source: https://doi.org/10.7892/boris.22560 | downloaded: 25.9.2021 eddfrhrdvlpeto rtcl o prere- for protocols of achieved development urgently the further However, be needed 1999). agents Coombs ineffective would and of (McEvoy release the risk eliminating through environmental min- to contribution biolog- imizing signiÞcant introduced A of agents. efÞciency control attention the ical less to 2003), paid been al. has et (Louda with control associated species biological native to In risk competing support 2003). the on Callaway to debate the and the Pearson intended on 1999, were al. impact et they (Callaway negative species plant a 1996, native to Fitter lead can which and 2003), even al. et Louda (Williamson 1998, GrifÞths and target release Julien their on after effects weak weeds only have biological on agents introduced impact control many negative However, a vigor. have hostÕs they its that biological is on agents demand control main a species speciÞcity, host plant 1999). Besides Coombs invasive and McEvoy 1998, alien GrifÞths and (Julien controlling prevalent of increasingly an practice is enemies, natural exotic introduction of the weeds, of control biological Classical eesug Russia. Petersburg, Switzerland. Bern, A HATTENDORF, JAN 3 2 1 ebvr matVru otSz rfrne nohgu Endophagous Preference: Size Host Versus Impact Herbivore olgclIsiue usa cdm fSine 904St. 199034 Science, of Academy Russian Institute, Zoological 3012 [email protected]. e-mail: 6, author, Baltzerstrasse Corresponding Bern, of University Institute, Zoological matassmn,hs iepreference size host assessment, cycle. impact life weedÕs WORDS the KEY in stages control. earlier biological on successful guarantee focus other not should with probably will comparison research here A Further studied guilds preference. feeding size the mature host to belonging assign or that to damage possible indicated not feeding was either it studies development, to larval was clearly long but their relationship root-feeding of plants, of this because small Occurrence but period. or plants, study big weak the either with within associated for damage preference serious caused strong them a of exhibited none species observed Most species. rmz heracleana gromyza sdisc xlsr prah eetmtdpatvgrbfr n fe ebvr takunder attack herbivore after and before species size vigor the host by plant dominated and were estimated herbivores impact Endophagous we commonly conditions. the the natural approach, of Instead examined exclosure range. native We insect weedÕs the America. used in North guilds insect and endophagous different Europe of preference into out. introduced carry to weed difÞcult noxious often reason are One environment targets. natural their the on mantegazzianum in impact studies negative impact weak prerelease a that only is exhibit agents control biological introduced ABSTRACT atsfausti Nastus on ete,and Reitter, lsia ilgclcnrli rciet oto le naiewes u many but weeds, invasive alien control to practice a is control biological Classical ealu mantegazzianum Heracleum ealu mantegazzianum Heracleum ome n eir(paee,wihi aiet h acss saperennial a is Caucasus, the to native is which (Apiaceae), Levier and Sommier ,2 1, lbn(itr:Armzde,ada ndnie otbrn goyi ßy agromyzid root-boring unidentiÞed an and Agromyzidae), (Diptera: Zlobin TE .HANSEN, O. STEEN tohnhstatarchani Otiorhynchus nio.Etml 54:11Ð00(2006) 1013Ð1020 35(4): Entomol. Environ. .mantegazzianum H. B IOLOGICAL 1 lsia ilgclcnrl naiewe,prerelease weed, invasive control, biological classical , 0046-225X/06/1013Ð1020$04.00/0 EGYY.REZNIK, YA. SERGEY C ete Clotr:Cruinde,teßy the ), (Coleoptera: Reitter ONTROL tde s xlsr xeiet ihÞl ae or cages Þeld with experiments exclosure use studies 1987). (Forsberg attacked be to likely plants more smaller where are examples et also are Inbar there 1991, 2001), Even (Price