Relationships Between Insect Pests and Weeds: an Evolutionary Perspective Author(S): John L

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Relationships between Insect Pests and Weeds: An Evolutionary Perspective Author(s): John L. Capinera Source: Weed Science, Vol. 53, No. 6 (Nov. - Dec., 2005), pp. 892-901 Published by: Weed Science Society of America and Allen Press Stable URL: http://www.jstor.org/stable/4046991 . Accessed: 10/02/2014 12:46

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This content downloaded from 128.227.138.29 on Mon, 10 Feb 2014 12:46:22 PM All use subject to JSTOR Terms and Conditions WeedScience, 53:892-901. 2005

Symposium Relationships between insect pests and weeds: an evolutionary perspective

John L. Capinera Weeds are an important plant resource for insects, although feeding by insects on Corresponding author. Entomology and Nematology weeds can have both positive and negative effects on crop productivity. Weeds also Department, P.O. Box 110620, University of indirectly affect crops via their influence on beneficial insects, and by harboringplant Florida, Gainesville, FL 3261 1; [email protected] and insect diseases. Weeds may affect the ability of dispersing insects to locate crop plants. The host relationship between insects and plants is highly variable, ranging from very specialized to generalized feeding behaviors. Despite the myriad interactions of weeds and insects, many aspects of the relationship are predictable. Most insects, including crop pests, are specialists, and preadapted to feed only on some plants, often within a single plant family. Even polyphagous insects often have a distinct preference hierarchy, feeding more widely only when preferred hosts are unavailable. Use of plants by insects is a dynamic interaction, with characteristicsof the insect (e.g., mandible structure) and the plant (e.g., allelochemicals) affecting feeding behavior. Thus, weeds that are closely related to crops are particularlyimportant in harboring insects that attack those crops. Crop production practices should seek to sever the taxonomic association between the crop and the weeds found within the crop, and nearby, by eliminating weeds related to the crop. This will make it less likely that insects will move easily from weed to crop plants, that damaging population densities of insects will develop in the field, and that insect vectors that harbor plant diseases will be harbored in the field. Particularlyimportant integrated pest management practices include crop rotation, reduced use of chemical herbicides, and management of weeds in noncultivated areas.

Key words: Allelochemicals, crop management, insect feeding behavior, insect mandible structure, preadaptation to hosts, plant disease transmission, weed hosts, weed management.

The earliest insects were not plant feeders, but insect di- the world. The importance and nature of crop-feeding (in- versity expanded greatly as angiosperms became diverse and cluding forest-feeding) insects are well documented, and it abundant in the Cretaceous period (about 100 million years is generally acknowledged that our horticultural practices ago) (Zherikhin 2002). Plants were, and remain, an abun- (e.g., inadvertent removal of plant defenses during the crop dant resource for the insect groups that have overcome the breeding process, monocultural practices, and other ill-ad- various evolutionary barriers (both physical impediments vised cropping decisions) have exacerbated insect-related such as a tough epidermis, and biochemical challenges such problems in crops (Herzog and Funderburk 1986; Smith as toxins) presented by plants. It often is surprising for non- and McSorley 2000). Less well understood is the relation- entomologists to learn that most insects have not adopted ship of insects to weeds. An important relationship between green plants as a food resource; only about one-third of the weeds and insects clearly exists-after all, crops were bred orders of insects and about 45% of insect species feed on from natural flora. Indeed, the review by Norris and Kogan living plants (Strong et al. 1984). The fact that there is so (2000) comprehensively summarizes the agricultural litera- much green vegetation is sometimes taken as evidence that ture on insect-weed relationships. No attempt will be made to plants are normally well protected from insect herbivory. repeat this recent review; instead, I will discuss an aspect not previously covered in detail: the evolutionary aspects of However, plants often are less adequate nutritionally than insect-weed relationships, and suggest how knowledge of are more protein-rich food sources such as dead animals or this relationship can impinge on strategies and tactics of even microbe-infested in plant material, so addition to the integrated pest management. aforementioned physical and biochemical hurdles, insects must deal with low nutrient content if they adopt plants as a food substrate. Weeds Are a Food Resource for Insects Nevertheless, many insects have evolved a strong associ- Weeds are a primary resource for many phytophagous ation with plants. These usually are herbivores (though some insects. From the perspective of crop protection, this has display beneficial relationships with plants, principally by both positive and negative aspects. In a positive sense, insect serving as pollinators). From the perspective of crop pro- feeding on weeds makes water, soil nutrients, and sunlight duction, insects can be quite destructive, particularlyin crop more available to crop plants, thereby reducing weed com- monocultures, where they damage many crops throughout petition with crops. Many insects feed exclusively, or nearly

