The Impact of the Carrot Rust Fly and Carrot Weevil Integrated Pest Management Program on the Ground-Dwelling Beetle Complex in Commercial Carrot Fields at the Holland Marsh, Ontario, Canada

The Impact of the Carrot Rust Fly and Carrot Weevil Integrated Pest Management Program on the... Abstract Carrot rust fly (CRF), Psila rosae (Fabricius, 1794) (Psilidae: Diptera) and carrot weevil (CW), Listronotus oregonensis (Le Conte, 1857) (Curculionidae: Coleoptera) are economic pests of carrot; larval tunneling on roots results in direct damage rendering the carrot unmarketable. The Holland Marsh in Ontario, Canada, is a major carrot production area. The ground-dwelling beetle (Coleoptera) fauna in commercial carrot fields in this region has not been described. In 2015 and 2016, eight commercial carrot fields were surveyed using pitfall traps to determine abundance and diversity of the ground-dwelling beetle complex. Research sites, which were used to evaluate the effectiveness of an existing integrated pest management (IPM) program, were also surveyed to determine the impacts of the IPM program on the natural enemy diversity, compared to insecticide-free sites. In total, 50 taxa and 4,127 individual ground-dwelling beetles were identified over the course of the 2 y. Known natural enemies of CRF and CW were identified and recovered in abundance. The abundance and diversity of ground-dwelling beetles among the commercial carrot fields varied greatly in 2015 and 2016 but was similar on research sites sprayed according to the IPM program compared to insecticide-free sites in both years. The importance of this research to promote conservation biological control through the naturalization of nonagricultural areas is discussed. Psila rosae, Listronotus oregonensis, conservation biological control, integrated pest management, Carabidae Carrot rust fly (CRF) (Psila rosae (Fabricius 1794) (Psilidae: Diptera)) and carrot weevil (CW) (Listronotus oregonensis (Le Conte 1857) (Curculionidae: Coleoptera)) are serious pests of carrots and other apiaceous crops. CRF is found throughout most of the temperate world (Dufault and Coaker 1987), while CW is found exclusively in northeastern North America (Boivin 1999). The Holland Marsh, Ontario, Canada, located 50 km north of Toronto, is 2,800 hectares in size and represents one of the major carrot production areas in Canada. This area is intensively cultivated due to its fertile soil. CRF deposits its eggs in the soil near carrot roots, while CW deposits its eggs in pits on the carrot leaf. Larva of both pests feed on the taproot (i.e., the carrot) creating mines, which render the carrot unmarketable. Foliar application of contact insecticides is the primary control method for carrot growers in the Holland Marsh and elsewhere in Canada. In agro-ecosystems, the importance of pest suppression by natural enemies is often neglected. Natural enemies save farmers more than $4.5 billion annually in the United States alone (Losey and Vaughan 2006). Several studies have shown that polyphagous predators can suppress dipteran pests, including the cabbage maggot (Delia radicum (Linnaeus 1758) (Diptera: Anthomyiidae)) (Coaker and Williams 1963, Finch and Elliot 1992), the turnip maggot (Delia floralis (Fallen 1824) (Diptera: Anthomyiidae)) (Andersen and Sharman 1983), the wheat bulb fly (Delia coarctata (Fallen 1825) (Diptera: Anthomyiidae)) (Jones 1975), and the frit fly (Oscinella frit (Linnaeus 1758) (Diptera: Chloropidae)) (Allen and Pienkowski 1975). CRF eggs are prone to predation from ground-dwelling beetles, such as carabids and staphylinids, as CRF eggs are deposited at or near the soil surface (Burn 1982). Furthermore, seed predators have also been shown to provide weed control in agroecosystems (Brust and House 1988). Carrot agro-ecosystems have previously been surveyed for ground-dwelling beetles (Berry et al. 1996, Sivasubramaniam et al. 1997, Colignon et al. 2002, Albert et al. 2003, Brunke et al. 2009, and Picault 2013), although only two studies (Wright et al. 1947, Burn 1982) evaluated the ability of specific natural enemies to consume CRF. Burn (1982) determined that small beetles (<8 mm in length), such as Trechus quadristriatus (Schrank 1781) (Coleoptera: Carabidae), Bembidion quadrimaculatum oppositum Say, 1823 (Coleoptera: Carabidae) and Aleocharinae Fleming, 1821 (Coleoptera: Staphylinidae) species, are responsible for the majority of the CRF egg predation. Few studies have evaluated the natural enemies of CW (Baines et al. 1990, Zhao et al. 1990, Cormier et al. 1996). Like CRF, it is likely that polyphagous ground-dwelling beetles prey on CW, and five carabids have been confirmed to feed on the various life stages of CW in a laboratory setting: Anisodactylus sanctaecrucis (Fabricius 1798) (Coleoptera: Carabidae), Pterostichus melanarius (Illiger 1798) (Coleoptera: Carabidae), Poecilus lucublandus (Say 1823) (Coleoptera: Carabidae), B. quadrimaculatum oppositum, and Clivina fossor (Linnaeus 1758) (Coleoptera: Carabidae) (Baines et al. 1990). The objectives of this study were to: 1) determine the diversity of polyphagous ground-dwelling beetles in carrot fields, including the presence of known CRF and CW natural enemies (i.e., predators), and 2) evaluate the effects of an existing integrated pest management (IPM) program for carrot insect pests at the Holland Marsh on the biodiversity of ground-dwelling beetles. Methods Determining the Biodiversity of Ground-Dwelling Beetles In 2015, four commercial carrot fields in the Holland Marsh (near Bradford, Ontario, [44°N, 79°W]) were selected to be surveyed. These fields were labeled A, B, C, and, D and represented the four quadrants of the Holland Marsh. This survey was repeated in 2016; however, four different commercial carrot fields labeled E, F, G, and H, were utilized. The location of these sites was chosen based on the proximity to fields, which had high pest pressure the previous year, and were currently participating in the IPM program administered by the University of Guelph—Muck Crops Research Station (MCRS). The fields chosen in 2015 were not seeded to carrots in 2016 because of the normal crop rotation followed by commercial growers. Evaluating the Effects of an Existing IPM Program An ongoing research trial at the MCRS that evaluated the IPM program used to manage carrot insect pests allowed for the collection of ground-dwelling beetles in areas free of insecticide applications as well as comparable areas, which followed IPM recommendations for CW and CRF (OMAFRA 1996). Based on CW monitoring and the IPM recommendations, a single application of phosmet (Imidan 70 WP) at a rate of 1.6 kg ai/ha was applied to the plots receiving the IPM insecticide treatments on 19 June 2015 and on 21 June 2016. Trapping rates for CRF exceeded the economic threshold of 0.1 CRF/trap/day and cypermethrin (Ripcord 400 EC, BASF Canada, Mississauga, ON) was applied to the insecticide plots at 175 ml ai/ha on 19 June, 4 August, and 25 August 2015, and applied on 4 and 16 August 2016. All insecticides were applied using a tractor-mounted sprayer calibrated to deliver 500 liters water/ha. No spray records were available for the commercial sites, but these would have been treated with similar insecticides. Pitfall traps were used to measure the presence of ground-dwelling arthropods (Southwood 1994). Two pairs of pitfall traps, each consisting of two nested 475 ml Pro-Kal polypropylene deli container (11.5 cm diameter × 7.5 cm depth; Fabri-Kal Corp, Kalamazoo, MI), were placed in each field. Traps were placed between carrot hills, 5 m from the side of the field. One pair of traps was placed 10 m from the edge while the pair of traps on the opposite sides of the field was placed 25 m from the edge. The individual traps within each pairing were placed approximately 5 m from each other. In the research trials, two traps were placed on opposite sides in each of the six 14 × 25 m blocks. In 2016, the research trial was expanded to two locations within the Holland Marsh, both locations had six 14 × 15 m plots, and they were sampled similarly to 2015. Pitfall traps were ¼ filled with 70% EtOH. All traps were placed in the ground so that the top lip was level with the soil surface. Pitfall traps were protected by foam plates (23 cm diameter) secured 1 cm above the soil with wooden skewers. In 2015, the contents of each trap were collected weekly between 28 May and 4 September except for field C for which the traps were removed