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Home , Bembidion, Ground beetle, Poecilus lucublandus, Poecilus scitulus, Sitona

J. Appl. Entomol.

Identification of potential natural enemies of the pea leaf , L. in western Canada M. A. Vankosky1,2,H.A.Ca´ rcamo2 & L. M. Dosdall1

1 Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada 2 Agriculture and Agri-Food Canada, Lethbridge Research Centre, Lethbridge, AB, Canada

Keywords Abstract biological control, carabid ground , conservation biological control, egg Sitona lineatus L., the pea leaf weevil, is an invasive pest of Pisum sativum L. (field pea) that has recently become established in Alberta, Canada. Correspondence Adults consume seedling foliage and larvae feed on Rhizobium root nod- M. A. Vankosky (corresponding author), ules thereby reducing nitrogen fixation; both life stages can reduce Department of Agricultural, Food and yield. Eggs and adults are vulnerable to predators and . In Nutritional Science, 4-10 Agriculture-Forestry 2009, a series of experiments was undertaken to identify potential indig- Centre, University of Alberta, Edmonton, AB, Canada T6G 2P5. enous natural enemies of S. lineatus in southern Alberta. In three test E-mail: [email protected] arenas, eggs were exposed to starved ground beetles in no-choice tests for 48 h. Egg debris was observed when eggs were exposed to Received: December 16, 2009; accepted: April quadrimaculatum L., linearis (LeConte), Bembidion rupicola (Kir- 9, 2010. by), Bembidion timidum (LeConte), scitulus LeConte, and staphyli- nid beetles. Of the two most abundant carabid , the smaller doi: 10.1111/j.1439-0418.2010.01542.x B. quadrimaculatum consistently removed significantly more eggs (94.6%) than the larger melanarius (17.4%). Similar results were observed in Petri dish and egg card tests. No egg debris was observed in tests with Pt. melanarius. Presence of the larger , Pt. melanarius, resulted in a lower rate of egg removal by the smaller B. quadrimaculatum relative to the rates observed for B. quadrimaculatum alone. Intraguild predation of B. quadrimaculatum by Pt. melanarius was observed in 47% of tests. These results suggest that B. quadrimaculatum is a potential predator of S. lineatus eggs in field pea agroecosystems and should be considered for use in conservation biological control and inte- grated pest management programs.

migrate to their primary hosts, pea and bean crops, Introduction and feed on seedlings (Stein 1972; Fisher and O’Kee- The pea leaf weevil, Sitona lineatus L. (Coleoptera: ffe 1979; Hamon et al. 1987; Landon et al. 1995). ), is a serious pest of field pea, Pisum After mating, females oviposit over the soil surface sativum L., and broad bean, Vicia faba L. (Fabales: (Jackson 1920; Hoebeke and Wheeler 1985). Larvae ), in Europe, Africa and burrow through the soil, penetrate root nodules (Jackson 1920; Hoebeke and Wheeler 1985). Within (Jackson 1920; Hoebeke and Wheeler 1985) and the past 10 years, S. lineatus has become established feed upon the nitrogen-fixing bacteria, Rhizobium in southern Alberta, Canada and has caused substan- leguminosarum Frank (Rhizobiales: Rhizobiaceae) tial economic damage (Vankosky et al. 2009). In (Johnson and O’Keeffe 1981). Defoliation by adult autumn, S. lineatus adults migrate to shelter belts can account for losses of up to 50% of where they consume foliage of secondary legumi- photosynthetic tissues, limiting the ability of plants nous hosts like alfalfa (Medicago sativa L., Fabales: to reproduce and support root nodules (Havlickova Fabaceae) before overwintering (Jackson 1920; 1982; Williams et al. 1995). Yield losses of up to Schotzko and O’Keeffe 1988). In early spring, adults 28% were attributed to decreased pod production by

J. Appl. Entomol. 135 (2011) 293–301 ª 2010 Blackwell Verlag, GmbH 293 Potential indigenous natural enemies of Sitona lineatus M. A. Vankosky, H. A. Ca´ rcamo and L. M. Dosdall