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This content downloaded from 128.227.138.29 on Mon, 10 Feb 2014 12:46:22 PM All use subject to JSTOR Terms and Conditions FIGURE 1. The army cutworm-weed-wheat relationship exemplifies some of the complexities in integrated management of crop pests. The cutworm larva (upper left) is nocturnal and not usually observed unless an effort is made to sample them, so farmers are often unaware of infestations early in the larval cycle. By digging away the upper soil (upper right) during the day, large numbers of cutworms may sometimes be found. Examination of the field at night (bottom left) reveals the cutworms climbing upon, and feeding on, a preferredweed host, tansy mustard. Examination of the wheat field during the daylight hours (bottom right) shows only the basal portion of the stems of tansy mustard between rows of wheat. Up to this point in time, there is no damage to the wheat. As the weeds are consumed by the insects, or if the farmer applies an herbicide to kill the weeds, the insects are forced to feed on the wheat. so, on weeds. For example, the sesiid moth Carmenta hae- of insect inoculum for the crop field (Capinera 2001; Met- matica (Ureta) attacks only snakeweeds, Guteirrezia and calf and Metcalf 1993). Grindeliaspp., in the family Asteraceae (Cordo et al. 1995). The example of the army cutworm, Euxoa auxiliaris Other insects prefer weeds, but may damage crops readily (Grote), will serve to demonstrate some of the complexities in the absence of attractive weeds. For example, the Colo- of the insect-weed-crop plant interaction. Army cutworm is rado potato beetle (Leptinotarsadecemlineata Say) prefers to a common lepidopteran pest in the western Great Plains oviposit on hairy nightshade (Solanum sarrachoidesSendt- region of North America in which wheat (Triticum aestivum ner) rather than on potato (Solanum tuberosumL.), and eggs L.) is grown. The larval stage of this insect (Figure 1) feeds are less abundant on potato in the presence of nightshade aboveground at night, and spends the daylight hours hiding (Horton and Capinera 1990). This preference for weeds also in the soil, so its feeding behavior is poorly documented. has been exploited effectively through the introduction of Although it is known predominantly as a pest of small selective herbivores for the biological suppression of adven- grains, it feeds on a large number of plants, including many tive (invader) weeds, sometimes with spectacular success weeds in preference to grain crops. In Figure 1, the feeding (Goeden and Andres 1999; Myers and Bazely 2003). This behavior of the army cutworm can be seen in a photograph process, which strives to reunite a natural predator (in this taken at night; note that they are clustered on pinnate tansy special case, an herbivorous insect) with its prey (in this case, mustard [Descurainia pinnata (Walt) Britt.]. Also, the effect a weedy plant), is called classical biological control, or in- of army cutworm feeding on this weed is clearly evident a troduction biological control. few days later; in an adjacent photograph, the foliage is There are negative aspects associated with insect feeding completely consumed and only the base of the plant re- on weeds, too, if the insect is not restricted in its feeding mains. Note that the wheat plants on both sides of the habits to the weed. When insects have a wide host range weeds are free of cutworms and cutworm feeding. Indeed, (oligophagous to polyphagous) they sometime move from up to this point the army cutworms are beneficial insects, weeds to crop plants, causing crop damage. Commonly, this serving to reduce competition by the weeds with the young follows weed destruction due to tillage or herbicides, but it wheat by killing or severely inhibiting the growth of the also may be a more natural process, following weed senes- tansy mustard plants. However, if the tansy mustard plants cence or consumption of the weed by the insects. Thus, a (or other weeds) are completely consumed before the larvae common recommendation in many crop production systems reach maturity, the cutworms are forced to feed on the is to keep weed populations at a low level, not only within wheat. Thereafter, they are no longer beneficial organisms, the crop field, but also in adjacent areas such as irrigation but pests. ditches and fence rows, as these sites are a common source It is tempting to conclude that the presence of weeds may

