Biological Control 41 (2007) 120–133 www.elsevier.com/locate/ybcon
Physiological host range of Ceratapion basicorne, a prospective biological control agent of Centaurea solstitialis (Asteraceae)
Lincoln Smith ¤
USDA-ARS Western Regional Research Center, 800 Buchanan Street, Albany, CA 94710, USA
Received 3 November 2006; accepted 18 December 2006 Available online 29 December 2006
Abstract
Ceratapion basicorne (Coleoptera: Apionidae) is a weevil native to Europe and western Asia that is being evaluated as a prospective classi- cal biological control agent of Centaurea solstitialis (yellow starthistle) in the United States. Host plant speciWcity of the insect was evaluated in no-choice oviposition experiments. Feeding on leaf tissue by adult females was highly correlated to oviposition rate, both of which occurred primarily on plants in the tribe Cardueae, and especially those in the monophyletic subtribe Centaureinae. The highest rates of lar- val development occurred on Ce. solstitialis and Centaurea cyanus (bachelor’s button, garden cornXower), and there was signiWcant develop- ment on Centaurea melitensis (Napa starthistle, tocalote), Cnicus benedictus (blessed thistle), Carthamus tinctorius (saZower), and Crupina vulgaris (common crupina). All the plants that supported some larval development are within a monophyletic clade within the Centaureinae. No native North American plants appear to be at risk of signiWcant damage by this insect. Additional testing of saZower and bachelor’s button under choice conditions should complement these results to help determine the degree to which these plants are at risk. 2006 Elsevier Inc. All rights reserved.
Keywords: Host plant speciWcity; Biological control; Weed; Invasive plant; Risk assessment
1. Introduction Yellow starthistle is highly invasive in grassland habitats and displaces desirable plants in both natural and grazing areas. 1.1. Weed distribution, ecology, and impact Spiny Xowerheads interfere with grazing animals and human recreation, and the plants displace desirable vegetation and Yellow starthistle (Centaurea solstitialis L.) is an invasive deplete soil moisture. Consumption of yellow starthistle by alien weed that was accidentally introduced into California horses causes a fatal syndrome known as “chewing disease” over 130 years ago, primarily by importation of contami- or nigropallidal encephalomalacia (Cordy, 1978). Total eco- nated alfalfa seed (Maddox et al., 1985; Gerlach, 1997a,b). nomic beneWts for controlling yellow starthistle in California The weed infests about eight million hectares in the western have been estimated to be between $40 million and $1.4 bil- US and Canada (Duncan, 2001; Pitcairn et al., 2006). Infesta- lion, depending on assumptions (Jetter et al., 2003). Environ- tions have been reported in 23 states, with the largest popula- mental beneWts due to reduced use of herbicides, increased tions in the states of California, Idaho, Oregon, and recreation and increased biodiversity have not been Washington (Maddox et al., 1985; Sheley et al., 1999). It is estimated, nor have any beneWts to nearby states. considered the most common weed in California, and it is Yellow starthistle is an herbaceous winter annual plant continuing to spread and threaten states to the east (Pitcairn native to southern Europe and the Near East (Maddox, et al., 2006). The weed is designated as noxious in 11 western 1981), occurring from Spain to Iran (Wagenitz, 1975; Dostál, states and two Canadian provinces (Skinner et al., 2000). 1976; Rechinger, 1980). The geographic center of origin may be in Turkey or Greece, based on the number of subspecies * Fax: +1 510 559 5737. occurring in these regions (Wagenitz, 1975; Dostál, 1976). E-mail address: [email protected] Although the plants in the western USA are genetically
1049-9644/$ - see front matter 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2006.12.015 L. Smith / Biological Control 41 (2007) 120–133 121 diverse, there is no evidence of genetically distinct subpopula- eVective for controlling it. Additional agents are needed, tions occurring there (Roché, 1965; Sheley et al., 1983a,b; especially ones that attack the foliage, stem, and roots of Schumacher et al., 1982; Sun, 1997). The plant is well rosettes and young bolting plants (Smith, 2004). adapted to a Mediterranean climate (dry summers and wet winters) and can tolerate winter snow. In California, seeds 1.3. Life history and behavior of Ceratapion basicorne germinate mainly in early winter, rosettes grow slowly until spring, then the plants “bolt” and bloom until they die from Ceratapion basicorne (Illiger) (Coleoptera: Apionidae) is a desiccation or frost (Pitcairn et al., 1999a; Sheley et al., 1999). weevil native to Europe and the Near East that develops in Some seeds are released during the summer as individual rosettes of yellow starthistle (Clement et al., 1989; Alonso- capitula (Xower heads) mature while others are retained until Zarazaga, 1990a; Wanat, 1994). In the wild this insect has the capitula disintegrate during winter. Seeds falling in sum- been reared from Ce. solstitialis, Ce. cyanus L., and Cnicus mer soon become dormant and require cooler temperatures benedictus L., which suggests that it is highly host-speciWc before germinating, usually soon after the start of winter (Alonso-Zarazaga, 1990a; Wanat, 1994; Campobasso et al., rains. Seeds buried in soil can remain viable for several years 1999). The insect is common on yellow starthistle in Turkey, and will germinate after exposure to light when the soil is Greece, and Georgia (Rosenthal et al., 1994; Balciunas, 1998; disturbed (Joley et al., 2003 and Refs. therein). Uygur et al., 2005) and is