The annual bluegrass weevil, Listronotus maculicollis Kirby, is the most difficult to control insect pest of short-mown golf course turf in the northeastern United States and Eastern Canada. We conducted a survey among golf course superintendents throughout the weevil's area of impact to better understand the severity of damage, prevalence of insecticide resistance, information sources, and trends in management practices. Responses were received from 293 golf courses in 14 U.S. states and 2 Canadian provinces. The average population caused damage to 6.6 fairways, 5.7 tee boxes, and 6.4 greens/collars, amounting to a total of 5.2 ha requiring protection on an 18-hole facility. On average, courses made 3.9 insecticide applications per year and spent US$9,270 on L. maculicollis management. Twenty percent of the responders reported having a pyrethroid-resistant L. maculicollis population. “Resistant” populations were located across the region, though higher-than-average incidence was reported from areas with long histories of managing L. maculicollis. “Resistant” populations caused more damage than “susceptible” populations, reported higher average insecticide budgets, and were more likely to make more than five insecticide applications per year than “susceptible” courses. Surveys indicated that, despite the reliance on chemical controls, 90% of turf managers used multiple monitoring tactics to better time and target controls. The greatest influence on management philosophy was by University personnel (43%) followed by colleagues (31%) and sales/distributors (21%). This survey highlights the need for developing alternatives to chemical insecticides to control L. maculicollis and provides insight into the costs associated with the development of pyrethroid resistance. Turfgrass areas, including golf courses, are a valuable and rapidly expanding component of urban and rural landscapes. Around 15,750 golf courses in the United States provide green space in the urban environment; offer recreation for 26 million Americans; generate jobs, commerce, economic development, and tax revenues for communities; and directly contribute US$68.8 billion worth of goods and services per year to the national economy (www.golf2020.com, accessed 30 September 2016). However, the profitability of golf course operations can be significantly affected by various pests. One of the most threatening pests is the annual bluegrass weevil, Listronotus maculicollis Kirby (Vittum et al. 1999).

Listronotus maculicollis is thought to be native to North America where it is broadly distributed and has been collected from various wetland habitats such as marshes and lake margins (O’Brien and Wibmer 1982). As a pest of golf course turfgrass, L. maculicollis was first isolated from damaged turf on Long Island in 1957 and until around 1990 was concentrated around the metropolitan area of New York including northeastern New Jersey and southwestern Connecticut (McGraw and Koppenhöfer 2007). The pest has consistently expanded its range of impact over the past decades, with infestations now reported from the southern parts of Quebec and Ontario south through western North Carolina and west to eastern Ohio. Within this area, there are >3,000 golf courses, providing over 222,000 jobs, with an estimated direct impact on the area's economy of >US$10 billion (www.golf2020.com, accessed 30 September 2016). Listronotus maculicollis larvae can cause severe turf damage on tees, fairways, collars, and greens with high percentages of annual bluegrass, Poa annua L., as this grass is particularly attractive to egg-laying females and has low tolerance to larval feeding (Kostromytska and Koppenhöfer 2014, 2016). Females place eggs between the leaf sheaths or inside the stem of the turfgrass plant. The first through third larval instars feed within the grass stem, causing the central leaf blades to yellow and die. The third instars eventually exit the stem, and the fourth and fifth instars feed externally at the soil and thatch surface. The late-instar larval feeding damage is most severe, as it damages the apical meristem of the turfgrass plant. With densities often exceeding 100 larvae/0.1 m2, damage can severely impact the visual and functional quality of the turf. Listronotus maculicollis overwinters in the adult stage in