Post-release non-target monitoring of Mogulones cruciger, a biological control agent released to control Cynoglossum officinalein Canada
J.E. Andreas,1,2 M. Schwarzländer,1 H. Ding1 and S.D. Eigenbrode1
Summary Non-target effects of approved biological control agents have raised questions about the safety of biological control of weeds and resulted in an increased emphasis on monitoring and reporting of non-target effects as part of post-release assessments. This is particularly important in the case of the root-mining weevil Mogulones cruciger (Herbst), which was approved in Canada to control hound- stongue, Cynoglossum officinale L., but not in the United States because of concerns over its envi- ronmental safety. To address these concerns and the potential for non-target effects, we monitored co-occurring confamilial Boraginaceae species at six M. cruciger release sites in Alberta and British Columbia over two years. All four co-occurring species were attacked by the weevil to varying de- grees although attack was inconsistent between years and sites, and non-targets were mostly attacked to a lesser degree than houndstongue. There was a positive relationship between the probability of non-target attack and houndstongue attack rate by M. cruciger indicating potential spillovers and early evidence suggests non-target attack may be transitory. The comparison between the pre- and post-release evaluations and preliminary plant volatile, electroantennogram, and host-choice behav- iour data suggest that chemical ecology may provide an important tool in understanding an insect’s host-choice selection in pre-release host-specificity assessments.
Keywords: houndstongue, non-target effects, host-choice behaviour, chemical ecology
Introduction determine an insect species’ physiological and ecologi- cal host range, which is then used to predict an insect’s Examples of non-target effects have created widespread realized host range once released in the invaded range interest and concern through both the scientific and (Schaffner, 2001; van Klinken and Edwards, 2002). public communities about the environmental safety of Studies demonstrate that the physiological host range, biological weed control agents (Simberloff and Stiling, which can be reliably determined experimentally (e.g. 1996; Louda et al., 1997, 2003 a, b; Strong, 1997; Tho- Papaj and Rausher, 1983; Szentesi and Jermy, 1990; mas and Willis, 1998; Pemberton, 2000). The predicta- van Klinken, 2000; van Klinken and Heard, 2000), ap- bility of an agent’s host range is often at the center of the pears to be an effective criterion for identifying species debate. Conventional host-specificity tests are used to at risk of attack by introduced agents, since there is no example of an insect agent attacking a plant outside its physiological host range (Fowler et al., 2000; Pember- ton, 2000; van Klinken and Edwards, 2002). A species’ 1 Department of Plant, Soil, and Entomological Sciences, University of realized host range, however, is almost certainly nar- Idaho, Moscow, ID 83844-2339, USA. rower than its physiological host range, which is evi- 2 Washington State University, King County Extension, Suite 100, 200 Mill dent from the narrowing host range that is frequently Avenue South, Renton, WA 98057, USA. observed under increasingly natural testing condi- Corresponding author: J.E. Andreas
75 XII International Symposium on Biological Control of Weeds predict this have not been developed (Van Driesche et source begins to be depleted (Strong, 1997). In sensi- al., 2000; Schaffner, 2001; Hopper, 2001; and references tization/central excitation, acceptance thresholds for therein). Realized host ranges will be limited due to non-targets are lowered after contact with the true host phenological, ecological, and behavioural constraints. or in the presence of ambient volatile organic com- While phenological and ecological factors likely differ pounds emitted by the true host (Marohasy, 1996, 1998; among continents and habitats, behavioural factors are Withers and Barton Browne, 1998). Regardless of the inherent to the agent and could be examined as part of specific mechanism, these recorded non-target attacks improved pre-release assessment protocols. indicate a need to determine the risk that M. cruciger The host selection process of phytophagous insects poses to native species that are within the physiologi- typically