Basic and Applied Ecology 8 (2007) 97—116 REVIEW Host plant location by Chrysomelidae Patricia Fernandez, Monika Hilker Freie Universita¨t Berlin, Angewandte Zoologie/O ¨ kologie der Tiere, Haderslebener Str. 9, 12163 Berlin, Germany Received 30 December 2005; accepted 27 May 2006 KEYWORDS Chrysomelidae; Leaf beetles; Host search; Host plant speciali- zation; Adaptive evolution; Plant volatiles; Plant damage; Phytopathogens Summary Chrysomelidae are a taxon with an enormous plethora of highly specialised herbivorous species. The present study provides an overview of the knowledge available so far on cues guiding chrysomelids to locate a host plant. Host location behaviour will be addressed from different trophic perspectives. Cues from undamaged host plants are distinguished from cues released from damaged ones. The role of host plant cues is considered with respect to the surrounding vegetation and to the presence of competitors. Only very little is known on how enemies searching for prey influence a chrysomelid’s choice for a plant. Finally, also the impact of phytopathogens on host location in Chrysomelidae is addressed. The pheno- and genotypic plasticity of chrysomelid host location behaviour might have facilitated pioneering new host plants. For a better understanding of adaptive evolution, we conclude that future studies on host plant location by chrysomelids need to address in addition to ecological and behaviourals aspects more intensively also the molecular questions of adaptation. & 2006 Gesellschaft fu ¨r O ¨ kologie. Published by Elsevier GmbH. All rights reserved. Zusammenfassung Chrysomelidae (Blattka ¨fer) bilden ein Taxon mit einer enormen Fu ¨lle an hoch spezialisierten herbivoren Arten. Diese Studie bietet eine Zusammenstellung des verfu ¨gbaren Wissens u ¨ber Signale, die Chrysomeliden zur Wirtpflanzensuche nutzen. Die Wirtsuche wird dabei auf verschiedenen trophischen Ebenen analysiert. Signale ausgehend von unbescha ¨digten Pflanzen werden unterschieden von Signalen bescha ¨digter Pflanzen. Die Rolle von pflanzlichen Signalen wird auch im Kontext der umgebenden Vegetation und der Gegenwart von Konkurrenten betrachtet. Es ist nur wenig daru ¨ber bekannt, wie die Gegenwart von Fraßfeinden die Wirtspflanzen- suche der Blattka ¨fer beeinflusst. Auch der Einfluss von Phytopathogenen auf die Wirtssuche von Chrysomeliden wird skizziert. Die große pha ¨no- und genotypische Plastizita ¨t des Wirtssuchverhaltens von Blattka ¨fern ko¨nnte das Erobern neuer Wirtspflanzenarten erleichtert haben. Die bisher vorwiegend verhaltensbiologischen und o¨kologischen Studien zeigen,dass esfu ¨r ein besseres Versta ¨ndnis der adaptiven Evolution der Chrysomelidae in Zukunft von besonderer Bedeutung sein wird, auch ARTICLE IN PRESS www.elsevier.de/baae 1439-1791/$ - see front matter & 2006 Gesellschaft fu ¨r O ¨ kologie. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.baae.2006.05.001 Corresponding author. Tel.: +49 30 8385 3918; fax: +49 30 8385 3897. E-mail address: [email protected] (M. Hilker).
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ARTICLE IN PRESS
Basic and Applied Ecology 8 (2007) 97—116
1439-1791/$ - sdoi:10.1016/j.
�CorrespondE-mail addr
www.elsevier.de/baae
REVIEW
Host plant location by Chrysomelidae
Patricia Fernandez, Monika Hilker�
Freie Universitat Berlin, Angewandte Zoologie/Okologie der Tiere, Haderslebener Str. 9, 12163 Berlin, Germany
SummaryChrysomelidae are a taxon with an enormous plethora of highly specialisedherbivorous species. The present study provides an overview of the knowledgeavailable so far on cues guiding chrysomelids to locate a host plant. Host locationbehaviour will be addressed from different trophic perspectives. Cues fromundamaged host plants are distinguished from cues released from damaged ones.The role of host plant cues is considered with respect to the surrounding vegetationand to the presence of competitors. Only very little is known on how enemiessearching for prey influence a chrysomelid’s choice for a plant. Finally, alsothe impact of phytopathogens on host location in Chrysomelidae is addressed. Thepheno- and genotypic plasticity of chrysomelid host location behaviour might havefacilitated pioneering new host plants. For a better understanding of adaptiveevolution, we conclude that future studies on host plant location by chrysomelidsneed to address in addition to ecological and behaviourals aspects more intensivelyalso the molecular questions of adaptation.& 2006 Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.
ZusammenfassungChrysomelidae (Blattkafer) bilden ein Taxon mit einer enormen Fulle an hochspezialisierten herbivoren Arten. Diese Studie bietet eine Zusammenstellung desverfugbaren Wissens uber Signale, die Chrysomeliden zur Wirtpflanzensuche nutzen.Die Wirtsuche wird dabei auf verschiedenen trophischen Ebenen analysiert. Signaleausgehend von unbeschadigten Pflanzen werden unterschieden von Signalenbeschadigter Pflanzen. Die Rolle von pflanzlichen Signalen wird auch im Kontextder umgebenden Vegetation und der Gegenwart von Konkurrenten betrachtet. Es istnur wenig daruber bekannt, wie die Gegenwart von Fraßfeinden die Wirtspflanzen-suche der Blattkafer beeinflusst. Auch der Einfluss von Phytopathogenen auf dieWirtssuche von Chrysomeliden wird skizziert. Die große phano- und genotypischePlastizitat des Wirtssuchverhaltens von Blattkafern konnte das Erobern neuerWirtspflanzenarten erleichtert haben. Die bisher vorwiegend verhaltensbiologischenund okologischen Studien zeigen, dass es fur ein besseres Verstandnis der adaptivenEvolution der Chrysomelidae in Zukunft von besonderer Bedeutung sein wird, auch
Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.
auf molekularer Ebene die Anpassung von Blattkafern an ihre Wirtspflanzen nochintensiver zu untersuchen.& 2006 Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.
Chrysomelidae form a taxon of enormous diver-sity with nearly 40,000 species, almost all of whichare phytophagous (Futuyma, 2004; Jolivet & Haw-keswood, 1995). The host plants range frombryophytes over tree ferns to gymno- and angio-sperms (Jolivet & Hawkeswood, 1995). Somespecies are specialised to feed upon roots, othersuse above-ground plant material and feed uponflowers and leaves. Many chrysomelids are feedingmono- and oligophagously on specific plant taxa,others – especially among the Eumolpinae, Crypto-cephalinae, and Clytrinae – are able to use a widerange of very different plants. Out of 139 chry-somelid genera in North America, 46.8% use onegenus of host plant, and 46.7% use between 2 and 5genera (Mitchell, 1981). However, even whenhaving specialised on a narrow range of plantspecies, no evolutionary dead end has beenentered. Instead, even highly specialised chry-somelids are able to switch to new host plantspecies, if, e.g., predation pressure on the ances-tral host plant becomes too strong (Gross, Fa-touros, & Hilker, 2004; Gross, Fatouros, Neuvonen,& Hilker, 2004; Termonia, Hsiao, Pasteels, &Milinkovitch, 2001).