al. size pos- plant plants. be usually with correlated vigorous is can itively preference for oviposition impact preference female or negative though a small a by preferring However, masked or host plants. could the weak herbivore damaging the com- be plants, performance either noninfested decreased with a at- pared host example, show for between plants If, distinguish tacked impact. to herbivore problem and is her- a selectivity studies and damage, 2003) impact sublethal Story with causes and usually Smith al. preference 2003, bivory size et al. host Fujiyama et a 2001, (Briese have al. herbivores Some et 2003). Ballabeni 1989, 1980, plant al. Karban et distribution, (Price predation plant or competition, temporal structure, or nutrient spatial as such quality, factors are ecological but several in ovipositioning, selective and con- feeding among for even plants hosts speciÞc their choose to randomly difÞcult not is insects do herbivorous range Many 1985). native (Wapshere weedÕs out carry the discussion in species under sect still is 2003). al. et evaluation (Louda impact lease lnsaeqietlrn ohrioy Insects herbivory. to tolerant quite are plants ocutrc hspolm h aoiyo impact of majority the problem, this counteract To in- phytophagous of assessment impact Prerelease ÐW EEDS nIsNtv Range Native Its in 3 ᭧ AND 06EtmlgclSceyo America of Society Entomological 2006 OFAGNENTWIG WOLFGANG iu iridis Lixus Heracleum Melana- Olivier, 1 1014 ENVIRONMENTAL ENTOMOLOGY Vol. 35, no. 4 insecticides to compare the performance of plants Materials and Methods exposed to herbivores with those protected from them Study Areas and Sampling. During the 2002 (Maron and Vila 2001). An essential assumption in growing season, Þve Þeld surveys to 14 different exclosure experiments using insecticides is that the H. mantegazzianum populations were conducted in treatment has no direct effect on plant growth. How- the Russian Caucasus (approximately monthly from ever, many studies have shown diverse physiological mid-May until early October). Many of the locations and ecological changes including phytotoxic or plant were visited several times. The altitude ranged from growth promoting effects, increased nutritive value, Ϸ500 to 2,000 m above sea level. changes in attractiveness for herbivores or parasitoids, Based on our experience in the previous season, direct and indirect effects on predators and parasi- we organized two Þeld surveys in 2003 to the Russian toids, and the activation of detoxiÞcation pathways in Caucasus (20Ð27 June and 18Ð31 July). According to herbivores for a broad range of insecticides (Hardin Otte and Franke (1998), the initial seed production of et al. 1995, Straw et al. 1996, Haile et al. 2000). Ma- H. mantegazzianum takes place only 6 wk after the nipulation of insect densities with Þeld cages is a com- beginning of the regenerative development. Our ob- mon method, but it becomes more complicated with servational time covered a large part of this period. On increasing plant size. In addition, cages may protect each trip, we visited the same two H. mantegazzianum potential biological control agents against natural en- populations, one located in the Arhyz nature pre- emies. Therefore, the efÞciency of biological control serve (43Њ39Ј18Љ N, 41Њ24Ј59Љ E, 1,710 m a.s.l.) and candidates could be overestimated, because predation the other on a long-abandoned Þeld near the village and parasitism were repeatedly reported to inhibit the Pregradnaja (43Њ54Ј27Љ N, 41Њ17Ј02Љ E, 920 m a.s.l.). establishment of biological control agents in their new Each population was comprised of several hundred environment (Goeden and Louda 1976). We chose a adult individuals. Different altitudes and the resultant different approach in this study, adapted to charac- difference in climatic conditions, especially the shift in teristics of giant hogweed, Heracleum mantegazzianum the beginning of the vegetation period, is the primary Sommier and Levier (Apiaceae). distinction between the two localities. In the follow- Giant hogweed is a monocarpic perennial plant ing, we will refer to these as the upper and lower (Tiley et al. 1996), which can reach a height of up to locations. 