progresses from host finding (dependent upon cal host range and within the potential range of the volatile and visual cues), through host examination weevil’s dispersal from target host populations. There- (dependent in addition on gustatory and tactile cues), fore, we explored the early stages of host-selection to host acceptance (oviposition or sustained feeding) behaviour and its underlying phytochemical basis to (Dethier, 1982; Miller and Strickler, 1984; Bernays determine the plant species likely to be colonized by and Chapman, 1994). Each stage is dependent upon M. cruciger. completion of the previous stage. Thus, in nature, host examination and acceptance, as evaluated in no-choice bioassays, cannot occur unless the insect arrives at the Materials and methods potential non-target host during the host-finding stage. Therefore, knowledge of the chemical basis for host- Study organisms finding behaviour might improve our ability to assess Houndstongue is a Eurasian herbaceous, faculta- whether a non-target plant species that can support the tive, short-lived perennial. Plants produce rosettes in development of a biocontrol agent would be at risk of the first year and typically reproduce in the second or attack in the field (Thomas and Willis, 1998; Heard, third year (Wesselingh et al., 1997). After sexual re- 2000; Schaffner, 2001). production, barbed nutlets are formed and dispersed The Mogulones cruciger Herbst, houndstongue via epizoochory (De Clerck-Floate, 1997). In Europe, (Cynoglossum officinale L.), system provides a prime the plant is found in sand dunes, roadsides, and open example of the importance of such testing. Mogu- woodlands (Tansley and Adamson, 1925; Tutin et al., lones cruciger is a root-feeding weevil that has been 1972; Hegi, 1975; Klinkhamer and de Jong, 1988). In released in Canada to control the noxious rangeland North America, this ruderal species colonizes disturbed weed, houndstongue. Release in the United States, areas, rangelands, pastures, and forests (Macoun, 1884; however, has been denied because of concerns about Upadhyaya and Cranston, 1991). its environmental safety. Previous host-specificity test- Mogulones cruciger is a root-feeding weevil native ing has demonstrated that M. cruciger’s physiological to central Europe. In spring, after hibernation, adults host range is fairly broad, but it has always shown a occur on above-ground plant parts, where they feed on strong preference for houndstongue (Jordan et al., leaves, mate, and oviposit into leaf petioles (Schwarz- 1993; De Clerck-Floate et al., 1996; De Clerck-Floate laender, 1997). Larvae hatch from eggs 7-10 days after and Schwarzlaender, 2002; Andreas, 2004). A recent oviposition and begin to mine down into the root crown study of six field sites in Canada found that M. cru- where they feed primarily in the vascular cylinder. Mo- ciger was utilizing four confamilial species growing gulones cruciger has three instars and pupates in the sympatrically with houndstongue (Andreas, 2004). The surrounding soil (Schwarzlaender, 1997). In late sum- attacked Boraginaceae species are Cryptantha spicu- mer, adults emerge and begin feeding on houndstongue lifera (Eastw.) Payson, Hackelia floribunda (Lehm.) rosettes between July and October. Oviposition begins I.M. Johnston, Lappula squarrosa (Retz.) Dumort and in late August until temperatures cool and oviposition Lithospermum ruderale Dougl. ex Lehm.. The first sites become unavailable. Adult weevils hibernate in three species are within the known physiological host leaf litter (Schwarzlaender, 1997; De Clerk-Floate and range of M. cruciger (De Clerck-Floate et al., 1996; Schwarzlaender, 2002). Mogulones cruciger often has De Clerck-Floate and Schwarzlaender, 2002; Andreas, overlapping generations. As a consequence, eggs and 2004) while the latter species has not been sufficiently larvae can be found in houndstongue roots and leaf tested because its cultivation has not been successful. petioles at most times of the year. Because M. cruciger is known to prefer houndstongue The native North American Boraginaceae species (Jordan et al., 1993; De Clerck-Floate et al., 1996; De Hackelia venusta (Piper) St. John was chosen as a non- Clerck-Floate and Schwarzlaender, 2002; Andreas, target species in this study because it is listed as endan- 2004), we hypothesize that these non-target attacks re- gered by the United States Fish and Wildlife Service sult from ‘spillover’, ‘sensitization/central excitation’ (USFWS) and laboratory tests indicated that M. cruciger effects or both. In spillover, high population densities on is capable of partial larval development on this species the target result in some insects colonizing non-targets (Andreas, 2004). Its distribution is limited to one small due to random dispersal especially after the target re- remaining population of approximately 150 individuals