after the week of 6 August. In 2016, the contents of the traps were collected weekly between 9 June and 31 August. These dates were chosen so that traps were placed in the fields shortly after carrot seeding and were removed prior to carrot harvest. Occasionally, traps were not collected (fields C and D on 30 July, and field A on 6 August, and 13 August in 2015; field E on 30 June, field F on 23 June, and field G on 28 July in 2016) due to reentry interval restrictions following pesticide applications. In those instances, trap contents were collected the following week. In 2015, soil from the traps, was processed through a series of sieves ranging from 8 mm decreasing to 820 μm. Concerned about the lack of small beetles recovered in 2015, an additional finer sieve with a screen size of 400 μm was added to the sieving process in 2016. In both years, all arthropods collected were placed into 475 ml polypropylene containers containing 75% ethyl alcohol and then into cold storage (6°C, 90–95% RH) until they were identified. Carabids were identified to the lowest taxonomic level using the key and nomenclature of Bousquet (2010). The most common Staphylinidae recovered in the traps were identified to the Aleocharinae subfamily based on Brunke et al. (2011). Aleocharinae are difficult to distinguish (Brunke et al. 2009), and therefore were not separated in this study. Lowest taxonomic level and abundance of each taxon, trap location, and collection date were recorded for every trap. Rarefaction curves were created for each commercial carrot field as well as the IPM and insecticide-free sites. Simpson’s diversity index (Simpson 1949) was used to determine species diversity for individual commercial carrot fields as well as the research plots. Rarefaction curves and Simpson’s diversity index where calculated with the Vegan package (version 2.3.5) in R (version 2.3.5) (R Core team 2016). Results Biodiversity of Ground-Dwelling Beetles In 2015, a total of 1,105 individuals from 25 taxa were recovered and identified from the pitfall traps in the Holland Marsh (Table 1). Nine taxa represented >95% of the captured insects, and are therefore considered dominant taxa. Dominant taxa were identified as: A. sanctaecrucis (26.3%), P. melanarius (23.4%), Stenolophus comma (Fabricius 1775) (Coleoptera: Carabidae) (18.6%), Amara spp. Bonelli (Coleoptera: Carabidae), 1810 (11.2%), Omophron americanum Dejean (Coleoptera: Carabidae), 1831 (8.2%), Aleocharinae spp. (Coleoptera: Staphylinidae) (2.7%), C. fossor (2.3%), and Cicindela duodecimguttata Dejean (Coleoptera: Carabidae), 1825 (1.9%), and Po. lucublandus (1.4%). All other taxa represented <1% of the total abundance. These were: Anisodactylus harrisii LeConte (Coleoptera: Carabidae), 1863, Atranus sp. LeConte (Coleoptera: Carabidae), 1847, Amerizus wingatei (Bland 1864) (Coleoptera: Carabidae), Dicaelus teter Bonelli (Coleoptera: Carabidae), 1813, Harpalus somnulentus Dejean (Coleoptera: Carabidae), 1829, Harpalus calignosus (Coleoptera: Carabidae), Histeridae Gyllenhal, 1808, Laemostenus complanatus (Dejean, 1828) (Coleoptera: Carabidae), Loricera pilicornis (Fabricius, 1775) (Coleoptera: Carabidae), Patrobus longicornis (Say, 1823) (Coleoptera: Carabidae), Poecilus chalcites (Say, 1823) (Coleoptera: Carabidae), Pseudamara arenaria (LeConte, 1847) (Coleoptera: Carabidae), Stenolophus fuliginosus Dejean (Coleoptera: Carabidae), 1829, Stereocerus sp. Kirby (Coleoptera: Carabidae), 1837, and Tachyta inornata (Say, 1823) (Coleoptera: Carabidae). The confirmed predator of CRF, B. quadrimaculatum, as well as Aleocharinae spp. which could include predators or parasitoids (Wright et al. 1947) of CRF were identified, but were not recovered in high numbers. In 2016, 2,753 individuals from 38 taxa were recovered and identified from the pitfall traps (Table 2). Increased abundance and diversity of specimens in 2016 was due to the addition of a finer screen in the soil sieving process. There were nine dominant taxa again in 2016 including: Staphylinidae (29.1%), P. melanarius (17.2%), A. sanctaecrucis (13.0%), Amara lunicollis Schiødte (Coleoptera: Carabidae), 1837 (11.5%), B. quadrimaculatum (8.6%), S. comma (7.3%), Bembidion spp. Latreille, 1802 (4.5%), Amara patruelis Dejean (Coleoptera: Carabidae), 1831 (2.3%), and C. fossor (1.6%). All other taxa, other than Dyschirius montanus LeConte (Coleoptera: Carabidae), 1879 (1.3%), represented <1% of the total abundance. These were: Acupalpus partiarius (Say, 1823) (Coleoptera: Carabidae), Amara avida (Say, 1823) (Coleoptera: Carabidae), Amara obesa (Say, 1823) (Coleoptera: Carabidae), Anisodactylus verticalis (LeConte 1847) (Coleoptera: Carabidae), Atranus sp., Bradycellus atrimedeus (Say, 1823) (Coleoptera: Carabidae), Bradycellus rupestris (Say, 1823) (Coleoptera: Carabidae), Carabus sp. Linnaeus (Coleoptera: Carabidae), 1758, Chlaenius cordicollis Kirby (Coleoptera: Carabidae), 1837, C. duodecimguttata, Clivina sp. Latreille (Coleoptera: Carabidae), 1802, Coccinella septempunctata Linnaeus, 1758, Coleomegilla maculata (De Geer, 1775), Dyschirius pallipennis (Say, 1823) (Coleoptera: Carabidae), Harpalus affinis (Schrank, 1781) (Coleoptera: Carabidae), Histeridae, L. pilicornis, O. americanum, Patrobus sp. Dejean (Coleoptera: Carabidae), 1821, Po. lucublandus, Polyderis laevis (Say, 1823) (Coleoptera: Carabidae), Porotachys bisulcatus (Nicolai, 1822) (Coleoptera: Carabidae), Pterostichus permundus (Say, 1830) (Coleoptera: Carabidae), Schizogenius lineolatus (Say, 1823) (Coleoptera: Carabidae), S. fuliginosus, and Tachys sp. Casey (Coleoptera: Carabidae), 1918). Commercial Carrot Fields In 2015, only 10 different taxa were identified in the four surveyed commercial carrot fields, with a total abundance of 228 individuals (Table 1). These numbers increased greatly in 2016, likely due to the addition of a finer screen in the soil sieving process, with 27 taxa and 1,401 individuals recovered from the four commercial carrot fields (Table 2). Rarefaction curves for 2015 and 2016 (Fig. 1) showed a substantial difference in species richness and abundance among fields. The Simpson’s index varied among fields, and was generally low in 2015 (Table 1). There was a substantial increase in Simpson’s index values and less variability among fields in 2016 (Table 2). Fig. 1. View largeDownload slide Rarefaction curves for four commercial carrot fields surveyed with pitfall traps for carrot insect pest natural enemies in 2015 and 2016 in the Holland Marsh, Ontario, Canada. Fig. 1. View largeDownload slide Rarefaction curves for four commercial carrot fields surveyed with pitfall traps for carrot insect pest natural enemies in 2015 and 2016 in the Holland Marsh, Ontario, Canada. Table 1. Diversity (number of insect species) and abundance (number of individual insects collected) of CRF and CW natural enemies collected in pitfall traps in the Holland Marsh, 2015 Location No. of species collected No. individuals collected Simpson’s index Commercial field A 7 136 0.290 Commercial field B 3 25 0.563 Commercial field C 6 35 0.464 Commercial field D 5 32 0.445 Research plot (IPM) 19 447 0.830 Research plot (Control) 18 430 0.832 Commercial field total 10 228 0.627 Research plot total 24 877 0.832 2015 Total 25 1,105 0.820 Location No. of species collected No. individuals collected Simpson’s index Commercial field A 7 136 0.290 Commercial field B 3 25 0.563 Commercial field C 6 35 0.464 Commercial field D 5 32 0.445 Research plot (IPM) 19 447 0.830 Research plot (Control) 18 430 0.832 Commercial field total 10 228 0.627 Research plot total 24 877 0.832 2015 Total 25 1,105 0.820 View Large Table 1. Diversity (number of insect species) and abundance (number of individual insects collected) of CRF and CW natural enemies collected in pitfall traps in the Holland Marsh, 2015 Location No. of species collected No. individuals collected Simpson’s index Commercial field A 7 136 0.290 Commercial field B 3 25 0.563 Commercial field C 6 35 0.464 Commercial field D 5 32 0.445 Research plot (IPM) 19 447 0.830 Research plot (Control) 18 430 0.832 Commercial field total 10 228 0.627 Research plot total 24 877 0.832 2015 Total 25 1,105 0.820 Location No. of species collected No. individuals collected Simpson’s index Commercial field A 7 136 0.290 Commercial field B 3 25 0.563 Commercial field C 6 35 0.464 Commercial field D 5 32 0.445 Research plot (IPM) 19 447 0.830 Research plot (Control) 18 430 0.832 Commercial field total 10 228 0.627 Research plot total 24 