The factors driving host plant specialisation ofinsects have been discussed intensively fromdifferent perspectives (e.g., Bernays & Graham,1988; Thompson, 1999). The composition of theherbivore community on host plants is influenced
by different factors, among them plant parameterssuch as plant primary and secondary metabolites,as well as by plant architecture, distribution andavailability (Ehrlich & Raven, 1964; Strong, Lawton,& Southwood, 1984). The success of a herbivorousinsect using a particular plant depends on theherbivore’s ability to locate this plant, to use itsnutrients, and to cope with its defensive devices.These abilities are dependant upon the pheno- andgenotypic plasticity of the herbivore (Bernays,2001; Chapman, 2003; Futuyma, 2000; Thompson,1996) and of the plant (Gardner & Agrawal, 2002).A particular herbivore individual feeding upon aplant is usually not feeding alone, but facesconspecific and heterospecific competitors as wellas phytopathogens altering the plant quality, andthus influencing the herbivore’s success on theplant (Denno, McClure, & Ott, 1995; Rostas, Simon,& Hilker, 2003). With respect to the third trophiclevel, predators and parasitoids may strongly affectthe use of suitable plants by herbivores (Bernays &Graham, 1988; Price et al., 1980; Vet & Dicke,1992).
Thus, ecological bottom-up and top-down factorsas well as geno- and phenotypic factors of theherbivore influence its association with a hostplant. The huge diversity of chrysomelids specia-lised on such a wide range of host plants offers anideal tool to study the mechanisms of adaptiveevolution. Unlike the Lepidoptera, which formanother important taxon of herbivorous insectsthat has been studied intensively with respect to
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host plant interactions, larvae and adults ofChrysomelidae generally use the same ecologicalniche. Like numerous herbivorous hemimetabolousinsects, also chrysomelids need to choose a hostplant suitable for egg deposition, larvae, andadults. In several species, the host plant even givesshelter for the pupal stage. When choosing a hostplant that serves for the entire development of theoffspring and nutrition of the adult stage, it mightbe beneficial to take into account the change ofhost plant quality in the course of time and season,as well as alteration of host plant quality due toprevious oviposition and feeding activity (Awmack& Leather, 2002; Hilker & Meiners, 2006).
The demands on a herbivorous insect for success-ful colonization of a suitable host plant areimmense. Refined perceptive abilities are neces-sary to locate a plant and enormous integrativeabilities to recognize the suitability of a plant.When having started feeding upon a plant, reliabledigestive abilities are necessary to gain sufficientnutrients from the plant and to detoxify possiblenoxious secondary plant components. De Jong andNielsen (2002) stated that ‘‘adaptive evolution canonly be fully understood when the genetic basis ofadaptations is unravelled’’. Even though generaladaptation such as, e.g., detoxification of planttoxins by P450-monooxygenases (Scott & Wen,2001) or glutathione-S-transferases (Ranson &Hemingway, 2005) have been studied in severalinsect species, so far little knowledge is availableon the genetics of specific adaptations of herbivor-ous insects to host plants. This is true also for thehuge taxon of Chrysomelidae. A few and highlyinteresting molecular studies are available on thedigestive adaptation of chrysomelids to plant toxins(see below), but very little is known about thegenes influencing host plant search. Several studieshave considered the questions how chrysomelidslocate their host plants, which cues stimulate themto feed upon a plant, and which factors might forcethem to leave a plant (Jermy, 1994; Matsuda, 1988;Mitchell, 1994). Many of these studies focus onspecific chrysomelid taxa or specific factors bywhich the insects orient to a host plant and‘‘decide’’ to accept it.
Our aim is (1) to outline the high diversity andplasticity of cues and factors that chrysomelidsface when searching for a host plant, and, byproviding such an overview, (2) to elucidate themost urgent future research questions we shouldaddress in this field. The review uses literature of atime period ranging from 1926, when McIndoo didfirst olfactometer experiments with the Coloradopotato leaf beetle, to 2006, when recent studies oninduction of plant defence by chrysomelid egg
deposition have been presented (Hilker & Meiners,2006). We will address questions such as, e.g.,which cues might guide a chrysomelid beetle duringhost plant search? Which factors influence itssearching behaviour? We will differentiate in thefollowing between cues and factors from non-colonised (Table 1) and already herbivore-colonisedplant individuals (Table 2) on the one hand, andphytopathogen-infected plants (Table 3) on theother hand. When encountering already colonisedplants, chrysomelids need to be able to respondselectively to the most beneficial cues among aplethora of information, i.e., herbivore-inducedplant cues, cues released by con- and heterospe-cific herbivores, cues released by predators orparasitoids. A colonised host plant might indicateon the one hand a suitable plant individual (notonly for feeding, but also for finding mates), and onthe other hand a place where intra- and inter-specific competition might lower performance. Acolonised host plant might also indicate a higherdanger of being detected by enemies, or a placewhere species interact through shared naturalenemies. In addition to herbivores and carnivorespresent on a host plant, phytopathogens are wellknown to change the attractiveness of a host plant.Thus, also the response of chrysomelids to diseasedplants will be addressed.
Cues from uncolonised host plants
The search pattern of a chrysomelid beetle for itshost plant needs to show a high flexibility and totake into account the enormous variation of: (a)the environment in which the plant is growing; (b)the geno- and phenotypic plasticity of the plantitself; and (c) also the beetle’s plasticity andmotivation. Moreover, host plant cues are usuallynot detected via a single perception ‘‘channel’’,but by visual, olfactory, and contact cues, thusrequiring highly integrative abilities of the chry-somelid. When having encountered a plant, thebeetles need to be able to efficiently digest theplant material and to cope with plant toxins. Theseaspects of host plant search and its acceptance willbe addressed below with respect to plants not yetbeing colonised by a herbivore (compare Table 1).
