogers et al. 1987

Wheat			Simple		Bird cherry oat aphid		Roberts and Foster 1983
Cereal leaf beetle		Hoxoe et al. 1975
Hessian fly			Roberts et al. 1979
Maize 			Simple		Stem borer			Kumar 1992
_________________________________________________________________________________
*All the references before 1987 were adapted from Smith (1987).


Ohiakhe et al., (1992), found that trichomes length of  resistant Cowpea varieties had an effect on larval 
feeding sites.  Negative and significant correlation between pod trichome density and pod damage showed 
that trichomes density and length contributes to a reduction in Maruca  testulalis damage to Cowpea pods.  
This result suggested that trichome length in varieties is playing an important role.  The long, dense 
trichomes found on the leaves of the Composite plant Anaphalis mangaritacea impart resistance to mesdow 
spittlebug, Philaenus spumarius L. (Hoffman and Mcevoy 1985).  Also Doss et al., (1987), showed that 
the resistance of strawberry clones to feeding and oviposition by black vine weevil, Oliorhynchus 
sulcotus, is somehow related to the density and length of trichomes on the underside of leaves.  

Oviposition behavior could be affected by the trichomes too.  Adult files lay fewer eggs, addition, egg 
hatch also larval mobility is impaired.  Some pubescent wheat cultivars also have antixinotic effects on the 
bird cherry oat aphid, Rhopalosiphum podi (Roberts and Foster 1983).  Oviposition of Bemisia 
argentifolii is  affected by acylsugars which reduced number of eggs and therefore in lower population 
density (Liedl et al. 1995).  Maize "Antigua" variety with reduced trichomes density and delayed seeding 
development of pubsence are found by Wiseman et al., (1976) less preferred for oviposition by ballroom 
larvae and possess resistance to feeding.  Oviposition by cereal leaf beetle Oulema  melanoplus is 
prevented by dense growth of long erected trichomes (Hoxie et al. 1975).

Surface Waxes:

Plant leaves are protected against desiccation, insect predation and disease by a layer  surface waxes over 
the epicuticle.  Epicuticular waxes affect the feeding behavior of insects, particularly the settling of probing 
insects, acting as phagostimulants or feeding deterrents.  There has been a number of reports about insect  
respond to chemicals on the leaf surface as obtained from experiments using surface extracts of leaves or 
pure chemicals that are known to occur on leaf surfaces.  Sanford et al., (1991), reported that behavior of 
neonate diamondback moth larvae on resistant cabbage leaves was  affected by leaf waxes.  As a 
conclusion, leaf waxes chemistry and their physical attributes act together with some plant characteristics,  
to affect  neonate diamondback behavior on cabbage plants.  They showed that the larvae spent 
significantly more time walking, walked more frequently, and  walked significantly faster on leaves of 
glossy resistance cabbage  (NY 8329) than on the susceptible (Round up).  Consequently, the average 
speed and walking speed were both significantly greater on the glossy cabbage leaves than on normal 
leaves (Sanford et al., 1991). 

Alkanes are amongst the commonest constituents of all plant waxes.  Specific alkane C32H66 common in 
the wax of Vicia faba caused the insect to probe for longer periods into parafilm sachets whereas the alkane 
fraction of nonhost deterred feeding (Kingauf et al, 1978).

Wax may physically prevent the movement of an insect across a leaf surface.  Stork (1980) reported that 
Mustard beetle stick fast to Brassica oleracea cultivars that don't have heavy wax bloom than to those with 
a bloom. In "bloom" cultivars, the culm is heavily waxed and the neonate larvae experience considerable 
difficulty in climbing, their prolegs get stuck in the wax and the larvae never reach the feeding site 
(Bernays et al. 1983).

Leaf surface chemicals undoubtedly affect insect behavior.  Insect possesses the sensory apparatus to 
detect these chemicals by contact or olfaction.  There are primary and secondary plant compounds, both 
can be detectable by the insect at the plant waxes (Panda and Khush 1995).  Chapman and Bernays (1989)  
suggested that the nature of the surface wax may be "recognized" by insect as indicative of internal 
constituents of a plant.  Therefore, studies are needed to understand the effect of plant-waxes chemistry on 
insect behavior.

Biochemical Factors:

Several chemical constituents of plants serve as olfactory and gustatory stimuli for insect.  These chemicals 
may be nutrients (i.e. sugars, amino acids, phospholipid etc) or non-nutritive constituents ( i.e. 
glycosides, alkaloids, terpenoids etc).

The insect may be repelled by plant volatile compounds without coming in contact with plant or having 
made contact, feeding may be suppressed, or having bitten the leaf, the insect may deterred from further 
feeding.  Chemicals inhibiting feeding behavior at these narrow points are called repellents, suppressants 
and deterrents respectively.  Other workers use antifeeding and feeding deterrents synonymously 
(Schoonhoven 1982).