4 m. The plant is native to the alpine and subalpine During our Þrst trip, we established two transects at belt of the Western Caucasus, from where it was in- each location. Along each transect, we tagged 24 troduced to Europe as an ornamental plant in the plants in the rosette stage and measured the length of early 19th century (Ochsmann 1996). Since its intro- each leaf. Flower shoots had just begun to grow, so duction, giant hogweed has been spreading with in- stem-feeders apparently did not attack before this creasing rapidity (Pysek 1991), and thus has become measurement. At the second visit, we additionally an important weed in central and northern Europe, measured fresh weight of all plant organs (root, leaves, Canada, and northern parts of the United States (Tiley terminal ßowering shoot, satellite ßowering shoots, et al. 1996). The ability of the seeds to ßoat often terminal inßorescence, and satellite inßorescences, results in a distribution along watercourses, but it also with a Pesola spring scale, 2,500 g). All roots and stems invades various other habitats, particularly disturbed were dissected and the number of larvae was re- corded. In accordance with Otte and Franke (1998), areas and meadows (Pysek 1994). Like other members we assumed that all plants that ßowered during the of the family, H. mantegazzianum contains phototoxic observation were in their third year, and all nonßow- furanocoumarins with insecticidal properties (Beren- ering plants in rosette stage were in their second year. baum 1978). The plant sap, in combination with UV Insects. The most common endophagous insects on radiation, causes blisters and burns on contact with giant hogweed belong to the orders Coleoptera and human skin (Lagey et al. 1995). Diptera. We frequently found three weevil species In this study, we tried to distinguish between host (Coleoptera: Curculionidae): Nastus fausti Reitter, size preference and herbivore impact by measuring Otiorhynchus tatarchani Reitter (found only at the the variables associated with plant vigor before and upper location at Arhyz), and Lixus iridis Olivier after herbivore infestation. The impact of phytopha- (found only at the lower location). The larvae of gous larvae on plant Þtness was estimated by their N. fausti and O. tatarchani are root feeders and are not abundance relative to the calculated plant growth distinguishable in the larval stage under Þeld condi- rate. To assess the host size preference, we studied the tions. We detected them inside the root and at the correlation between insect occurrence and plant rootÕs surface. Larvae of L. iridis develop inside the vigor. The main focus was on endophagous insects, hollow stems. Flies were mainly represented by a stem which seem to be more often host speciÞc than ec- boring agromyzid, newly described as Melanagromyza tophages (Cornell and Kahn 1989, Gaston et al. 1992). heracleana Zlobin (2005) (Diptera: Agromyzidae), Until now, no such experiments have been conducted and an unidentiÞed root-boring agromyzid species. in the native area of giant hogweed. Hence, this Lixus iridis and O. tatarchani develop on different study gives a Þrst estimation on the impact of Cauca- plant genera in the Apiaceae. Therefore, their use sian insect species and insect guilds on H. mantegaz- related to biological control of H. mantegazzianum is zianum. limited. Results belonging to this species can only be August 2006 HATTENDORF ET AL.: HERBIVORE IMPACT ON Heracleum mantegazzianum 1015

