Establishment, dispersal, and prevalence of Rhinocyllus conicus (Coleoptera: Curculionidae), a biological control agent of thistles, Carduus species (Asteraceae), in Argentina, with experimental information on its damage

Biological Control 67 (2013) 186–193

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Establishment, dispersal, and prevalence of Rhinocyllus conicus (Coleoptera: Curculionidae), a biological control agent of thistles, Carduus species (Asteraceae), in Argentina, with experimental information on its damage Alba E. Enrique de Briano a, Horacio A. Acciaresi b, Juan A. Briano c,⇑ a

Dirección de Laboratorio Vegetal, SENASA, Huergo 1001 – (1109) Ciudad Autónoma de Buenos Aires, Argentina Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, Calle 60 y 119 – (1900) La Plata, Provincia de Buenos Aires, Argentina c Fundación para el Estudio de Especies Invasivas, Bolívar 1559 – (1686) Hurlingham, Provincia de Buenos Aires, Argentina b

h i g h l i g h t s

g r a p h i c a l a b s t r a c t

 We surveyed central Argentina for the

establishment of Rhinocyllus conicus.  We recorded the presence and

prevalence of the weevil.  The weevil is firmly established and

spread in Argentina.  These results encourage the

implementation of the IPM approach in South America.

a r t i c l e

i n f o

Article history: Received 11 December 2012 Accepted 15 July 2013 Available online 25 July 2013 Keywords: Rhinocyllus conicus Carduus spp. Thistles Biological control Seed production Weed control

a b s t r a c t Use of the weevil, Rhinocyllus conicus Froelich, for classical biological control of Carduus species in Argentina has not been controversial, as it has been in Canada and the United States, because there are no native thistle species in the South American release areas. In this study, 30 years after its first field release in Argentina, the Pampas region was surveyed to confirm the establishment of R. conicus, covering the original release sites and most of the overall area of distribution of its host thistles, Carduus species. Sites (n = 121) were systematically selected and natural populations of thistles were examined to confirm the presence of the weevil. Twenty four sites with R. conicus were selected to record the weevil’s prevalence on Carduus thoermeri Weinman and Carduus acanthoides L. Additional opportunistic surveys were conducted in other regions of Argentina and Uruguay, more distant from the original release sites. Rhinocyllus conicus was found at 81% of the original release sites and at 69% of the total sites surveyed, an area of approximately 370.000 km2. On average, 92% of the examined heads had damage in areas where the weevil was present, showing its high prevalence. A pilot study showed that the oviposition period of the weevils lasted 119 days and seed production of C. acanthoides was reduced by 15.5%. These results encourage the implementation of an integrated management of thistles in Argentina, and maybe in other parts of South America. Ó 2013 Elsevier Inc. All rights reserved.

1. Introduction ⇑ Corresponding author. Fax: +54 11 4662 0999. E-mail addresses: [email protected] (A.E. Enrique de Briano), [email protected] (H.A. Acciaresi), [email protected] (J.A. Briano). 1049-9644/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.biocontrol.2013.07.009

In the Pampas region of central Argentina, the predominant species of thistles are plumeless thistle, Carduus acanthoides L.,