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This content downloaded from 128.227.138.29 on Mon, 10 Feb 2014 12:46:22 PM All use subject to JSTOR Terms and Conditions be beneficialto wheat culture because it lures cutworms mostly on vision. In other words, chemicalsplay a more from the wheat. However,the weeds use soil moisture,a importantrole in the evolution of specific host-herbivore limiting resourcein drylandwheat culture, and so wheat relationsthan does vision.When resourcesare concentrated, farmersapply herbicides to eliminatethe weeds. If they ap- as in agriculturalmonocultures, presumably insects can ply herbicidesbefore the cutwormsare mature, they deprive readilyfind their host plant due to the concentratedhost- the larvaeof food, forcingthem onto the wheat.An enlight- producedodors. On the other hand, in polyculturalsystems ened approach,therefore, is to delay herbicideapplication or in weedy fields (particularlyweeds that are unrelatedto until afterthe larvaeare mature, reducing or eliminatingthe the crop plant), the chemicalstimuli may be less concen- herbivoryof wheat. This necessitatesan extensivesoil sam- tratedor confusingto the potentialherbivores. Another hy- pling effort,however, because the cutwormsare not easyto pothesisis that weeds or other noncropplants may release detect during the daylight hours. Another approachis to repellentchemicals that deterinsects from alightingor feed- apply insecticideat the same time as the herbicide,and al- ing (Stanton1983). though this also requiressome samplingto be surethat the Finchand Collier(2000) proposedthat host-locationbe- cutwormsare presentin potentiallydamaging numbers, it havior resultingfrom visual and chemicalorientation was is considerablymore economical than having the wheat modifiedby the retentiontime and behaviorof insectsin a damaged,or applyinginsecticide as a separateapplication at crop. They postulatedthat insects may not oviposit upon a later date. firstencountering a suitablehost, insteadinvestigating nearby vegetation.If continuouslystimulated by the appropriate stimuli (as would occur in a crop monoculture)the insect Weeds Affect Host-Finding by Herbivores would ovipositand begin an infestation.On the otherhand, if an Weedscan modifythe attractivenessof cropsto the insect unacceptablehost was encounteredduring the inves- herbivore,thereby affecting the rate of colonization.Both tigatoryphase (this is more likely in a polycultureor weed- vision and odor play an importantrole in host locationby infestedcrop), or chemicalstimuli were inadequate(as in a most insects(Stanton 1983). In the caseof vision-basedhost polycultureor weed-infestedcrop), the insect would be more finding, it is the spectralprofile (nonvisibleto humans as likelyto move on, therebyreducing the likelihoodthat a be well as visible) to which the insect responds.In their land- crop would infested.Despite the well-documentedim- mark work with aphids, J. S. Kennedy and collaborators portanceof chemicalsfor host finding among many specialist the postulatedthat during the dispersalphase, insects herbivores, exact mechanismof populationsup- (aphids, pression for example)were attractedto short-wavelengthultraviolet associatedwith mixed populationsof plantsis un- certainor variable light, and this tendedto takeinsects upward toward the sky. (Herzogand Funderburk1986). How- After a period of flight, they were no longer attractedto ever, many studies have documentedthat mixed plantings are less ultravioletlight, instead preferring affected by specialistherbivores (Smith and Mc- long-wavelength(often so heat emanatingfrom the soil or plants) light (Kennedyet Sorley2000), weedsmay contribute to reductionin insect to al. 1961). Vegetation(weeds vs. baresoil, or weeds damage crops by interferingwith host location in some plus crop manner. plants vs. crops plus bare soil) could influencethe spectral reflectancepattern of a site, therebyaffecting the propensity of flying insects to alight. Weeds can also modify the at- Weeds Affect Beneficial Insects tractivenessof crops to insects by affectingthe hue (color) of the foliage;as firstdemonstrated conclusively by V. Moer- Weedscan directlyaffect the abundanceof beneficialin- icke (Kennedy1976), manyherbivorous insects are attracted sects, includingpredators, parasitoids, and pollinators(Al- to yellow or yellowishgreen duringthe host-seekingphase, Doghairi and Cranshaw2004; Alteiri 1988; Showlerand relativeto dark green or other colors (Kostal and Finch Greenberg2003). Some predatorsand parasitoidsalso feed 1996; Moericke1969). Thus, light greenweeds interspersed on weeds. For example,many predatoryinsects with pierc- amongdarker green crops could be relativelymore attractive ing-suckingmouthparts are facultativepredators, feeding to alightinginsects. Conversely,rows of crops interspersed preferentiallyon other insectsbut imbibingplant sap when with bare soil have sometimesbeen shown to be more at- necessaryto sustain their existence.Predators, and parasit- tractiveto flying insectsthan dense standsof vegetation,so oids duringthe adult stage,often feed on nectarfrom flow- weeds in crop fields may also deter alighting.Crop produc- ers or from extrafloralnectaries. Thus, the presenceof cer- ers sometimesmanipulate alighting behavior by mulching tain weeds (thosewith accessiblenectar from flowersor ex- the crop with silverplastic mulch to increasethe amountof trafloralnectaries) enhances the survivalof beneficialinsects ultravioletlight being reflected,effectively disorienting fly- and assistsin biologicalsuppression of pests (Russell1989; ing insects and reducingthe rate of alightingby airborne Southwood1986). insects (Rhaindset al. 2001; Stapletonand Summers2002; Weeds also can indirectlyaffect the abundanceof bene- Stavinskyet al. 2002; Summersand Stapleton2002). ficial insects. Predators,and to a lesserdegree parasitoids, Weeds also affect chemical-basedhost finding.Many in- may have severalinsect host species.The presenceof phy- sects do not depend on vision, or they use vision only to tophagous insects on weeds may support populationsof identify an appropriatehabitat and then use odor to identify beneficialinsects; elevated populations of generalistbenefi- a suitable host. Some argue that the host-location process is cial insects will spill over onto crops and help suppresspests. the other way around, but most agree that both vision and In some cropping situations, weeds or other noncrop plants odor are important (Judd and Borden 1992a, 1992b). In (called refugia or banker plants) are deliberately planted to many cases, insects using odor for host location tend to be foster development of beneficial insects that will affect pest more selective in their feeding habits than insects depending populations on cropplants.