widely distributed in Europe and western Asia (Alonso-Zarazaga, 1990a; Wanat, 1994). Over- 1.2. Weed management options wintering adults become active in the early spring and feed on rosette leaves (Clement et al., 1989). Eggs are deposited Although several herbicides are eVective (Sheley et al., inside leaves, and larvae tunnel down the leaf petiole and 1999; DiTomaso, 2005), conventional herbicide control develop inside the upper root and basal stem (root crown), strategies have often been inadequate because of the large where they pupate (Smith and Drew, 2006). Females oviposit areas infested, the economic and environmental costs of about 1.5 eggs per day during an oviposition period of about herbicides, or the relatively low monetary return from land 20days. Development time of eggs until eclosion of larvae is used for grazing, rights-of-way, conservation or recreation. 8.5days at room temperature (19°C), and development time Other control strategies such as tillage, mowing, burning, from oviposition until adult emergence is about 77days. and grazing have been evaluated and can sometimes be Adults emerge from the plant in early summer, when it bolts. eVective, but are not practical for managing the weed over Adults feed brieXy on yellow starthistle foliage then aestivate large areas of rangeland (DiTomaso et al., 2000; DiTom- and hibernate until the following spring. Mating occurs soon aso, 2005 and Refs. therein). In the Mediterranean region, after new adults emerge in early summer and after hiberna- where it originates, yellow starthistle generally occurs in tion ends in the following spring (Smith and Drew, 2006). low densities and appears to be under natural control There is one generation per year. (Uygur et al., 2004). Research to discover, evaluate, and Some data on host speciWcity were reported by Clement introduce classical biological control agents began in the et al. (1989), indicating that Carthamus tinctorius L. 1960s (Maddox, 1981; Rosenthal et al., 1992; Turner et al., (saZower), Galactites tomentosus Moench, and Carduus 1995; Sheley et al., 1999). Some biological control agents pycnocephalus L. can support larval development. However, have been previously introduced, with the establishment of absence of reports of the development of this insect from six exotic insect species, all of which attack Xowerheads and these hosts in the Weld (Alonso-Zarazaga, 1990a; Wanat, destroy developing seeds (Turner et al., 1995; Balciunas and 1994; Campobasso et al., 1999; Uygur et al., 2005) prompted Villegas, 2001). A few indigenous invertebrates and diseases me to further evaluate its host speciWcity. The purpose of the have been described on yellow starthistle in California (Pit- present study was to determine what non-target plants are cairn et al., 1999a,b). Of these, only a few attack plants later susceptible to damage by C. basicorne and to measure the rel- than the seedling stage, and these have little eVect (Kli- ative amount of damage the insect can cause under no-choice siewicz, 1986), but some can cause signiWcant mortality laboratory conditions. Such data provide part of the basis for among very young seedlings (Woods et al., 2000). The rust assessing the risk that the insect would pose to non-target pathogen, Puccinia jaceae var. solstitialis, was introduced in plants if it were to be introduced as a biological control agent California in 2003 (Woods et al., 2004; Fisher et al., 2006), (USDA-APHIS, 1998; Withers et al., 1999; Jacob and Briese, but it does not appear to be causing signiWcant damage to 2003; Coombs et al., 2004; Smith, 2006). the plant. The combined eVect of these natural enemies has not signiWcantly reduced yellow starthistle over most of its 2. Materials and methods range (Balciunas and Villegas, 1999; Pitcairn et al., 2002; Smith, 2002), although there are some local reductions, 2.1. Insect population especially in the presence of competing vegetation (Pitcairn et al., 2005; E.M. Coombs, personal communication). Com- The parental generation and descendents of a colony of parative life history studies of the plant in California (Pit- C. basicorne held in the USDA-ARS quarantine laboratory cairn et al., 2002) and Turkey (Uygur et al., 2004) suggest in Albany, CA were used for these experiments. The colony that natural enemies that damage the rosettes may be most was established from adults reared from naturally infested, 122 L. Smith / Biological Control 41 (2007) 120–133 wild yellow starthistle plants that were collected at 15 sites tube (3.5cm diameter 11cm long) mounted on an intact near Kayseri, Sivas, Erzincan, Erzurum, and Malatya, Tur- rosette leaf of a nonta£rget plant species for four to 5days key between 28 May and 2 June 2001 (Smith and Drew, (Fig. 1B). Afterwards, we put each female back with a cut 2006). Emerged adults were identiWed by the author before yellow starthistle leaf for two to three days to determine if using them in experiments. IdentiWcation of representative she could still oviposit. If the female failed to oviposit on the specimens was conWrmed by B.A. Korotyaev, and vouchers post-trial yellow starthistle or died during the experiment, were deposited at the USDA-ARS Systematic Entomology then the trial was considered invalid and the experiment was Laboratory in Beltsville, MD. Reproductive diapause was repeated. After removing the insect from the test plant, the terminated by holding adults in the dark at 5 °C for at least exposed leaf was labeled, and we counted the number of three months (Smith and Drew, 2006). Experiments were adult feeding holes and eggs oviposited. After 10–21days, conducted between March 2002 and April 2005. which allowed time for eggs to