Nielsen (1990). Larval damage to root nodules can Carabidae can play a key role in S. lineatus predation, range from 40% to 98% of nodules (El-Dessouki both of eggs and adults, as several spe- 1971; Cantot 1986; Verkleij et al. 1992). Larval feed- cies or their congeners identified as S. lineatus preda- ing reduces seed protein content, especially in nutri- tors in Europe also occur in Alberta, for example, ent-poor soils, and the amount of nitrogen returned (Illiger) and Bembidion proper- to the soil (Dore´ and Meynard 1995; Corre-Hellou ans (Larochelle and Lariviere 2003). and Crozat 2005). Control of S. lineatus using insecti- cides is difficult as a result of its high fecundity Materials and Methods (Jackson 1920), migratory behaviour (Fisher and O’Keeffe 1979; Hamon et al. 1987), and concealed Egg collection larval (Jackson 1920); however, the egg stage of S. lineatus is prone to mortality. Adult weevils, collected from field peas in late May Employing biological control agents against S. line- were sexed and mating pairs were reared in Petri atus populations has been explored extensively in dishes provisioned with fresh pea foliage that was Europe. For example, adult ground beetles (Coleop- replaced every 48 h. Weevil eggs were collected tera: Carabidae), including Pterostichus cupreus L., were from the Petri dishes every 48 h. Eggs were placed shown to prey upon adult weevils and Bembidion on moist filter paper in Petri dishes and stored at properans (Stephens) was found to prey upon eggs 4C until needed. Female weevils continued to ovi- and hatching larvae in Poland (Ropek and Jaworska posit until mid-August. 1994). Biological control of S. lineatus in North America using its natural enemies from Europe may Egg predation be a viable option. Before launching studies to assess potential classi- Potential ground beetle predators of S. lineatus eggs cal biological control agents for introduction to were collected from field pea plots near Lethbridge southern Alberta, an evaluation of indigenous preda- (4941¢39¢¢N; 11249¢58¢¢W) and Vauxhall (5004¢ tors should be undertaken to determine if any of 08¢¢N; 11205¢51¢¢W), Alberta. Plots at Lethbridge these species impact S. lineatus populations. If suc- were planted on 04 May 2009 and at Vauxhall on 06 cessful, a conservation biological control program May 2009. At Lethbridge, eight dry pitfall traps (1.0-l may be initiated as a significant component of an containers), provisioned with moist paper towel, rocks integrated pest management (IPM) program for and soil were placed around the perimeter of the field S. lineatus in Alberta. Conservation biological control pea research plot on 14 May 2009. Traps were emptied programs are designed to promote populations of every 24–48 h and traps remained in the field until beneficial species by providing refugia, alternative the plots were harvested. Carabidae and Staphylinidae hosts, and corridors between populated patches were collected from the traps while spiders and other (Dent 1995; Van Driesche and Bellows 1996; Eilen- were released. At Vauxhall, small beetle spe- berg et al. 2001). In agroecosystems, additional con- cies, such as Bembidion quadrimaculatum L. (Coleop- servation methods can include using selective tera: Carabidae), were collected by hand from the soil insecticides, implementing favourable tillage regimes, surface using aspirators when field peas were at the six strip harvesting, cover crops, intercropping, winter to nine leaf stage in June, at the late flowering stage in seeding, crop rotation and installing shelter belts July and before harvest in August. In the laboratory, (Van Driesche and Bellows 1996; Eilenberg et al. beetles were sorted by morphospecies and placed in 2001). A constraint of conservation biological control rearing dishes containing moist soil, leaf litter and is intraguild predation (see review by Polis et al. rocks for refugia. Rearing dishes were stored at 10C 1989), which occurs commonly between carabid (photoperiod 16 : 8 light : dark). beetles of different size classes (Polis et al. 1989; Pra- The potential of ground beetles to prey upon sad and Synder 2004; Prasad and Snyder 2006). S. lineatus eggs was investigated in three no-choice The objective of this research was to identify tests with different substrates. In each test, one bee- potential indigenous predators of S. lineatus eggs, a tle (starved for 48 h) was confined for 48 h (20C, life stage susceptible to predation, from southern 16 : 8 light : dark photoperiod, controlled humidity) Alberta for future use in an IPM program. The in a Petri dish or rearing dish provisioned with a potential for intraguild predation in southern Alberta known number of S. lineatus eggs. The number of field pea production systems was investigated. remaining eggs, presence or absence of egg debris, We hypothesize that members of the beetle beetle location and egg location were recorded upon

