Agapeta Zoegana L

Biological Control 26 (2003) 270–278 www.elsevier.com/locate/ybcon

Plant size preference of Agapeta zoegana L. (Lepidoptera: Tortricidae), a root-feeding biological control agent of spotted knapweed

L. Smitha,* and J.M. Storyb

a USDA-ARS, Western Regional Research Center, 800 Buchanan Street, Albany, CA 94710, USA b Montana Agricultural Experiment Station, Western Agricultural Research Center, Corvallis, MT 59828, USA

Received 26 December 2001; accepted 22 October 2002

Abstract

Agapeta zoegana L. (Lepidoptera: Tortricidae) is an oligophagous herbivore that was introduced to North America as a biological control agent of spotted knapweed, Centaurea stoebe L. subsp. micranthos (Gugler) Hayek (often called Centaurea maculosa Lam.). Spotted knapweed is a perennial plant that usually increases in size each year. A previous field study reported that more larvae were found on larger plants and that infested plants tended to be larger than uninfested ones. Precisely quantifying the size- specific attack rate can help us model the impact of this agent on the weed population and better understand the interspecific interactions to improve the effectiveness of biological control. Field data were analyzed to determine the relative preference of attack for each size class of the host plant. Plants were classified based on root diameter at 2 cm below the root crown. Although small plants (<3 mm root diameter) were more abundant in the field population, the highest infestation rates occurred in large plants. ChessonÕs electivity index was generally positive for root diameters >3.5 mm, indicating preferential attack of large plants. Because of its host-size preference, A. zoegana is expected to primarily affect large plants, which is contrary to previous expectations. Quantifying the insectÕs direct impact is a difficult challenge, which may require several field seasons of measuring accumulated damage on individual plants. In order to complement the biological control agents already established, foreign exploration should focus on finding an agent that attacks young knapweed plants. These results also indicate that the efficiency of sampling roots in the field to detect the presence of A. zoegana can be improved by choosing only the largest plants. Published by Elsevier Science (USA).

Keywords: Biological control; Herbivore; Preference; Spotted knapweed

1. Introduction suspected to have arrived in North America as a con- taminant of alfalfa seed from Asia Minor, especially Spotted knapweed is an important rangeland weed in Turkmenistan, or from Germany (Maddox, 1982; the western United States (Sheley et al., 1998, 1999) that Ochsmann, 2000). Twelve species of introduced insect has been a target for biological control (Lang et al., biological control agents of this weed have become es- 2000; Schroeder, 1985; Smith, 2001; Story, 1995). This tablished in North America (Rees et al., 1996), and some plant has often been reported in North America as are now being evaluated in the ﬁeld for impact (Smith, Centaurea maculosa Lam. (Asteraceae), but should more 2001). properly be called Centaurea stoebe L. subsp. micranthos The root-feeding moth, Agapeta zoegana L. (Lepi- (Gugler) Hayek (Ochsmann, 2000) because it is peren- doptera: Tortricidae), was introduced from Austria and nial, polycarpic, and tetraploid, whereas C. maculosa is Hungary (Story et al., 1991) and has become well es- biennial, monocarpic, and diploid. Spotted knapweed is tablished in western Montana. Several attempts have been made to measure its impact on spotted knapweed * Corresponding author. Fax: +510-559-5737. plants (Callaway et al., 1999; Clark et al., 2001; Muuller-€ E-mail address: [email protected] (L. Smith). Schaarer,€ 1991; Steinger and Muuller,€ 1992; Story et al.,

1049-9644/02/$ - see front matter. Published by Elsevier Science (USA). doi:10.1016/S1049-9644(02)00169-X L. Smith, J.M. Story / Biological Control 26 (2003) 270–278 271