protected areas along the edge of woods or in the rough. In spring, between early April and early May around the New York metropolitan area, these adults walk on to the short-mown areas to feed on grass blades and mate. Toward the end of this period, females start depositing eggs and continue to do so for several weeks. Around mid-May, larvae of this first or spring generation start to emerge from the plants and feed externally. The resulting turf damage appears between late May and mid-June. The mature larvae pupate near the soil surface and spring-generation adults appear on the turf surface around late June. These adults mate and lay eggs. The second generation is present as large larvae around late July-early August, when additional damage may occur. The second generation pupates in August and adults start emerging around mid-August. A third generation may develop between mid-August and mid-September, but is usually lower in density, rarely causing damage. Presently, chemical control is the only effective strategy for L. maculicollis management (Vittum 2012). Consequently, turfgrass managers often overuse broad-spectrum insecticides, primarily pyrethroids used to prevent adults from ovipositing. Not surprisingly, pyrethroid resistance has been reported (Ramoutar et al. 2009a) and seems to be on the rise (B.A.M and A.M.K., unpublished data). Effective alternatives to pyrethroids include the larvicides chlorantraniliprole and cyantraniliprole (class: anthranilic diamides), spinosad (class: spinosyns), indoxacarb (class: oxadiazines), and trichlorfon (class: organophosphates) (Koppenhöfer et al. 2012). However, pyrethroid resistance in L. maculicollis seems to be at least in part due to enhanced enzymatic detoxification (Ramoutar et al. 2009b, A. M. Koppenhöfer, unpublished data), a rather nonspecific mechanism that breaks down active ingredients before they can reach their targets in the organism. As a result, most of the presently available insecticides seem to be less effective against resistant L. maculicollis populations (Koppenhöfer et al. 2012; A. M. Koppenhöfer, unpublished data). Clearly, insecticide resistance is a rising issue and a driving force in the rethinking of L. maculicollis management. Efforts continue on the development of more sustainable management practices and improving L. maculicollis monitoring (e.g., Kostromytska and Koppenhöfer 2014, 2016). But with the continued high expectations on turf quality, synthetic insecticide will remain an important part of L. maculicollis management. Careful measures need to be taken to prevent resistance development in new populations and to new chemistries and to effectively manage already resistant populations. But very limited information is available on L. maculicollis resistance to insecticides. Our ultimate goal is to develop optimal management recommendations for L. maculicollis population with different levels of insecticide resistance. To this end we are conducting laboratory and field studies to better understand the scope of resistance in L. maculicollis (degree of resistance to different insecticide classes, stages affected). However, it also important to gather information from the practitioners to better understand the geographic spread and severity of the pest and its resistance issues as well as the prevalence of currently used monitoring and management practices. To achieve the latter we conducted a survey, the results of which are summarized below. ## Materials and Methods A survey was created in the fall of 2014 to capture regional trends in L. maculicollis management and understand the severity and extent of L. maculicollis damage throughout the area in which the pest currently is causing problems on golf courses. The survey aimed at capturing responses from superintendents who manage L. maculicollis populations, though responses within the known area of impact from superintendents that do not experience damage were not dissuaded. The link to the survey was sent to golf course superintendents through a variety of avenues, including social media (e.g., Twitter), hardcopies distributed during presentations at educational conferences and extension meetings, and e-mails from local and regional Golf Course Superintendent Association of America (GCSAA) chapters. The goal was to capture responses from