294 J. Appl. Entomol. 135 (2011) 293–301 ª 2010 Blackwell Verlag, GmbH M. A. Vankosky, H. A. Ca´ rcamo and L. M. Dosdall Potential indigenous natural enemies of Sitona lineatus conclusion of the exposure period. After the experi- land, OH, USA) repositionable glue using a plastic ment, each beetle was killed, preserved and deter- template marked out into a 4 · 5 grid with five open mined to species using Lindroth (1961–1969). spaces. Five S. lineatus eggs were placed along the Voucher specimens were deposited in the Strickland edges of each square of glue on the card after the Museum of the University of Alberta. Each beetle was glue had partially set. Cards were prepared within an used only once and replication varied for each species hour of their use in each predation trial; prior to depending on the number of individuals collected commencement of each trial one egg card was placed (table 1). The specific conditions of each test are in each rearing dish, as described above. Egg place- described below and control trials were set up using ment on egg cards was designed to mimic the deposi- the same conditions in the absence of a predator. tion of weevil eggs over the soil surface and was intended to determine if beetles would search out eggs in these conditions and to obtain an estimate of Petri dish tests egg predation rates under field conditions. Twenty melanized S. lineatus eggs were placed on a single layer of moistened filter paper. No other Beetle competition organic matter was added to the Petri dishes aside from any soil that was transferred to the dish at the The potential for intraguild predation and competi- time of beetle addition. tion among small and large beetle species for prey was investigated by exposing S. lineatus eggs to single specimens of Pt. melanarius and B. quadrimaculatum Rearing dish tests simultaneously using the rearing dish experimental Soil was placed to a depth of approximately 2 cm in design as described above. After 48 h, beetles were 250 mL rearing containers and moistened. Filter removed, killed, identified and the length and width paper (4.25 cm diameter) was placed on top of the of all surviving beetles was determined using digital soil in the centre of the dish and moistened with dis- calipers. The number of eggs remaining in each dish tilled water. Twenty eggs were placed on the filter was recorded. paper. Soil was added to the dishes in to pro- vide the beetles with a more natural habitat in which Statistical analysis their behaviours, for example, burrowing by Pt. mel- anarius (Wallin 1988), could be observed in relation Predation upon S. lineatus eggs by each ground beetle to their tendency to prey upon S. lineatus eggs. species was analyzed based on the percentages of missing eggs using the PROC GLM procedure (SAS Institute 2004). Each test described above was ana- Egg card tests lyzed separately. Beetle species were included if at Following the procedure for seed cards (Westerman least four replicate trials were performed using that et al. 2003a,b; O’Rourke et al. 2006; Saska 2008), species. If the ANOVA results were significant (a < weevil eggs were glued to sandpaper egg cards. Med- 0.05), the contrast function (with Bonferroni adjust- ium grain sandpaper was cut into 5 · 6 cm rectangles ment) was used to identify differences in egg removal and sprayed with Krylon Easy-TackTM (Sherwin- between beetle species of interest. Where data were Williams Company, Krylon Products Group, Cleve- non-normal and did not benefit from logarithmic transformation, the Kruskal–Wallis test was used and Table 1 Sample sizes for each beetle species for the Petri dish, rear- the Chi-square statistic was reported. For tests inves- ing dish, egg card and competition tests tigating intraguild predation and beetle competition, the mean percentage of eggs removed with two bee- Petri Rearing Egg Beetle species dish dish card Competition tles was compared to data from the rearing dish test, for individual species and the control. Control 20 35 20 35 Bembidion quadrimaculatum 18 35 29 35 Results Pterostichus melanarius 20 29 31 29 Microlestes linearis 9NANANA 4NANANA Predators 7NANANA Thirteen species of carabid beetles were collected at Staphylinidae 11 NA NA NA Lethbridge and Vauxhall. Large species, including

J. Appl. Entomol. 135 (2011) 293–301 ª 2010 Blackwell Verlag, GmbH 295 Potential indigenous natural enemies of Sitona lineatus M. A. Vankosky, H. A. Ca´ rcamo and L. M. Dosdall