2000). However, impact of this agent has been difficult Although there is a substantial literature on host size to measure, even in laboratory studies (Muuller,€ 1989). preference for insect parasitoids and predators (e.g., Also, it has been suggested that mycorrhizal interactions Godfray, 1994; Jervis and Kidd, 1996; Smith, 1993), between spotted knapweed and neighboring grasses little has been reported for herbivores. However, some could cause this agent to harm competing perennial herbivorous insects have been shown to exercise size grasses more than spotted knapweed, on which it feeds preference when ovipositing in flowers (Fondriest and (Callaway et al., 1999; Marler et al., 1999). Nevertheless, Price, 1996), fruits (Messina, 1990), stems (Pires and Story et al. (2000) measured a 43% reduction in above Price, 2000), leaves (Stuart and Sridhar, 1998), or plants ground biomass per plant and a 43% reduction in the (Langan et al., 2001; Tinney et al., 1998). There is some number of capitula per plant by comparing field plots variation in the literature regarding usage of the terms that had high versus low infestation rates of this agent. ‘‘preference’’ and ‘‘electivity’’ (Singer, 2000), but here we However, rosette densities did not decrease during the follow definitions used by Manly et al. (1972) and 2.5 year study. Chesson (1983). Preference reflects the relative proba- Measuring impact of this agent is difficult because the bility that a host of a particular type is attacked when all direct damage to mature plants generally appears to be types are equally abundant. Preference can include dif- sublethal (Muuller,€ 1989). The plant is perennial and has ferent components, such as active searching behavior by the potential to recover from damage. Environmental ovipositing females, ability of larvae to enter the host, variation and the complexities of ecological interactions and of larvae to survive until the time of sampling. In a make it difficult to measure impact on individuals in field study, the relative proportion of host plants of a field studies (e.g., reduction of seed production or sur- given size that are infested is a function of the relative vivorship). Reduction of knapweed plant densities can abundance of plants of that size and the preference of reduce plant competition causing an increase in size and the insect for that plant size. The electivity index fecundity of individual plants (Myers et al., 1990). (Chesson, 1983) adjusts for unequal numbers of plants Furthermore, seeds buried in the soil can persist up to 7 of the different size classes. Thus, the electivity index years (Davis et al., 1993), causing a lag before reduction provides an estimate of the relative preference for each of seed production affects seedling recruitment. Multi- host plant size class that is unbiased by the relative year, field population studies are confounded by dis- abundance of the size classes. persal of agents into check sites or by the effects of cages The purpose of this study is to analyze field data from or insecticides used to exclude them (Luck et al., 1999). Story et al. (2000) to describe the host plant size pref- The more we can learn about the components of the erence of spotted knapweed plants attacked by A. zo- plant–insect interactions, the better we can understand egana. Size preference is important because if insects the impact of the biological control agents. Efforts to preferentially attack plants of a particular size (e.g., model these interactions have begun to provide a basis small plants) then the direct impact will be limited to for understanding the effects of these interactions on such plants. Understanding which plants are most likely population dynamics (Cloutier and Watson, 1990; to be infested will improve our ability to: (1) monitor Jacobs and Sheley, 1998; Myers and Risley, 2000). direct impact and (2) predict the ultimate impact on Relatively little is known about the field ecology of A. population demographics of the target weed. zoegana. Adults live only a few days, and females ovi- posit on spotted knapweed leaves and stems and on nearby vegetation (Muuller€ et al., 1988). Larvae attack 2. Materials and methods the root crown, initially feed on the root cortex, and eventually burrow into the center of the root, especially 2.1. Experimental procedures on small plants. They overwinter as small larvae, com- plete development the following spring, and emerge as The study was conducted in an 8-ha, level field on the adults in summer. Story et al. (2000) discovered in a field Teller Wildlife Refuge near Corvallis, Montana (see study that the number of larvae per root was not sig- Story et al., 2000 for more description). The field was an nificantly different from that predicted by random at- abandoned pasture dominated by spotted knapweed tack (binomial model), suggesting that there was no (59% of vegetation cover), grass species (35%), and other tendency for the moth to avoid plants already infested. forbs (6%). Spotted knapweed density was 383 24 (SE) However, there was a positive relationship between the plants/m2 (excluding seedlings). A total of 788 and 2080 number of larvae per infested plant and root diameter, A. zoegana adults were released at the site in 1988 and regardless of whether the plant was in bolted or rosette 1989. All the knapweed plants were collected in each of stage. These results suggest that the insect may prefer to 16 randomly placed plots (50 50 cm) during each of attack large plants, but no data were presented regard- five periods: June and October of 1992 and 1993, and in ing the proportion of plants attacked for different plant June 1994 (i.e., total of 80 plots) to study establishment sizes. and impact of the insect on the knapweed population 272 L. Smith, J.M. Story / Biological Control 26 (2003) 270–278