877 0.832 2015 Total 25 1,105 0.820 View Large Table 2. Diversity (number of insect species) and abundance (number of individual insects collected) of CRF and CW natural enemies collected in pitfall traps in the Holland Marsh, 2016 Location No. of species collected No. of individuals collected Simpson’s index Commercial field E 19 870 0.783 Commercial field F 10 70 0.805 Commercial field G 15 227 0.783 Commercial field H 20 234 0.768 Research plot (IPM) 24 686 0.797 Research plot (Control) 23 666 0.769 Commercial field total 27 1,401 0.851 Research plot total 30 1,352 0.786 2016 total 38 2,753 0.848 Location No. of species collected No. of individuals collected Simpson’s index Commercial field E 19 870 0.783 Commercial field F 10 70 0.805 Commercial field G 15 227 0.783 Commercial field H 20 234 0.768 Research plot (IPM) 24 686 0.797 Research plot (Control) 23 666 0.769 Commercial field total 27 1,401 0.851 Research plot total 30 1,352 0.786 2016 total 38 2,753 0.848 View Large Table 2. Diversity (number of insect species) and abundance (number of individual insects collected) of CRF and CW natural enemies collected in pitfall traps in the Holland Marsh, 2016 Location No. of species collected No. of individuals collected Simpson’s index Commercial field E 19 870 0.783 Commercial field F 10 70 0.805 Commercial field G 15 227 0.783 Commercial field H 20 234 0.768 Research plot (IPM) 24 686 0.797 Research plot (Control) 23 666 0.769 Commercial field total 27 1,401 0.851 Research plot total 30 1,352 0.786 2016 total 38 2,753 0.848 Location No. of species collected No. of individuals collected Simpson’s index Commercial field E 19 870 0.783 Commercial field F 10 70 0.805 Commercial field G 15 227 0.783 Commercial field H 20 234 0.768 Research plot (IPM) 24 686 0.797 Research plot (Control) 23 666 0.769 Commercial field total 27 1,401 0.851 Research plot total 30 1,352 0.786 2016 total 38 2,753 0.848 View Large Effects of an Established IPM Program In 2015, 447 individuals from 19 taxa were recovered in the IPM plots and 430 individuals from 18 taxa in the control plots (Table 1). A similar trend was found in 2016, as 686 individuals from 24 taxa were recovered in the IPM plots and 666 individuals from 23 taxa in the control plots (Table 2). Rarefaction curves for 2015 and 2016 (Fig. 2) showed that the species richness and abundance for the IPM plots and non-IPM (insecticide-free, control plots) were nearly identical. These curves indicate that while the sampling effort was insufficient to determine the entire species richness of a site, the use of 12 traps per plot in the research sites captured more of the total species richness than the four traps per site used in the commercial fields. The Simpson’s index did not differ between IPM or control plots, and this was consistent in both 2015 and 2016. The Simpson’s index for these research plots were much greater than those found in commercial fields, especially in 2015 (Tables 1 and 2). Fig. 2. View largeDownload slide Rarefaction curves for plots which received insecticides based on the existing IPM program for CRF and CW and insecticide-free control plots in the Holland Marsh, Ontario, Canada. Plots were surveyed with pitfall traps for natural enemies of carrot insect pests in 2015 and 2016. Fig. 2. View largeDownload slide Rarefaction curves for plots which received insecticides based on the existing IPM program for CRF and CW and insecticide-free control plots in the Holland Marsh, Ontario, Canada. Plots were surveyed with pitfall traps for natural enemies of carrot insect pests in 2015 and 2016. Discussion Few studies have evaluated the diversity of ground-dwelling beetles in carrot fields or in the Holland Marsh. To our knowledge, the last survey for ground-dwelling beetles in the Holland Marsh was conducted in 1985 (Tomlin et al. 1985). However, that study focused on natural enemies of onion maggot (Delia antiqua (Meigen 1826) (Diptera: Anthomyiidae)) and used onion maggot mass-rearing beds as an attractant, rather than utilizing pitfall traps. Brunke et al. (2009) conducted the only survey for ground-dwelling beetles in carrot fields in North America, and identified 50 carabid species, 12 of which were also identified in the present survey. However, the purpose of that survey was to identify natural enemies of millipedes in both carrot and sweet potato fields. Furthermore, edge habitats were also sampled rather than just within the crop sites, as in this survey. Two of the eight dominant species in Brunke et al. (2009) were found to be dominant in this study (i.e., P. melanarius and B. quadrimaculatum). All other surveys in carrot fields have been conducted in either Europe (Colignon et al. 2002, Albert et al. 2003, Picault 2013) or New Zealand (Berry et al. 1996, Sivasubramaniam et al. 1997) and represent a much different fauna. A total of 49 unique taxa, including confirmed natural enemies of CRF and CW, were identified in 2015–2016 from 3858 individual specimens. The total abundance, as well as the number of taxa identified in 2016 was much greater than that in 2015. This is largely due to the addition of the 400 μm sieve to the sieving process used to recover insects from the pitfall traps. This resulted in better collection of small taxa, especially Bembidion species and Staphylinidae. This correction was important due to the findings by Burn (1982) that smaller carabid (<8 mm in length) species are likely responsible for most of the CRF predation. In 2016, there was a 10-fold increase in the number of Bembidion individuals recovered compared to 2015. Staphylinidae collection also increased greatly, from 30 individuals in 2015 to 800 in 2016. Both taxa are of special interest in the survey as they include known natural enemies of carrot insect pests. Absent from the survey in both years was the known CRF predator T. quadristriatus. This is significant as it has previously been recorded in carrot fields in Ontario (Brunke et al. 2009, Bousquet 2012). The absence of this species could indicate that our trapping methods were not effective at recovering this ground-dwelling beetle. The generated rarefaction curves failed to converge, indicating that an insufficient sampling effort was conducted to determine the entire species diversity. However, while the curves did not reach an asymptote, a substantial decrease in the slope for each curve was observed, indicating that a near-sufficient sampling effort was achieved. Future work will focus on expanding the number of sites and traps per site to achieve a sufficient sampling effort. However, all five known natural enemies of CW were recovered in this survey, most of which were found in high abundance. Chaput (1993) suggested that there are other potential natural enemies present in the Holland Marsh including Hemipterans such as Anthocoridae, Reduviidae, and Nabidae, as well as lacewings (Neuroptera: Chrysopidae) and ladybirds (Coleoptera: Coccinellidae). Many of these insects, while not captured in the pitfall traps, were observed in carrot fields during this survey. In a mark and recovery experiment, Burn (1982) found that the greatest levels of CRF egg loss coincided with the greatest activity from small carabids (<8mm in length). It is likely that CRF eggs are too small and dispersed to be of interest to larger carabids (Rämert 1996). Yet, some of the most abundant taxa recovered (e.g., P. melanarius, A. sanctaecrucis, and Amara spp.) were large carabids. Nevertheless, a large proportion of the taxa recovered are small and could predate on CRF eggs. While many of these smaller taxa were rarely captured in the traps, pitfall trapping is not an effective measure of population density, and small carabids are often under-represented in pitfall captures (Kromp 1999). Therefore, the importance of the numerous rare species found in this survey should not be ignored. While P. melanarius is likely too large to predate on CRF eggs, it has been found to feed on adult CW (Baines et al. 1990, Zhao et al. 1990). However, it was noted that P. melanarius is unable to feed on CW adults when they are on a carrot plant (Zhao et al. 1990), raising questions about their effectiveness in suppressing CW in a field setting. Many small carabids will feed on dipteran eggs when they are present on the soil surface, but a significant reduction in predation often occurs when eggs are laid below the surface (Finch and Elliot 1992) as is the case with CRF. However, B. quadrimaculatum has been observed to feed on