Pterostichus melanarius, Poecilus lucublandus (Say), and Pt. melanarius (fig. 1). Staphylinid beetles and P. scitulus Poecilus scitulus LeConte were most commonly found removed intermediate numbers of eggs (fig. 1). Bembi- in dry pitfall traps. Pt. melanarius accounted for the dion quadrimaculatum consumed significantly more pea vast majority of beetles collected in pitfall traps. At leaf weevil eggs than all other beetle species. Staphy- Vauxhall, where beetles were collected by hand, linidae consumed more eggs, on average, than P. lucu- B. quadrimaculatum accounted for the majority of blandus, M. linearis, and Pt. melanarius. Poecilus scitulus beetles captured. Microlestes linearis (LeConte) and did not remove significantly more eggs than the sta- Bembidion timidum (LeConte) were collected in low phylinids, P. lucublandus, M. linearis or Pt. melanarius, numbers at Vauxhall, and low numbers of lit- but did differ significantly from the control. Poecilus toralis Mannerheim and placidum (Say) were lucublandus, M. linearis and Pt. melanarius beetles did collected with dry pitfall traps and by hand. Few not remove significantly more eggs than were missing staphylinid beetles were collected from dry pitfall from the control, to which no beetle was added. traps. The majority of these individuals belonged to two species of the Philonthus Stephens (Cole- Rearing dish test optera: Staphylinidae). Petri dish test results for Staphylinidae were pooled for statistical analysis. Only two beetle species, B. quadrimaculatum and Pt. melanarius were tested in the rearing dish arena. After 48 h, significantly more eggs were missing Egg predation from B. quadrimaculatum rearing dishes (94.6%) than

In all predation arenas (Petri dish, rearing dish, egg from Pt. melanarius dishes (17.4%) (F2, 96 = 367.92, card), B. quadrimaculatum removed the greatest per- P < 0.0001; fig. 2). Compared to the control, both centage of S. lineatus eggs. In dishes to which species removed significant numbers of eggs. B. quadrimaculatum had been added, S. lineatus egg debris was often observed. Egg debris was also Egg card test observed in dishes with M. linearis, Bembidion rupicola (Kirby), B. timidum, Staphylinidae, and occasionally Under conditions designed to simulate field condi- in P. scitulus trials. No evidence of egg debris was tions, 45% of eggs were missing from dishes with observed in Pt. melanarius or P. lucublandus trials, B. quadrimaculatum, which was significantly greater although both species disturbed and moved eggs than the 3.4% of eggs missing from Pt. melanarius within the dishes. dishes (Kruskal–Wallis test: v2 = 15.65, P = 0.0004). There was no difference in egg consumption between Pt. melanarius and the control (fig. 3). Petri dish test Egg removal in Petri dishes differed significantly Beetle competition among species (F6, 102 = 67.65, P < 0.0001) and ranged from 98% by B. quadrimaculatum to 11.75% by Bembidion quadrimaculatum (1.60 · 5.60 mm) speci- mens were significantly smaller than Pt. melanarius 120

A 100 120

80 A eggs missing B 100

60 BC 80 eggs missing 40

S. lineatus 60 CD CD CD 20 40

D S. lineatus Per cent B 0 20 C 0 Per cent B. quadrimaculatum Pt. melanarius Control Beetle species Beetle species

Fig. 1 Mean percentage of 20 Sitona lineatus eggs destroyed or Fig. 2 Mean percentage of 20 Sitona lineatus eggs destroyed or missing from Petri dishes after 48 h of exposure to various beetle spe- missing from rearing dishes after 48 h of exposure to adult carabid cies. Means with the same letter are not significantly different. beetles. Means with the same letter are not significantly different.

296 J. Appl. Entomol. 135 (2011) 293–301 ª 2010 Blackwell Verlag, GmbH M. A. Vankosky, H. A. Ca´ rcamo and L. M. Dosdall Potential indigenous natural enemies of Sitona lineatus

60 Table 2 Summary of beetle survival, given in number of rearing dishes, and the range of egg consumption for dishes in which both 50 beetles or only the large beetle was recovered

40 Number of dishes within each range of missing eggs missing S. lineatus eggs 30 0% 1–20% 21–75% 76–99% 100% Total dishes

S. lineatus 20

10 B. quadrimaculatum 1 1 2 6 15 25

Per cent recovered 0 B. quadrimaculatum 05 8 1 8 22 B. quadrimaculatum Pt. melanarius Control not recovered Beetle species Total test dishes 1 6 10 7 23 47

Fig. 3 The mean percentage of 25 Sitona lineatus eggs destroyed or recovered, the number of missing eggs ranged from missing from rearing dishes with egg cards after 48 h of exposure to adult carabid beetles. 5% to 100%; in 36% of these dishes, all S. lineatus eggs were removed (table 2).