(Story et al., 2000). Data were collected on the root those >8 mm were combined into one class. The average diameter (measured 2 cm below the root crown) and number of plants in a class was 134 (range: 32–374). infestation by A. zoegana larvae of 7347 roots (see also Story et al., 2000). Root diameter of spotted knapweed 2.3. Statistical analysis is correlated with plant age and many other measures of plant size, including aboveground biomass, numbers of The diﬀerence in distribution patterns of available seedheads and probability of bolting (Story et al., 2001). and infested host plants was tested by a two-tailed Smirnov test, and the Cox and Stuart test was used for 2.2. Analysis of preference trends (Conover, 1980).

We calculated the following parameters describing host-size preference that are based on formulas devel- 3. Results and discussion oped by Chesson (1983). The probability that the next food item attacked is in size class i is The size distribution of spotted knapweed plants changed after spring 1993, when there were relatively aini Pi ¼ P ; ð1Þ fewer small plants (Fig. 1; Smirnov tests: P < 0:01 for m a n j¼1 j j any of the first three dates versus any of the last two dates and P > 0:2 for all other pair-wise comparisons). where n is the number of hosts available in size class i, m i Nevertheless, plants with root diameters of 1–1.5 mm is the number of size classes. This is a calculation of the were always the most abundant size class. Median root proportion of all host plants infested that are in size diameter was 2.0, 2.1, 2.0, 2.45, and 2.4 mm in spring class i. The a can be interpreted as the proportion of the i 1992, fall 1992, spring 1993, fall 1993, and spring 1994, total number of plants infested that is associated with respectively. The corresponding number of plants sam- each size class, and a has the range ½0; 1. The a can be i pled was 1240, 1303, 1911, 1724, and 1180. calculated, assuming no depletion of host plants during In general, more large plants were infested by A. the period of attack, by zoegana larvae than small ones (Fig. 2; Cox and Stuart ri=ni test, P > 0:3 for spring and fall 1992, P ¼ 0:03 for the a ¼ P ; ð2Þ i m other 3 dates). Median root diameter of infested plants ð j¼1 rj=njÞ was 3.7, 3.1, 4.6, 4.3, and 4.9 mm in spring 1992, fall where ni is the number of hosts available in size class i, 1992, spring 1993, fall 1993, and spring 1994, respec- and ri is the number of hosts infested. The equation can tively. The number of infested plants rose over the be modified to adjust for the depletion of host plants course of the study (199, 249, 247, 253, and 290) as did (e.g., when infested hosts are effectively eliminated the number of A. zoegana larvae collected (301, 383, 380, without replacement by ovipositional marking phero- 391, and 502). Infestation rate generally increased as a mone or plant death): function of root size (Fig. 3; Cox and Stuart test, P > 0:3 for fall 1992, P ¼ 0:03 for the other 4 dates). P lnððni0 À riÞ=ni0Þ ai ¼ m ; ð3Þ Infestation rate tended to level off above root diameter 4 lnððnj0 À rjÞ=nj0Þ j¼1 and 2.5 mm in the spring 1992 and fall 1992, respec- where ni0 is the number of hosts initially available in size tively, but continued to increase at higher root diameters class i. The electivity index: on the later three sample dates. It is possible that the change in relative infestation rate of large plants over ðmai À 1Þ ei ¼ ; ð4Þ time is related to the combination of the decreasing ððm À 2Þa þ 1Þ i relative abundance of small plants (Fig. 1) and increas- where m is the number of size classes, provides a more ing abundance of the insects (from 16% infestation in convenient parameter for describing preference. The spring 1992 to 25% in spring 1994; Story et al., 2001), electivity index is a calculation of the preference for class given that A. zoegana prefers to attack large plants (see i relative to the average of all other classes. It has the below). That is, when there are few insects and mainly range ½À1; þ1, where )1 corresponds to no hosts at- small plants, the probability of insects encountering tacked, +1 to all hosts attacked, and 0 to no preference. large plants will be low (the case in 1992). As large In the field study by Story et al. (2000), small plants plants become relatively more abundant and the insect were much more abundant than large plants, so we in- population increases, the probability of encountering creased the width of the root-diameter size classes for large plants rises, allowing the insects to exercise more diameters above 4 mm to increase the number of plants choice (the case in 1993–1994). in the higher size classes and to reduce variability (Fig. The distribution of infested plants (Fig. 2) differed 1). Class width was 0.5 mm for plants <4.0 mm diameter, from that of available plants (Fig. 1) on each sample date 1 mm for those <6 mm, 2 mm for those <8 mm, and all (Smirnov test, P < 0:01), indicating nonrandom attack L. Smith, J.M. Story / Biological Control 26 (2003) 270–278 273