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This content downloaded from 128.227.138.29 on Mon, 10 Feb 2014 12:46:22 PM All use subject to JSTOR Terms and Conditions In addition to the benefitsof weeds on naturalenemies 2000 for a more complete discussion). Although there are of pest insects,weeds affectthe activitiesof pollinators.Pol- situations in which certain weeds are beneficial, overall, the linatorscollect nectarand pollen, and often are not abun- presence of weeds in crops is detrimental to insect manage- dant in the absenceof weeds. Thus, cropsthat requirepol- ment. Thus, we need be concerned not only with the direct lination (e.g., many fruit crops and cucurbits)may benefit effects of weeds on crops (e.g., competition for light, water, from the presenceof a diversityof weeds (Backmanand and nutrients) but also with the effects of weeds on insects, Tiainen 2002). On the other hand, if weeds are too attrac- including herbivores (by providing harborage and food for tive, they may inhibit crop pollinationby attractingthe pol- the insects), pollinators (by competing with the crop for linatorsaway from the crop. pollinators), and plant diseases vectored by insects (by serving as a reservoir for plant diseases). Some considerations Weeds Are a Source of Diseases associated with weed-insect management issues include the following: Weeds can serve as a source of diseases,including both diseasesof insects and of crop plants. The importanceof * Weeds that harbor plant diseases are a special concern, and weeds as refugiafor entomopathogenicdiseases may be mi- should be eliminated, or controlled at the earliest possible nor, or relativelyunstudied, but it certainlyexists. For ex- stage before potential insect vectors infest them. ample, weedy areasaround crop fields are often the over- * Weed control must be carefully timed if the weeds are winteringsite for grasshoppers(as eggs in the soil), which infested with insects that can infest crops, so that they are initially feed (weeds may be the only source of food early not driven onto the crop plants. in the growingseason) and roost there (preferringthe taller * Conservation and minimum-tillage fields sometimes have weeds for thermoregulationand possiblyfor nutrition).In higher weed densities, which can lead to unusual problems the case of summit diseaseof grasshoppers,caused by the with insects and insect-transmitted diseases. fungusEntomophaga grylli, such weeds are sometimes heavily * Weeds and crop residue in out-of-production fields can be populated by dying grasshoppersthat cling to elevated a major source of insects and the plant diseases they trans- percheseven afterdeath (Carrutherset al. 1997). The high mit, so crop placement (location), and area-wide manage- grasshopperdensities at such sites serve as foci of disease ment of the insects, become more important to consider infection, and foster the spreadof the insect pathogenin as options in management of insects and insect-transmit- the insect population. ted diseases. The beneficialeffects of weeds on insect pathogensis far * Weeds are a special problem for area-wide insect manage- overshadowed,however, by the negativeeffects of weedson ment programs if they host insects, because the number disease;in this case, plant disease.Crop plants,particularly of insects that must be managed is higher, and the area annualcrops, start their life fairlydisease-free. Weeds, how- that must be treated is greatly expanded. ever, often harbordiseases that can be transferredto crop plants by insects feeding first on weeds, and then on the Predictability of the Weed-insect Relationship crop (Chellemiet al. 1994). Plant diseasescaused by viruses and mollicutes,and to a lesserdegree by fungi and bacteria, The weed-insect relationship is complex, and may appear are commonly transmittedby insects from weeds. Aphids, to be unpredictable. However, there are insightful elements whiteflies, leafhoppers,and thrips are the most common of the herbivore-plant relationship, particularly the evolu- vectorsof plant diseasebecause they have piercing-sucking tion of insect feeding, that are useful for prediction. mouthparts,and in some casessecrete the diseasepropagules Insects are more selective in their feeding behavior than as they feed (Hunter 2004). However,many other insects is commonly believed. Even polyphagous insects have strong are implicatedin diseasetransmission, and piercing-sucking and consistent feeding preferences. Part of the problem is insects are not particularlyeffective in the transmissionof due to an inability by many people to accurately identify fungi and bacteria.The diseasesmay be introducedinto a some insects, and so they do not distinguish among species crop by only a few insects, followed by rapid secondary within groups of related insects (e.g., flea beetles, grasshop- transmissionwithin the crop. It is difficult to preventthe pers, white grubs) even though individual species within inoculationof a disease,though secondarytransmission can these groups may have greatly varying host preferences.This be reducedthrough effective insect suppression(usually by leads to the perception that the host range is much broader using insecticides).Because in most cases it is not possible than is actually the case. Another important issue is that to preventsome disease-bearinginsects from alightingand host lists are extremely deceptive. Most insects, on occasion, feeding on a crop, and it is usually not possible to cure develop very high populations, over-run their food supply, plants once they have become infectedwith plant disease, and are forced to feed on nonpreferred or unacceptable insect-transmitteddisease is a formidableproblem. Elimi- plants. During these periods of population outbreak, insects nation of the sourceof the diseaseand vectorsis often the are observed on plants that are not normally eaten, but in most effective approachto management,and this often the entomological literature these become recorded as hosts, meansweed control (Agrios1997, 2004). adding to the perception that these rarely eaten crops are at risk when they probably are not. Effective Weed Management Can Be Key to What makes insects selective in their feeding habits? In- sects are often constrained Insect Management in Crops in their feeding behavior by mouthpart morphology and chemical preferences, and feed I have tried to summarize, from an entomological per- on plants within certain families. For example, grasshopper spective, some of the benefits and costs of having weeds and cutworm larval mandibles, and likely those of most oth- present in, and adjacent tO, crops (see Norris and Kogan er insects, are often adapted tO optimize feeding on certain