a minimum of 150 superintendents representing all areas within the known area of impact of L. maculicollis, including robust survey numbers (n > 20) in areas where L. maculicollis damage has been most problematic (i.e., areas surrounding the New York City metropolitan area). The survey was made available from November 14, 2014 through the end of January 2015. Multiple reminder notifications were issued throughout the polling period through e-mails and social media by both the authors and the GCSAA chapters. The decision to close the survey came after more than the expected number of responses was collected (n = 293) and no further responses were received for a 2-wk period. The survey was created in Google documents (www.google.com, accessed 30 September 2016), which allowed for it to be circulated through a web address link, responses to be collected with minimal effort, and answers to be organized in a spreadsheet. The survey consisted of 26 questions, with nearly equal amounts of "fill-in-the-blank" (13) and "radio button" questions (e.g., "check all that apply" or "make only one selection")(12), as well as one optional response to provide feedback. It was mentioned that individual responses would remain anonymous, though the pooled results would be shared in a presentation at the annual Golf Industry Show in 2015 and in peer-reviewed and trade publications. Questions in the survey could be grouped into three general categories (A complete listing of the questions in the survey as it was published is included in the Appendix): 1. Local and regional damage: Turfgrass areas damaged (e.g., greens, tees, fairways), number of damaged areas, seasonal occurrence of damage 2. Management of L. maculicollis populations: Number of insecticide applications, total insecticide budget, pyrethroid use, and suspected (or confirmed) development of insecticide-resistant populations 3. Integrated Pest Management practices: Scouting techniques, spot treatment frequency, acquiring information, and influence of university recommendations on management decisions We examined the survey locations to ensure that only one person per facility completed the survey. The only redundant survey response that was found was omitted from the analysis. Many polled superintendents failed to respond to all questions. These surveys were not omitted, but rather the frequency of the response was adjusted based on the total answered for the specific question. ### Data Analysis The majority of surveys were completed by superintendents of 18-hole facilities (233 of the 293 responses = 79.5%). Therefore, budget values were transformed into 18-hole equivalents for reporting several economic statistics. The proportion of insecticide budgets within the annual maintenance budgets was calculated only from the responses from the 18-hole golf courses since turf managers were asked for a range of maintenance budgets, rather than an exact dollar amount. Transforming these data to 18-hole equivalents would likely lead to over- or underestimations. The responses for the number of damaged turf areas (e.g., tees, greens, fairways) were also converted to 18-hole equivalents before using descriptive statistics. Differences between pyrethroid-susceptible and “resistant” course in number of areas (tee, fairway, green), insecticide budget, L. maculicollis applications, and pyrethroid use were analyzed by nonparametric Rank Sum Tests using Statistix 9.0 software package (Tallahassee, FL, USA). All data were transformed into 18-hole equivalents before analysis. The null hypothesis that the variance of the data from the two populations was equal was rejected at the α = 0.05 level. ## Results and Discussion ### Responses Responses were collected from 293 golf courses in 14 states and 2 Canadian provinces in the 2 mo the survey remained open (Fig. 1). The survey was completed by an estimated 5.6% of the 5,197 facilities in the surveyed area (Golf Canada 2015; GCSAA, personal communication). The survey required providing a course location at the state or province level (minimum), though more detail was encouraged. Most responders provided city and state/province data, which allowed us to develop detailed survey maps and divide the responses into regions in most instances (Table 1). The majority of responses (86%) came from courses