The plant’s environment
The preferences of Chrysomelidae for host plantswere shown to change according to abiotic con-ditions. Feeding preferences of Colorado potatoleaf beetles (CPB) for Solanum tuberosum and
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Table 1. Cues/Factors from undamaged host plants affecting host location in leaf beetles; reference: exemplifyingthe impact of the respective cue/factor (F ¼ field study; L ¼ laboratory study; studies of a ¼ adults, l ¼ larvae)
Soil texture Diabrotica spp. F; l Population density Beckler et al. (2004)Elevation F; l Population density French et al. (2004)
Vegetation diversity Leptinotarsadecemlineata
L; a Attraction (�) Thiery and Visser (1986)
Vegetation density Galeruca tanaceti F; a Oviposition (+) Meiners and Obermaier (2004)Trirhabda canadensis F; a Host colonisation (+) Morrow et al. (1989)
Plant genotype Altica spp. F, L; a Feeding Pettis et al. (2004)Chrysophthartaagricola
F, L; a Oviposition, feeding Rapley et al. (2004)
Chrysomela scripta F, L; a Feeding Lin et al. (1998)Phyllotreta spp. L; a Feeding Nielsen et al. (2001)Phratora vulgatissima L; l Development Glynn et al. (2004)
Agelastica alni F, L; a, l Feeding, oviposition Dolch and Tscharntke (2000)
Plant size Leptinotarsadecemlineata
L; a Attraction (+) Visser (1976)
L; a Attraction (+) Bolter et al. (1997)F; a Attraction (+) Hoy et al. (2000)
Altica subplicata F; a Abundance(+), feeding(+)
Bach (1993a)
F; a Colonisation (+) Bach (1993b)Cassida canaliculata F; a Oviposition (+) Heisswolf et al. (2005)
F; l Survival (+) Heisswolf et al. (2005)
Leaf age Chrysophtarta agricola F; a Feeding (+) Nahrung and Allen (2003)F, L; a Oviposition (�) Nahrung and Allen (2003)
Several willow leafbeetles
L; a Feeding (�) Ikonen (2002)
L; a Feeding (�) Miyamoto and Nakamura(2004)
F, L; a, l Feeding, oviposition King et al. (1998)Larval development
Galerucellanipponensis
F, L; a Oviposition (�) Tanaka and Nakasuji (2002)
Plant visual cues Leptinotarsadecemlineata
L; a Attraction (+) Zehnder and Speese (1987)
L; a Attraction (+) Jermy et al. (1988)L; a Attraction (+) Szentesi et al. (2002)
Phyllotreta striolata L; a Attraction (+) Yang et al. (2003)Oreina cacaliae L; a Attraction (+) Kalberer et al. (2001)
Plant volatiles Leptinotarsadecemlineata
L; a Attraction (+) Visser and Thiery (1986)(undamaged plant) L; a Attraction (+) Thiery and Visser (1995)
Agelastica alni L; a Attraction (+) Park et al. (2004)Trirhabda canadiensis L; a Attraction (+) Puttick et al. (1988)Diabroticites spp. L, F; a Attraction (+) Metcalf and Metcalf (1992)
F; a Attraction (+) Naranjo (1994)L; l Attraction (+) Hibbard and Bjostad (1988)
Leaf morphology Willow leaf beetles F; a, l Feeding Rowell-Rahier (1984a)L; a Feeding Rowell-Rahier (1984b)L; a, l Abundance Soetens et al. (1991)
Phyllotreta cruciferae L; a Feeding Palaniswamy and Bodnyark(1994)
Cerotoma trifurcata F, L; a Feeding Lam and Pedigo (2001)
Plant nutrients Diverse chrysomelids L; a, l Feeding Matsuda (1988)L; F; a Feeding (+) Hunt et al. (1994)L; a Feeding (+) Ikonen (2002)
Plant secondarychemistry
Flea beetles L; a, l Feeding Nielsen (1978, 1988)
Diabroticites L, a Feeding Metcalf et al. (1980)L; a Feeding Abe et al. (2000)
Willow leaf beetles F, a, l Feeding Rowell-Rahier (1984a)L, a Feeding Rowell-Rahier (1984b)L; a, l Abundance, oviposition Rank (1992)F; a Feeding Rank (1992)L; a Feeding Kohlemainen et al. (1995)L; a Feeding Ikonen (2002)
Ophraella communa L; a Feeding Tamura et al. (2004)
A positive or negative correlation between the plant cue/factor and the parameter studied is indicated by (+) and (�), respectively. Ifno (+) or (�) label is given, the cues/factors had varying effects.
Table 2. Cues/factors from damaged or colonised host plants affecting host location in leaf beetles; reference:exemplifying the impact of the respective cue/factor (F ¼ field study; L ¼ laboratory study; studies of a ¼ adults,l ¼ larvae)
Plant volatiles Leptinotarsa decemlineata L; a Attraction (+) Bolter et al. (1997)(induced bydamage)
L; a Attraction (+) Schutz et al. (1997)
L; a Attraction (+) Landolt et al. (1999)Oreina cacaliae L; a Attraction (+) Kalberer et al. (2001)Phyllotreta spp. F; a Attraction (+) Vincent and Stewart,
(1984)F; a Attraction (+) Pivnick et al. (1992)L; a Feeding (�) Palaniswamy and Lamb
(1993)
Plant volatiles Xanthogaleruca luteola L; a Attraction Meiners et al. (2005)(induced by eggdeposition)
Acalymma vittatum L, F; a Feeding (�)Emigration (+)
Williams and Wise (2003)
A positive or negative correlation between the plant cue/factor and the parameter studied is indicated by (+) and (�), respectively. Ifno (+) or (�) label is given, the cues/factors had varying effects.
Table 3. Phytopathogen infection of a host plant affecting host location in leaf beetles (F ¼ field study;L ¼ laboratory study; studies of a ¼ adults, l ¼ larvae)
Phytopathogentaxon
Chrysomelid taxon Field/labadult/larvae
Observed behaviour Reference
Uromyces rumici Gastrophysa viridula F, L; a Oviposition (�) Hatcher et al. (1994)Hatcher (1995)
Puccina carduorum Cassida rubiginosa L; a Oviposition (–)Feeding (–)
Kok et al. (1996)
Phoma destructiva Cassida rubiginosa L; a Oviposition (–)Feeding (–)
Kruess (2002)
L; l Development time (–),weight (–),mortality (–)
Kruess (2002)
Alternaria brassicae Phaedon cochleariae L; a Oviposition (–)feeding (–)
Rostas and Hilker (2002)
L; l Feeding (+) Rostas and Hilker (2002)
Melampsora allii-fragilis
Plagiodera versicolora L; a Oviposition (–)feeding (–)
Simon and Hilker (2005)
L; l Development time (�),weight (–),mortality (–)
Simon and Hilker (2003)
Melampsora epitea Phratora vulgatissima L; a Feeding (�) Peacock et al. (2003)
Erysiphecichoracearum
Diabroticites F; a, l Population density (�) Moran and Schultz (1998)
Cladosporiumcucumerinum
Diabroticaundecimpunctata
L; l Feeding (+) Moran (1998)
A positive or negative effect of the plant infection by a pathogen on the parameter studied is indicated by (+) and (�), respectively.
P. Fernandez, M. Hilker102
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S. dulcamara appeared to depend on the tempera-ture (Bongers, 1970). Wind speed affected move-ments of Trirhabda canadensis towards host plants.At high wind speeds, host plants located upwindwere colonised, whereas at low wind speeds, alsohost plants located not upwind were found (Mor-row, Tonkyn, & Goldburg, 1989).