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musk thistle, Carduus thoermeri Weinman, and bull thistle, Cirsium vulgare (L) Gaerthner (Crouzel et al., 1983). They are considered important weeds of pastures, crops, roadsides, and modified areas (Crouzel et al., 1983; González Crende, 2009; Josifovich, 1969; Lewis, 2005; Marzocca et al., 1976; Rodríguez et al., 2002; Scheneiter, 2007). In Argentina, thistles have been considered excellent targets for biological control because: (1) they do not have con-generic species of economic importance; (2) no native thistles occur in this area: (3) in addition to pastures, crops, roadsides, and modified areas, they also grow in stable environments which are highly suitable for biological control and; (4) they have not acquired any natural enemies in South America (DeLoach et al., 1989). In the 1970s, the weevil Rhinocyllus conicus Froelich (Coleoptera: Curculionidae) was introduced in Canada (Laing and Heels, 1978; Schroder, 1980) and in the United States (Rees, 1978; Rees, 1977; Surles and Kok, 1977) for classical biological control of C. thoermeri (=nutans). However, during the last decade, the use of the weevil in North America has been considered controversial because of its non-target effects on native Cirsium species in the areas of release (Hoddle, 2003; Louda and Stiling, 2004; Simberloff, 2012). This controversy, however, is not applicable in Argentina where all thistles (C. acanthoides L., C. thoermeri, Carduus pycnocephalus var. pycnocephalus L and var. tenuiflorus Curtis, Silybum marianum (L) Gaerthner, C. vulgare, Onopordon acanthium L and Cynara cardunculus L.), are exotic species and considered as pest plants. The North American program on biological control of C. thoermeri provided considerable knowledge on host-specificity and control efficacy, facilitating the implementation of a similar approach in Argentina without additional risk assessment studies (Crouzel et al., 1983). The program was developed in the 1980s by the Instituto Nacional de Tecnología Agropecuaria (INTA), Castelar, Buenos Aires, against C. acanthoides and C. thoermeri. The French biotype of R. conicus was imported from the United States and New Zealand, mass reared, and released. The two provenances were kept separate in time and space. Twenty seven releases were conducted from 1981 to 1991 at 21 field sites in the Provinces of Santa Fe, Buenos Aires, Córdoba, La Pampa, and Chubut (Fig. 1). Approximately 20,000 adult weevils were released, representing an average of 741 per release and 952 per site (range 33–3,000). Only six of the 27 releases were made in cages (1  1.5  1.6 m). A limited number of post-release observations detected the establishment of R. conicus in the experimental station of INTA Castelar and in southern Santa Fe Province (Enrique de Briano, 1987; Feldman, 1997; Molinari et al., 1994); however there have been no extensive assessments of this biological control agent. Thus, nearly 30 years after the first release, extended surveys of the insect and its impact are lacking and the dispersal of the weevil across South American habitats is unknown. The objectives of this study were: (1) to check the establishment of R. conicus in the original release sites; (2) to study its prevalence and dispersal and; (3) to conduct a pilot damage experiment. This post release assessment will be useful in implementing an integrated management strategy for thistles in Argentina, based on that proposed by Tipping (1991) for the use of R. conicus in IPM programs in the United States of America.

2. Materials and methods 2.1. Establishment and distribution In November-December (late spring) 2006, all the original release sites (and surroundings) of R. conicus were visited, covering most of the distribution area of Carduus spp. in the Pampas region of central Argentina (Crouzel et al., 1983). Spring surveys are the