Fig. 1. Size distribution of spotted knapweed at the study site, based on diameter of roots, measured 2 cm below the crown. with respect to root diameter size. The number of plants root diameter less than about 3.5 mm, although this of a given size class that are attacked is a function of their varied between 2.5 and 4 mm for the various sample relative abundance and the preference of the insect for dates, and was positive above these thresholds (Fig. 4). that size class. ChessonÕs (1983) electivity index is a useful On the last three sample dates, electivity varied approx- way to represent this preference, independent of the eﬀect imately linearly with root diameter, indicating highest of relative abundance of the diﬀerent host plant size preference for the biggest plants. In spring and fall 1992, classes. Electivity was generally negative for plants with plants in the largest size classes had lower electivity, 274 L. Smith, J.M. Story / Biological Control 26 (2003) 270–278

Fig. 2. Number of spotted knapweed plants infested by A. zoegana. possibly as a result of lower insect density and lower number of plants infested (Fig. 2) and the percentage of relative abundance of large plants (reducing the proba- plants infested (Fig. 3), respectively, so ﬁgures of Pi and bility that insects would encounter such plants). The in- ai distributions are not presented. sect evidently does not prefer to infest, or perhaps does It has been suggested that A. zoegana larvae can kill not survive well, on small plants, and was most fre- small spotted knapweed plants (Muuller-Sch€ aarer,€ 1991), quently found on large plants. The shapes of the distri- although hard data are lacking. Such mortality would butions of Pi and ai are nearly identical to those for cause a decrease in observed infestation rate of small L. Smith, J.M. Story / Biological Control 26 (2003) 270–278 275

Fig. 3. Percentage of spotted knapweed plants infested by A. zoegana. plants (e.g., root diameter < 2 mm) between fall and the large plants would presumably be more tolerant of following spring. This happened between fall 1992 and damage than small ones, more larvae are found infesting spring 1993, but not between fall 1993 and spring 1994 large plants (Story et al., 2000), which may well increase (Smirnov tests: P < 0:01 and P > 0:2, respectively). So, their impact. our results are equivocal regarding this hypothesis. This At this study site, spotted knapweed plants did not type of mortality is diﬃcult to measure in the ﬁeld but bolt until they were about 3 years old (Story et al., could be studied in controlled experiments. Although 2000), at which time they had a root diameter of 3 mm 276 L. Smith, J.M. Story / Biological Control 26 (2003) 270–278

Fig. 4. Electivity index ðei)ofA. zoegana for diﬀerent sizes of spotted knapweed ()1, no hosts attacked; 0, no preference; +1, all hosts attacked).

(Story et al., 2001). Electivity was negative for plants immediate reduction of seed production when potted with root diameters less than 2.5–4 mm. Thus, it appears plants were infested with 6 3 larvae (Muuller,€ 1989; that spotted knapweed may not be attacked by this in- Muuller-Sch€ aarer,€ 1991). Perhaps larger numbers of larvae sect during its ﬁrst three years of growth. Insects that per plant would change this result. However, during our attack larger plants, which are also the most fecund, ﬁeld study, the average number of larvae per infested would theoretically be useful in reducing seed produc- plant was less than 3 for all except the largest root- tion, but A. zoegana appeared to cause little or no diameter size class in spring 1992 and spring 1994. L. Smith, J.M. Story / Biological Control 26 (2003) 270–278 277

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