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This content downloaded from 128.227.138.29 on Mon, 10 Feb 2014 12:46:22 PM All use subject to JSTOR Terms and Conditions a. b

c.d

FIGuRE 2. The mandibular structure of grasshoppersand other insects reveals adaptations that allow some degree of host-choice predictability.Forb-feeding grasshoppers, such as the grasshopper Schistocercaceratiola, have mandibles with short and pointed incisor teeth, and with the molar teeth irregularand well developed: (a) right incisor region, (b) left incisor region, (c) right molar region, (d) left molar region. types of plants (Gangwere 1966; Isley 1944; Kang et al. examination of the mandibles will allow some predictive 1999; Patterson 1984). ability relative to their tendency to damage crops. Even bet- In the case of grasshopper mandibles, there are two im- ter, of course, would be species-level identification of the portant regions: the distal incisor region and the proximal insects, but this is not always possible. molar region. These regions slice and crush the excised leaf Preferencesbased on plant chemistry similarly are not ful- material, respectively. In the case of grasshoppers that feed ly appreciated by plant protection specialists. Many insects, on forbs (broad-leaf plants, with netlike veins), the incisor but particularly those more selective in their feeding habits, teeth are short and pointed, and the molar teeth are irregular are influenced by allelochemicals, also known as secondary and well developed. In distinct contrast, grasshoppers that plant compounds or secondary metabolites (Hanson 1983; feed on graminoids (narrow leaf blades, with parallel veins) Harborne 1982). Plants synthesize a variety of allelochemi- have long but blunt incisor teeth, and a molar region with cal compounds of differing chemical structure (terpenoids, ridges and furrows rather than teeth. These are adapted for flavonoids, alkaloids) that affect selection and suitability of slicing through, and feeding parallel to, the tough parallel the plant by the insect. Although most of these chemicals veins of graminoids (primarily grasses). Mixed-feeding spe- can be classified as toxins, they need not be truly toxic, but cies (feeding on both forbs and graminoids) have interme- only distasteful (distasteful compounds are often classified diate arrangement of the mandibular structures. Thus, ex- as repellents or deterrents), to deter herbivory. From an evo- amination of the mandibles (Figures 2 and 3) can provide lutionary perspective, it is not even essential that a plant be considerable information on the feeding behavior of these distasteful; lack of adequate nutrition and the inability of insects. Grasshoppers and cutworm larvae are not readily an insect to survive and reproduce (e.g., due to the presence identifiable by many plant protection specialists, and these of tannins) can be adequate over time. insects tend not to be identified to the species level (for Of interest, a compound that is toxic or repellent to one which specific feeding habits are known), so the damage species of insect can be an attractant to another species. potential of the insects is commonly uncertain. Yet, simple This is due to the coevolutionary process that sometimes