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most effective in detecting the presence of R. conicus because the colonized heads are deteriorated and are easily observed, and all the stages of the weevil’s life cycle can be found in the plants at this time (Rees, 1982b; Zwolfer, 1967). The surveyed areas included the Provinces of Buenos Aires, south of Entre Ríos, south-central Santa Fe, south-central Córdoba, and east of La Pampa, covering 4100 km of main and secondary roads (Fig. 1). Sampling locations were systematically selected approximately every 30 km, giving a total of 121 sites where roadsides or pastures were visually inspected for natural populations of thistles. A GPS reading was recorded for each site, together with general observations on the adjacent habitat, such as open countryside, agricultural field, or other activities. At each site the heads of the thistles were visually examined for the presence of adults and/or eggs of R. conicus and, once in the laboratory, they were dissected to determine the presence of larvae, pupae and/or empty pupal cells. Sites with any of these life stages present were considered positive detections. Sites were considered free of R. conicus if none of the weevil stages (eggs to adults) were detected after a search effort of 60 min (two persons each working 30 min). At each site, the relative abundance of C. acanthoides, C. thoermeri, C. vulgare and S. marianum was estimated visually. Additionally, more-widespread field surveys were made in north-central Córdoba (during October 2006), eastern Chubut (November 2006), southern Uruguay (November 2009), and south-western Rio Negro (2012). 2.2. Prevalence Every 100 km along the monitoring route, collections (n = 24) were made to quantify R. conicus prevalence. At these sites, the first 30 flowering heads of C. acanthoides and/or C. thoermeri were collected within a 1 m-wide transect parallel to the road, starting at a kilometer marker. A total of 720 heads (30 heads/site  24 sites) were collected, stored in paper bags, transported to the laboratory and dissected later to determine the presence of different life stages of R. conicus. The percentage of colonized heads was recorded for the total number of thistles sampled and for each individual host species. 2.3. Damage A pilot study was conducted during spring-summer 2006–2007 in a 500 m2 field plot (34° 410 S; 59° 230 W) located in Mercedes, Buenos Aires, Argentina. Within the plot, all plants and stems (n = 316) of C. acanthoides were numbered; then, 60 of the stems (experimental units) were selected at random, labeled, and monitored weekly from October 16, 2006 to February 17, 2007, resulting in 19 monitoring dates (Boldt and DeLoach, 1985). Strong winds, and damage caused by birds and rodents, determined that only 27 stems (45% of those originally selected) survived to the end of the experiment and only these were considered in the final analysis. A total of 5909 mature flower heads was collected over 11 collecting dates and no flower heads were collected on eight monitoring dates. The heads were transported in paper bags to the laboratory and dissected to determine the presence of R. conicus. Prior to dissection, the heads diameters (d) were measured and the area (a) of the receptacles was calculated (a = p  d2/4). The damage of the weevil was ranked as 0 (undamaged), 25%, 50%, 75%, and 100% of the receptacle area (Supplementary material). 2.4. Oviposition period For each monitoring date, the appearance of eggs on the flower heads was recorded. Oviposition was considered to have ended

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Fig. 1. Area-wide map showing most of the release sites of R. conicus in the 1980’s, and all sites observed with and without the weevil during the surveys in 2006–2012. Because of a scale limitation, not all the release sites are shown in northern Buenos Aires Province.

when three sequential weekly examinations revealed no new eggs, as proposed by Goeden and Ricker (1977). 2.5. Statistical analysis The numbers of damaged and undamaged heads were compared with a Chi-square test (Statistix v. 8.0, 2008). The diameters of the heads were analyzed thru a linear regression. Values of percentages, area of receptacles, and oviposition were logtransformed. 3. Results 3.1. Establishment and distribution R. conicus was observed at (or close to) 17 (81%) of the 21 original release sites and at 84 (69%) of the 121 sites that were surveyed (Table 1, Fig. 1). The weevil was found throughout Buenos Aires Province, south of Entre Ríos, south of Santa Fe, south of Córdoba, and east of La Pampa, representing a total colonized area of 370,000 km2. R. conicus was also found at isolated localities in eastern Chubut and southern Uruguay. Consequently, the current distribution of R. conicus was confirmed to be approximately between 32°–43° S and 64°–57° W (Fig. 1). Table 1 Presence of Rhinocyllus conicus and Carduus species at 121 field sites surveyed in Argentina during November–December 2006. Host species

C. acanthoides C. thoermeri Both Total

Number (%) of sites with R. conicus present

R. conicus absent

Total

64 (81) 15 (47) 5 (50) 84 (69)

15 (19) 17 (53) 5 (50) 37 (31)

79 (66) 32 (26) 10 (8) 121 (100)