located in Pennsylvania (PA; 25%), New York (NY; 19%), New Jersey (NJ; 11%), Massachusetts (MA; 11%), Virginia (VA; 11%), and Connecticut (CT; 9%). Data were grouped by regions where n > 20, which tended to be by state, or further subdivided where there were enough responses and it made geographical sense (i.e., eastern versus western Pennsylvania and Long Island versus Upstate New York). Delaware (DE) and Maryland (MD) had very few responses and were combined with Virginia (DE-MD-VA). The “Western” (Ohio (OH)-West Virginia (WV)) and “Northern” peripheral states/provinces (Maine (ME)-New Hampshire (NH)-Vermont (VT)-Ontario (ONT)-Quebec (QUE)) were the only regions that had < 20 responses that were included in the analyses. In total, there were eight distinct regions and four subregions that are represented in the descriptive statistics. Fig. 1. Distribution of the L. maculicollis Management Survey responses. Fig. 1. Distribution of the L. maculicollis Management Survey responses. Table 1. Regions and subregions used for categorizing survey data for L.maculicollis geographically, number of completed surveys by region, and total golf facilities in the region (percent surveyed) Region Subregion Responses Total facilities in the region Northern Periphery (ME, NH, VT, QUE, ONT) 13 1,506 (0.9) MA 33 370 (8.9) CT 25 174 (14.4) NY 56 799 (7.0) Long Island 20 Upstate NY 26 NJ 32 285 (11.2) PA 74 661 (11.2) Eastern PA 30 Western PA 38 DE-MD-VA 42 541 (7.4) Western Periphery (OH, WV) 16 804 (2.0) Region Subregion Responses Total facilities in the region Northern Periphery (ME, NH, VT, QUE, ONT) 13 1,506 (0.9) MA 33 370 (8.9) CT 25 174 (14.4) NY 56 799 (7.0) Long Island 20 Upstate NY 26 NJ 32 285 (11.2) PA 74 661 (11.2) Eastern PA 30 Western PA 38 DE-MD-VA 42 541 (7.4) Western Periphery (OH, WV) 16 804 (2.0) CT, Connecticut; DE, Delaware; MD, Maryland; ME, Maine; NH, New Hampshire; NJ, New Jersey; NY, New York; OH, Ohio; ONT, Ontario; PA, Pennsylvania; QUE, Quebec; WV, West Virginia; VA, Virginia; VT, Vermont. ### Local and Regional L. maculicollis Damage #### Areas Damaged Most (90%) respondents indicated that L. maculicollis was present in damaging densities on their course. Twenty-nine respondents (10%) either stated that they did not observe damage or they failed to provide any answers to questions regarding seasonal damage, locations of damage, or number of turfgrass areas damaged by L. maculicollis. These courses were located throughout the surveyed area, including VA (n = 15), PA (4), OH (3), MA (2), NJ (2), VT (2), and MD (1). Only surveys that indicated L. maculicollis was a pest were used in reporting damage incidence to select turf areas. To better understand the average extent of damage across a site and to best gauge the total amount of turf that requires insecticide applications, we asked superintendents to determine the average number of turf areas (e.g., number of tees) that experienced damage in a year. The average course experienced damage to 6.6 fairways, 5.7 tee boxes, and 6.4 greens/collars (Table 2). A survey of members by the Golf Course Superintendents of America member (GCSAA 2007) estimated total areas per 18-hole golf course of 12.1 ha (30 ac) of fairways, 1.2 ha (3 ac) of tees, and 0.43 ha (1.06 ac) of greens/collars. Using these figures as a base, we estimated that on average 4.4 hectares (10.8 acres) of fairway, 0.38 ha (0.95 ac) of tees, and 0.43 ha (1.06 ac) of greens/collars, for a total of 5.2 ha (12.8 ac) require protection on an 18-hole golf course. Table 2. Listronotus maculicollis damage to turfgrass by location on golf course and by season Regiona Damage by season (%) Location of damageb (%) No. damagedc % w/o Damaged Height-of-cute Spring Summer Fall All C/A FW G/C FW All Regions 38 84 14 26 34 58 69 10 6.4 5.7 6.6 14 3.02 (0.119) Northern Periphery 77 38 31 69 54 5.0 4.7 4.9 15 3.20 (0.126) MA 21 82 12 20 30 57 57 6.6 5.0 6.0 3.02 (0.119) CT 52 88 20 40 64 96 68 7.4 4.7 5.1 3.12 (0.123) NY 43 88 16 38 54 70 5.9 6.4 7.7 11 3.00 (0.118) Long Island 40 90 15 10 45 55 65 6.3 7.7 9.1 2.82 (0.111) Upstate NY 46 85 19 23 58 69 12 4.9 6.6 6.3 19 3.12 (0.123) NJ 47 75 31 22 31 22 63 66 7.4 5.0 6.7 3.05 (0.120) PA 39 70 11 20 36 55 64 12 6.3 6.6 7.5 2.82 (0.111) Eastern PA 50 66 11 21 37 55 47 6.6 6.2 7.4 3.00 (0.118) Western PA 21 58 16 26 42 55 