hatch and larvae to tunnel down the petiole and into the root crown, the leaf was 2.2. Test plants removed and examined under a microscope for signs of egg hatch and larval tunneling (see Smith and Drew, 2006). Six Test plant species were selected following Technical weeks after exposure to oviposition, each plant was enclosed Advisory Group (TAG) guidelines, which emphasize evalu- in a Wne mesh bag and held in a quarantine greenhouse until ation of native and economically important species the insects could complete development (three months), then (USDA-APHIS, 1998; see discussion below). We generally the plants were dissected to observe signs of insect damage used plants grown from seed that were two to four months and development. Any plants that deteriorated prematurely old and in the rosette stage (except for species that do not were dissected immediately. In general, we tested eight repli- form a rosette). However, because of scarcity of seed, many cates per plant species in the tribe Cardueae and four in the of the Saussurea americana Eaton plants were transplanted more distantly related taxa. We doubled the number of from the Weld. Cuttings of Hemizonia minthornii Jepson replicates if there were any signs of larval development. were used instead of potted plants. Seeds for test plants In general, no statistical tests were conducted on the were obtained from commercial sources or from the wild results, because the purpose was to describe the risk and with the assistance of cooperators (see Acknowledgements). amount of damage or oviposition rather than to test A representative specimen of each species was grown to hypotheses. However, !2 tests of independence were con- maturity to provide herbarium vouchers that are kept at ducted to compare adult feeding damage and oviposition the USDA-ARS Western Regional Research Center, rates among the varieties of saZower tested to determine if Albany, CA. IdentiWcations were conWrmed by G.F. Hrusa any were more susceptible than the others. (California Department of Food and Agriculture). 3. Results and discussion 2.3. No-choice tests 3.1. Test plants Individual mated females that had completed reproduc- tive diapause were held in a sealed container with a cut leaf Test plant species were selected following Technical of yellow starthistle, inserted in a water vial, until she ovipos- Advisory Group (TAG) guidelines, which emphasize ited (Fig. 1A). Each female was then placed in a clear plastic protection of native and economically important species
Fig. 1. Individual females were held in a sealed plastic cylinder on an intact leaf of a nontarget test plant for 5 days (A), then placed in a tube with a cut yellow starthistle leaf (B) to feed and oviposit before use in a subsequent test. L. Smith / Biological Control 41 (2007) 120–133 123
(USDA-APHIS, 1998; TAG, 2006). The guidelines gener- The two subtribes Centaureinae and Carduinae have ally follow the “centrifugal phylogenetic” approach out- distinctly diVerent secondary chemical compounds lined by Wapshere (1974), in which more species are tested (Susanna et al., 1995), which are probably important in in taxonomic ranks closely related to the target weed, and determining host plant speciWcity of specialist herbivores. the number of test species decreases as relatedness to the Centaureinae produce acetylene aldehydes, chlorhydrins, target decreases. The validity of this approach is supported and acetates, germacronolide-type sesquiterpenoids, highly by the historical data that indicates that close relatives are methoxylated Xavonoids (including Xavanones), and fully most likely to suVer damage (Pemberton, 2000; Sheppard methoxylated lignans (Wagner, 1997). In contrast, the Car- et al., 2005). Other factors that contributed to the choice of duinae produce distinctive classes of acetylenes, including test species included: nativity in North America; ornamen- C17 acetylenes and acetylene glycosides, guainolide-type tal or other economic value; whether the species is sympat- sesquiterpenoids, monomethoxylated Xavonoids, and ric with the target’s present or potential range in North simple cinnamic acids and their derivatives. America; similarity of growth form, life history and second- The genus Centaurea is very large, comprising 200–600 ary chemistry, if known; the presence of rare or protected species, and its deWnition and extent is still being resolved species in the same genus; and availability of the species for (Klokov et al., 1963; Dostál, 1976; Susanna et al., 1995; testing. For rare or protected species that were proposed Garcia-Jacas et al., 2000; Hellwig, 2004). Some groups for testing, we often tested a close relative to avoid nega- within the genus Centaurea (e.g., Centaurea sensu stricto, tively impacting an already stressed species and/or because Cyanus, Jacea, and Psephellus groups) appear to be as phy- of unavailability of specimens. Species names are based on logenetically distinct as other well recognized genera (e.g.., the PLANTS Database (USDA-NRCS, 2006) with the sup- Amberboa, Carduncellus, Carthamus, Cnicus, Crupina, and port of other regional Xora, primarily Barkley (1986), Keil Seratula) (Garcia-Jacas et al., 2001; J.F. Gaskin, unpub- (1993) and Hitchcock and Cronquist (1998). Test plant spe- lished data). Two North American species, Centaurea amer- cies were selected following the higher taxonomy of Bremer icana Nutt. and Centaurea rothrockii Greenm. have been (1994). A recent phylogenetic revision (Funk et al., 2005) assigned to the genus Plectocephalus, which has distinct has changed some taxonomic relationships; however the pollen morphology and is thought to have diverged from level of signiWcance of the