onion maggot eggs buried up to 1 cm deep (Grafius and Warner 1989). B. quadrimaculatum, is also known to prey on CRF eggs (Burn 1982), and CW eggs (Baines et al. 1990). However, its ability to prey on CW eggs in a field setting has been questioned (Baines et al. 1990). In 2015, only P. melanarius and staphylinids were recovered in all four commercial fields as well as the research site. However, in 2016, seven taxa were recovered in all four commercial fields and both research sites (A. sanctaecrucis, B. quadrimaculatum, Bembidion spp., C. fossor, P. melanarius, S. comma, staphylinids, and spiders). The research sites had much greater diversity and abundance than the commercial sites, but were sampled with a much greater effort (12 traps per research site compared to four traps per commercial field). The commercial carrot fields with the most diverse insect species supported 70% (field A, 2015) and 75% (field H, 2016) of the total diversity identified, while the least diverse commercial fields supported only 30% (field B, 2015) and 39% (field F, 2016). A substantial difference in both the species abundance and richness was observed among the four commercial fields surveyed both years, suggesting that there are currently unknown drivers of ground-dwelling beetles diversity in the Holland Marsh. Increasing plant diversity has been shown to lead to an increase in herbivore diversity, and through a bottom-up cascade—an increase in predator and parasitoid diversity (Hunter and Price 1992, Siemann 1998). While not quantitatively measured, there was a trend where fields with greater plant diversity had greater ground-dwelling beetles diversity in this study. Notably, field A and E had much greater abundance and species richness of ground-dwelling beetles than the other three fields surveyed in their respective years. These agricultural fields were unique in their agro-ecosystem structure. Unlike most of the Holland Marsh, field A was bordered on three sides by naturalized areas, including a forested area and an overgrown greenhouse. Field E, on the other hand, was bordered by crop fields but had a poorly managed bank of weeds along the eastern border. The pitfall traps were also placed near residential property, which was surrounded by naturalized areas, with trees and vegetable gardens. Most notably, field E and the fields to its north and south were essentially overgrown by weeds for most of the trapping period. No other surveyed field had nearly the same plant species richness in close proximity as these two fields. This is consistent with the results of Bosch (1987) which found twice as many carabids in beets with 15–20% weed cover compared to weed-free plots. However, B. quadrimaculatum and T. quadristriatus were more active in weed-free plots (Bosch 1987). The same trend was found in this study, as B. quadrimaculatum was less abundant in field E compared to the more weed-free fields. Field H was also unique as it was the only field surveyed near the Holland River, which transects the Holland Marsh. This riparian zone along the river banks was likely responsible for the high species richness which occurred at this site. Both the species richness and abundance of ground-dwelling beetles in IPM program and insecticide-free control plots were nearly identical in 2015 and 2016. Furthermore, the Simpson’s index for the IPM program plots were consistent across both years, and was similar to the most diverse commercial field—field F in 2016. These results provide positive evidence for the sustainability of the IPM program currently used in the Holland Marsh. The recommendations of the IPM program resulted in a single application of phosmet and multiple cypermethrin applications in both years. Yet ground-dwelling beetles were just as abundant and diverse as in areas, which received no insecticides. While no other study evaluated the effects of CRF or CW natural enemies under an established IPM program, Sivasubramaniam (1996) found that the application of diazinon and phorate decreased the abundance of natural enemies in carrot fields in New Zealand. Freuler et al. (2003) looked at the effects of cypermethrin on carabid species richness in white cabbage in Switzerland, and found no fundamental change, but a slight reduction in abundance in B. quadrimaculatum was seen. Conversely, Wick and Freier (2000) found that applications of lambda-cyhalothrin in winter wheat in Germany reduced the species density and activity of carabids, but beetle numbers recovered by the following year. Not all the carabids that were recovered in the pitfall traps are potential CRF or CW predators. For example, L. pilicornis is a collembolan predator (Kromp 1999). However, Pterostichus, Bembidion, Carabus, and Dyschirius are among the few true predator genera in the Carabidae (Lindroth 1992). Certain Amara and Harpalus species are predominantly phytophagous (Lindroth 1992) and have been found to provide some weed control through seed predation (Brust and House 1988). It is likely that both omnivory and scavenging are more common within the Carabidae than is currently accepted (Lovei and Sunderland 1996). Therefore, it is important that an adequate and diverse food supply be present in an agro-ecosystem if the goal is to support a large and diverse natural enemy population. As CRF and CW are not always available, it is crucial that other food sources be present. Flowering plants play an important role by providing pollen, nectar, and seeds on which ground-dwelling beetles, including natural enemies, can feed in the absence of prey. Furthermore, by attracting other insects, flowering plants provide a source of prey for polyphagous predators (Isaacs et al. 2009). Previous conservation biological control efforts resulted in an insufficient increase in natural enemy pressure to provide substantial control of CRF in France (Picault 2013). Denser vegetation types (i.e., hedgerows) were found to increase the CRF population more than that of natural enemies. However, less dense vegetation such as grasses had less of an effect on CRF populations. It was suggested that future studies should evaluate the effectiveness of augmentative biological control in combination with conservation biological control efforts (Picault 2013). Previous attempts to introduce natural enemies of CRF within the Holland Marsh were focused on the introduction the parasitoids, Chorebus gracilis (Nees 1834) (Hymenoptera: Braconidae), and Loxotropa tritoma Thomson, 1859 (Hymenoptera: Diapriidae) (Maybee 1954). Unfortunately, the parasitoids, native to England, failed to survive the Canadian winter. Wright et al. (1947) also described Aleochara sparsa Heer, 1839 (Coleoptera: Staphylinidae) and a Kleidotoma sp. Westwood, 1833 (Hymenoptera: Figitidae) as CRF parasitoids found in England. Additionally, Cormier et al. (1996) determined that two parasitoids, Anaphes victus Huber, 1997 and Anaphes listronoti Huber, 1997 (Hymenoptera: Mymaridae) could parasitize CW eggs. While Picault (2013) evaluated the potential for Al. sparsa as part of a conservation biological control program in France, the three other parasitoids remain unstudied. The work presented here provides a description of the abundance and diversity of ground-dwelling beetles in carrot fields in the Holland Marsh, Ontario. The knowledge gained will be used in future conservation biological control efforts to naturalize uncultivated areas (i.e., canal berms) in the Holland Marsh, starting in 2017. This survey identified over 50 different insect species, most of which are polyphagous predators within the Carabidae, as was expected due to the study design using only pitfall traps. Many of these beetles play a vital role in the agro-ecosystem by suppressing pest populations. Known natural enemies of both major carrot insect pests, CRF and CW, were found in abundance in both research plots and commercial carrot fields. Furthermore, the application of insecticides based on the recommendations of an existing IPM program for carrot insect pests was not found to negatively impact the abundance or diversity of ground-dwelling beetles. 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Google Scholar CrossRef Search ADS PubMed Zhao , D. X. , G. Boivin , and R. K. Stewart . 1990 . Consumption of carrot weevil, Listronotus oregonensis (Coleoptera: Curculionidae) by four species of carabids on host plants in the laboratory . Entomophaga . 35 : 57 – 60 . Google Scholar CrossRef Search ADS © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Environmental Entomology Oxford University Press