used for the identiÞcation of plant parts, which are sensitive to herbivory. The host range limits of the other herbivores are not exactly known. Further com- ments on the dietary requirements are given in the Agromyzidae discussion. Preference and Impact Assessment. To estimate the plant biomass at the beginning of our observational

b time (henceforth referred to as the initial plant bio- mass), we measured the size and weight of 111 leaves not included in the experiment during our Þrst survey.

N. fausti Curve estimation provided a suitable equation to de- O. tatarchani termine leaf weight {ln(weight) ϭ ln(0.07) ϩ [2.07 ϫ ln(length)]; r2 ϭ 0.89}. Stem weight, as far as present, at the Þrst survey was calculated as the stem weight at the second survey multiplied by the ratio of the stem n lengths of both visits. To evaluate host size preference of the insect species, we analyzed the relationship between larval abundance and log-transformed initial plant biomass using linear regression. After log-transformation of the variables regres- sion analysis showed that the initial plant biomass exhibited a clear linear relationship with the Þnal

Agromyzidae plant biomass measured on the second survey (log- ϭϪ ϩ ϫ ϭ biomassÞnal 0.01 1.06 log-biomassinitial; r 0.90) as well as with the umbel weight (log- ϭϪ ϩ ϫ ϭ weightumbel 0.10 0.8363 log-biomassinitial; r b 0.73). If an insect species has a negative impact on the plant, high larval densities should be associated with plants whose observed Þnal biomass and umbel N. fausti weights are lower than the values predicted by the O. tatarchani regression model. Therefore, we studied the relation- ship between the occurrence of insect larvae and the residuals from the regression to assess the herbivore impact. The central premise of our host size preference and impact assessment is that oviposition roughly co- incided with our Þrst survey and that feeding damage of developing larvae occurred mainly between both visits. This is certainly the fact for the stem-boring insects, because ßower stems just started to develop during the Þrst survey. Spot tests during the Þrst visit

M. heracleana n and the developmental stage of the root-boring agro- myzid ßy larvae indicates that this assumption is most likely true for this species. On the contrary, the life cycle of the root-boring weevils is comparatively long. plants attacked by different endophagous insects (numbers in parenthesis represent average no. of larvae per attacked plant) a Oviposition and larval feeding started in the previous season. For this reason, it was not possible to split the relationship between plant and insect performance in

Stem feeder (3-yr-old plants) Root feeder (3-yr-old plants)selectivity and impact. Root feeder (2-yr-old plants) Therefore, both possibilities will be discussed. Linear regressions were conducted for each plant H. mantegazzianum n L. iridis variable and each insect species separately. Only the mature 3-yr-old plants were included in the analyses, because insect performance on plants in rosette stage was too low to calculate a meaningful regression. Plant variables were log-transformed to normalize the re- siduals. Location was included in the models as a binary predictor when the related insect species oc- plants Occurred only at the upper location. Occurred only at the lower location.

Table 1. Proportion of curred on both plant populations. All statistical anal- a b Percent attacked Lower locationUpper location 30 20 83 (4.7) 0yses were 60 (22) performed 90 (44) 30 with 20 SPSS 30 (2.6) 12. 20 (1.3) 77 (7.0) 60 (4.2) 17 27 6 (3.0) 11 (1.5) 0 0 1016 ENVIRONMENTAL ENTOMOLOGY Vol. 35, no. 4

Table 2. Regressions analyses of herbivore insect species and plant variables of mature H. mantegazzianum

Initial biomass Final biomass Umbel wt Regression model ␤ tPr2 ␤ tPr2 ␤ tPr2 Stem feeder Lixus iridis Ϫ0.40 Ϫ2.29 0.03 0.16 Ϫ0.10 Ϫ0.55 0.58 0.01 Ϫ0.11 Ϫ0.58 0.57 0.01 M. heracleana 0.59 4.61 Ͻ0.001 0.43 Ϫ0.00 Ϫ0.01 0.99 0.19 0.20 1.59 0.12 0.38 Location 0.10 1.53 0.13 0.43 2.96 0.005 Ϫ0.67 Ϫ5.32 Ͻ0.001 Root feeder N. fausti, O. tatarchani Ϫ0.33 Ϫ2.56 0.01 0.29 Ϫ0.09 Ϫ0.66 0.52 0.19 Ϫ0.14 Ϫ1.15 0.25 0.35 Location 0.38 2.97 0.005 0.42 3.10 0.003 Ϫ0.60 Ϫ4.94 Ͻ0.001 Agromyzidae gen. spec. 0.27 2.08 0.04 0.25 Ϫ0.16 Ϫ1.18 0.24 0.21 0.18 1.42 0.15 0.36 Location 0.46 3.56 0.001 0.41 3.14 0.003 Ϫ0.56 Ϫ4.68 Ͻ0.001

A signiÞcant relationship between no. of insect larvae and initial plant biomass indicates host size preference for small (negative standardized ␤ weights and t-values) or big plants (positive ␤ and t). Herbivore impact was estimated with associations between larval abundance and Þnal plant biomass or the wt of all umbels (both adjusted for initial plant biomass). Plant variables are log-transformed. Except for L. iridis, the location was included in the models as binary predictor (0 ϭ lower location, 1 ϭ upper location).