Establishment of R. conicus was confirmed on musk thistle, C. thoemeri, in arid areas such as eastern La Pampa, between 35° and 38° S and at one locality in eastern Chubut, at 43° S. It was also recorded from humid areas such as Oliveros, Santa Fe Province. These regions show mean annual temperatures between 11 and 14 °C with a mean maximum between 20 and 23 °C and a mean minimum between 8 and 9 °C (INTA, 2006). The highest annual temperatures since the release of the weevil ranged from 40.7 to 41.2 °C and the lowest temperatures ranged from 6.8 to 11.3 °C (Servicio Meteorológico Nacional, personal communication). R. conicus was established on C. acanthoides in Buenos Aires Province and south of Santa Fe Province but was not found on this host in most of southern Entre Rios Province, suggesting that it did not establish readily in this area. The distribution and abundance of the host thistles in the surveyed area revealed striking differences in that pure stands of C. acanthoides were observed in the east, while pure stands of C. thoermeri were observed in the north and west, and C. vulgare was irregularly distributed, with higher densities in northern Buenos Aires, central Santa Fe and southern Córdoba (50%, 90% and 60% of the populations, respectively). S. marianum was found at only one site, 100 km north of Bahía Blanca, in southern Buenos Aires Province, representing less than 5% of the thistle population across the entire area surveyed. In 65.5% of the surveyed sites, C. acanthoides was the only thistle species present, in 26.5% of the sites C. thoermeri was the only thistle species present, while both species co-occurred at only 8% of the sites (Table 1). R. conicus was detected in 81% of the sites with C. acanthoides, in 47% of the sites with C. thoermeri, and in 50% of the sites where both species were present (Table 1). 3.2. Prevalence At the 24 detailed collection sites, C. acanthoides was the only thistle species present at 58% (14/24) of the sites, C. thoermeri

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A.E. Enrique de Briano et al. / Biological Control 67 (2013) 186–193 Table 2 Prevalence of Carduus species and Rhinocyllus conicus at the 24 detailed collection sites surveyed in Argentina during November–December 2006. Locality (province)1

1 Gualeguay (ER) 2 General Levalle (CBA) 3 Tarragona (SF) 4 Pergamino (BA) 5 Duggan (BA) 6 Alberti (BA) 7 Carlos Casares (BA) 8 Paso (BA) 9 Fortín Olavarría (BA) 10 Larroude (BA) 11 Alta Italia (LP) 12 Winifreda (LP) 13 Padre Buodo (LP) 14 Jacinto Arauz (LP) 15 Bahía Blanca (BA) 16 Coronel Pringles (BA) 17 Krabbe (BA) 18 Santa Lucía (BA) 19 Francisco Meeks (BA) 20 Lobería (BA) 21 San Agustín (BA) 22 Coronel Vidal (BA) 23 Gral. Guido (BA) 24 Dolores (BA) Total heads (n = 720) Total heads/species Total % of colonized heads Total % of colonized heads/species Mean % of colonized heads/site 1 2 3 a b c d e

Carduus prevalence2 (%)

Number of heads with or without weevils3 (n = 30 heads per site)

Ca

Ct

P

A

P

A

100 0 60 100 100 100 100 100 99 100 10 100 0 0 0 0 98 99 100 100 100 100 100 100

0 100 40 0 0 0 0 0 1 0 90 0 100 100 100 100 2 1 0 0 0 0 0 0

23 0 18 30 29 30 12 29 27 27 1 1 0 0 0 0 30 30 24 29 27 30 28 29 454 498 68a 91c

7 0 1 0 1 0 18 1 0 3 0 0 0 0 0 0 0 0 6 1 3 0 2 1 44

0 28 11 0 0 0 0 0 3 0 28 28 23 30 30 30 0 0 0 0 0 0 0 0 211 222 32b 95d

0 2 0 0 0 0 0 0 0 0 1 1 7 0 0 0 0 0 0 0 0 0 0 0 11

Ca

Prevalence of R. conicus per site (%)

Ct

77 93 97 100 97 100 40 97 100 90 93 93 77 100 100 100 100 100 80 97 90 100 93 97

92e

Nearest locality; ER: Entre Ríos; CBA: Córdoba; SF: Santa Fe; BA: Buenos Aires; LP: La Pampa. Ca = Carduus acanthoides; Ct = Carduus thoermeri. P = Rhinocyllus conicus Present; A = Rhinocyllus conicus Absent. 68% = 454/(454 + 211)*100. 32% = 211/(454 + 211)*100. 91% = 454/498*100. 95% = 211/222*100. 92% = (454 + 211)/720*100.

was the only thistle present at 21% (5/24) of the sites, while both thistles coexisted at the remaining 21% (5/24) of the sites, with C. acanthoides most abundant at four of these (Table 2). The weevil colonized 92% (range 40–100%) of the heads, 68% of which were C. acanthoides and 32% were C. thoermeri. Considering the total number of colonized heads per host species, the prevalence of R. conicus was 91% in C. acanthoides and 95% in C. thoermeri (Table 2).