76 Post-release non-target monitoring of Mogulones cruciger in a ponderosa pine (Pinus ponderosa P. & C. Lawson) tative coefficient, Bray-Curtis, commonly used for eco- and Douglas fir Psuedotsuga( menziesii (Mirbel) Franco) logical studies (Southwood and Henderson, 2000). clearing in Chelan County, Washington, just south of the Canada/U.S. border (Center for Plant Conservation, EAG and GC/EAD/FID 2004). Fire suppression has been an important factor in the reduction of H. venusta populations (Center for EAG assay methods were modified from those of Plant Conservation, 2004). Cryptantha spiculifera and Evans and Allen-Williams (1992). Recordings were Hackelia floribunda were selected for this experiment taken from single antennae on partially excised heads because they co-occur with houndstongue at field sites using sharpened stainless steel electrodes coated with in Canada (Kartesz, 1999) and were monitored in a an electrolyte gel. To measure antennal response to post-release open field study (Andreas, 2004). the total blend of VOCs from each species, samples of headspace volatile that had been standardized based on plant dry weight were applied in solvent to a filter Olfactometer bioassay paper strip and delivered to the antenna in a puff of pre- Our methods for an olfactometer bioassay and for filtered air. Antennal response to VOCs of each species electroantennogram (EAG) and GC/EAD have been was standardized on the basis of a response to a single adapted from those proven effective for a close relative concentration of linalool. Responses from ten weevils of M. cruciger, the cabbage seed weevil, Ceutorhyn- (three males and seven females) were obtained from chus obstrictus Marsham (C. assimilis Payk.) (Evans H. floribunda. and Allen-Williams, 1992; Evans and Bergeron, 1994). Gas chromatography using EAG and flame ioniza- The olfactometer was a four-arm configuration (Vet tion detectors (GC/EAD/FID) (Bjostad, 1998) can help et al., 1983) (Syntech, Hilversham, The Netherlands). identify the components of potential host VOCs that We conducted preliminary 3-way choice bioassays in are most important for observed behavioural responses. the olfactometer with air streams directed over intact A 1-µl sample of headspace VOCs dissolved in methy- plants of H. floribunda, C. spiculifera, houndstongue, lene chloride was injected onto a Shimadzu GC17-A and a blank (carrying humidified air). Intake air for all GC (Shimadzu Corp., Kyoto Japan) fitted with a column treatments was prefiltered through activated charcoal. splitter delivering approximately half the column efflu- Airflow was balanced at 300 ml/min through each arm ent to a flame ionization detector and half via a heated of the olfactometer. transfer line to the electroantennograph (Syntech, Hil- Illumination was with overhead fluorescent fixtures, versam, The Netherlands) with the insect preparation. diffused through a white, translucent plastic pail inverted Temperature programme and column specifications over the olfactometer. The lens of a video camera was were conducted as described in Eigenbrode et al. inserted through the top center of the pail to permit (2002). Antennal responses (expressed as mV of depo continuous recording of weevil behaviour during the larization) were standardized based on an external bioassay. Twelve female weevils (having fed previously sample of linalool injected through the GC/FID/EAD on houndstongue but not having encountered other between each injected sample of headspace VOCs. One hosts) were tested simultaneously in a single run. The female was tested. weevils were placed at the center of the olfactometer and their positions and movements recorded on vid- Results eotape for 30 minutes for later review and recording using a computer program (Noldus Observer, Wagenin- Olfactometer bioassay gen, The Netherlands). Relative attractiveness of each The results from the behavioural bioassay (Figure 