The landscape structure in which a host plantgrows may significantly influence its detectabilityand, thereby, the degree of plant attack(Tscharntke & Brandl, 2004). For example, theabundance of Diabrotica virgifera virgifera and D.barberi was found to be associated with soil textureand elevation (Beckler, French, & Chandler, 2004;French, Beckler, & Chandler, 2004). Also vegetationdiversity may influence host plant finding. Diversevegetation might lower the detectability of aspecific host plant species. Specific host plantodour might be masked by volatiles from non-hostplants (Bruce, Wadhams, & Woodcock, 2005). Forexample, mixing non-host odour with host odourneutralised the usually positive response of theColorado potato beetle (CPB), Leptinotarsa decem-lineata, to host odour (Thiery & Visser, 1986).
When searching for a host plant, the patch sizeand host density can influence the herbivore0schoice (Bach, 1984; Meiners & Obermaier, 2004;Schoonhoven, Jermy, & van Loon, 1998). Thevegetation structure where the host plant growsis well known to influence the success of locating ahost plant (Bach, 1984; Hassel, 1978; Meiners &Obermaier, 2004). The polyphagous tansy leafbeetle Galeruca tanaceti, for example, preferredto lay eggs in a structurally highly complexvegetation (in terms of host density and vegetationheight and coverage), which might be a strategy tohide from an abundant egg parasitoid (Meiners &Obermaier, 2004). The goldenrod leaf beetle,Trirhabda canadensis, preferred to colonise plotswith a higher density of host plants (Morrow et al.,1989).
The plant’s plasticity
Like other herbivores, chrysomelids need to copewith the genotypic plasticity of their host plants.For several species, preferences for specific geno-types are well known, like Altica spp. preferringcertain cultivars of crape myrtles, Lagerstroemiaindica L., for feeding (Pettis, Boyd, Braman, &Pounders, 2004), or Chrysophtharta agricola pre-ferring particular strains of Eucalyptus globulus foroviposition (Rapley, Allen, & Potts, 2004). Feedingpreferences of the cottonwood leaf beetle, Chry-somela scripta, varied significantly among poplar
clones depending on the amount of a specificsurface component, alpha-tocopheryl quinone(Lin, Binder, & Hart, 1998). In contrast, Phyllotretaspp. did not discriminate between wild Arabidopsisthaliana and metabolically engineered plants con-taining four-fold more sinalbine, suggesting thatonly the presence (and not the concentration) ofthis compound stimulated feeding (Nielsen, Han-sen, Agerbick, Petersen, & Halkier, 2001). Neitherdid Phratora vulgatissima show any preference forone of the 10 genotypes generated from a crossbetween Salix viminalis and S. dasyclados, eventhough the genotypes differed significantly in foliarnitrogen concentrations and phenolic substances(Glynn, Ronnberg-Wastljung, Julkunen-Tiitto, &Weih, 2004).
The phenotype of an uncolonised host plant canalso change with the neighbourhood to colonisedplants from the same species (see review in Bruin,Dicke, & Sabelis, 1995; Dicke & Bruin, 2001; Karban& Baldwin, 1997). Volatiles induced by herbivoresin one plant may enhance the production ofvolatiles in undamaged, neighboured plants whichmay change their attractiveness to herbivores. Afield study showed that undamaged alder treeswere less attractive to the alder leaf beetleAgelastica alni when located in the neighbourhoodof alder trees damaged by this species (Dolch &Tscharntke, 2000).
The size of a plant may influence the chrysome-lid’s choice. When encountering patches of unco-lonised host plants, the largest one might be themost attractive one because it might release thehighest quantities of attractive odour or the mostconspicuous visual cues. The CPB was shown to beattracted by large (460 cm height), but not bysmall plants (o 25 cm height) (Bolter, Dicke, vanLoon, Visser, & Posthumus, 1997; Visser, 1976). Infield studies, larger potato plants also attractedmore CPB than smaller ones (Hoy, Vaughn, & East,2000). Willow flea beetles, Altica subplicata,tended to colonise and damage taller hosts (Bach,1993a, b). Furthermore, the monophagous tortoisebeetle Cassida canaliculata preferred to oviposit onlarge host plants, Salvia pratensis. These largeplants provided significantly higher nitrogen con-tent. Larvae feeding upon leaves of large plantsdeveloped significantly faster than those on leavesof small plants (Heisswolf, Obermaier, & Poethke,2005).
Intra-plant differential foliage selection by chry-somelids has been found in several studies. Nogeneral pattern of preference for, e.g., youngleaves is detectable so far. Different foliage maybe used for different purposes, a possible strategyto provide intra-plant niches for different
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developmental stages. The paropsine leaf beetleChrysophtharta agricola preferred adult eucalyptfoliage to juvenile leaves for feeding, but juvenilefoliage was preferred for oviposition (Nahrung &Allen, 2003). Some willow leaf beetles were shownto prefer feeding upon young host plant leaves withthe highest nitrogen content (Ikonen, 2002; Miya-moto & Nakamura, 2004). Likewise, female adultsof Galerucella nipponensis preferred young ormiddle-aged leaves to old leaves as ovipositionsites on its aquatic host plant Trapa japonica(Tanaka & Nakasuji, 2002). The willow leaf beetlePlagiodera versicolora preferred to oviposit in thefield on leaves near the centre of branchlets (i.e.,older leaves), whereas in the laboratory, femalespreferred young leaves to old ones (King, Crowe, &Blackmore, 1998). These results indicate that in thefield other cues such as light or danger of predationmight have influenced the choice for ovipositionsites in P. versicolora.
The beetle’s plasticity
Host plant preference of the individual herbivor-ous insect usually changes during its life time,because the selection of a plant depends on theinternal state of the individual herbivore, e.g., itsage and hormonal state, hunger, or experience(Bernays, 1995; Courtney, Chen, & Gardner, 1989;Jermy & Szentesi, 2003; Papaj & Prokopy, 1989;Schoonhoven et al., 1998; Szentesi & Jermy, 1990).Diabrotica virgifera virgifera larvae were found tobe strictly monophagous, feeding only on cornroots, while the adult beetles are polyphagous(Chyb, Eichenseer, Hollister, Mullin, & Frazier,1995). Age, sex, and dietary history affected thefeeding response to cucurbitacins in Acalymmavittatum feeding on cucumber (Smyth, Tallamy,Renwick, & Hoffmann, 2002). Orientation of adultCPB to host odour was shown to depend on thesatiation of the beetles (Thiery & Visser, 1995). InGalerucella lineola, preferences seemed to beunstable because they could be modified by foodexperience in the early adult stage (Ikonen, Sipura,Miettinen, & Tahvanainen, 2003). Experience wasfound to change feeding preference or host plantacceptance also in bruchid species (e.g., Szentesi &Jermy, 1990). Such changes in feeding preferencecan be explained as changes in the sensitivity ofdeterrent and phagostimulant receptors, as hasbeen shown for other taxa in relation to age,nutrient status, and experience (Chapman, 2003;Schoonhoven, Simmonds, & Blaney, 1991; Sim-monds, Blaney, & Schoonhoven 1992; Simmonds,Schoonhoven, & Blaney, 1991).