The Impact of the Carrot Rust Fly and Carrot Weevil Integrated Pest Management Program on the Ground-Dwelling Beetle Complex in Commercial Carrot Fields at the Holland Marsh, Ontario, Canada

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Entomological Society of America
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10.1093/ee/nvy078
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Abstract

Abstract Carrot rust fly (CRF), Psila rosae (Fabricius, 1794) (Psilidae: Diptera) and carrot weevil (CW), Listronotus oregonensis (Le Conte, 1857) (Curculionidae: Coleoptera) are economic pests of carrot; larval tunneling on roots results in direct damage rendering the carrot unmarketable. The Holland Marsh in Ontario, Canada, is a major carrot production area. The ground-dwelling beetle (Coleoptera) fauna in commercial carrot fields in this region has not been described. In 2015 and 2016, eight commercial carrot fields were surveyed using pitfall traps to determine abundance and diversity of the ground-dwelling beetle complex. Research sites, which were used to evaluate the effectiveness of an existing integrated pest management (IPM) program, were also surveyed to determine the impacts of the IPM program on the natural enemy diversity, compared to insecticide-free sites. In total, 50 taxa and 4,127 individual ground-dwelling beetles were identified over the course of the 2 y. Known natural enemies of CRF and CW were identified and recovered in abundance. The abundance and diversity of ground-dwelling beetles among the commercial carrot fields varied greatly in 2015 and 2016 but was similar on research sites sprayed according to the IPM program compared to insecticide-free sites in both years. The importance of this research to promote conservation biological control through the naturalization of nonagricultural areas is discussed. Psila rosae, Listronotus oregonensis, conservation biological control, integrated pest management, Carabidae Carrot rust fly (CRF) (Psila rosae (Fabricius 1794) (Psilidae: Diptera)) and carrot weevil (CW) (Listronotus oregonensis (Le Conte 1857) (Curculionidae: Coleoptera)) are serious pests of carrots and other apiaceous crops. CRF is found throughout most of the temperate world (Dufault and Coaker 1987), while CW is found exclusively in northeastern North America (Boivin 1999). The Holland Marsh, Ontario, Canada, located 50 km north of Toronto, is 2,800 hectares in size and represents one of the major carrot production areas in Canada. This area is intensively cultivated due to its fertile soil. CRF deposits its eggs in the soil near carrot roots, while CW deposits its eggs in pits on the carrot leaf. Larva of both pests feed on the taproot (i.e., the carrot) creating mines, which render the carrot unmarketable. Foliar application of contact insecticides is the primary control method for carrot growers in the Holland Marsh and elsewhere in Canada. In agro-ecosystems, the importance of pest suppression by natural enemies is often neglected. Natural enemies save farmers more than $4.5 billion annually in the United States alone (Losey and Vaughan 2006). Several studies have shown that polyphagous predators can suppress dipteran pests, including the cabbage maggot (Delia radicum (Linnaeus 1758) (Diptera: Anthomyiidae)) (Coaker and Williams 1963, Finch and Elliot 1992), the turnip maggot (Delia floralis (Fallen 1824) (Diptera: Anthomyiidae)) (Andersen and Sharman 1983), the wheat bulb fly (Delia coarctata (Fallen 1825) (Diptera: Anthomyiidae)) (Jones 1975), and the frit fly (Oscinella frit (Linnaeus 1758) (Diptera: Chloropidae)) (Allen and Pienkowski 1975). CRF eggs are prone to predation from ground-dwelling beetles, such as carabids and staphylinids, as CRF eggs are deposited at or near the soil surface (Burn 1982). Furthermore, seed predators have also been shown to provide weed control in agroecosystems (Brust and House 1988). Carrot agro-ecosystems have previously been surveyed for ground-dwelling beetles (Berry et al. 1996, Sivasubramaniam et al. 1997, Colignon et al. 2002, Albert et al. 2003, Brunke et al. 2009, and Picault 2013), although only two studies (Wright et al. 1947, Burn 1982) evaluated the ability of specific natural enemies to consume CRF. Burn (1982) determined that small beetles (<8 mm in length), such as Trechus quadristriatus (Schrank 1781) (Coleoptera: Carabidae), Bembidion quadrimaculatum oppositum Say, 1823 (Coleoptera: Carabidae) and Aleocharinae Fleming, 1821 (Coleoptera: Staphylinidae) species, are responsible for the majority of the CRF egg predation. Few studies have evaluated the natural enemies of CW (Baines et al. 1990, Zhao et al. 1990, Cormier et al. 1996). Like CRF, it is likely that polyphagous ground-dwelling beetles prey on CW, and five carabids have been confirmed to feed on the various life stages of CW in a laboratory setting: Anisodactylus sanctaecrucis (Fabricius 1798) (Coleoptera: Carabidae), Pterostichus melanarius (Illiger 1798) (Coleoptera: Carabidae), Poecilus lucublandus (Say 1823) (Coleoptera: Carabidae), B. quadrimaculatum oppositum, and Clivina fossor (Linnaeus 1758) (Coleoptera: Carabidae) (Baines et al. 1990). The objectives of this study were to: 1) determine the diversity of polyphagous ground-dwelling beetles in carrot fields, including the presence of known CRF and CW natural enemies (i.e., predators), and 2) evaluate the effects of an existing integrated pest management (IPM) program for carrot insect pests at the Holland Marsh on the biodiversity of ground-dwelling beetles. Methods Determining the Biodiversity of Ground-Dwelling Beetles In 2015, four commercial carrot fields in the Holland Marsh (near Bradford, Ontario, [44°N, 79°W]) were selected to be surveyed. These fields were labeled A, B, C, and, D and represented the four quadrants of the Holland Marsh. This survey was repeated in 2016; however, four different commercial carrot fields labeled E, F, G, and H, were utilized. The location of these sites was chosen based on the proximity to fields, which had high pest pressure the previous year, and were currently participating in the IPM program administered by the University of Guelph—Muck Crops Research Station (MCRS). The fields chosen in 2015 were not seeded to carrots in 2016 because of the normal crop rotation followed by commercial growers. Evaluating the Effects of an Existing IPM Program An ongoing research trial at the MCRS that evaluated the IPM program used to manage carrot insect pests allowed for the collection of ground-dwelling beetles in areas free of insecticide applications as well as comparable areas, which followed IPM recommendations for CW and CRF (OMAFRA 1996). Based on CW monitoring and the IPM recommendations, a single application of phosmet (Imidan 70 WP) at a rate of 1.6 kg ai/ha was applied to the plots receiving the IPM insecticide treatments on 19 June 2015 and on 21 June 2016. Trapping rates for CRF exceeded the economic threshold of 0.1 CRF/trap/day and cypermethrin (Ripcord 400 EC, BASF Canada, Mississauga, ON) was applied to the insecticide plots at 175 ml ai/ha on 19 June, 4 August, and 25 August 2015, and applied on 4 and 16 August 2016. All insecticides were applied using a tractor-mounted sprayer calibrated to deliver 500 liters water/ha. No spray records were available for the commercial sites, but these would have been treated with similar insecticides. Pitfall traps were used to measure the presence of ground-dwelling arthropods (Southwood 1994). Two pairs of pitfall traps, each consisting of two nested 475 ml Pro-Kal polypropylene deli container (11.5 cm diameter × 7.5 cm depth; Fabri-Kal Corp, Kalamazoo, MI), were placed in each field. Traps were placed between carrot hills, 5 m from the side of the field. One pair of traps was placed 10 m from the edge while the pair of traps on the opposite sides of the field was placed 25 m from the edge. The individual traps within each pairing were placed approximately 5 m from each other. In the research trials, two traps were placed on opposite sides in each of the six 14 × 25 m blocks. In 2016, the research trial was expanded to two locations within the Holland Marsh, both locations had six 14 × 15 m plots, and they were sampled similarly to 2015. Pitfall traps were ¼ filled with 70% EtOH. All traps were placed in the ground so that the top lip was level with the soil surface. Pitfall traps were protected by foam plates (23 