13 5.6 8.2 7.4 13 2.77 (0.109) DE-MD-VA 14 52 14 20 17 23 31 6.8 4.0 4.4 48 3.15 (0.124) VA 11 44 19 21 11 26 26 16 6.4 2.0 3.3 59 3.18 (0.125) Western Periphery 11 3.1 1.3 1.7 19 3.07 (0.121) Regiona Damage by season (%) Location of damageb (%) No. damagedc % w/o Damaged Height-of-cute Spring Summer Fall All C/A FW G/C FW All Regions 38 84 14 26 34 58 69 10 6.4 5.7 6.6 14 3.02 (0.119) Northern Periphery 77 38 31 69 54 5.0 4.7 4.9 15 3.20 (0.126) MA 21 82 12 20 30 57 57 6.6 5.0 6.0 3.02 (0.119) CT 52 88 20 40 64 96 68 7.4 4.7 5.1 3.12 (0.123) NY 43 88 16 38 54 70 5.9 6.4 7.7 11 3.00 (0.118) Long Island 40 90 15 10 45 55 65 6.3 7.7 9.1 2.82 (0.111) Upstate NY 46 85 19 23 58 69 12 4.9 6.6 6.3 19 3.12 (0.123) NJ 47 75 31 22 31 22 63 66 7.4 5.0 6.7 3.05 (0.120) PA 39 70 11 20 36 55 64 12 6.3 6.6 7.5 2.82 (0.111) Eastern PA 50 66 11 21 37 55 47 6.6 6.2 7.4 3.00 (0.118) Western PA 21 58 16 26 42 55 13 5.6 8.2 7.4 13 2.77 (0.109) DE-MD-VA 14 52 14 20 17 23 31 6.8 4.0 4.4 48 3.15 (0.124) VA 11 44 19 21 11 26 26 16 6.4 2.0 3.3 59 3.18 (0.125) Western Periphery 11 3.1 1.3 1.7 19 3.07 (0.121) a Abbreviations see Table 1. b G, Green; T, Tees; C/A, Collar/Approaches; FW, Fairway; R, Rough. b G/C, Greens/collars; T = Tee; FW, Fairway. Transformed to an 18-hole equivalent; no responses removed from statistics. d Proportion of respondents that did not report damage to any area. e Average putting green height-of-cut in mm (inches). #### Damage by Turf Area Listronotus maculicollis damage was reported to occur in all turf areas or playing surfaces, including areas where damage is rarely reported by turfgrass managers to University personnel (e.g., greens and roughs). Damage was most common on fairways (69%) and collars/aprons (58%; Table 2). Only 10% of respondents reported damage to roughs. These data are not surprising, given the weevil’s preference for P. annua and A. stolonifera maintained under 1.25 cm (Rothwell 2003, Kostromytska and Koppenhöfer 2014) and the composition of turfgrasses likely to be found in rough (e.g., Poa pratensis L., Festuca spp., Lolium perenne L.). The incidence of damage to putting greens (26%) was unexpectedly high given the low mowing heights reported across the region and the traditionally high intensity of insecticide use in these areas. Average putting green mowing height in the region varied little, ranging from 2.77 mm (0.109 in) western PA to 3.20 mm (0.126 in) in the northern peripheral states/provinces. Two thirds (66%) of the courses that reported L. maculicollis damage to greens had heights-of-cut greater than the average, which was 3.02 mm (0.119 in) across all survey responses (Fig. 2). Fig. 2. The percentage of surveyed golf courses categorized by putting green mowing height (A) and those that experienced L. maculicollis damage to putting surfaces (B) by mowing height treatment. Fig. 2. The percentage of surveyed golf courses categorized by putting green mowing height (A) and those that experienced L. maculicollis damage to putting surfaces (B) by mowing height treatment. Regions with the highest incidence of damage to putting greens included CT (40%), northern peripheral states/provinces (38%), and NJ (31%; Table 2). The average putting green height-of-cut in these areas (3.05–3.20 mm [0.120–0.126 in]) was greater than the survey average. The lowest incidence of L. maculicollis damage to greens was reported in Long Island (11%) and western PA (16%), the two regions with the lowest average green heights-of-cut (2.79 and 2.77 mm [0.110 and 0.109 in], respectively). Most (88%) golf courses experiencing putting green damage reported their greens were a mix of Poa annua and Agrostis stolonifera L. Four courses (6%) reported damage to pure A. stolonifera greens, and only one (1.5%) reported damage to pure P. annua greens. Interestingly, one course reported damage to a Cynodon dactylon L.P. annuaA. stolonifera mixed green, though it is currently not known whether L. maculicollis can develop in C. dactylon. #### Seasonal Damage Most superintendents (84%) reported damage appearing in the summer, followed by 38% reporting springtime damage (Table 2). This result was surprising since larvae are more dense and aggregated in the first generation than in following generations (Vittum et al. 1999). Few reported fall damage (14%) or damage appearing during