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This content downloaded from 128.227.138.29 on Mon, 10 Feb 2014 12:46:22 PM All use subject to JSTOR Terms and Conditions co d FicGuRE3. Grasshoppers that feed on graminoids, such as the grasshopper Amblytropidiamysteca, have long but blunt incisor teeth, with a molar region consisting of ridges and furrows rather than teeth: (a) right incisor region, (b) left incisor region, (c) right molar region, (d) left molar region. occurs between insects and plants. Insects that can over- of plants, although there are other examples in which an come a particular chemical barrier (usually by possessing insect feeds more selectively (e.g., the silkworm moth, Bom- the ability to detoxify the chemical) produced by a plant byx mori (L.), on white mulberry, Morus a/ba (L.); or the have an important competitive advantage in feeding, as rosemary grasshopper, Schistocercaceratiola, on Florida rose- they are able to feed on the plant with impunity. Thus, it mary, Ceratiola ericoidesMichx.) or more broadly (e.g, Jap- is useful to be able to detect that chemical barrier (which anese beetle, Popilliajaponica Newman, with about 400 spe- is not really a barrier to feeding for insects possessing the cies from many plant families recorded as hosts; or green proper detoxification mechanism, but a very effective bar- peach aphid, Myzus persicae (Sulzer), which feeds on plants rier for those lacking the detoxification mechanism). This from 40 plant families). results in an important pattern of selective feeding because the smell or taste of a plant that is repellent to most her- Using Knowledge of the Weed-Crop-Insect bivores is a signal to others that this is a good food re- Relationship to Increase Effectiveness of Insect source. Soon, in a coevolutionary sense, insects that are attracted to a plant's smell or taste may feed only on those Management plants with the particular chemical which was (and remains Despite the tendency of some insects (generalists) to feed for some insects) a barrier to feeding (Futuyma 1983; Ko- broadly on host plants from several families, many show gan 1986). distinct preference for certain plant families. Bernays and Many chemical compounds found in plants are common Graham (1988), for example, estimated that less than 10% to a group of plants, often most, or all of, the members of of phytophagous insects feed on plants in more than three a plant family. Some examples of insect herbivores, and the different plant families. Thus, taxonomic similarity between plants on which they feed, are shown in Table 1. These were the weed and crop plant becomes an important element in selected to show that these insects feed on a single family predicting damage to crops by weed-feeding insects. Insects