cm diameter) secured 1 cm above the soil with wooden skewers. In 2015, the contents of each trap were collected weekly between 28 May and 4 September except for field C for which the traps were removed after the week of 6 August. In 2016, the contents of the traps were collected weekly between 9 June and 31 August. These dates were chosen so that traps were placed in the fields shortly after carrot seeding and were removed prior to carrot harvest. Occasionally, traps were not collected (fields C and D on 30 July, and field A on 6 August, and 13 August in 2015; field E on 30 June, field F on 23 June, and field G on 28 July in 2016) due to reentry interval restrictions following pesticide applications. In those instances, trap contents were collected the following week. In 2015, soil from the traps, was processed through a series of sieves ranging from 8 mm decreasing to 820 μm. Concerned about the lack of small beetles recovered in 2015, an additional finer sieve with a screen size of 400 μm was added to the sieving process in 2016. In both years, all arthropods collected were placed into 475 ml polypropylene containers containing 75% ethyl alcohol and then into cold storage (6°C, 90–95% RH) until they were identified. Carabids were identified to the lowest taxonomic level using the key and nomenclature of Bousquet (2010). The most common Staphylinidae recovered in the traps were identified to the Aleocharinae subfamily based on Brunke et al. (2011). Aleocharinae are difficult to distinguish (Brunke et al. 2009), and therefore were not separated in this study. Lowest taxonomic level and abundance of each taxon, trap location, and collection date were recorded for every trap. Rarefaction curves were created for each commercial carrot field as well as the IPM and insecticide-free sites. Simpson’s diversity index (Simpson 1949) was used to determine species diversity for individual commercial carrot fields as well as the research plots. Rarefaction curves and Simpson’s diversity index where calculated with the Vegan package (version 2.3.5) in R (version 2.3.5) (R Core team 2016). Results Biodiversity of Ground-Dwelling Beetles In 2015, a total of 1,105 individuals from 25 taxa were recovered and identified from the pitfall traps in the Holland Marsh (Table 1). Nine taxa represented >95% of the captured insects, and are therefore considered dominant taxa. Dominant taxa were identified as: A. sanctaecrucis (26.3%), P. melanarius (23.4%), Stenolophus comma (Fabricius 1775) (Coleoptera: Carabidae) (18.6%), Amara spp. Bonelli (Coleoptera: Carabidae), 1810 (11.2%), Omophron americanum Dejean (Coleoptera: Carabidae), 1831 (8.2%), Aleocharinae spp. (Coleoptera: Staphylinidae) (2.7%), C. fossor (2.3%), and Cicindela duodecimguttata Dejean (Coleoptera: Carabidae), 1825 (1.9%), and Po. lucublandus (1.4%). All other taxa represented <1% of the total abundance. These were: Anisodactylus harrisii LeConte (Coleoptera: Carabidae), 1863, Atranus sp. LeConte (Coleoptera: Carabidae), 1847, Amerizus wingatei (Bland 1864) (Coleoptera: Carabidae), Dicaelus teter Bonelli (Coleoptera: Carabidae), 1813, Harpalus somnulentus Dejean (Coleoptera: Carabidae), 1829, Harpalus calignosus (Coleoptera: Carabidae), Histeridae Gyllenhal, 1808, Laemostenus complanatus (Dejean, 1828) (Coleoptera: Carabidae), Loricera pilicornis (Fabricius, 1775) (Coleoptera: Carabidae), Patrobus longicornis (Say, 1823) (Coleoptera: Carabidae), Poecilus chalcites (Say, 1823) (Coleoptera: Carabidae), Pseudamara arenaria (LeConte, 1847) (Coleoptera: Carabidae), Stenolophus fuliginosus Dejean (Coleoptera: Carabidae), 1829, Stereocerus sp. Kirby (Coleoptera: Carabidae), 1837, and Tachyta inornata (Say, 1823) (Coleoptera: Carabidae). The confirmed predator of CRF, B. quadrimaculatum, as well as Aleocharinae spp. which could include predators or parasitoids (Wright et al. 1947) of CRF were identified, but were not recovered in high numbers. In 2016, 2,753 individuals from 38 taxa were recovered and identified from the pitfall traps (Table 2). Increased abundance and diversity of specimens in 2016 was due to the addition of a finer screen in the soil sieving process. There were nine dominant taxa again in 2016 including: Staphylinidae (29.1%), P. melanarius (17.2%), A. sanctaecrucis (13.0%), Amara lunicollis Schiødte (Coleoptera: Carabidae), 1837 (11.5%), B. quadrimaculatum (8.6%), S. comma (7.3%), Bembidion spp. Latreille, 1802 (4.5%), Amara patruelis Dejean (Coleoptera: Carabidae), 1831 (2.3%), and C. fossor (1.6%). All other taxa, other than Dyschirius montanus LeConte (Coleoptera: Carabidae), 1879 (1.3%), represented <1% of the total abundance. These were: Acupalpus partiarius (Say, 1823) (Coleoptera: Carabidae), Amara avida (Say, 1823) (Coleoptera: Carabidae), Amara obesa (Say, 1823) (Coleoptera: Carabidae), Anisodactylus verticalis (LeConte 1847) (Coleoptera: Carabidae), Atranus sp., Bradycellus atrimedeus (Say, 1823) (Coleoptera: Carabidae), Bradycellus rupestris (Say, 1823) (Coleoptera: Carabidae), Carabus sp. Linnaeus (Coleoptera: Carabidae), 1758, Chlaenius cordicollis Kirby (Coleoptera: Carabidae), 1837, C. duodecimguttata, Clivina sp. Latreille (Coleoptera: Carabidae), 1802, Coccinella septempunctata Linnaeus, 1758, Coleomegilla maculata (De Geer, 1775), Dyschirius pallipennis (Say, 1823) (Coleoptera: Carabidae), Harpalus affinis (Schrank, 1781) (Coleoptera: Carabidae), Histeridae, L. pilicornis, O. americanum, Patrobus sp. Dejean (Coleoptera: Carabidae), 1821, Po. lucublandus, Polyderis laevis (Say, 1823) (Coleoptera: Carabidae), Porotachys bisulcatus (Nicolai, 1822) (Coleoptera: Carabidae), Pterostichus permundus (Say, 1830) (Coleoptera: Carabidae), Schizogenius lineolatus (Say, 1823) (Coleoptera: Carabidae), S. fuliginosus, and Tachys sp. Casey (Coleoptera: Carabidae), 1918). Commercial Carrot Fields In 2015, only 10 different taxa were identified in the four surveyed commercial carrot fields, with a total abundance of 228 individuals (Table 1). These numbers increased greatly in 2016, likely due to the addition of a finer screen in the soil sieving process, with 27 taxa and 1,401 individuals recovered from the four commercial carrot fields (Table 2). Rarefaction curves for 2015 and 2016 (Fig. 1) showed a substantial difference in species richness and abundance among fields. The Simpson’s index varied among fields, and was generally low in 2015 (Table 1). There was a substantial increase in Simpson’s index values and less variability among fields in 2016 (Table 2). Fig. 1. View largeDownload slide Rarefaction curves for four commercial carrot fields surveyed with pitfall traps for carrot insect pest natural enemies in 2015 and 2016 in the Holland Marsh, Ontario, Canada. Fig. 1. View largeDownload slide Rarefaction curves for four commercial carrot fields surveyed with pitfall traps for carrot insect pest natural enemies in 2015 and 2016 in the Holland Marsh, Ontario, Canada. Table 1. Diversity (number of insect species) and abundance (number of individual insects collected) of CRF and CW natural enemies collected in pitfall traps in the Holland Marsh, 2015 Location No. of species collected No. individuals collected Simpson’s index Commercial field A 7 136 0.290 Commercial field B 3 25 0.563 Commercial field C 6 35 0.464 Commercial field D 5 32 0.445 Research plot (IPM) 19 447 0.830 Research plot (Control) 18 430 0.832 Commercial field total 10 228 0.627 Research plot total 24 877 0.832 2015 Total 25 1,105 0.820 Location No. of species collected No. individuals collected Simpson’s index Commercial field A 7 136 0.290 Commercial field B 3 25 0.563 Commercial field C 6 35 0.464 Commercial field D 5 32 0.445 Research plot (IPM) 19 447 0.830 Research plot (Control) 18 430 0.832 Commercial field total 10 228 0.627 Research plot total 24 877 0.832 2015 Total 25 1,105 0.820 View Large Table 1. Diversity (number of insect species) and abundance (number of individual insects collected) of CRF and CW natural enemies collected in pitfall traps in the Holland Marsh, 2015 Location No. of species collected No. individuals collected Simpson’s index Commercial field A 7 136 0.290 Commercial field B 3 25 0.563 Commercial field C 6 35 0.464 Commercial field D 5 32 0.445 Research plot (IPM) 19 447 0.830 Research plot (Control) 18 430 0.832 Commercial field total 10 228 0.627 Research plot total 24 877 0.832 2015 Total 25 1,105 0.820 Location No. of species collected No. individuals collected Simpson’s index Commercial field A 7 136 0.290 Commercial field