120 Discussion A 100 B In plots of P. sativum, B. quadrimaculatum and Pt. mel- 80 eggs missing anarius were the most abundant ground beetle spe- 60 cies. Poecilus lucublandus, P. scitulus, M. linearis, B. timidum, and were 40 S. lineatus C collected in low to moderate numbers. A few staphy- 20 linid beetles of the genus Philonthus were collected in D

Per cent 0 dry pitfall traps. Trap catch results for this research B. quadrimaculatumB. quadrimaculatum Pt. melanarius Control are similar to those reported for this region. For + Pt. melanarius Predator group example, in his work to determine the activity den- sity of ground beetles in agroecosystems near Leth- Fig. 4 Representation of the effects of beetle competition, between bridge and Vauxhall, Bourassa (2006) reported that beetles of different sizes, on the rate of egg removal from rearing B. quadrimaculatum accounted for 28% of the trap dishes over a 48-h period. Twenty eggs were exposed to ground catches in the summer of 2004, with their peak activ- beetle predation. Means with the same letter are not significantly ity occurring in late June. Pterostichus melanarius was different. the dominant large carabid beetle, accounting for 43.1% of trap catches with its peak activity occurring (3.5 · 15.4 mm) specimens in both length (F1, in late summer (Bourassa 2006). Both B. quadrimacul- 69 = 3428.96, P < 0.0001) and width (F1, atum and Pt. melanarius were among the six most 69 = 2025.11, P < 0.0001). Simultaneous exposure of abundant species in agricultural fields near Vauxhall S. lineatus eggs to both species significantly reduced (Bourassa et al. 2008) and among the four most the rate of egg removal to 75.3% compared to abundant species near Lethbridge (Floate et al. 2007). 94.6% removal for B. quadrimaculatum alone (F3, Floate et al. (2007) collected 128 beetles on average 143 = 129.77, P < 0.0001; fig. 4). Egg removal in per sample over four years, with Pt. melanarius dishes with B. quadrimaculatum and Pt. melanarius accounting for 27.5% of trap catches while B. quadr- was significantly greater than in dishes with Pt. mel- imaculatum accounted for 9.9% of trap catches. anarius only (17.4%). Egg removal was significantly In Petri dish trials, P. scitulus and staphylinids con- greater in all dishes with beetles than in control sumed 36% and 55% of eggs respectively. Members dishes. of the genus Philonthus, the taxa of Staphylinidae After 48 h, both the large and small beetles were most commonly collected, are known to be predators recovered in 53.2% of trial dishes. Only one large of the eggs, larvae, pupae and adults of Lepidoptera, beetle was not recovered, and was likely not added Coleoptera and Diptera (Good and Giller 1991) and to the dish. In dishes with only the large beetle have been extensively investigated as predators of