all three seasons (5%). NJ and Eastern PA had the highest incidence of spring (first generation larval) damage (50 and 47%, respectively). The regions further to the north, including Long Island (90%), CT (88%), Upstate NY (85%), and MA (82%) reported very high incidence of summer damage. NJ, CT, and VA reported the highest amounts of fall damage (31, 20, and 19%, respectively). The northern peripheral states/provinces (ME, NH, VT, ONT, QUE) reported most damage in summer (77%), with no observations of damage occurring in all three seasons or solely in the fall. The greater summer damage observed with northern populations may be a result of first-generation larval populations developing later in the spring/early summer compared more southern locations. ### Management of L. maculicollis Populations #### Budget The annual maintenance budgets for all surveyed golf courses in the region demonstrated peaks between US$1.0 million and US$1.5 million and between US$350,000 and US$550,000 per year. Removing the 9-, 27-, and 36-hole golf course budgets did not change the distribution of annual budgets (26.0% = US$1 − 1.5 million; 19.4% = US$350,000 − 550,000 per year; Table 3). Table 3. Distribution of annual maintenance budgets of surveyed golf facilities (9-, 18-, 27-, and 36-hole courses) Maintenance budget (US$) No. of responses
$1,500,001–$2,000,000 29 10
$1,000,001–$1,500,000 64 22
$750,001–$1,000,000 37 13
$550,001–$750,000 41 14
$350,001–$550,000 55 19
$200,001–$350,000 42 14
<$200,000 18 Maintenance budget (US$) No. of responses
$1,500,001–$2,000,000 29 10
$1,000,001–$1,500,000 64 22
$750,001–$1,000,000 37 13
$550,001–$750,000 41 14
$350,001–$550,000 55 19
$200,001–$350,000 42 14
<$200,000 18 Annual insecticide budgets averaged US$9,270 and ranged between US$50 and US$75,000 per year. The average annual insecticide budgets, when adjusted for an 18-hole equivalent, ranged between approximately US$4,000 and approximately US$17,000 in subregions where there were enough responses to summarize (Table 4). CT (US$14,627), NJ (US$13,770), NY (US$10,000), and MA (US$10,843) had the highest average annual insecticide budgets. Upstate New York and the northern peripheral states/provinces ranked the lowest with median insecticide budgets of US$4,072 and US$4,781, respectively. Interestingly, Long Island, despite being the most restricted region in terms of insecticide registration and use, was the highest in median insecticide spending (US$17,047). Table 4. Average insecticide budgets and trends in chemical management of L.maculicollis populations Region Median insecticide budget (US$) L. maculicollis applications/year

Pyrethroid applications/year for all pests on golf course Resistance suspected? (% Yes) Noticed decrease in effectiveness of treatments? (% Yes)
Average per year >5 Apps (%) >9 Apps (%)
All Regions 9,270 3.9 18 2.7 19 14
Northern Periphery 4,781 2.2 3.6
MA 10,843 4.4 13 10 3.9
CT 14,627 4.2 20 12 1.7 48 24
NY 10,112 4.1 18 14 3.3 29 29
Long Island 17,047 5.5 30 20 2.9 55 35
Upstate NY 4,072 2.3 2.7
NJ 13,770 4.4 23 2.4 28 19
PA 9,628 4.2 24 3.0 22 12
Eastern PA 11,422 4.4 24 2.9 24 18
Western PA 8,914 3.9 23 3.3 17
DE-MD-VA 7,422 3.6 17 2.8
Western Periphery 10,444 2.9 2.0 19
Region Median insecticide budget (US$) L. maculicollis applications/year Pyrethroid applications/year for all pests on golf course Resistance suspected? (% Yes) Noticed decrease in effectiveness of treatments? (% Yes) Average per year >5 Apps (%) >9 Apps (%) All Regions 9,270 3.9 18 2.7 19 14 Northern Periphery 4,781 2.2 3.6 MA 10,843 4.4 13 10 3.9 CT 14,627 4.2 20 12 1.7 48 24 NY 10,112 4.1 18 14 3.3 29 29 Long Island 17,047 5.5 30 20 2.9 55 35 Upstate NY 4,072 2.3 2.7 NJ 13,770 4.4 23 2.4 28 19 PA 9,628 4.2 24 3.0 22 12 Eastern PA 11,422 4.4 24 2.9 24 18 Western PA 8,914 3.9 23 3.3 17 DE-MD-VA 7,422 3.6 17 2.8 Western Periphery 10,444 2.9 2.0 19 Region/state abbreviations can be found in Table 1. The percentage of the total annual budget used on insecticides was calculated by using a weighted average of the responses on an 18-hole equivalent and dividing by the median value of the range of the annual maintenance budgets for 18-hole golf courses. Using these values, insecticides were determined to account for 1.23% of the total maintenance budget. #### Chemical Management A significant portion