Results the regression coefÞcient is negative in the initial plant biomass analysis (Table 2; Fig. 1d). The Þnal plant Insect Abundance. The occurrence of endophagous biomass and the umbel weight showed no response herbivores associated with giant hogweed is summa- to the presence of larvae (Table 2; Fig. 2b and d). The rized in Table 1. We found stem-boring L. iridis larvae coefÞcients of the regression analysis indicate in ad- inside almost each hogweed plant at the lower location dition that regional distinctions explain a signiÞcant but never at the upper location. In addition, we never proportion of the variation of the plant variables found adults or larvae in altitudes above 1,300 m dur- (Table 2). The decreased Þnal plant biomass at the ing the 2002 surveys. Therefore, L. iridis might be lower location is based on the fact that the ground absent in high altitudes. Larvae of M. heracleana were leaves, which constitute a considerable part of total very common in both plant populations and reached plant biomass, start senescing with the beginning of a maximum density of 135 larvae per plant. The in- the generative development (Otte and Franke 1998). festation rate was signiÞcantly higher at the upper Because of the earlier start of the vegetation period at location (␹2 ϭ 5.36; P ϭ 0.02). The number of insects the lower location, the reproductive growth and si- per plant was also increased. Root-feeding weevil lar- multaneous decomposition of ground leaves is more vae were the least common species but repeatedly advanced compared with the upper location. In con- found at both locations on 3-yr-old plants; occasion- trast to the Þnal biomass, the umbel weight was in ally, they also occurred on 2-yr-old plants. Root-feed- average higher at the lower location. ing Diptera attacked mature plants at signiÞcantly higher frequency in the lower location. They were never found on 2-yr-old plants. Because root-boring Discussion ßy larvae are sometimes located in deep secondary roots, the real number might be somewhat higher. Most observed insect species showed a distinct host Selectivity and Impact of Stem-boring Insects. Both size preference for either small or big plants, whereas insect species showed a signiÞcant host size prefer- the observed impact on plant vigor appeared negligi- ence. High quantities of L. iridis larvae were associ- ble. Most plants at the lower location started fruiting ated with small H. mantegazzianum plants. Their num- during our second survey. From there it is unlikely ber decreased signiÞcantly with increasing initial that the herbivores are able to cause serious damage plant biomass (Table 2; Fig. 1b). The M. heracleana later in the year. In contrast to the other observed larvae showed an opposite pattern. High numbers insect species, the larval development of the root- were prevalent found inside bigger plants (Table 2; feeding weevils takes almost 1 yr and started long Fig. 1a). Both insect species exhibited no negative before the beginning of our study. It is difÞcult to state impact on H. mantegazzianum. Neither the Þnal plant whether the relationship between feeding traces and biomass nor the weight of umbels as indicators for reduced plant vigor is associated with herbivore dam- changes in plant development after herbivore attack age or with oviposition preference for weak plants. showed a reaction to either larval density of L. iridis The observed reduction of plant biomass and ßower or to Melanagromyza larvae (Table 2; Fig. 2a and c). weight could be a meaningful contribution to reduce Selectivity and Impact of Root-Boring Insects. plant competition. According to the plant-vigor hy- Abundance of root-boring Agromyzidae was posi- pothesis (Price 1991), many herbivores prefer to feed tively correlated with the initial plant biomass (Table on vigorous plants, because they are more nutritious. 2; Fig. 1c), indicating a preference for larger plants by Therefore, preference for weak plants should be an ovipositing female ßies. The Þnal plant biomass and exception. However, there are also several reasons the weight of umbels are not affected, so impact on why small plants could be more suitable for herbivores plant development is absent (Table 2; Fig. 2b and d). (Mayhew 1997). For instance, stress conditions, like In case of the weevil species N. fausti and O. tatarchani, limited resources, could lead to reduced plant growth August 2006 HATTENDORF ET AL.: HERBIVORE IMPACT ON Heracleum mantegazzianum 1017