(range 12–17) and that of heads which developed at the end of the season was 8.1 ± 1.6 mm (range: 4–11) (Fig. 3; p < 0.05; R2 = 0.94; y = 16.03–0.819x). The total area of the receptacles producing seeds during the entire study was 4330 cm2 and the damaged area was 671.9 cm2, representing 15.5% of the total. Although the highest number of damaged heads was observed on December 31, 2006, the highest damage on the area producing seeds was observed on December 23, 2006 (Fig. 4).

3.3. Damage The total number of heads per monitoring date increased gradually, reaching a maximum of 1543 heads on January 28, 2007 before declining sharply towards the end of the study (Fig. 2). The mean number of heads collected per stem was 218.8 ± 154.4 (range: 30–570). During the first four monitoring dates (first month), which corresponded with the early flowering of C. acanthoides, 81–100% of the heads were damaged by R. conicus. There was an abrupt decline in damaging on subsequent sample dates (Fig. 2). Although the highest number of damaged heads (n = 165) was observed on December 31, 2006, it represented less than 40% of the heads. During the entire study, 5,384 (91.1%) heads were undamaged by R. conicus, while the remaining 525 (8.9%) showed different levels of damage, including 400 (76%) with total destruction of the receptacle (Supplementary material). The mean diameter of the heads of C. acanthoides which developed at the beginning of the flowering season was 15 ± 2.6 mm

3.4. Oviposition period The first eggs were observed on the heads from October 21 until November 27, 2006, and the peak of initial oviposition was observed on November 4. The latest eggs were observed on February 3, 2007. However, the additional weekly examinations conducted afterwards revealed that R. conicus oviposited on late-flowering heads of 14 thistle plants. The end of the oviposition period was February 17, 2007, representing a total period of 119 days.

4. Discussion 4.1. Establishment and distribution This work represents the first large-scale post-release survey of R. conicus in Argentina. Thirty years after the first release of this agent, it is clear that both the establishment and dispersal of this

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Fig. 2. Number of Carduus acanthoides flower heads collected, total and damaged by Rhinocyllus conicus during the field experiment in Mercedes, Argentina, in 2006–2007.

Fig. 3. Size of Carduus acanthoides flower heads collected during the experiment in Mercedes, Argentina, 2006–2007.

weevil have been highly successful, currently occupying most of the distribution areas of C. acanthoides and C. thoermeri. The dispersal mechanisms of R. conicus remained unknown; however, it seemed that, in most areas, R. conicus has naturally dispersed. For example, in southeastern Buenos Aires Province, the weevil probably spread from the release sites in the north-central part of the province (Fig. 1). In contrast, the low occurrence of R. conicus in southern Entre Rios with the Paraná River as a natural barrier, would suggest its probably recent anthropic transportation. The same can be speculated for Uruguay, with the barrier of La Plata River. The presence of R. conicus further north in Entre Rios Province and in Uruguay needs to be assessed and confirmed with additional surveys. There are a number of studies that report a high natural dispersal rate of R. conicus after its release and establishment in the United States (Hodgson and Rees, 1976; Kok and Surles, 1975; Puttler et al., 1978; Rees, 1978; Rees, 1977; Surles and Kok, 1977) and in Canada (Laing and Heels, 1978; Schroder, 1980).