B 3 25 0.563 Commercial field C 6 35 0.464 Commercial field D 5 32 0.445 Research plot (IPM) 19 447 0.830 Research plot (Control) 18 430 0.832 Commercial field total 10 228 0.627 Research plot total 24 877 0.832 2015 Total 25 1,105 0.820 View Large Table 2. Diversity (number of insect species) and abundance (number of individual insects collected) of CRF and CW natural enemies collected in pitfall traps in the Holland Marsh, 2016 Location No. of species collected No. of individuals collected Simpson’s index Commercial field E 19 870 0.783 Commercial field F 10 70 0.805 Commercial field G 15 227 0.783 Commercial field H 20 234 0.768 Research plot (IPM) 24 686 0.797 Research plot (Control) 23 666 0.769 Commercial field total 27 1,401 0.851 Research plot total 30 1,352 0.786 2016 total 38 2,753 0.848 Location No. of species collected No. of individuals collected Simpson’s index Commercial field E 19 870 0.783 Commercial field F 10 70 0.805 Commercial field G 15 227 0.783 Commercial field H 20 234 0.768 Research plot (IPM) 24 686 0.797 Research plot (Control) 23 666 0.769 Commercial field total 27 1,401 0.851 Research plot total 30 1,352 0.786 2016 total 38 2,753 0.848 View Large Table 2. Diversity (number of insect species) and abundance (number of individual insects collected) of CRF and CW natural enemies collected in pitfall traps in the Holland Marsh, 2016 Location No. of species collected No. of individuals collected Simpson’s index Commercial field E 19 870 0.783 Commercial field F 10 70 0.805 Commercial field G 15 227 0.783 Commercial field H 20 234 0.768 Research plot (IPM) 24 686 0.797 Research plot (Control) 23 666 0.769 Commercial field total 27 1,401 0.851 Research plot total 30 1,352 0.786 2016 total 38 2,753 0.848 Location No. of species collected No. of individuals collected Simpson’s index Commercial field E 19 870 0.783 Commercial field F 10 70 0.805 Commercial field G 15 227 0.783 Commercial field H 20 234 0.768 Research plot (IPM) 24 686 0.797 Research plot (Control) 23 666 0.769 Commercial field total 27 1,401 0.851 Research plot total 30 1,352 0.786 2016 total 38 2,753 0.848 View Large Effects of an Established IPM Program In 2015, 447 individuals from 19 taxa were recovered in the IPM plots and 430 individuals from 18 taxa in the control plots (Table 1). A similar trend was found in 2016, as 686 individuals from 24 taxa were recovered in the IPM plots and 666 individuals from 23 taxa in the control plots (Table 2). Rarefaction curves for 2015 and 2016 (Fig. 2) showed that the species richness and abundance for the IPM plots and non-IPM (insecticide-free, control plots) were nearly identical. These curves indicate that while the sampling effort was insufficient to determine the entire species richness of a site, the use of 12 traps per plot in the research sites captured more of the total species richness than the four traps per site used in the commercial fields. The Simpson’s index did not differ between IPM or control plots, and this was consistent in both 2015 and 2016. The Simpson’s index for these research plots were much greater than those found in commercial fields, especially in 2015 (Tables 1 and 2). Fig. 2. View largeDownload slide Rarefaction curves for plots which received insecticides based on the existing IPM program for CRF and CW and insecticide-free control plots in the Holland Marsh, Ontario, Canada. Plots were surveyed with pitfall traps for natural enemies of carrot insect pests in 2015 and 2016. Fig. 2. View largeDownload slide Rarefaction curves for plots which received insecticides based on the existing IPM program for CRF and CW and insecticide-free control plots in the Holland Marsh, Ontario, Canada. Plots were surveyed with pitfall traps for natural enemies of carrot insect pests in 2015 and 2016. Discussion Few studies have evaluated the diversity of ground-dwelling beetles in carrot fields or in the Holland Marsh. To our knowledge, the last survey for ground-dwelling beetles in the Holland Marsh was conducted in 1985 (Tomlin et al. 1985). However, that study focused on natural enemies of onion maggot (Delia antiqua (Meigen 1826) (Diptera: Anthomyiidae)) and used onion maggot mass-rearing beds as an attractant, rather than utilizing pitfall traps. Brunke et al. (2009) conducted the only survey for ground-dwelling beetles in carrot fields in North America, and identified 50 carabid species, 12 of which were also identified in the present survey. However, the purpose of that survey was to identify natural enemies of millipedes in both carrot and sweet potato fields. Furthermore, edge habitats were also sampled rather than just within the crop sites, as in this survey. Two of the eight dominant species in Brunke et al. (2009) were found to be dominant in this study (i.e., P. melanarius and B. quadrimaculatum). All other surveys in carrot fields have been conducted in either Europe (Colignon et al. 2002, Albert et al. 2003, Picault 2013) or New Zealand (Berry et al. 1996, Sivasubramaniam et al. 1997) and represent a much different fauna. A total of 49 unique taxa, including confirmed natural enemies of CRF and CW, were identified in 2015–2016 from 3858 individual specimens. The total abundance, as well as the number of taxa identified in 2016 was much greater than that in 2015. This is largely due to the addition of the 400 μm sieve to the sieving process used to recover insects from the pitfall traps. This resulted in better collection of small taxa, especially Bembidion species and Staphylinidae. This correction was important due to the findings by Burn (1982) that smaller carabid (<8 mm in length) species are likely responsible for most of the CRF predation. In 2016, there was a 10-fold increase in the number of Bembidion individuals recovered compared to 2015. Staphylinidae collection also increased greatly, from 30 individuals in 2015 to 800 in 2016. Both taxa are of special interest in the survey as they include known natural enemies of carrot insect pests. Absent from the survey in both years was the known CRF predator T. quadristriatus. This is significant as it has previously been recorded in carrot fields in Ontario (Brunke et al. 2009, Bousquet 2012). The absence of this species could indicate that our trapping methods were not effective at recovering this ground-dwelling beetle. The generated rarefaction curves failed to converge, indicating that an insufficient sampling effort was conducted to determine the entire species diversity. However, while the curves did not reach an asymptote, a substantial decrease in the slope for each curve was observed, indicating that a near-sufficient sampling effort was achieved. Future work will focus on expanding the number of sites and traps per site to achieve a sufficient sampling effort. However, all five known natural enemies of CW were recovered in this survey, most of which were found in high abundance. Chaput (1993) suggested that there are other potential natural enemies present in the Holland Marsh including Hemipterans such as Anthocoridae, Reduviidae, and Nabidae, as well as lacewings (Neuroptera: Chrysopidae) and ladybirds (Coleoptera: Coccinellidae). Many of these insects, while not captured in the pitfall traps, were observed in carrot fields during this survey. In a mark and recovery experiment, Burn (1982) found that the greatest levels of CRF egg loss coincided with the greatest activity from small carabids (<8mm in length). It is likely that CRF eggs are too small and dispersed to be of interest to larger carabids (Rämert 1996). Yet, some of the most abundant taxa recovered (e.g., P. melanarius, A. sanctaecrucis, and Amara spp.) were large carabids. Nevertheless, a large proportion of the taxa recovered are small and could predate on CRF eggs. While many of these smaller taxa were rarely captured in the traps, pitfall trapping is not an effective measure of population density, and small carabids are often under-represented in pitfall captures (Kromp 1999). Therefore, the importance of the numerous rare species found in this survey should not be ignored. While P. melanarius is likely too large to predate on CRF eggs, it has been found to feed on adult CW (Baines et al. 1990, Zhao et al. 1990). However, it was noted that P. melanarius is unable to feed on CW adults when they are on a carrot plant (Zhao et al. 1990), raising questions about their effectiveness in suppressing CW in a field setting. Many small carabids will feed on dipteran eggs when they are present on the soil