J. Appl. Entomol. 135 (2011) 293–301 ª 2010 Blackwell Verlag, GmbH 297 Potential indigenous natural enemies of Sitona lineatus M. A. Vankosky, H. A. Ca´ rcamo and L. M. Dosdall the eggs and larvae of the horn fly, Haematobia irri- 2004; Prasad and Snyder 2006) and Drosophila pupae tans (L.) (Diptera: Muscidae) (Roth 1982; Fincher (Ca´rcamo 1992). In similar studies, B. quadrimacula- 1995). Neither P. scitulus nor the staphylinid beetles tum consumed the eggs of Delia antiqua (Meigen) were collected in sufficient numbers to be included (Diptera: Anthomyiidae) (Grafius and Warner 1989), in the rearing dish and egg card trials. Further inves- Delia floralis Falle´n (Diptera: Anthomyiidae) (Ander- tigation of the potential of Philonthus beetles as pre- sen et al. 1983), and Listronotus oregonensis LeConte dators of S. lineatus in southern Alberta should be (Coleoptera: Curculionidae) (Baines et al. 1990). undertaken, as this group consumed significant Based on the results of the current study and the numbers of weevil eggs. abundance and widespread distribution of B. quadr- Of the most abundant carabid species, the fewest imaculatum in agroecoystems (Grafius and Warner S. lineatus eggs were missing from dishes with 1989; Holopainen and Helenius 1992; Ca´rcamo Pt. melanarius. When exposed to Pt. melanarius in 1995; Ellsbury et al. 1998; Melnychuk et al. 2003; Petri dishes, 11.8% of eggs were missing after 48 h Fox et al. 2005; Bourassa 2006; Floate et al. 2007), and no egg debris was observed. In the rearing dish this carabid species has great potential for use in a trials, 17.4% of eggs were missing after 48 h; how- conservation biological control program against ever, Pt. melanarius in rearing dishes burrowed S. lineatus. Furthermore, its habit of remaining on or actively, scattering soil over the filter paper and eggs, near the soil surface rather than burrowing deep and as a result, eggs were often found on the soil belowground implies that it is likely an efficient surface rather than on the filter paper. Indirect dis- predator of S. lineatus eggs, as S. lineatus eggs are turbance may account for missing eggs in rearing found in the same section of the soil profile. dishes, as again, no egg debris was observed, provid- Conservation biological control initiatives aim to ing no conclusive evidence of consumption. In the increase populations of predators or parasitoids egg card test, only 3.4% of S. lineatus eggs were through agronomic practices that maintain removed. These results were not unexpected, as for natural enemies of pests (Dent 1995; Van Driesche Pt. melanarius has been investigated as an egg preda- and Bellows 1996; Eilenberg et al. 2001). Conserva- tor in the past with similar results (Baines et al. tion biological control of pests by indigenous 1990; Finch 1996; Prasad and Synder 2004; Prasad species such as B. quadrimaculatum may become com- and Snyder 2006). Finch (1996) suggested that plicated by intraguild predation as conservation bio- Pt. melanarius adults were unable to manipulate logical control practices often promote populations of insect eggs as prey due to their size, as in a survey of a variety of species in addition to the target species ground beetles, species larger than 10 mm in length (Polis et al. 1989; Prasad and Snyder 2004; Prasad only erratically consumed Delia radicum (L.) (Diptera: and Snyder 2006). Intraguild predation and competi- Anthomyiidae) eggs. Investigations regarding the use tion for prey is expected to reduce the efficiency of of Pt. melanarius as a biological control agent seem prey removal in assemblages of generalist predators, limited to their efficacy against larger prey, including such as B. quadrimaculatum (Clark et al. 1994), espe- (Symondson et al. 2002; McKemey et al. cially where there are species of different sizes pres- 2003), mollusks and annelid worms (Symondson ent in the community. Prasad and Snyder (2006), for et al. 2002) and adult insects (Baines et al. 1990; example, observed that Pt. melanarius rarely con- Holopainen and Helenius 1992). sumed insect eggs, but did consume small Bembidion After 48 h of exposure to B. quadrimaculatum, sig- ground beetles which subsequently reduced the nificantly higher numbers of S. lineatus eggs were number of fly eggs preyed upon by Bembidion beetles. absent from Petri dishes, rearing dishes, and egg When S. lineatus eggs were exposed to both cards, relative to numbers remaining after exposure B. quadrimacualum and Pt. melanarius simultaneously, to the other beetle species. Across all test conditions, B. quadrimacultum continued to consume significant there was no evidence of burrowing by B. quadrima- numbers of S. lineatus eggs, although at a reduced culatum beetles and all individuals were found on rate relative to tests with B. quadrimaculatum alone. the soil surface at the conclusion of the exposure In 46% of the rearing dishes, the B. quadrimaculatum period. Egg debris was observed in Petri dishes, rear- specimens were not recovered, but in 36% of those ing dishes and egg card tests, providing strong evi- dishes, the B. quadrimaculatum had consumed all of dence of egg consumption. Overall, these results the S. lineatus eggs before being killed. The effects of were expected, as previous research has shown that intraguild predation were tested in relatively small small ground beetles (<10 mm) readily preyed upon arenas, which likely increased the chances of the Delia spp. eggs (Finch 1996; Prasad and Synder beetles encountering one another and in turn the