1) source was quantified in terms of the proportion of time indicate that M. cruciger females responded to host spent in the respective quadrants of the olfactometer. VOCs in the olfactometer. The weevils spent the small- est proportion of time in the H. floribunda quadrant of VOC analysis the olfactometer, approximately 20% of their time in C. spiculifera and the no-plant control quadrants, and Volatile organic compounds (VOCs) were trapped the greatest amount of time (approximately 40 %) in the from the headspace of houndstongue, H. venusta, houndstongue quadrant (One-way ANOVA; F = 4.71, H. floribunda, and C. spiculifera with a volatile col- P = 0.006). lection apparatus (Analytical Research Systems, Inc., Gainesville, FL) following methods modified from Ei- genbrode et al. (2002). The headspace VOC profiles VOC analysis were compared for similarity based on the number of Of the 44 VOCs detected in headspace of the four shared compounds detected and by calculating similar- species, six were shared by all and six were unique to ity coefficients based on occurrence and relative abun- houndstongue. Hackelia venusta headspace had the dance of each component. We employed two binary most compounds in common with houndstongue, fol- coefficients, Jaccard’s and Sørensen’s, and one quanti- lowed by C. spiculifera and then H. floribunda. All
77 XII International Symposium on Biological Control of Weeds
Control
C. spiculifera
H. floribunda
C. officinale
0 10 20 30 40 50 60
Average % time in quadrant
Figure 1. Response of Mogulones cruciger females to volatile organic compounds (VOCs) from houndstongue (Cynoglos- sum officinale), two non-target plant species (Cryptantha spiculifera and Hackelia floribunda) and a blank (car- rying humidified air) in a four-arm olfactometer. Values are percentage of time in extremity of the test arm with stimulus (n=12). three similarity coefficients follow a similar trend, with (Figure 2) (2-way ANOVA P values = 0.08, 0.16 and H. venusta most similar to houndstongue, followed by 0.28 for species, sex and interaction, respectively). GC/ C. spiculifera and then H. floribunda (Table 1). FID/EAD: The combined FID/EAD trace resulting from chromatography of H. venusta volatiles showed that EAG and GC/FID/EAD an individual M. cruciger female antenna responded to a subset of the VOCs present. EAG: Antennal preparations exhibited depolariza- tion (i.e. peaks in impulses indicate excitation to par- Discussion ticular compounds) in response to puffs of extracted headspace VOCs and this response tended to be Despite the recognized need to include host-choice stronger for houndstongue compared to H. floribunda behaviour and chemical ecology in host-range inves-
Table 1. Measures of similarity for headspace volatile profiles of Hackelia venusta, Cryptantha spiculifera and Hackelia floribunda, as compared with houndstongue (Cynoglossum officinale) headspace volatiles. Species compared to C. officinale Shared components Sørensena Jaccardb Bray-Curtisc H. venusta 21 0.84 0.72 0.26
C. spiculifera 11 0.41 0.26 0.23 H. floribunda 9 0.36 0.22 0.22 a The Sørensen coefficient is binary in that it is based on the presence/absence of each compound. It is calculated as: Cs= 2a/(2a + b + c) in which a = the number of compounds held in common, b = the number of compounds unique to houndstongue and c = the number of com- pounds unique to the species compared to houndstongue. It ranges from zero for non-overlapping profiles to one for identical profiles. b Jaccard similarity is also binary. It is calculated as: Cj= a/(a + b + c) and also ranges from zero to one. c The Bray-Curtis coefficient is a quantitative index of similarity that takes into account abundance of the components. It is calculated as
Cn = 2jN/(aN + bN), in which jN = the sum of lesser values for those compounds shared between species and aN and bN are the sum of total values for each species. The coefficient scales from near one for equivalent profiles to zero.
78 Post-release non-target monitoring of Mogulones cruciger
C. officinale male H. floribunda
C. officinale female H. floribunda
0 0.5 1 1.5 2 2.5 Standardized EAG response
Figure 2. EAG responses by male and female Mogulones cruciger to puffs of total VOC from its host, houndstongue (Cynoglossum officinale) and a non-target species, Hackelia floribunda (response standardized relative to lin- alool), (n= three males and seven females).