surface, but a significant reduction in predation often occurs when eggs are laid below the surface (Finch and Elliot 1992) as is the case with CRF. However, B. quadrimaculatum has been observed to feed on onion maggot eggs buried up to 1 cm deep (Grafius and Warner 1989). B. quadrimaculatum, is also known to prey on CRF eggs (Burn 1982), and CW eggs (Baines et al. 1990). However, its ability to prey on CW eggs in a field setting has been questioned (Baines et al. 1990). In 2015, only P. melanarius and staphylinids were recovered in all four commercial fields as well as the research site. However, in 2016, seven taxa were recovered in all four commercial fields and both research sites (A. sanctaecrucis, B. quadrimaculatum, Bembidion spp., C. fossor, P. melanarius, S. comma, staphylinids, and spiders). The research sites had much greater diversity and abundance than the commercial sites, but were sampled with a much greater effort (12 traps per research site compared to four traps per commercial field). The commercial carrot fields with the most diverse insect species supported 70% (field A, 2015) and 75% (field H, 2016) of the total diversity identified, while the least diverse commercial fields supported only 30% (field B, 2015) and 39% (field F, 2016). A substantial difference in both the species abundance and richness was observed among the four commercial fields surveyed both years, suggesting that there are currently unknown drivers of ground-dwelling beetles diversity in the Holland Marsh. Increasing plant diversity has been shown to lead to an increase in herbivore diversity, and through a bottom-up cascade—an increase in predator and parasitoid diversity (Hunter and Price 1992, Siemann 1998). While not quantitatively measured, there was a trend where fields with greater plant diversity had greater ground-dwelling beetles diversity in this study. Notably, field A and E had much greater abundance and species richness of ground-dwelling beetles than the other three fields surveyed in their respective years. These agricultural fields were unique in their agro-ecosystem structure. Unlike most of the Holland Marsh, field A was bordered on three sides by naturalized areas, including a forested area and an overgrown greenhouse. Field E, on the other hand, was bordered by crop fields but had a poorly managed bank of weeds along the eastern border. The pitfall traps were also placed near residential property, which was surrounded by naturalized areas, with trees and vegetable gardens. Most notably, field E and the fields to its north and south were essentially overgrown by weeds for most of the trapping period. No other surveyed field had nearly the same plant species richness in close proximity as these two fields. This is consistent with the results of Bosch (1987) which found twice as many carabids in beets with 15–20% weed cover compared to weed-free plots. However, B. quadrimaculatum and T. quadristriatus were more active in weed-free plots (Bosch 1987). The same trend was found in this study, as B. quadrimaculatum was less abundant in field E compared to the more weed-free fields. Field H was also unique as it was the only field surveyed near the Holland River, which transects the Holland Marsh. This riparian zone along the river banks was likely responsible for the high species richness which occurred at this site. Both the species richness and abundance of ground-dwelling beetles in IPM program and insecticide-free control plots were nearly identical in 2015 and 2016. Furthermore, the Simpson’s index for the IPM program plots were consistent across both years, and was similar to the most diverse commercial field—field F in 2016. These results provide positive evidence for the sustainability of the IPM program currently used in the Holland Marsh. The recommendations of the IPM program resulted in a single application of phosmet and multiple cypermethrin applications in both years. Yet ground-dwelling beetles were just as abundant and diverse as in areas, which received no insecticides. While no other study evaluated the effects of CRF or CW natural enemies under an established IPM program, Sivasubramaniam (1996) found that the application of diazinon and phorate decreased the abundance of natural enemies in carrot fields in New Zealand. Freuler et al. (2003) looked at the effects of cypermethrin on carabid species richness in white cabbage in Switzerland, and found no fundamental change, but a slight reduction in abundance in B. quadrimaculatum was seen. Conversely, Wick and Freier (2000) found that applications of lambda-cyhalothrin in winter wheat in Germany reduced the species density and activity of carabids, but beetle numbers recovered by the following year. Not all the carabids that were recovered in the pitfall traps are potential CRF or CW predators. For example, L. pilicornis is a collembolan predator (Kromp 1999). However, Pterostichus, Bembidion, Carabus, and Dyschirius are among the few true predator genera in the Carabidae (Lindroth 1992). Certain Amara and Harpalus species are predominantly phytophagous (Lindroth 1992) and have been found to provide some weed control through seed predation (Brust and House 1988). It is likely that both omnivory and scavenging are more common within the Carabidae than is currently accepted (Lovei and Sunderland 1996). Therefore, it is important that an adequate and diverse food supply be present in an agro-ecosystem if the goal is to support a large and diverse natural enemy population. As CRF and CW are not always available, it is crucial that other food sources be present. Flowering plants play an important role by providing pollen, nectar, and seeds on which ground-dwelling beetles, including natural enemies, can feed in the absence of prey. Furthermore, by attracting other insects, flowering plants provide a source of prey for polyphagous predators (Isaacs et al. 2009). Previous conservation biological control efforts resulted in an insufficient increase in natural enemy pressure to provide substantial control of CRF in France (Picault 2013). Denser vegetation types (i.e., hedgerows) were found to increase the CRF population more than that of natural enemies. However, less dense vegetation such as grasses had less of an effect on CRF populations. It was suggested that future studies should evaluate the effectiveness of augmentative biological control in combination with conservation biological control efforts (Picault 2013). Previous attempts to introduce natural enemies of CRF within the Holland Marsh were focused on the introduction the parasitoids, Chorebus gracilis (Nees 1834) (Hymenoptera: Braconidae), and Loxotropa tritoma Thomson, 1859 (Hymenoptera: Diapriidae) (Maybee 1954). Unfortunately, the parasitoids, native to England, failed to survive the Canadian winter. Wright et al. (1947) also described Aleochara sparsa Heer, 1839 (Coleoptera: Staphylinidae) and a Kleidotoma sp. Westwood, 1833 (Hymenoptera: Figitidae) as CRF parasitoids found in England. Additionally, Cormier et al. (1996) determined that two parasitoids, Anaphes victus Huber, 1997 and Anaphes listronoti Huber, 1997 (Hymenoptera: Mymaridae) could parasitize CW eggs. While Picault (2013) evaluated the potential for Al. sparsa as part of a conservation biological control program in France, the three other parasitoids remain unstudied. The work presented here provides a description of the abundance and diversity of ground-dwelling beetles in carrot fields in the Holland Marsh, Ontario. The knowledge gained will be used in future conservation biological control efforts to naturalize uncultivated areas (i.e., canal berms) in the Holland Marsh, starting in 2017. This survey identified over 50 different insect species, most of which are polyphagous predators within the Carabidae, as was expected due to the study design using only pitfall traps. Many of these beetles play a vital role in the agro-ecosystem by suppressing pest populations. Known natural enemies of both major carrot insect pests, CRF and CW, were found in abundance in both research plots and commercial carrot fields. Furthermore, the application of insecticides based on the recommendations of an existing IPM program for carrot insect pests was not found to negatively impact the abundance or diversity of ground-dwelling beetles. 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Environmental EntomologyOxford University Press

Published: May 25, 2018

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