298 J. Appl. Entomol. 135 (2011) 293–301 ª 2010 Blackwell Verlag, GmbH M. A. Vankosky, H. A. Ca´ rcamo and L. M. Dosdall Potential indigenous natural enemies of Sitona lineatus chances of intraguild predation. However, these better quantify the ability of indigenous ground bee- results indicate that in field pea crops intraguild pre- tle predators to suppress S. lineatus populations, as dation has the potential to reduce both the popula- well as to understand the effects of alternative prey, tion of B. quadrimaculatum and its effectiveness as a competition and intraguild predation on B. quadrima- predator of S. lineatus eggs. Further work to investi- culatum. Research should also be undertaken in gate the relationships between predatory carabid southern Alberta to determine the most effective beetles should be done in the field, and should con- conservation biological control practices for ground sider the effects of prey availability and the timing of beetles in agroecosystems. Beetle banks as described peak beetle activity on the extent of intraguild pre- by Thomas et al. (1991), for example, have been dation. In the presence of the large Pt. melanarius, shown to provide carabid beetles with a suitable however, B. quadrimaculatum did consume a signifi- overwintering habitat and to contribute to the over- cant number of pea leaf weevil eggs relative to the all biological diversity of agroecosystems (Collins control, suggesting that if conservation biological et al. 2003; MacLeod et al. 2004). control efforts increase Pt. melanarius and B. quadr- imaculatum populations simultaneously, S. lineatus Acknowledgements eggs will continue to be preyed upon to a significant degree. We are grateful to M. Adams, K. Burgess, D. Kanas- In addition to being a victim of intraguild preda- hiro and C. Herle for their technical assistance and tion, B. quadrimaculatum are classified as generalists valuable advice during this research. We also thank that prey upon various life stages of insects from S. Bourassa and C. Wood for assistance with staphy- several orders, including Coleoptera, Diptera, linid identification. Funding for S. lineatus research Homoptera and Lepidoptera (Sunderland 2002; Fox in Alberta was provided by the Alberta and Sas- et al. 2005). The role of generalists in biological con- katchewan Pulse Grower Commissions, the Alberta trol is under debate (see review by Symondson et al. Crop Industry Development Fund, and Agriculture 2002). Generally, specialists are considered to be and Agri-Food Canada – Matching Investment Initia- most effective against exotic pests, whereas general- tive and Abase Funds. ists or generalist assemblages are most effective against native pests (Symondson et al. 2002). How- References ever, as Symondson et al. (2002) observed in their review of biological control research, in 75% of Andersen A, Hansen A˚ G, Rydland N, Øyre G, 1983. cases, generalists significantly reduced both exotic Carabidae and Staphylinidae (Col.) as predators of the and indigenous pests. New pest-enemy associations turnip root fly Delia floralis Falle´n (Diptera: Antho- are also effective for controlling exotic pests, as Hok- myiidae) in cage experiments. Z. Angew. Entomol. kanen and Pimentel (1984) found that generalist 95, 499–506. enemies had significant suppressive effects in 45% of Baines D, Stewart R, Boivin G, 1990. Consumption of new associations for exotic pests. In the case of carrot weevil (Coleoptera: Curculionidae) by five spe- S. lineatus, an exotic pest, the indigenous ground cies of carabids (Coleoptera: Carabidae) abundant in beetle species, B. quadrimaculatum, appears to have carrot fields in southwestern Quebec. Environ. Ento- significant potential for conservation biological con- mol. 19, 1146–1149. Bourassa S, 2006. Response of carabid assemblages to trol, despite its generalist habit. genetically modified herbicide-tolerant corn and to sus- In the field, pea leaf weevil egg consumption by tainable farming. MSc Thesis, Department of Renew- B. quadrimaculatum is expected to be lower than in able Resources, University of Alberta, Edmonton, the laboratory, due to the presence of alternative p. 20, 60. prey, competition and intraguild predation. How- Bourassa S, Ca´rcamo HA, Larney FJ, Spence JR, 2008. ever, a conservation biological control program to Carabid assemblages (Coleoptera: Carabidae) in a promote B. quadrimaculatum, as well as P. scitulus and rotation of three different crops in southern Alberta, staphylinid beetles, which also preyed upon S. linea- Canada: a comparison of sustainable and conventional tus eggs, albeit in lower numbers, should be benefi- farming. Environ. Entomol. 37, 1214–1223. cial in agroecosystems. Conservation biological Cantot P, 1986. 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J. Appl. Entomol. 135 (2011) 293–301 ª 2010 Blackwell Verlag, GmbH 299 Potential indigenous natural enemies of Sitona lineatus M. A. Vankosky, H. A. Ca´ rcamo and L. M. Dosdall

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