Perception of host plant cues
The role of visual cues for host plant location inchrysomelids has most intensively been studied inCPB. These beetles use a light compass reaction tomaintain a course when foraging. They approachhost and non-host plants by orientating to silhou-ettes (Jermy, Szentesi, & Horvath, 1988) and colour(Szentesi, Weber, & Jermy, 2002; Zehnder &Speese, 1987). But also for a few other chrysome-lids, visual cues were shown to influence orienta-tion. Sensitivity to different wavelengths may evenchange according to the time of the day, as wasshown for the flea beetle Phyllotreta striolata(Yang, Lee, & Wu, 2003). The perception of plantvisual cues may also modify the response to hostplant volatiles, as was shown by Kalberer, Turlings,and Rahier (2001): More adult Oreina cacaliae werefound to respond to host plant volatiles in a windtunnel when the beetles could see the plant insteadof only perceiving the volatiles.
Olfactory attraction to host plants has beenstudied intensively in several chrysomelid species.The first demonstration that volatile emissions byplants attract a chrysomelid species was performedby McIndoo (1926) who showed the attractivenessof volatiles emitted by potato plants to CPB adults,which was later confirmed in more detail by severalother studies (e.g., Thiery & Visser, 1995; Visser &Thiery, 1986). Since then numerous lab and fieldstudies have been conducted on the attractivenessof host plant volatiles to chrysomelids. For exam-ple, the alder leaf beetle Agelastica coeruleae wasshown to clearly distinguish between leaf odourfrom nine different Betulaceae species (Park, Lee,Shin, Kim, & Ahn, 2004). Also the goldenrod leafbeetle Trirhabda canadensismoved upwind towardshost odours in an olfactometer (Puttick, Morrow, &Lequesne, 1988). In the field these beetles movetowards the highest concentration of host plants(Morrow et al., 1989). Several adult Diabroticiteshave been shown to be attracted by volatilesreleased from blossoms of Curcurbitaceae (Metcalf& Metcalf, 1992). Diabrotica species have also beenshown to display oriented movement towards theirhost when forced to fly at a distance of 1m fromthe edge of the crop (Naranjo, 1994). Furthermore,CO2 was found to be an attractant for larvae of thewestern corn rootworm Diabrotica virgifera virgi-fera. The attraction was enhanced when cornvolatiles were added to the CO2 source (Hibbard& Bjostad, 1988).
Once on the host plant, several traits perceivedby contact such as morphological leaf character-istics and the concentration of chemical constitu-ents (both nutrients and secondary metabolites)
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are well known to affect host plant choice inChrysomelidae (Chapman, 2003; Jermy, 1994;Matsuda, 1988; Mitchell, 1994; Morris, Grevstad,& Herzig, 1996; Schoonhoven et al., 1998). Leaftrichomes, for example, were shown to influencehost selection in a wide range of chrysomelidspecies (e.g., Lam & Pedigo, 2001; Palaniswamy &Bodnaryk, 1994; Rowell-Rahier, 1984a, b; Soetens,Rowell-Rahier, & Pasteels, 1991).
The role of plant nutrients has mainly beenstudied with respect to performance of chrysome-lids, but several former studies reviewed byMatsuda (1988) also addressed the role of primaryplant metabolites such as sugars, amino acids,vitamins, and lipids as feeding stimulants. Forexample, some studies showed that preference ofChrysomelidae for specific leaves was due tonutritive traits such as nitrogen (Hunt, Liptay, &Drury, 1994; Ikonen, 2002).
Several classes of secondary plant metaboliteshave intensively been studied as feeding stimulantsfor Chrysomelidae, especially glucosinolates ofBrassicaceae in flea beetles (e.g., Nielsen, 1978,1988; Renwick, 2002), cucurbitacins of Cucurbita-ceae in Diabroticites (Abe, Matsuda, & Tamaki,2000; Metcalf, 1994; Metcalf, Metcalf, & Rhodes,1980), phenolglycosides of Salicaceae in willow leafbeetles (e.g., Ikonen, 2002; Kohlemainen, Julku-nen-Tiitto, Roininen, & Tahvanainen, 1995; Pas-teels, Braekman, Daloze, & Ottinger, 1982; Rank,1992; Rowell-Rahier, 1984a, b; Topp, Kulfan, Zach,& Nicoloni, 2002), or ragweed triterpenoid andcaffeic acid derivatives in an Ophraella species(Tamura et al., 2004).
Detoxification of noxious plant secondarycomponents
Other secondary plant metabolites, especiallypyrrolizidine alkaloids (PA) from Asteraceae andBoraginaceae, have been investigated with parti-cular respect to the physiological detoxificationmechanisms by chrysomelids. Different strategiesof PA detoxification evolved in the Chrysomelidae.Neotropical Chrysomelinae (Platyphora) take upthe toxic plant tertiary PA and shift them todefensive glands where they are stored unchanged.The efficient transport of the toxins from the gutinto the glands obviously prevents detrimentaleffects of the toxins (Hartmann, Theuring, Witte,& Pasteels, 2001; Pasteels, Theuring, Windsor, &Hartmann, 2003). Alpine Chrysomelinae (Oreina)convert toxic plant tertiary PA into non-toxicglucosides, while non-toxic plant PA-N-oxides aresequestered in the haemolymph and defensive
glands (Hartmann, Theuring, Schmidt, Rahier, &Pasteels, 1999; Rowell-Rahier, Witte, Ehmke, Hart-mann, & Pasteels, 1991). The N-oxides are trans-ferred through the gut without previous reduction,most probably by specific membrane carriers(Narberhaus et al., 2004). In contrast to Oreina,flea beetles (Longitarsus) do not conjugate tertiaryPA with glucosides, but are instead able to oxidisethese toxins, so that also in these species PA-N-oxides are accumulating in the haemolymph anddefensive glands (Dobler, Haberer, Witte, & Hart-mann, 2000; Narberhaus et al., 2004). Severalother plant toxins are known to be sequestered bychrysomelids and stored in the haemolymph ordefensive glands (Pasteels, Rowell-Rahier, Braek-man, & Daloze, 1994). However, the mechanisms oftransfer of the plant toxins through the gut intoglands of the leaf beetles have most intensivelybeen studied for PA.
Cues from colonised host plants
Both cues released by the herbivores alreadycolonizing the plant and plant cues induced byherbivore feeding or by oviposition can influencethe choice for a host plant (compare Table 2).
Cues from colonised host plants emitted bythe herbivores
Conspecifics already colonizing a plant mayrelease pheromones attracting more conspecifics.There is ample evidence for the use of pheromonesin Chrysomelidae (literature overview: Metcalf,1994; Morris et al., 1996; Muller & Hilker, 2004).One of the first chrysomelid species, in whichfemale-produced sex pheromones were detected,was the banded cucumber beetle, Diabroticabalteata (Cuthbert & Reid, 1964). Later, the femalesex pheromones of 11 further Diabrotica spp. havebeen identified (Chuman et al., 1987; Guss, Sonnet,Carney, Branson, & Tumlinson, 1984). These pher-omones are aliphatic ketones as well as propano-ates and acetates. Female sex pheromones are alsosupposed to be present in the ragwort flea beetleLongitarsus jacobaea (Zhang & McEvoy, 1994) andthe CPB (Jermy & Butt, 1991; Levinson, Levinson, &Jen, 1979).