cladogram branches was not the Centaurea clade during late Oligocene and Miocene reported, so the relationships should be interpreted as the (Wagenitz, 1955; Hellwig, 2004). This is much earlier than current, though possibly imperfect, state of knowledge. In the divergence of Cyanus and the Carthamus/Carduncellus particular, the subfamily Cichorioideae was reduced and groups, which probably arose during the Pliocene–Pleisto- Carduoideae was erected. The tribe Cardueae was previ- cene transition. The Flora of North America (Keil and ously placed in the subfamily Cichorioideae s.l.; however, Ochsmann, 2006) uses the treatments: Centaurea benedicta the latter was determined to be a paraphyletic grade (Gar- ( Cn. benedictus), Plectocephalus americana and Plecto- cia-Jacas et al., 2002) and has since been redeWned as a ceDphalus rothrockii, although the PLANTS website has not monophyletic group that does not include Cardueae (Funk adopted these changes (USDA-NRCS, 2006). Although et al., 2005). The tribe Mutisieae was removed from Cicho- many of the phylogenetic relationships among the remain- rioideae s.s. and is now a basal, probably still paraphyletic, ing species within the genus Centaurea are not precisely clade of the Asteraceae (Funk et al., 2005). known, some groups have clearly emerged. The strongest Yellow starthistle is in the family Asteraceae, subfamily grouping reXects diVerences in pollen structure (Wagenitz, Carduoideae, tribe Cardueae, and subtribe Centaureinae 1955) and DNA nucleotide base sequences (Susanna et al., (Bremer, 1994; Funk et al., 2005). Both the subfamily Car- 1995; J.F. Gaskin, unpublished data). Yellow starthistle is duoideae and the tribe Cardueae appear to be monophyletic in the Jacea group, which is monophyletic and includes groups. The exact taxonomic relationships within the tribe many of the other weedy Centaurea species adventive to Cardueae are not completely understood, but the subtribe North America. Centaureinae segregates as a monophyletic group from Plants of economic interest in the family Asteraceae dis- the rest of the tribe, whereas the subtribe Carduinae is a tributed within the geographic range of yellow starthistle in paraphyletic grade (Bremer, 1994; Susanna et al., 1995; Gar- North America include artichoke (Cynara scolymus L.), cia-Jacas et al., 2002). However, of the Carduinae genera of saZower (Ca. tinctorius L.) and sunXower (Helianthus interest in this study, Carduus, Cirsium, Cynara, and Silybum annuus L.). Because a population of C. basicorne from Italy appear to be in a monophyletic group, whereas Onopordum is has been reported to damage and develop in saZower positioned more basally (Funk et al., 2005). So, all these gen- (Clement et al., 1989), and this is an important crop in Cali- era are more distantly related to Centaurea than are those in fornia and other western states, we evaluated nine varieties. the Centaureinae. The monophyletic Arctium–Cousinia–Sau- Bachelor’s button (Ce. cyanus) is an introduced ornamental ssurea–Jurinea group within the Centaureinae is considered in North America, but is also considered an invasive weed to be the closest related monophyletic group that includes in some areas of the western US (Lorenzi and JeVery, 1987; Centaurea, Acroptilon, Carthamus, Cnicus, and probably Taylor, 1990), and is a common weed in wheat Welds in east- Crupina (Garcia-Jacas et al., 2002; Funk et al., 2005, J.F. ern Europe (Voronov, 1977; Kapeluszny and Pawlowski, Gaskin, unpublished data). 1978; Snarska, 2004). The native North American plants 124 L. Smith / Biological Control 41 (2007) 120–133 most closely related to yellow starthistle include: Ce. ameri- of two S. americana plants were damaged, but the damage cana and Ce. rothrockii (discussed above), S. americana, was not consistent with that usually caused by C. basicorne. and the many species of Cirsium. Several Cirsium species These plants had been collected from the Weld shortly are becoming rare, and six species or varieties are federally before being tested, so it is likely that the damage was listed as endangered (E) or threatened (T): Cirsium fonti- caused by other species of insect that had attacked the plant nale (Greene) Jepson var. fontinale (E), Ci. fontinale in the Weld. Other S. americana plants that were not infested (Greene) Jepson var. obispoense J.T. Howell (E), Ci. hydro- by C. basicorne had similar damage. These results indicate philum (Greene) Jepson var. hydrophilum (E), Cirsium lon- that there is zero to very low risk that C. basicorne will cholepis Petrak (E), Cirsium pitcheri (Torr. ex Eat.) Torr. damage any North American native plant species. and Gray (T), and Cirsium vinaceum Woot. and Standl. (T) Our results generally corroborated those of Clement et al. (USFWS, 2005). A total of 20 native species, including Ci. (1989), indicating no larval development on any Cirsium fontinale var. fontinale and Ci. fontinale var. obispoense, species tested, Cy. scolymus (artichoke) or Ce. calcitrapa L. occur in California. Eleven California species are consid- However, there were some discrepancies. Clement et al. ered rare (Tibor, 2001), and Cirsium ciliolatum (Henderson) (1989) reported larval development on Car. pycnocephalus J.T. Howell and Cirsium rhothophilum Blake are listed by L. in 11% of trials, in which four neonate larvae were trans- the state of California as endangered and threatened, ferred to each replicate plant, whereas we observed no devel- respectively. opment on Car. pycnocephalus, despite oviposition of ten eggs on one out of ten plants tested. The seven eggs ovipos- 3.2. No-choice tests ited in the leaf blade either did not hatch or the larvae failed to reach the