The occurrence of R. conicus in the single spot in eastern Chubut (43.2° S) on musk thistle, represents its southernmost location which is warmer than the distribution of the weevil in Europe where it affects thistles up to 54° N (Zwolfer, 1967; Zwolfer and Harris, 1984). Furthers surveys should be conducted between this location and Buenos Aires-La Pampa Provinces to confirm an eventual continued distribution of the weevil. The southern distribution of R. conicus reported here for Argentina is in concordance with that observed in North America (Boldt and DeLoach, 1985; Harris, 1986; Laing and Heels, 1978), and New Zealand (Popay et al., 1984), where R. conicus was used as a biological control agent. However, climate matching studies should be conducted for a more reliable comparison as other factors beyond latitude are sure to affect the survival and development of this species. Despite the natural occurrence of C. thoermeri in central Santa Fe and north-central Córdoba, R. conicus failed to establish (latitudes lower than 32° S). Release methodology within those prov-

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Fig. 4. Total area of Carduus acanthoides flower heads and area damaged by Rhinocyllus conicus in Mercedes, Argentina, 2006–2007.

inces did not differ from others sites and average number of adults released per site (952) seemed to be high enough to ensure establishment. The main reasons for failure might have been the higher temperatures affecting the weevil activity in the absence of refuges. This was also suggested by Boldt and DeLoach (1985) for failures in the United States. In addition, several studies indicated that establishment failure might be a consequence of using the wrong weevil biotype, insufficient thistle heads or seeds due to grazing and/or rodents damage, parasitism, flooding and fire, and temperature extremes in winter (Goeden, 1978; Goeden and Ricker, 1977; Kok, 2001; Puttler et al., 1978; Rees, 1982a; Surles and Kok, 1976; Wilson and Andres, 1986). However, the actual reasons for the lack of establishment in those regions of Argentina remain uncertain and should be further investigated before implementing additional introductions. On several occasions, adults of R. conicus were found colonizing isolated thistle plants located along roadsides and under fences, close to cultivated fields treated with herbicides. This is surprising considering the increasing production of annual crops in the Pampas region of Argentina and the use of roadsides for cultivation (Piñeiro and Villareal, 2005; Quirós et al., 2006). Both the ability of the weevil to find isolated hosts and its apparent high persistence in the field are features of a good biological control agent. 4.2. Prevalence The prevalence of R. conicus on thistle populations in the Pampas region was very high (92%). Kok (2001), Kok and Surles (1975), Popay et al. (1984) and Rees (1977), also reported a prevalence of 90–100% for the early flowering of C. thoermeri in the United States. However, the values reported in this study were recorded during the peak of weevil activity. As reported by Harris (1986) and Kok (2001), the prevalence decreases through the end of the flowering season and the adults hide for overwintering until the next warm season. 4.3. Damage The total percentage of C. acanthoides heads damaged by R. conicus (8.9%) was slightly lower than the levels reported in other studies (Surles and Kok, 1977; Harris, 1986; Feldman, 1997), a consequence, at least in part, of the asynchrony between the phenology of the plant and the oviposition period of the weevil. A sim-

ilar asynchrony was reported by Feldman (1997), Harris and Alex (1986), Kok (2001), Molinari et al. (1994) and Surles and Kok (1977, 1976). On the contrary, in the United States, Kok and Surles (1975) reported that R. conicus damaged 90% of the heads of the close-relative musk thistle, C. thoermeri which shows a high synchrony with the weevil (Schroder, 1980). Although similar studies should be conducted in other areas of Argentina and including C. thoermeri, it seems that the synchrony between the flowering of the thistles and the oviposition of the weevil is essential to achieve high levels of damage. During the first month of the flowering of C. acanthoides, most (81–100%) of the heads were damaged by the weevil with 75% of the damaged heads totally consumed and producing no seeds. As suggested by McCarty and Scifres (1969), the oviposition of R. conicus on the first heads during the season and the consequent damage would increase the control potential of the weevil by impeding the development of large rosettes, and larger amount of seeds in the season. This indicates that the weevil has potential to reduce seed production, at least at the beginning of the flowering season. The decrease in the size of the heads reported here during the flowering season of C. acanthoides agrees with the studies on other thistle species (Harris, 1986; Enrique de Briano, 1989; Enrique de Briano, 1988). Because the earlier the flowering, the larger the heads, the effect on the seed-producing area of the receptacles reached higher levels (15.5%) compared to the percentage of damaged heads (8.9%), as shown by Feldman (1997) and Harris (1986). These results suggest that the direct damage of R. conicus on C. acanthoides would not be sufficient to substantially decrease seed production and biological control should be complemented with other control techniques, such as mowing and/or the use of herbicides. However, an eventual integrated management should be conducted without affecting either the plant-herbivore interaction at the beginning of the flowering season or the life cycle of the weevil. According to the results reported here, a general recommendation would include the implementation of additional control techniques not earlier than two months after the initial oviposition of the weevil. This way, the complete development of R. conicus would be allowed in most of the heads. Similarly, studies on C. thoermeri showed that mowing or the use of herbicides after the senescence of the first heads did not affect the development of R. conicus (Trumble and Kok, 1979; Kok, 1980; Harris, 1986; Tipping, 1991). The fact that C. acanthoides is a weed highly dependent of the seed bank accumulated during the previous season (Tipping,