Also several aggregation pheromones have beendetected in chrysomelids. A male-produced aggre-gation pheromone was recently identified in theCPB (Dickens, Oliver, Hollister, Davis, & Klun, 2002;Oliver, Dickens, & Glass, 2002). Males of thecereal leaf beetle Oulema melanopus produce an
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aggregation pheromone (Cosse, Bartelt, & Zilkows-ki, 2002; Rao, Cosse, Zilkowski, & Bartelt, 2003).Furthermore, the presence of an aggregationpheromone produced by males was proposed forthe flea beetle Phyllotreta cruciferae (Peng &Weiss, 1992; Peng, Bartelt, & Weiss, 1999) and forthe striped cucumber beetle Acalymma vittatum(Smyth & Hoffmann, 2003).
Several studies indicate that chrysomelids aggre-gate in response to faecal cues on the plant as hasbeen reviewed by Muller and Hilker (2004). Forexample, adults of Altica carduorum aggregated onfaeces of larvae and adults that had fed on thethistle Cirsium arvense. When other Cirsium spp.served as hosts, faeces were not attractive (Wan &Harris, 1996). This result suggests that attractiveplant compounds and/or their metabolites wereconcentrated in the gut and excreted with faeces.
However, conspecifics on a plant do not onlyrelease cues attracting further conspecifics. TheCPB oviposited less on sites with larval traces,which suggests a deterrence effect of larval faeces,but the role of other herbivore or plant semio-chemicals cannot be excluded (Szentesi, 1981).Several chrysomelid larvae also release exocrinedefensive secretions when disturbed by conspecificadults (Pasteels et al., 1982). The adults arestrongly deterred by secretion of these larvae(Hilker, 1989; Raupp, Milan, Barbosa, & Leonhardt,1986; Schindek & Hilker, 1996).
Heterospecific Chrysomelidae have also beenshown to deter each other. Larvae of the willowleaf beetle species Phratora vulgatissima and P.vitellinae mutually deterred adults of the otherspecies by their defensive secretions (Hilker, 1989;Hilker, unpublished data). Chrysomelids have alsobeen shown to deter heterospecific non-chrysome-lid insects. The willow leaf beetle Plagioderaversicolora was able to deter caterpillars ofNymphalis antiopa by its exocrine defensive secre-tion (Raupp et al., 1986). Female potato leafhoppers Empoasca fabae oviposited less on plantsthat were infested by CPB or covered by theirfaeces (Tomlin & Sears, 1992).
In several chrysomelid species, attraction ofconspecifics to an already colonised plant wasreported, but the causes are not clear. The loose-strife leaf beetle Galerucella calmariensis wasstrongly attracted by conspecifics when settlingon a plant after dispersal (Grevstad & Herzig,1997). Females of the blue willow beetle, Phratoravulgatissima, were shown to be much strongerattracted to potted willow plants with conspecificbeetles and feeding damage than to control plantswith either only damage or beetles (Peacock,Lewis, & Herrick, 2001).
Cues from colonised host plants emitted bythe damaged foliage
For a wide range of plants it has been shown thatattack by herbivorous insects induces defensiveplant responses. Especially the induction of plantvolatiles in response to herbivore feeding (Agrawal,Tuzun, & Bent, 1999; Arimura, Kost, & Boland,2005; Dicke & van Loon, 2000; Karban & Baldwin,1997) or egg deposition by herbivorous insects(Hilker & Meiners, 2002, 2006) can affect thesearch of herbivores for a host plant.
The odour released from damaged host plantsoften differs qualitatively and quantitatively fromthe one of undamaged plants (Vet & Dicke, 1992).Since herbivore-infested plants emit volatiles inmuch larger amounts than undamaged ones, it wasproposed that herbivore-infested plants are moreeasily perceived from a distance (Dicke, Sabelis,Takabayashi, Bruin, & Posthumus, 1990; Turlings,Tumlinson, & Lewis, 1990). Indeed, several chry-somelids have been shown to orient preferably tofeeding-damaged plants. For example, odour fromdamaged potato plants was more attractive to theCPB than odour from undamaged ones (Bolter etal., 1997; Landolt, Tumlinson, & Alborn, 1999;Schutz, Weissbecker, Klein, & Hummel, 1997). AlsoOreina cacaliae was preferentially attracted todamaged host plants of Petasites paradoxus andAdenostyles alliariae (Kalberer et al., 2001). In thefield, Phyllotreta cruciferae and P. striolata wereattracted by traps baited with allyl isothiocyanate,one of the compounds released especially bydamaged crucifers (Pivnick, Lamb, & Reed, 1992;Vincent & Stewart, 1984).
The herbivore’s response to induced plant vola-tiles may significantly depend on the degree ofdamage, and thus, the quantity and quality ofvolatiles released by the damaged plant. Most ofthe studies that considered different levels ofherbivore damage found that the strength ofinduced responses usually correlates positively withthe level of damage (reviewed in Karban &Baldwin, 1997). Behavioural assays in a locomotorcompensator showed that mechanical damageinflicted with scissors in potato foliage resulted inshort-term (less than 15min) attraction of CPB(Bolter et al., 1997). On the contrary, more severedamage with carborundum powder resulted in alonger lasting attraction (at least 1 h). The elm leafbeetle Xanthogaleruca luteola has been shown toadjust its behavioural response to oviposition-induced elm leaf volatiles with respect to the eggdensity. When elm twigs were carrying a small eggload, the oviposition-induced volatiles attractedelm leaf beetle females. However, when elm twigs
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were heavily laden with eggs, the volatiles induceddeterred X. luteola (Meiners, Hacker, Anderson, &Hilker, 2005). Volatiles from a plant with low eggload might indicate a suitable host plant to the elmleaf beetle females, whereas odour from a heavilyegg-laden plant might indicate a high risk of eggparasitisation. The eulophid egg parasitoid Oomy-zus gallerucae is known to be attracted by elmvolatiles induced by a high egg load (Meiners &Hilker, 2000).
Other studies show that chrysomelids are alsoable to adjust their behaviour according to herbi-vore density on the host plant. However, it is notclear from these studies whether induced plantvolatiles or other insect-derived cues mediatethese adjustments. For example, the golden rodleaf beetle Trirhabda virgata was observed to leavehost patches that had a high density of conspecificadults and heavy larval damage, but no emigrationflights were detected from low-density patcheswith little defoliation (Herzig, 1995). For larvae ofDiabrotica virgifera virgifera, it was suggested thatunder low to moderate plant infestation levels,little or no larval movement occurs after initialestablishment on a susceptible host. However,under high infestation levels, significant movementoccurred from damaged to undamaged neighbourplants (Hibbard, Higdon, Duran, Schweikert, &Ellersieck, 2004). This behaviour might protectthem from infestation by entomopathogens, sinceentomopathogenic nematodes have been shown tobe attracted to root volatiles induced by Diabroticafeeding (Rasmann et al., 2005).