Repellents:

Repellents are  plant defense compounds that prevent or reduce contact between the insect and the 
substrate.  The formation of the behavioral reaction when testing repellents is affected by opposite 
tendencies.  On the one hand, there is the feeding reaction of the unfed insect motivated by the internal 
condition of the organism.  At this moment the appropriate centers of the central nervous system are 
activated, the sensory "input" of the insect is "open" and the sensitivity of the receptors more acute-the 
organism is set up to search and take food.  On the other hand, there is the defensive motivation, arising 
under the action of the repellent on the olfactory and contact receptors, which heightens self-persevation in 
the insect and is expressed as flight.  The final behavioral reaction of the insect depends on the relationship 
between these two opposing motivations-those of feeding and defense.   A number of insects have been 
reported to be affected by the plant volatile that are specific to their host plant (Visser 1986).  Watson and 
Baron (1995) observed an avoidance behavior response shown by Faceby Loge saw-toothed grain beetle 
Oryzaephilus surinawensis, while exposed to repellent of reapeseed.  Bark beetle expressed an aggregation 
behavior in response to the host odors which is more important.  Specifically, Verbenone that is 
synthesized from the pine trees was also found to  reduce, the colonization of the insect (Kohnle et al., 
1992).  Gritsay (1991) tested the effects of repellents on the behavior of the bloodsucking mosquitoes by 
using olfactometer test method. When he expressed a repellence to the mosquito the reaction was flight 
against wind, escape when aroused, positive phototaxis.   Moreover, insect expressed another behavior 
against repellents such as fly with higher humidity or sometimes they increase the number of bites per 
unite of time.  But, laboratory simulated condition are not optimal for understanding insect behavior to 
repellents, this was a final conclusion of Gritsay (1991).

Cells of glandular trichomes secrete and accumulate a large variety of terpene oils and other essential oils 
that generally act as insect repellents in plants.  Peterson et al.  1994 reported that a bout fourteen volatile 
compounds,  were identified in leaf trichomes of yellow squash.  These compounds were tested and 
identified to effect as repellents of female of pickleworm moth Diaphania  nitidalis. 

There results showed that the compounds extracted from trichomes lead  to reduction in significant 
oviposition of female. Recently  Liedl et al., (1995), they isolate acylsugars from the trichomes of 
resistance wild tomato that cause reduction in the settling of the adult silverleaf whiteflies.  The exudate 
from the glandular trichomes of Solanum berthaultii  contain volatile substances including sesquiterpenes.  
These volatile repel the aphid Myzus persica and thus fewer aphids seedle on feeding areas (Ave et al., 
1987).

Deterrents:

Insect pests deterrence by allelochemicals exists across abroad taxonomic range of plants.  Alleleochemical 
compounds available  most frequently to cause deterrence are alkaloids favonoids, terpene, lactones and 
phenols (Smith, 1989).  Tingle and Mitchell, (1991) found that female Heliothis virescens moths 
responded by positive anemotaxis to volatile from extracts of two host plants susceptible (cotton and 
tobacco), but they didn't fly to an extract from elderberry, a nonhost that contain an oviposition deterrent 
for H. Virescens. Moreover, in the lab work the moth doesn't showed any positive response to the mixed 
volatile extracted from cotton and elderberry compared to the response of cotton deterrent alone (Tingle 
and Mitchel 1991).

Insect feeding deterrents also occur in several forage crops.  Larvae of grassgrub, Costeelytra zealandica, 
are deterred from feeding by the isoflavone vestitol from  Lotus pedunculatas (Russell et al. 1978).  
Renwick and Huang (1995), showed that nasturtium, Tropaeolum majus contains strong feeding 
deterrents to cabbage-reared Pieris rapae larval and one of the deterrents has been identified as chlorogenic 
acid (Huang and Renwick 1995).  Larvae transferred from a cabbage plant refused to feed on nasturtium. 
Larvae reared on nasturtium were much less sensitive than cabbage-reared larvae to the deterrents isolated 
from nasturtium (Huang and Renewick 1995).  An aglucone in the foliage of maize, 2, 4-dihydroxy-7-
methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA), is one of the most widely studied plant 
allelochemicals affecting insect resistance.  When normal, healthy maize foliage is mechanically damaged, 
the glucoside 2-O-glucosyl-4-hydroxy-1, 4-benzoxazin-3-one is enzymatically converted to DIMBOA 
(Wahlroos and Virtanen 1959).  DIBOA work as deference for feeding by European corn borer (Renwick 
and Huang, 1996).

Terpene lactones deter the feeding of several insects.  The sesquiterpene lactone 8, B- 
sarracinoyloxycumam branolide, from the insect resistant sunflower, Helianthus maxmiliani, deter feeding 
by southern armyworm, Spodoptera eridania, the migratory grasshopper, Melanoplus sanguinipes and the 
sunflower moth (Gershenzon et al., 1985).  Insect-resistant species of rhododendron alon contain high 
levels of the sesquiterpene lactone germacrone, which deters feeding by the obscure root weevil, 
Sciopithes obscurus (Doss et al. 1980).

Plant tannins have been considered as insect growth inhibitors for several years, owing to their presumed 
action in binding with proteins to form insoluble digestion-inhibiting complexes (Smith 1989).  Martin et 
al., (1987), however indicated that there is little evidence to suggest that tannins inhibit insect digestion.  
The observed effects of tannins appear more likely to be due to their actions as feeding deterrents. The 
favonoid chrysanthemin from cotton cultivars with red floral pigmentation also deters feeding of tobacco 
budworm larvae (Hedin et al. 1983).

In conclusion, it is obvious that insects have been only one selectional force affecting the changes that 
plant have  undergone throughout evolutionary time.  The plant's physical and chemical changes that have 
occurred in response to insect herbivore and the behavioral and metabolic changes that insects have 
undergone in order to adapt to new host plants underscore the genetic plasticity of each of the participating 
organisms.  Finally, plant repellents and deference can be used as insecticides against some of the harmful 
pests.

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