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This content downloaded from 128.227.138.29 on Mon, 10 Feb 2014 12:46:22 PM All use subject to JSTOR Terms and Conditions TABLE 1. Some important specialist vegetable-feeding insects, the principal plant family on which they feed, and the biochemicals char- acteristic of the plant families on which they feed.a Insect Plantfamilyb Chemical(s) Onion maggot, Delia antiqua (Meigen) Alliaceae Organosulfur compounds Spinach flea beetle, Disonychaxanthomelas (Dalman) Chenopodiaceae1 Phytoecdysteroids Striped flea beetle, Phyllotretastriolata (Fabricius) Beet leafminer, Pegomyabetae Curtis Sugarbeet root maggot, Tetanopsmyopaeformis (Roder) Sugarbeet root aphid (summer host), Pemphigusbetae Doane Hawaiian beet webworm, Spoladea recurvalis(Fabricius) Lettuce aphid (summer host), Nasonovia ribisnigri(Mosley) Compositae2 Sesquiterpene lactones, flavo- Lettuce root aphid, Pemphigusbursarius (Linnaeus) noids, phenolic acids Artichoke plume moth, Platyptilia carduidactyla(Riley) Sweetpotato flea beetle, Chaetocnemaconfinis Crotch Convolvulaceae Tropane alkaloids Sweetpotato leaf beetle, Typophorusnigritis (Crotch) Golden tortoise beetle, Charidotellabicolor (Fabricius) Sweetpotato weevil, Cylasformicarius (Fabricius) West Indian sweetpotato weevil, Euscepespostfasciatus (Fairmaire) Sweetpotato sawfly, Sterictiphoracellularis (Say) Morningglory leafminer, Bedellia somnulentella(Zeller) Sweetpotato vine borer, Omphisaanastomasalis (Guenee) Sweetpotato hornworm, Agrius cingulatus(Fabricius) Cabbage leafminer, Liriomyza brassicae(Riley) Cruciferae3 Glucosinolates, cysteine sulfox- Cabbage aphid, Brevicorynebrassicae (Linnaeus) ide, volatile isothiocyanates, Cabbage maggot, Delia radicum (Linnaeus) and thiosulfinates Radish root maggot, Delia planipalpis (Stein) Turnip root maggot, Deliafloralis (Fallen) Turnip aphid, Lipaphis erysimi (Kaltenbach) Imported cabbageworm, Pieris rapae (Linnaeus) Mustard white, Pieris napi (Linnaeus) Southern cabbageworm, Pontia protodice (Boisduval and LeConte) Cabbage webworm, Hellula rogatalis(Hulst) Cross-striped cabbageworm, Evergestisrimosalis (Guenee) Diamondback moth, Plutella xylostella(Linnaeus) Purplebacked cabbageworm, Evergestispallidata (Hufnagel) Yellowmarginedleaf beetle, Microthecaochroloma Stal Cabbage curculio, Ceutorhynchusrapae Gyllenhall Pickleworm, Diaphania nitidalis Stoll Cucurbitaceae Cucurbitacins Melonworm, Diaphania hyalinata Linnaeus Squash beetle, Epilachna borealis(Fabricius) Squash bug, Anasa tristis (De Geer) Squash vine borer, Melittia cucurbitae(Harris) Corn blotch leafminer, Agromyzaparvicornis Loew Graminae4 Hydroxamic acids Northern corn rootworm (larva), Diabrotica barberiSmith and Lawrence Western corn rootworm (larva), Diabrotica virgiferaLeConte Southern corn billbug, Sphenophorusmaidis Chittenden Corn leaf aphid, Rhopalosiphummaidis Fitch Corn leafhopper, Dalbulus maidis (DeLong and Wolcott) Corn delphacid, Peregrinusmaidis (Ashmead) Armyworm, Pseudaletiaunipuncta (Haworth) Striped grass looper, Mocis latipes (Guenee) Southern cornstalk borer, Diatraea crambidoides(Grote) Southwestern corn borer, Diatraea grandiosellaDyar Sugarcane borer, Diatraea saccharalis(Fabricius) Grass thrips, Anaphothripsobscurus (Miiller) Bean leaf beetle, Ceratomatrifircata (Forster) Leguminosae5 Isoflavonoids, flavonoids, and Mexican bean beetle, Epilachna varivestrisMulsant alkaloids Pea leaf weevil, Sitona lineatus (Linnaeus) Pea aphid, Acyrthosiphonkondoi Shinji Bean leafroller, Urbanusproteus (Linnaeus) Green cloverworm, Hypena scabra (Fabricius) Limabean pod borer, Etiella zinzchenalla(Treitschke) Pea moth, Cydia nigricana (Fabricius)