The induced release of volatiles is not limited tothe site of damage, but can occur systemically,which means that undamaged leaves near damagedones also emit attractants (Dicke et al., 1990;Turlings & Tumlinson, 1992). When the water lilyNuphar luteum macrophyllum was damaged byfeeding of Galerucella nymphaeae, adult beetlesconsumed significantly more immature leaf tissue(undamaged leaves that had not yet reached thepond surface) from heavily damaged plants thanfrom the less damaged ones (Bolser & Hay, 1998).Also feeding and oviposition of the elm leaf beetleXanthogaleruca luteola induced field elm leaves(Ulmus minor) to emit volatiles systemically (Mei-ners & Hilker, 2000; Wegener, Schulz, Meiners,Hadwich, & Hilker, 2001). Beetles preferred to feedupon systemically induced leaves compared touninfested ones (Meiners et al., 2005).
The volatiles from a herbivore-infested plantrepresent a food source with competitors andelevated risk of influx of predators and parasitoids.Thus, it is difficult to predict whether herbivoreswill be attracted or repelled. Even when attracted
by induced plant volatiles, other cues encounteredwhen already arrived at the damaged plant mightinduce the insect to leave this plant. For example,even though allyl isothiocyanate was attractive toP. cruciferae, induced plants were obviouslyavoided for feeding. When exposing feeding-in-duced crucifer plants to P. cruciferae several daysafter wounding, the induced plants suffered lessfurther feeding damage than the non-inducedcontrol ones (Palaniswamy & Lamb, 1993). In thefield, the abundance of the flea beetle Epitrixhirtipennis was reduced on tomato plants that hadbeen treated with jasmonate over 3 years (Thaler,1999).
The attractiveness of herbivore-induced plantvolatiles to chrysomelids was shown to dependupon the internal state of a chrysomelid beetle (seeabove) as well as on the background of odour atwhich specific volatiles are perceived. For exam-ple, in CPB the amplitudes of electroantennogramsfor (Z)-3-hexenyl acetate, a typical green leafvolatile released from potato after damage, in-creased from the day of beetle emergence over atleast 6–8 days of adulthood (Dickens, 2000a).However, CPB was not attracted to a single greenleaf volatile (Visser & Ave, 1978). A green leafvolatile obviously needed to be perceived incontext with other plant volatiles to becomeattractive, since CPB was shown to significantlyrespond to specific blends of green leaf volatiles inbehavioural tests (Dickens, 2000b). In Cassidadenticollis, the common green leaf volatile (Z)-3-hexenol did not attract larvae, when offered singly,but the presence of this green leaf volatileenhanced the herbivore’s ability to differentiatebetween host and non-host plants (Muller & Hilker,2000).
Cues from colonised host plants emitted bythe predators
Volatiles from herbivore-induced plants are wellknown to attract enemies of the feeding stages orof the eggs (Hilker & Meiners, 2006; Hilker,Rohfritsch, & Meiners, 2002; Price et al., 1980;Vet & Dicke, 1992). Several studies are availableshowing or strongly indicating that herbivores areable to recognise the presence of enemies byinfochemicals (Dicke & Grostal, 2001). However,there is only very little evidence that chrysomelidspossess the ability to detect enemies in time.
The cucumber leaf beetle Diabrotica undecim-punctata howardi was able to detect the presenceof a spider. The mere presence of the spiderRabidosa rabida caused females D. u. howardi to
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spend less time on the host plant and to feed less(Williams, Snyder, & Wise, 2001). Adults of D. u.howardi were able to instantaneously recognisedangerous predators versus taxonomically relatedones that are no true risk. Beetles might use bothsize and shape to recognise a predator (Snyder &Wise, 2000). When present at higher densities onhost plant leaves, spiders were detected by thestriped cucumber leaf beetle, Acalymma vittatum.It was shown that this chrysomelid species mainlyrelies on tactile cues, but also visual ones to detectthe enemy (Williams & Wise, 2003). So far, it isunknown whether these chrysomelid species arealso able to respond to deposits released by aspider (silk, feces), as was shown for the scarabbeetle Popillia japonicae and the coccinellidEpilachna varivestis (Hlivko & Rypstra, 2003).
Cues from phytopathogen-infectedplants
In the last years, an increasing number of studiesis focusing on microorganisms affecting the inter-action between plants and herbivores, adding anew level of complexity to this system (for aliterature overview see Hatcher & Paul, 2001;Rostas et al., 2003). A fungal infection can changethe host plant’s suitability for herbivores and viceversa (Hatcher, 1995). Although both, beneficialand detrimental impacts can be found, moststudies demonstrated that fungal infection of thehost plant had negative or no effects on theherbivore (Rostas et al., 2003). Infection of planttissue by rust fungi is well known to affectherbivore behaviour (compare Table 3). The leafbeetle Gastrophysa viridula fed and oviposited lesson dock plants (Rumex obtusifolius) infected by therust fungus Uromyces rumicis than on healthyplants in laboratory experiments. These resultswere partly confirmed in manipulative field experi-ments (Hatcher, 1995; Hatcher, Paul, Ayres, &Whittacker, 1994). When giving the choice, adultsof Cassida rubiginosa consumed more of healthyleaves of Carduus thoemeri than of tissue infectedby the rust fungus Puccina carduorum. But thenumber of eggs laid did not differ between healthyand diseased plants. On infected leaves, feedingand oviposition were confined to pustule-free areas(Kok, Abad, & Baudoin, 1996). In cage experiments,adults of C. rubiginosa also fed and oviposited lesson leaves of Cirsium arvense if they were infectedby the necrotroph Phoma destructiva (Kruess,2002). Likewise, Chinese cabbage leaves infectedby Alternaria brassicae were avoided by females of
the mustard leaf beetle Phaedon cochleriae. Leafconsumption and oviposition were higher onhealthy leaves (Rostas & Hilker, 2002). The adultwillow leaf beetle Plagiodera versicolora avoidedfeeding and oviposition on leaves infected by therust Melampsora allii-fragilis. Leaves closely ad-jacent to the infection site were avoided whileleaves farther away from the site of damage wereaccepted as readily as healthy ones (Simon &Hilker, 2005). In the same system, larval perfor-mance was also detrimentally affected by rustinfection: increase of mortality, decrease of larvalweight and prolonging of developmental time(Simon & Hilker, 2003). Likewise, Phratora spp.avoided feeding upon rust infected willow leaves(Peacock, Hunter, Yap, & Arnold, 2003). By asses-sing the insect and fungus community structure inthe field, the density of Diabrotica undecimpunc-tata howardi, D. virgifera virgifera, and Acalymmavittatum was found to correlate negatively withthe presence of powdery mildew Erysiphe cichor-acearum on leaves of Cucurbita cepo x texana(Moran & Schultz, 1998).