tigations of candidate weed biocontrol agents (Briese, 2003), the response by M. cruciger to these alkaloids 2005; Sheppard et al., 2005), few studies have attempted and other gustatory cues of target and non-target plants this (Heard, 2000; Hopper, 2001; Schaffner, 2001). Our should be examined. data provide an illustration of the type of information The basis of apparent M. cruciger discrimination that can be obtained with behavioural and chemical among odours of houndstongue and non-target species ecological experiments. remains unknown. Some insects apparently integrate Our olfactometer results indicate greater responsive- information from the VOC blend of their host plants ness of M. cruciger to odour cues from houndstongue (Roseland et al., 1992), while others, including a close than to the tested non-target species. We did not de- relative of M. cruciger, the cabbage seedpod weevil, tect directed upwind movement by the weevils in this C. obstrictus, use a few specific VOCs to orient to bioassay (data not shown), indicating that M. cruciger potential hosts (Smart and Blight, 1997). The VOC pro- dispersal among potential hosts could be undirected files ofH. floribunda, H. venusta and C. spiculifera dif- but that host VOCs can stimulate arrested or restricted fer from houndstongue. Hackelia floribunda VOCs are searching behaviour on or near the host. Our bioassay the least similar to those of houndstongue. Among the has some limitations for fully understanding relevant three tested non-target species, the VOCs of only two, host-selection responses to target and non-target VOCs C. spiculifera and H. floribunda, were subjected to the in the field. We studied walking behaviour, but flying is olfactometer bioassay, where H. floribunda was once likely also important in host location. The three-odour again less preferred. If specific compounds are required choices we offered may not represent the situation en- for host acceptance, they may be present in hound- countered from isolated non-target plants in the field. stongue but lacking in H. floribunda. Moreover, since Further testing is required to address these concerns. H. floribunda appeared repellent in our tests, VOCs Our focus on VOC isolates behaviour during early present in its profile, but lacking in houndstongue’s stages of host selection. After contact with potential (i.e. benzaldehyde, undecane and dodecane) are candi- hosts, appropriate tactile and gustatory cues are re- date repellents. On the other hand, the weevils may in- quired for host acceptance. Further study of the so- tegrate information from several cues during response called ‘examination’ phase of host selection is needed to the VOC blends of potential hosts. For determining for a more complete understanding of factors deter- host-range tendencies in pre-release studies, it may not mining the realized host ranges of candidate biological be necessary to determine these mechanisms. Our re- control agents. For example, M. cruciger may respond sult indicates that it is feasible to include responses to to detectable pyrrolizidine alkaloids on the plant sur- cues used during host finding in assessing risks of colo- face. Although recent work failed to find that these nization of non-targets as part of pre-release studies. alkaloids could explain oviposition preference by an- Our results with M. cruciger indicate that H. floribunda other specialist insect, the cinnabar moth, Tyria jaco- may be at less risk than the other species tested here baeae L. (Lepidoptera: Arctiidae) (Macel and Vrieling, because the weevils are not attracted and possibly even
79 XII International Symposium on Biological Control of Weeds repelled by this plant, whereas H. venusta may be at ods similar to those presented here, behavioural and greater risk because of the similarity of its VOC pattern electrophysiological bioassays could form the basis to that of houndstongue. of risk-assessment studies. Specifically, the release of The weevil’s response to several components in the M. cruciger into North America provides an opportunity GC/FID/EAD test may help determine the basis of its to compare its realized host range with host-selection host selection behaviour, as these volatiles are candi- predictions based on phytochemical and behavioural date components whose presence could attract the wee- studies. vil to a non-target host that produces them. However, given that only one weevil species and one plant spe- Acknowledgements cies was used, the results presented here simply re- vealed that M. cruciger can detect plant stimuli. The authors thank Brad Harmon for lab assistance, the Our approach could help elucidate the risk M. cru- Idaho Agricultural Experiment Station, Terry Miller ciger poses to non-targets near (e.g. Andreas, 2004) for the use of the quarantine at Washington State and remote from colonized houndstongue infesta- University and the editors for manuscript revisions. tions. In the former setting, weevils dispersing from Dr. Sarah Reichard kindly provided the H. venusta houndstongue into the environment will be influenced plant material. Travel funds for the presenting author by their responsiveness to VOCs and other long- kindly provided by the United States Forest Service distance cues from potential hosts. If there is little or no and Washington State University. response to non-target cues (as we may have found for two non-targets), the risk of non-target attack should be reduced. Spillover effects or central excitation/sen- References sitization potentially alter this assessment. If weevils Andreas, J.E. (2004) Non-target effects of Mogulones cru- are sufficiently abundant and mobile, regardless of ciger Herbst (Coleoptera: Curculionidae), a biocontrol responses to VOC from potential hosts, they may en- agent released to control houndstongue in Canada. MSc counter and colonize the non-targets (spillover). If prior thesis, Department of Plant, Soil and Entomological Sci- contact with hosts or host odours lowers acceptability ences, University of Idaho, Moscow, ID. thresholds to subsequently encountered plants (central Bernays, E.A. and Chapman, R.F. (1994) Host plant selec- excitation/sensitization), temporary non-target attack tion by phytophagous insects. Chapman and Hall, New could be facilitated. Longer-distance colonization of York, NY. non-targets is also potentially mediated by VOCs. Our Bjostad, L.B. (1998) Electrophysiological methods. In: Millar, J. and Phelan L. (eds) Methods in Chemical Ecology. Klu- result suggests that, while walking, weevil colonization wer Academic, Dordrecht, The Netherlands, pp. 339–376. of the two non-targets we tested are not increased due Briese, D.T., Sheppard, A.W.and Reifenberg, J.M. (1995) to their released VOCs. Open-field host specificity testing for potential biological Our approach could help assess risks of attack of control agents of Onopordum thistles. Biological Control other sensitive non-targets by M. cruciger. Three of the 5, 158–166. five endangered Boraginaceae species in the United Briese, D.T. (1999) Open field host-specificity tests: is “natu- States are within the weevil’s physiological host range. ral” good enough for risk assessment? In: Wither, T.M., Complete development was possible on Plagiobothrys Barton Browne, L. and Stanley, J. (eds) Host specificity hirtus (Greene) I.M. Johnston and Amsinckia grandi- testing in Australasia: towards improved assays for bio- flora (Kleeb. ex Gray) Kleeb. ex Greene and partial logical control. CRC for Tropical Pest Management, Bris- development occurred on H. venusta (Andreas, 2004). bane, Australia, pp. 44–59. Briese, D.T. (2005) Translating host-specificity test results The two remaining confamilial species that are listed as into the real world: The need to harmonize the yin and endangered in the United States, Cryptantha crassipes yang of current testing procedures. Biological Control 35, I.M. Johnston and Plagiobothrys strictus (Greene) I.M. 208–214. Johnston were not tested. VOC profiles of these species Center for Plant Conservation (2004). CPC National collec- could be tested to assess weevil attraction. H. venusta tion plant profile. http://ridgwaydb.mobot.org/cpcweb/ VOC profiles are more similar to houndstongue than CPC_ViewProfile.asp?CPCNum=2109 others we have tested and are potentially attractive or Clement, S.L. and Cristofaro, M. (1995) Open-field tests in arrestant for M. cruciger. host-specificity determination of insects for biological Comparisons of realized and predicted host ranges control of weeds. Biocontrol Science and Technology 5, from pre-release studies (Cullen, 1990; Briese et al., 395–406. 1995; Clement and Cristofaro, 1995; Briese, 1999) can Cullen, J.M. (1990) Current problems in host specificity screen- ing In: Delfosse, E.S. (ed.) Proceedings of the VII Interna- evaluate the soundness of prior risk-assessment proce- tional Symposium on Biological Control of Weeds. Ministry dures (Ewel et al., 1999; Hopper, 2001). Selection be- for Agriculture and Forestry, Rome, Italy, pp. 27–36. haviour and its phytochemical basis could, in contrast, De Clerck-Floate, R., Schroeder, D., and Schwarzlaender, M. greatly improve predictions of eventual host ranges of (1996) Supplemental information to the petition (Can-93-4 released agents (Marohasy, 1998; Thomas and Willis, and TAG 93-06) to release Ceutorhynchus (Mogulones) 1998; Heard, 2000; Schaffner, 2001). By using meth- cruciger for the biological control of hound’s-tongue
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