Fig. 1. Relationship between occurrence of herbivore larvae and initial plant biomass of mature H. mantegazzianum as measure for host size preference. E, upper location; F, lower location. and to decreased allocation of defensive compounds at herbivore impact is known to depend on several fac- the same time (White 1984). Studies investigating tors (e.g., weather conditions) and can differ from these two contradictory hypotheses have yielded in- year to year (Dhileepan 2003, Russell and Louda consistent results (Inbar et al. 2001), indicating that 2004). the interactions are more complex and other impor- It is possible that only the interaction of several tant factors are involved. antagonists will lead to a meaningful impact. Accord- It is possible that root-feeding weevil larvae living ing to McEvoy and Coombs (1999), there currently externally in the beginning of their live cycle are exists no general conclusion whether successful bio- boring into the roots after a certain time. This could logical control is usually related to one effective con- explain why we only occasionally found damaged trol agent as assumed by Myers (1985) or to the in- roots of biennial plants. The larval development of teraction of small effects caused by several antagonists almost 1 yr should result in similar infestation rates of (Schroeder and Goeden 1986). Although some studies biennial plants after oviposition and triennial plants associated with biological control showed a mutual- before pupation, if we disregard plant and insect mor- istic relationship of the effectiveness of different an- tality. Nevertheless, it is difÞcult to generalize about tagonists (Bacher and Friedli 2002), the interactions of our results derived only from one Þeld season because several weed antagonists do not necessarily result in a 1018 ENVIRONMENTAL ENTOMOLOGY Vol. 35, no. 4

Fig. 2. Impact of stem feeding (a and c) and root boring (b and d) insects on biomass (a and b) and seed production (c and d) of mature H. mantegazzianum. Plant variables are adjusted for the initial plant biomass. The dotted line is the mean prediction line calculated from linear regression. Symbols below the prediction line represent plants with lower biomass or seed production than expected from their initial biomass. Dark or large sized symbols represent plants attacked by many Curculionidae or Agromyzidae larvae, respectively.