midrib. Of the three eggs oviposited in the mid- We tested a total of 51 species of nontarget host plants rib, two larvae tunneled down the petiole, but no damage to from the Asteraceae family, including 25 native species and the stem was observed. Apparently placing neonate larvae in 4 economic species (Table 1). This includes species from all a hole in the central rosette meristem is more conducive to Wve genera in the subfamily Carduoideae, all three tribes in larval development. On the other hand, we observed devel- the subfamily Cichorioideae s.s., and all eight tribes in the opment of some larvae on Cn. benedictus, whereas Clement subfamily Asteroideae that contain native North American et al. (1989) observed no development on the three plants species or economic species. In no-choice oviposition tests, tested. Although we did not test G. tomentosus Moench, C. basicorne females oviposited at least once on 94% of the absence of development in any Cardueae outside the sub- plant species in the subtribe Centaureinae, including Ca. tribe Centaureinae, suggests that we would not have tinctorius (saZower) and the native species Ce. americana observed development in this plant; however, Clement et al. and Ce. rothrockii. At least one egg was deposited on 62% (1989) reported development in 20% of their larval transfer of the plant species in other subtribes of the Cardueae, and trials. The diVerences between our results and those of most frequently on S. americana and Ci. loncholepis. Eggs Clement et al. (1989) indicate that estimates of host plant were observed on only three plants outside the tribe Card- suitability that are based on transfer of neonate larvae to a ueae: one egg on one plant of Liatris punctata Hook., two potentially susceptible part of the plant (into a hole in the eggs on one plant of Gazania rigens (L.) Gaertn., and six central meristem) can diVer from those based on naturally eggs on one plant of Pluchea odorata (L.) Cass. None of the oviposited eggs. The reason is probably because eggs and eggs on the Wrst two plants hatched. Two eggs on P. odo- emerging larvae oviposited in the leaf blade and midrib face rata hatched, but larvae died when they reached the end of diVerent plant defenses than larvae artiWcially placed in the the petiole. These results indicate no risk of signiWcant central meristematic tissue. Thus, when designing larval larval damage to plants outside the tribe Cardueae. transfer experiments, it is important to place larvae in as The highest rates of larval survival and development natural a location as possible to improve the validity of were observed on Ce. solstitialis (yellow starthistle) and Ce. extrapolating the results to predict what would occur under cyanus (bachelor’s button), and there was development on natural conditions. Larval transfer is less preferable for Centaureinae melitensis L. (Napa starthistle, tocalote), insects that oviposit into plant tissue than for those that Centaureinae montana L., Centaureinae nigrescens Willd. oviposit externally (Sheppard, 1999). ( Centaureinae x pratensis, meadow knapweed), Centau- Development of larvae in saZower and bachelor’s but- reDinae sulphurea Willd., Cn. benedictus L. (blessed thistle), ton may not be normal for C. basicorne because these Ca. tinctorius (saZower), and Crupina vulgaris Cass. (com- plants do not form a rosette. Thus, when young larvae tun- mon crupina). There was no larval development on any nel down a leaf on either of these plants, they cannot reach Cirsium species tested, which is consistent with Clement the root crown. The stem of these plants has a pithy center, et al.’s (1989) results for Cirsium douglasii DC. and Cirsium and larvae only feed in the woody outer portion of the campylon H. Sharsm. There was no larval development in stem. The relatively thin cortex provides a limited space for any threatened or endangered species, nor their surrogates the insect, and as the plant continues to grow, it sometimes that we tested. Regarding the two North American native crushes the pupae. Nevertheless, there was high infestation Centaurea species, no development was observed in 18 tri- and survivorship to the pupal stage on bachelor’s button als of Ce. rothrockii or 21 trials of Ce. americana. The roots and saZower in no-choice experiments, so both these L. 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a b e b b l T T T T T T T T T T T T a r f l c e a a b d l u u n G S A T S i P L. Smith / Biological Control 41 (2007) 120–133 127 plants require additional choice testing in the laboratory group, and Ca. tinctorius in the Carthamus group (Garcia- and Weld to determine risk of infestation under more Jacas et al., 2001; J.F. Gaskin, unpublished data). Within natural conditions (Smith et al., 2006). this clade, there are no native North American plants, and The host plants suitable for C. basicorne development the only plants of economic interest are Ca. tinctorius, a sig- correspond to a clearly deWned phylogenetic group. Our niWcant crop, and Ce. cyanus, an ornamental. The two results indicate that C. basicorne is able to develop on a native North American species, Ce. americana and Ce. small number of plants within a monophyletic “derived rothrockii, which were not suitable hosts, are in a diVerent clade” within the subtribe Centaureinae that includes the clade and have recently been assigned to the genus Plecto- Jacea, Cyanus and Carthamus groups (Fig. 2). Delineation cephalus (Susanna et al., 1995; Hellwig, 2004). Cr. vulgaris of this clade is based on nucleotide sequences of ITS may be an outlier because it appears to be more distantly nuclear ribosomal DNA and agrees with other morpholog- related to Ce. solstitialis than other groups containing ical characters (Garcia-Jacas et al., 2001); however, the rela- unsuitable plants: Acroptilon, Plectocephalus and Psephel- tionships within it are not fully certain because of low lus. Some species within the “derived clade” were not suit- bootstrap values (J.F. Gaskin, unpublished data). The clade able for C. basicorne development: Ce. calcitrapa, Ce. includes the suitable species: Ce. solstitialis, Ce. melitensis, cineraria, Centaurea diVusa, and Centaurea stoebe (often Ce. nigrescens, Ce. sulphurea and Cn. benedictus in the called Centaurea maculosa in North America (Ochsmann, Jacea group, Ce. cyanus and Ce. montana in the Cyanus 2001)). So, although the “derived clade” includes almost all