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2008) emphasizes the importance of the complementation of the weevil with other control techniques. This pilot damage experiment should be repeated in other areas and with both C. acanthoides and C. thoermeri. 4.4. Oviposition period The duration of the oviposition period reported here (119 days) is much longer than those reported by Feldman (1997) for the Province of Santa Fe, Argentina (52 days), and by Rowe and Kok (1984) for Virginia, United States (82 days). Considering the longevity of the females reported by Rowe and Kok (1984), the duration of the egg to adult period recorded by Zwolfer (1967), and the absence of eggs reported here during almost the entire month of January, the late oviposition might correspond to a second generation of R. conicus within the season. This happens on C. thoermeri in New Zealand at similar latitudes (Jessep, unpublished information). Again, the eventual presence of a second generation in Argentina should be confirmed with studies in other areas including C. thoermeri. In conclusion, after more than 30 years from its first field release, R. conicus is widely established and spread in several regions of Argentina on C. acanthoides and C. thoermeri. The weevil showed high prevalence and, apparently, high search ability and field persistence. The asynchrony of C. acanthoides flowering with the oviposition of R. conicus produced a low impact on the total seed production. The greatest damage of the weevil was observed at the beginning of the flowering season and should be complemented with other control method. In some situations and conditions, the existence of a second generation of R. conicus might increase its detrimental effect on plumeless thistle populations. These results encourage the implementation of an integrated management of thistles in Argentina, and maybe in other parts of South America. Acknowledgments The authors deeply thank Hugo Cordo (retired ARS-SABCL) for providing transportation and field assistance during one of the surveys in central Argentina, Silvina Bado (INTA, Chubut) for helping with the field survey in Trelew, and Octavio Bruzzone (INTA Bariloche) for his assistance with the statistical analysis. Also, the revision of an earlier version of this manuscript by Ray Carruthers (ARS, Albany, CA) and Phil Tipping (ARS, Ft. Lauderdale, FL) is highly appreciated. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.biocontrol.2013. 07.009. References Boldt, P.E., DeLoach, C.J., 1985. Evaluating Rhinocyllus conicus (Coleoptera: Curculionidae) on Silybum marianum (Compositae) in Texas. In: Proceedings of VI International Symposium on Biological Control of Weeds. Vancouver, Canada, pp. 417–422 (1984). Crouzel, I.S., Cordo, H.A., Enrique, A.E., Pardo, R., 1983. Control biológico de ‘‘cardos’’ en la República Argentina – Investigaciones básicas. In: Actas de la IX Reunión Argentina sobre la Maleza y su Control, Santa Fe, 1982, ASAM, Buenos Aires, Argentina, pp. 165–215. DeLoach, C., Cordo, H.A., Crouzel, I.S., 1989. Control Biológico de Malezas. El Ateneo, Buenos Aires (266). Enrique de Briano, A.E., 1987. Establecimiento y dispersión en Castelar (provincia de Buenos Aires) del gorgojo Rhinocyllus conicus agente de control biológico del ‘‘cardo pendiente’’ y del ‘‘cardo’’. Acintacnia 26, 64–66.

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