Although it is less common, herbivores may alsoprefer plant tissue infected by pathogenic fungi.Diabrotica undecimpunctata removed more leafarea from cucumber leaf discs if these had beeninfected with the necrotrophic fungus Cladospor-ium cucumerinum for 3 days (Moran, 1998). Like-wise, second instar larvae of P. cochleariaeconsumed more from Chinese cabbage leavesinfected with A. brassicae than from healthy ones(Rostas & Hilker, 2002).
While the effects of plant infection by phyto-pathogens on herbivores have been addressed in aconsiderable range of studies, only little is knownabout how these interactions are mediated (Rostaset al., 2003). Changes in nitrogen contents werefound in rust-infected dock plants that are avoidedby G. viridula. But these diseased plants alsocontained higher concentrations of calcium oxalate(Hatcher, 1995; Hatcher, Paul, Ayres, & Whittaker,1995). Whether these or other cues were indeedresponsible for the reduced feeding activity onrust-infected dock plants is unclear. In Chinesecabbage infected by Alternaria brassicae, probablyan increased peroxidase activity caused avoidanceof diseased plants by the mustard leaf beetle(Rostas, Bennett, & Hilker, 2002).
Future challenges
Huge knowledge is available on factors influen-cing chrysomelid behaviour during host location.
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However, only little is known on the mechanismshow these factors affect a chrysomelid, and,moreover, how they act in concert. Further knowl-edge on this proximate level will endow us toelucidate the evolution of host specialization inChrysomelidae. Knowledge on the receptors bywhich chrysomelids perceive plant cues as well asmore information about the enzymes and transportproteins necessary for digestion and detoxificationwill show us which physiological and molecularchanges are necessary to successfully use a hostplant.
When addressing the perception of host plantcues by chrysomelids, we need to ask how specificare the receptors detecting host plant volatiles orfeeding stimulants. How finely tuned is the percep-tion of plant cues and how are all the signalsintegrated by the beetles? Electrophysiologicalrecordings of neural activity of chemosensorysensilla exposed to combinations of componentsprovide some information on the integration ofsignals on the neuron level, as, e.g., the study byHollister, Dickens, Perez, and Deahl (2001) ongaleal taste neurons in CPB showed. Even simplestructure–activity bioassays may give us first hintson the binding domains of receptors and, thus,provide us with information on receptor specificity,as did the studies by Metcalf and Lampman (1991),Chyb et al. (1995), or Kim and Mullin (1998) ontaste and olfactory receptors in Diabroticites.
Phylogenetic analyses using molecular and mor-phological data sets may shed some light on themonophyly of chrysomelids feeding on plants withspecific secondary metabolites. By such studies,Gillespie, Kjer, Duckett, and Tallamy (2003) couldshow that feeding upon cucurbitacins in Chrysome-lidae has developed convergently in several taxa.They suggest that the affinity of Old and New Worldrootworm species to cucurbitacins is due to slighttaste receptor modifications (loose receptor hy-pothesis, Tallamy, Mullin, & Frazier, 1999). Simi-larly, feeding upon pyrrolizidine alkaloid containingplants by Longitarsus flea beetles has evolvedseveral times independently (Dobler, 2001), thusagain suggesting that the evolution of the physio-logical prerequisites of feeding on these toxicplants may require only slight modifications of anancestral character. Labeyrie and Dobler (2004)could demonstrate that a very tiny change of aprotein enabled a chrysomelid to conquer a newhost plant. They showed that two Chrysochusspecies evolved the ability to feed on plants withtoxic cardenolides by substituting a single aminoacid of the binding site of the cardenolide sensitiveenzyme, thus acquiring cardenolide insensitivity.Likewise, the ability of larvae of the flea beetle
Phyllotreta nemorum to survive on certain types ofBarbarea vulgaris depends on the presence ofmajor, dominant R-genes. Some of these genesare located on the sex chromosomes (X and Y). TheB. vulgaris types studied cannot be successfullyattacked by beetles lacking the R-genes. A single Y-linked R-gene has been shown to be sufficient toconvert a flea beetle genotype incapable of livingon the B. vulgaris types into a genotype that is ableto survive on these plants (Nielsen, 1997, 1999).
When considering the adaptation of leaf beetlesto so many plant toxins, more studies are neededthat address detoxification mechanisms of leafbeetles. The ability of sequestration of plant toxinsis widespread in Chrysomelidae. The excitingstudies on the fate of plant pyrrolizidine alkaloidsin leaf beetles, as outlined above, provide deepinsight into the transport mechanisms of theseplant secondary components and their storage(e.g., Dobler & Rowell-Rahier 1994; Hartmann etal., 1999; Hartmann, Theuring, Witte, Schulz, &Pasteels, 2003; Narberhaus, Theuring, Hartmann, &Dobler, 2003; Narberhaus et al., 2004). Thestimulating studies by Termonia, Pasteels, Windsor,& Milinkovitch (2002) on sequestration abilities ofPlatyphora leaf beetles revealed that these speciesmay sequester both plant amyrins and pyrrolizidinealkaloids. They suggest that this dual sequestrationcould be a key mechanistic strategy to enable hostplant switches. Also the dual abilities of sequestra-tion of toxic plant components and of de novosynthesis of defensive devices could facilitate hostplant shifts. The elegant studies by Feld, Pasteels,and Boland (2001) and Kuhn et al. (2004) showedthat some chrysomeline larvae possess the abilityboth to transport plant glycosides to defensiveglands and to produce iridoid monoterpene denovo.
When trying to elucidate the evolution of hostplant specialisation in a chrysomelid species, amultitrophic view is needed taking into accountalso the impact of microorganisms, predators, andparasitoids in addition to plant characters. Forexample, Gross, Podsiadlowski, and Hilker (2002)and Gross, Fatouros, and Hilker (2004), Gross,Fatouros, Neuvonen et al. (2004) studied thedriving forces of a shift from Salix spp. to birch inChrysomela lapponica. Costs and benefits of feed-ing on either plant type were evaluated. Finally,the results suggest that not a better nutrition onbirch, but a specialist natural enemy present onSalix spp. might have forced this leaf beetle speciesto pioneer birch as new host plant.
A straightforward combination of molecular,physiological, (bio)chemical, and ecological studiesin the future will help to understand how
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chrysomelids evolved the ability to conquer somany different plants. As outlined here, numerousecological and behavioural studies are available.Thus, more of our future studies need to usegenomics, quantitative genetic analyses, as well asthe candidate gene approach as tools to provide adeeper insight into the ecology and evolution ofhost location behaviour in chrysomelids (Anholt &Mackay, 2004; Fitzpatrick et al., 2005; Thomas &Klaper, 2004; Via, 1990).
Acknowledgements
We would like to thank two anonymous reviewersas well as Klaus Hovemeyer, Gottingen, for theirvery useful and valuable comments on an earlierversion of this manuscript. Many thanks are alsodue to all members of our lab in Berlin, especiallyto Roland Schroeder, who helped to collect theliterature. P.F. was supported by the FundacionAntorchas, Argentina.
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