Fig. 2. Suitability of plants within the subtribe Centaureinae to oviposition and larval development by C. basicorne. ClassiWcation of the species into “groups” is based on plant morphology, pollen type and DNA sequences of introns (Garcia-Jacas et al., 2001; J.F. Gaskin, unpublished data). Oviposition is mean eggs per female per day of exposure to the plant ( 95% CI), and development is percentage of oviposition trials in which at least one insect § developed to at least the pupal stage. 128 L. Smith / Biological Control 41 (2007) 120–133 species that are suitable, not all species within the clade are for nontarget species, and (2) it included the “positive con- suitable. These results conWrm that although phylogenetic trol” trials that followed exposure to nontarget plants, relationships explain a high degree of host plant speciWcity, many of which may have negatively aVected the insects. they do not explain all of it. The exceptions presumably are There was moderate acceptance of nine other species of caused by evolutionary divergence of critical characters Centaurea, Ca. tinctorius (saZower) and Cn. benedictus. (e.g., allelochemics and plant morphology) in close relatives Low adult feeding occurred on the other Centaureinae, that cause them to be less suitable, and evolutionary con- about half the other Cardueae, and one other species of vergence in more distant relatives that make them more Cichorioideae (G. rigens). There was, at most, only trace suitable. Thus, selection of plant species to test should not feeding on test plants in the subfamily Asteroideae. These rely only on phylogeny, as some have proposed (Briese, results suggest that under extreme conditions C. basicorne 2005, 2006), lest we overlook a more distant relative that adults may feed on other species of plants, particularly in may be suitable because of similarity of critical characters the subtribe Centaureinae. Risk of adult feeding damage is (e.g., Wheeler, 2005; Haines et al., 2004). generally limited to plants within the tribe Cardueae. Each All the reported larval host plants from Weld collections: adult feeding hole is about 1-mm2, and they were smaller on Ce. solstitialis, Ce. cyanus, and Cn. benedictus (Alonso- most nontarget species. Therefore, adult feeding is not Zarazaga, 1990a; Wanat, 1994; Campobasso et al., 1999; J. expected to cause any noticeable damage to nontarget Balciunas, unpublished data) were suitable in the labora- species except possibly to Ce. cyanus and Ce. diVusa. tory experiments. However, other species that were suitable in the laboratory, such as Ca. tinctorius, Ce. melitensis, Ce. 3.3. SaZower varieties sulphurea, Ce. nigrescens and Ce. montana, have not been reported as a host in the Weld. This agrees with current the- All nine saZower varieties were susceptible to adult ory that the physiological range, delineated in no-choice feeding and oviposition under no-choice conditions (Table laboratory experiments, is broader than the ecological 2). Adult feeding (7.4–16.2 holes/days) and oviposition (0.3– range realized in the Weld (Briese, 2005; Sheppard et al., 0.8 eggs/days) rates tended to be lower than on yellow star- 2005). Field experiments conducted in Turkey indicated thistle (16.6 and 1.5, respectively) but are clearly a concern that Ca. tinctorius was not attacked by C. basicorne, despite regarding susceptibility of this plant. Larval damage and natural infestation of 48–98% of adjacent Ce. solstitialis development to at least the pupal stage occurred in 30–50% plants (Smith et al., 2006). Thus, Ca. tinctorius is not likely of plants tested, depending on variety. There were no sig- to be attacked in the Weld. Similar experiments have not niWcant diVerences among varieties (!2, df 9, P > 0.5), even been done for Ce. cyanus, so risk to this species in the Weld when varieties with less than ten replicatDes were excluded is not well known. from analysis. These results conWrm those of Clement et al. Intensity of adult feeding on leaves was highly correlated (1989) indicating that C. basicorne is physiologically able to to the number of eggs oviposited in test plants (R2 0.88, feed, oviposit and develop on saZower under no-choice D P < 0.0001; Fig. 3), probably because adult feeding is neces- laboratory conditions. sary for egg development. Adult feeding damage was high- est on Ce. solstitialis (yellow starthistle), Ce. cyanus 3.4. Relationship of host range to Ceratapion phylogeny (bachelor’s button) and Ce. diVusa Lam. (diVuse knapweed) (Fig. 3 and Table 1). Feeding rate on Ce. solstitialis may The genus Ceratapion contains 55 species and subspe- have been underestimated because (1) exposure was usually cies, divided among Wve subgenera: Acanephodous, Cerata- for 3 days on cut leaves versus for 5 days on intact plants pion, Clementiellus, Echinostroma, and Angustapion (Wanat, 1994). Most speciation occurred in Pliocene–Mio- cene, with the last events in the Pleistocene Glacial Period (including