cumulative effect; they can even affect each other sidered as potential biological control agents (Kru¨ ss negatively. For example, adults of the leaf Cas- 2002). sida rubiginosa Muell. avoid thistles, Cirsium arvense Some studies have reported serious damage on Le- L., infected with the fungus Phoma destructiva Plowr. visticum officinale Koch (Eichler 1951) and Heracleum for oviposition and feeding. Both were formerly con- sosnowski Manden. (Volovnik 1988) caused by L. iri- August 2006 HATTENDORF ET AL.: HERBIVORE IMPACT ON Heracleum mantegazzianum 1019 dis. Unfortunately, both quantiÞed neither the level of be carried out. Even if side effects like predation attack nor the reduced plant Þtness. However, it seems remains unclear, a potential bias caused by host size that tolerance to herbivory is pronounced in mature preference can be excluded. However, the approach H. mantegazzianum compared with other plants. The used here could be suitable if the situation in the preference of L. iridis to smaller plants results from weedÕs native range is largely unknown, as in our case, the morphology of the proboscis. Females bore cavi- or if population dynamics of the potential biological ties into their host stems for oviposition. As a conse- control agent are likely to be strongly top-down reg- quence, the stem wall has to be thinner than the ulated. The negative impact of the examined insect length of the rostrum of the beetle. Eber et al. (1999) species on the weed was small. This study suggests that found that body size of Lixus elongatus Goeze is pos- mature giant hogweed plants can tolerate rather high itively correlated with the host stem diameter. This herbivore loads. Further studies should try to identify means that they exhibit a host size preference for more crucial stages in the weedÕs life cycle. larger plants within their morphological restrictions. Thus, the large size of giant hogweed is probably responsible for the fact that we found most larvae in Acknowledgments the smallest size class. In addition, we found all larvae We thank Sˇ. Jahodova, O. Booy, and M. Schmidt for fruitful of L. iridis in the upper narrow parts of the ßower discussions and for critical comments on this manuscript. The stem. On the contrary, thick stems provide a greater project is funded by EU Þfth framework program “Energy, food source for M. heracleana, which oviposit in the Environment and Sustainable Development”ÐAssessing and outer layer of the stem. The larvae were mostly lo- Conserving Biodiversity and the Swiss Federal OfÞce for cated in the lower part of the stem. This opposite Education and Science (EC EVK2-2001-00128). preference leads to a specialization in separate niches in plant individuals, perhaps to avoid interspeciÞc References Cited competition (Zwo¨lfer and Brandl 1989). Detailed within-plant distribution is discussed elsewhere (Hat- Arzanov, Yu. G., and G. E. Davidyan. 1996. Review of the tendorf 2005). genus Nastus Schoenherr (Coleoptera, Curculionidae) of The host range of potential agents is a critical factor the fauna of Crimea, European Russia and the Caucasus. in biological control. Lixus iridis and O. tatarchani are Entomol. Rev. 75: 134Ð153. known to feed on several plant genera; therefore, they Bacher, S., and J. Friedli. 2002. Dynamics of a mutualism in are not suitable as biological control agents. The re- a multi-species context. Proc. Roy. Soc. Lond. B Biol. 269: 1517Ð1522. production of O. tatarchani was parthenogenetic in Ballabeni, P., D. Conconi, S. Gateff, and M. Rahier. 2001. the laboratory. Because exotic biological control Spatial proximity between two host plant species inßu- agents have to adapt to exploit the new habitat and ences oviposition and larval distribution in a leaf beetle. target weed, a high level of genetic diversity would be Oikos 92: 225Ð234. preferable. However, Roderick and Navajas (2003) Berenbaum, M. R. 1978. Toxicity of a furanocoumarin to found no evidence that genetic adaptation is impor- armyworm: a case of biosynthetic escape from insect tant for the success of insect biological control agents. herbivores. Science 201: 532Ð534. The diet of N. fausti is not known in detail yet. Ac- Briese, D. T., S. Bo¨ttcher, J. Vitou, and T. Thoman. 2003. cording to Arzanov et al. (1996), adults are wide- Prevalence and impact of the crown ßy, Botanophila spi- nosa, on its host thistle, Onopordum acanthium, in south- spread in the forest belt of the Caucasus and were ern France. Acta. Oecol. 24: 77Ð86. repeatedly found on leaves of Heracleum. M. hera- Callaway, R. M., T. H. DeLuca, and W. M. Belliveau. 1999. cleana and the undetermined root-boring agromyzid Biological-control herbivores may increase competitive ßy are in terms of dietary requirements more prom- ability of the noxious weed Centaurea maculosa. Ecology ising. Many members of this family seem to be highly 80: 1196Ð1201. host-speciÞc; 79 of 87 agromyzids on Apiaceae are at Cornell, H. V., and D. M. Kahn. 1989. Guild structure in the least restricted to this plant family (Spencer 1990). British arboreal : is it stable and predictable? However, because of the big size of giant hogweed, it J. Anim. Ecol. 58: 1003Ð1020. could be difÞcult to develop mass-rearing techniques Dhileepan, K. 2003. Seasonal variation in the effectiveness of the leaf-feeding beetle Zygogramma bicolorata for the stem-feeding M. heracleana. Another species of (Coleoptera: Chrysomelidae) and stem-galling moth the genus Melanagromyza, M. eupatorialla (Spencer), Epiblema strenuana (Lepidoptera: Tortricidae) as bio- was suggested as a biological control agent for the control agents on the weed Parthenium hysterophorus weed Chromolaena odorata L. R. M. King and H. Rob., (Asteraceae). Bull. Entomol. Res. 93: 393Ð401. but several attempts failed to rear it in quarantine Eber, S., S. Knoll, and R. Brandl. 1999. Endophagous insects (Lorraine and Zachariades 2002). and structural niches on plants: ecology and evolutionary In conclusion, most phytophagous insects showed consequences. Ecol. Entomol. 24: 292Ð299. a strong host size preference for either big or small Eichler, W. 1951. Die Entwicklung und Lebensweise des plants. Because this behavior seems to be widespread, Schierlingsru¨ sslers (Lixus iridis). Entomol. Bull. 47: 87Ð 95. at least in herbivores on giant hogweed, the develop- Forsberg, J. 1987. 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