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This content downloaded from 128.227.138.29 on Mon, 10 Feb 2014 12:46:22 PM All use subject to JSTOR Terms and Conditions TABLE 1. Continued. Insect Plantfamilyb Chemical(s) Colorado potato beetle, Leptinotarsadecemlineata (Say) Solanaceae Alkaloids Tobacco flea beetle, Epitrix hirtipennis (Melsheimer) Tuber flea beetle, Epitrix tuberisGentner Pepper weevil Tomato hornworm, Manduca quinquemaculata(Haworth) Tobacco hornworm, Manduca sexta (Linnaeus) Potato flea beetle, Epitrix cucumeris(Harris) Eggplant tortoise beetle, Gratianapallidula Boheman Potato stalk borer, Trichobaristrinotata (Say) Pepper maggot, Zonosemataelecta (Say) Eggplant lace bug, Gargaphiasolani Heidemann Eggplant leafminer, Tildenia inconspicuella(Murtfeldt) Potato psyllid, Paratrioza cockerelli(Sulc) Potato tuberworm, Phthorimaeaoperculella (Zeller) Tomato pinworm, Keiferia lycopersicella(Walsingham) Carrot weevil, Listronotusoregonensis (LeConte) Umbelliferae6 Furanocoumarins,polyacety- Carrot rust fly, Psila rosae (Fabricius) lenes, and diterpenes Parsnip leafminer, Euleia fratria (Loew) Parsnip webworm, Depressariapastinicella (Duponchel) Carrot root aphid, Dysaphisfoeniculus(Theobald) Willow-carrot aphid, Cavariellaaegopodii Scopoli Black swallowtail, Papilio polyxenesFabricius a Host datafrom Capinera(2001). b Also knownas 1 Amaranthaceae,2 Asteraceae, 3 Brassicaceae,4 Poaceae, 5 Fabaceae,6 Apiaceae. with a narrow host range (specialists) are likely to be pre- when excellent chemical weed suppression is attainable, adapted to accept crops in the same family as the weeds on helping to eliminate those related weeds. Another useful ap- which they feed (Capinera 2002). Various cropping practices proach is to use alternativesto chemical weed control, prin- can cause shifts in weed composition within crop fields (Bar- cipally tillage, or perhaps cover crops. Although chemical beri and Mazzoncini 2001; Tworkoski et al. 2000). Also, weed suppression may be more economical in the short run, herbicides can display taxonomic discrimination, favoring it may be logical to use selected tillage or other practices to survival of weed populations that are related to the crop interfere with development of insect problems or to disrupt plant. Therefore, continuous cropping of the same crop in the weed seed reservoir,leading to long-term economic ad- the same field and repeated application of the same herbi- vantages. In some cases, herbicides are selective, so use of cides can lead to shifts in weed populations, including shifts such products may provide benefits to both insect and weed to weeds that are taxonomically related to the crop. For management, and may be a good choice even if it comes at example, use of 2,4-D for control of broadleaf weeds in- a premium price. Finally, the vagility of insects must be creases frequency of grass weeds in corn (Zea mays L.) and considered. Insects more commonly invade crop fields from wheat. Increase in grass weed incidence sets the stage for nearby areas than emerge from within crop fields (Figure 4). insects that are attracted to these weeds to also feed on the There are some insects that overwinter in the soil within crops. Nearby areas, including irrigation ditches, fencerows, crop fields, of course, but most insect pests are crop field and fallow fields are likely similarly infested with these tax- invaders, overwintering in wooded or waste areas,sometimes onomically related weeds due to the abundance of weed seed including suburban areas (ornamental plants and trees can and herbicide drift. be an important source of certain overwintering insects) or It is imperative that the taxonomic link between the abandoned crop fields (destruction of crop residue is vital weeds and crop plants be broken if insect management is for management of some insects). to be optimized. This is especially important for selective Agriculturalists are faced with many decisions, and some insects; those with a narrow host range. So how can we choices have far-reachingeffects that extend well beyond the disrupt this taxonomic link? There are several possibilities, proximate issue. Weed management is one of those; the de- including the following: cisions sometimes influence insect pests as well. Although the relationships are sometimes complex, and decisions dif- * Crop rotation; ficult to make, they are most successful if based on knowl- * Use herbicides more selectively, or implement herbicide/ edge of weed-insect relationships, particularlythe relatedness tillage/cover crop practices that eliminate reservoirweeds; of weeds and crops, and the feeding behavior of insects. * Seek out important weeds and selectively eliminate them from noncultivated areas. Crop rotation can help to reduce the herbicide-based se- Acknowledgments lection for weeds that are related to the crop. Although the I thank Susan Webb for helpful comments, and Heather Mc- weed seed reservoir can persist for many years, and weeds Auslane for information in the biochemistry of plants as well as related to the crop may emerge annually, there will be years review of the manuscript. Trevor Smith provided the mandible

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