vicariance of sibling species). Species are distrib- uted almost throughout the entire Palearctic. In general, larvae and adults of species in the genus Ceratapion feed only on Asteraceae in the tribe Cardueae ( “Cynareae”) (Alonso-Zarazaga, 1990b). Genera recorded Das food plants are: Arctium, Carduus, Centaurea, Cirsium, Cynara, Echin- ops, Galactites, Onopordum, Silybum, and Xeranthemum. Hypotheses of the phylogenetic relationships among spe- cies of Ceratapion have been proposed by Alonso-Zarazaga (1990a) and Wanat (1994), based on morphological charac- ters (Fig. 4). Species in the subgenus Echinostroma, which includes C. basicorne, are associated with plants in the gen- Fig. 3. Relationship of mean number of adult feeding holes (ca. 1-mm2) to mean number of eggs on the diVerent test plant species under no-choice era Arctium, Carlina, Carthamus, Centaurea and Silybum conditions. Each point represents a diVerent test plant species (Alonso-Zarazaga, 1990a; Wanat, 1994). Larval host plants (YST Centaurea solstitialis, saZower Ca. tinctorius). of Ceratapion curtii (Wagner), the closest relative of D D L. Smith / Biological Control 41 (2007) 120–133 129
Table 2 Physiological suitability of diVerent varieties of saZower to oviposition and development of Ceratapion basicorne in a no-choice oviposition experiment SaZower No. of trials Adult feeding Eggs/day No. of trials Percentage of trials varietya oviposition holes/day development Adult feeding Eggs Internal plant Adults or holes present present damage present pupae present CW-88-OLb 23 10.7 0.6 10 91 61 50 50 CW-1221 16 16.2 0.4 16 44 63 31 31 CW-4440 16 9.1 0.5 15 38 63 40 40 Gilac 10 7.4 0.4 — 80 80 — — Hartmand 7 — 0.3 7 — 43 43 43 S-345-OL 6 14.8 0.8 6 100 67 50 33 S-400d 2 — 0.3 2 — 100 50 0 S-518-OL 10 8.4 0.4 10 90 50 40 30 S-541d 10 — 0.4 10 — 50 50 50 a Seed producers: CW, CalWest; S, SeedTec; OL, high oleic oil content. b Cut leaves in vials were used in 12 trials of CW-88, for which no development data are available. c No development data are available because plants died during malfunction of cooling system. d Adult feeding holes were not counted.
vulgaris (Ehret, 1983) as hosts for this species may be mis- taken. Ceratapion scalptum (Mulsant and Rey), which is also in the same subgenus, has one subspecies that develops on Carthamus and another on Silybum. Thus, each of the species or subspecies in the subgenus Echinostroma appear to develop only on plants within a genus. The historical restriction of evolutionary radiation of species within the genus Ceratapion to host plants within the Cardueae, and of species within the subgenus Echinostroma to a few gen- era within the Cardueae, suggests that C. basicorne is not likely to ever adapt to host plants outside this tribe. Inter- estingly, the two species that attack crops, Cer. scalptum (Mulsant and Rey) on saZower and Ceratapion damryi (Desbrochers) on artichoke (Cy. scolymus), are very speciWc and have never been reported to develop on Ce. solstitialis or Ce. cyanus. So, conversely, it is not surprising that C. basicorne, which is speciWc to the latter species, does not develop on either of the former species, at least under Weld conditions (Smith et al., 2006). The current theories on the phylogeny of species within the tribe Cardueae (Bremer, 1994; Susanna et al., 1995; Garcia-Jacas et al., 2002; Funk et al., 2005) and the genus Ceratapion (Alonso-Zarazaga, 1990a; Wanat, 1994) sug- gest that there is not an overall one-to-one pattern of Cer- atapion species coevolving with Cardueae species (Fig. 4). Fig. 4. Phylogenetic relationships among species and subgenera in the For example, Ceratapion onopordi appears to be relatively genus Ceratapion are after Alonso-Zarazaga (1990a) and Wanat (1994). Larval host records are from both authors and Balciunas (unpublished polyphagous, being reported from hosts in six genera from data). Hosts of C. curtii, C. armatum, C. dentirostre and C. uniseriatum are both the Centaureinae and Carduinae (Alonso-Zarazaga, unknown. All host plants are in the tribe Cardueae, and subtribe assign- 1990a; Wanat, 1994). The two Cer. scalptum subspecies ments are from Funk et al. (2005). (YST, Ce. solstitialis; “ƒ”, other Card- attack diVerent genera in diVerent subtribes (Carthamus ueae species; “?”, uncertain host plant). spp. [Centaureinae] and Silybum marianum [Carduinae]), suggesting taxonomically how far a species in this group C. basicorne, are unknown. Reported hosts of the next clos- can jump when adopting a new host. However, most of the est relative, Ceratapion penetrans (Germar), which has three species in the subgenera Echinostroma, Clementiellus and subspecies, are: Centaurea rhenana [ stoebe, maculosa, Acanephodus, for which host plants are known, use hosts D D paniculata], Centaurea jacea, Ce. cyanus, Ce. diVusa, Cen- in the Centaureinae (especially Centaurea and Carthamus D taurea nigra, Centaurea scabiosa, and Ce. solstitialis species); however, Silybum is in the Carduinae. Species in (Alonso-Zarazaga, 1990a; Wanat, 1994; Balciunas unpub- the subgenus Ceratapion are associated with Carduinae lished data). Older reports of Arctium lappa and Carlina (Carduus, Cirsium, Cynara, and Onopordum), and those in 130 L. Smith / Biological Control 41 (2007) 120–133 the subgenus Angustapion are generally associated with conducted at sites with natural populations of C. basicorne more basal taxa of the Cardueae (Echinops, Xeranthemum), in Turkey showed no larval development on saZower by but one species is associated with Ce. scabiosa. C. basicorne (Smith et al., 2006). However, three other Although all Ceratapion species are restricted to plants insects did develop on saZower: Cer. scalptum, Ceratapion in the tribe Cardueae, they vary in their degree of host plant orientale, and Ceratapion onopordi. Therefore, if C. basi- speciWcity. Because all species within the subgenus Echi- corne is approved for release, it will be important to cor- nostroma are only known to develop on plants in the Cent- rectly identify all specimens to prevent accidental aureinae and Carduinae, it appears that C. basicorne and its introduction of any of these species. Taxonomic keys with recent ancestors have been specializing on these host plants detailed illustrations have been developed to assist proper for a long time. This suggests that host plant speciWcity is identiWcation of C. basicorne (J.K. Balciunas and B.A. deeply ingrained and that the insect is not likely to drasti- Korotyaev, unpublished manuscript). cally change its host range. Thus, it appears that if C. basi- Centaurea cyanus (bachelor’s button) is at risk of adult corne were to adopt a new host after being released in feeding, oviposition and larval damage. This plant has pre- North America, it would most likely be a close relative of viously been reported as a host of C. basicorne in its native Ce. solstitialis and Ce. cyanus. The closest native species are range in Eurasia, but the frequency of such attack has not Ce. americana and Ce. rothrockii, but they are so distantly been studied. The plant is both an ornamental and an inva- related as to be considered in a diVerent genus (Plectoceph- sive weed in parts of North America. The developing larva alus), and they were not able to sustain larval development causes a small swelling of the stem at the base of the petiole in our no-choice experiments. Therefore, it seems improba- down which it tunneled. Although this may cause cosmetic ble that the insect could adapt to developing on any native damage to the ornamental, it is not known how frequently North American species in the foreseeable future. this may occur, especially when the plant is grown as an intensively managed monoculture. Because this plant is an 4. Conclusions invasive weed in some regions of the western US, damage to it in rangeland habitats would be beneWcial. The no-choice results indicate that no plant species out- W side the subtribe Centaureinae are at risk of signi cant lar- Acknowledgments val damage. Although adult feeding on foliage and oviposition occurred on many nontarget plants under no- I thank M. Pitcairn, P. Akers and B. Villegas (CDFA); J. choice conditions, they were at much lower rates than on Sigg and D. Dibor (California Native Plant Soc.); Bruce Ce. solstitialis, Ce. cyanus and Ce. diVusa. Under choice Baldwin (U.C. Berkeley); J. LittleWeld (Montana St. U.) and conditions, the nontarget attack rates would be expected to W.L. Bruckart (USDA-ARS) for assistance preparing the be lower. Because C. basicorne is synovigenic, and must host plant test list. Test plant seeds were obtained with the feed to continue producing eggs, absence of its preferred assistance of M. Pitcairn, D. Woods, P. Akers, B. Villegas, host plant would probably reduce egg production and con- and C. Pirosko (CDFA), R. Deering (U.C. Davis), P.J. sequently the risk of oviposition on nontarget plants. The GriYn (Siskiyou County), A. Yost (US Forest Service), H. oviposition rates that we observed on nontarget plants are Forbes (U.C. Berkeley), J. Herr (USDA-ARS), and S. probably elevated because of feeding on Ce. solstitialis Edwards (East Bay Regional Park District). M. Cristofaro prior to exposure to each nontarget test plant. Nontarget and C. Tronci (ENEA C.R. Casaccia, Italy) discovered sites plants that supported oviposition and larval development in Turkey and helped me collect C. basicorne for these stud- warrant further evaluation under choice conditions to fur- ies. Drs. J. Balciunas and S.L. Clement (USDA-ARS) pro- ther assess the degree to which they are at risk. These vided useful advice for conducting this research and Z include the two cultivated species: Ca. tinctorius (sa ower) comments on the manuscript. California Department of and Ce. cyanus (bachelor’s button), and the native North Transportation provided partial funding for this research. American species: Ce. americana, Ce. rothrockii, Ci. lon- My assistants D. Boughter, K.J. Baxter, A.E. Drew, M.J. cholepis and S. americana. Larval damage to Acroptilon Kabler, R. Chang and M.I. Wibawa helped obtain and repens, Cn. benedictus, Cr. vulgaris and the other Centaurea grow test plants, maintain the insect colony and conduct species is acceptable because are all alien noxious weeds in laboratory experiments. Insects were identiWed by B.A. North America. Korotyaev (Russian Acad. Sci.), and E. Colonnelli (U. of Successful development of an insect on a crop in labora- Rome), and plants by G.F. Hrusa (CDFA). tory experiments is usually suYcient to discourage further evaluation of it as a biological control agent. However, the absence of Weld records of C. basicorne developing on References saZower, despite records of its close relative, Cer. scalptum, Alonso-Zarazaga, M.A., 1990a. Revision of the sub-genera Ceratapion S. on this plant, suggest that risk to saZower under Weld con- W Str. and Echinostroma Nov. of the genus Ceratapion Schilsky, 1901. ditions may be insigni cant. Only by conducting further Fragmenta Entomologica, Roma 22, 399–528. choice experiments under laboratory or Weld conditions can Alonso-Zarazaga, M.A., 1990b. Revision of the supraspeciWc taxa in the we improve our estimation of this risk. Field trials that were Palaearctic Apionidae Schoenherr, 1823 (Colepotera, Curculionoidea). L. Smith / Biological Control 41 (2007) 120–133 131
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