of the survey’s questions dealt with insecticides, as this is a main component of most L. maculicollis management programs (McGraw and Koppenhöfer 2007). Each superintendent surveyed identified at least one product that was used in managing the weevil, despite the fact that 10% of responders reported no damage to any areas (Fig. 3). The pyrethroids and chlorpyrifos (e.g., Dursban), used by 79% and 65% of respondents, respectively, were the most popular means of controlling L. maculicollis adults, despite development of pyrethroid resistance (Ramoutar et al. 2009a, b) and indications that chlorpyrifos efficacy may also be reduced (Clavet et al. 2010, A. M. Koppenhöfer, unpublished data). The anthranilic diamide chlorantraniliprole (Acelepryn) was the most widely used larvicide (51%), which may, in part, be due to its broad spectrum of activity and role in preventive white grub management. Cyantraniliprole (Ference), another anthranilic diamide, was not yet registered for turfgrass at the time of our survey. Fig. 3. Chemical insecticides used in L. maculicollis management. Combination products include insecticides with two active ingredients (e.g., bifenthrin + imidacloprid). Fig. 3. Chemical insecticides used in L. maculicollis management. Combination products include insecticides with two active ingredients (e.g., bifenthrin + imidacloprid). Courses made an average of 3.9 insecticide applications per year to manage L. maculicollis (Table 4). States/regions where courses had above average application frequency were located around the epicenter of L. maculicollis distribution (NJ = 4.4; MA = 4.35; CT = 4.2; PA = 4.2; NY = 4.1). Superintendents on Long Island, where the relatively long-residual anthranilic diamides are not registered, made the most applications to control L. maculicollis per year (5.5), with the highest use of pyrethroids (85%). Thirty percent of superintendents in this area reported making six or more annual L. maculicollis applications (survey average = 18%), and 20% made 10 or more applications (survey average = 6%). The Northern (2.2) and Western peripheral states/regions (2.7) and Upstate NY (2.3) had the fewest annual applications. #### Development of Pyrethroid-Resistant Populations On average, superintendents reported making 2.7 pyrethroid applications per year (including all targeted insect pests; Table 4). The regions with highest number of pyrethroid applications included MA (3.9) and the northern peripheral states/provinces (3.6). One in five courses (20.1% of the courses with damaging L. maculicollis populations) reported having a pyrethroid-resistant L. maculicollis population either suspected or confirmed by bioassay. "Resistant" populations were located all across the region, though higher than average incidence came from areas with long histories of managing L. maculicollis, including Long Island (55% surveyed suspected resistance), CT (48%), and NJ (28%; Table 4; Fig. 4). Interestingly, no superintendents in regions with the highest pyrethroid use (MA, northern peripheral states/provinces), as well as Western peripheral states suspected that they had a pyrethroid-resistant population. This may be due to the fact that L. maculicollis has become problematic more recently in these areas and pyrethroids have not been used for as long. Fig. 4. Distribution of surveyed courses with suspected or confirmed pyrethroid-resistant L. maculicollis populations. Fig. 4. Distribution of surveyed courses with suspected or confirmed pyrethroid-resistant L. maculicollis populations. On the whole, “resistant” L. maculicollis populations caused more damage than susceptible populations when grouped by seasonal damage incidence (93% vs. 74% of courses, respectively). Courses with “resistant” populations had a significantly greater number of turf areas damaged (n > 256; U > 3021.5; P < 0.001), including 84% and 85% of collars/approaches and fairways damaged, versus 48% and 52% for courses with susceptible populations. Courses reporting resistance also had higher numbers of sites damaged (21.2 vs. 9.8 combined turf areas, respectively). Interestingly, a significantly higher percentage of “resistant” courses (36%) than susceptible courses (21%) reported damage to putting greens (n = 278; U = 3451.5; P < 0.001) despite the “resistant” courses having significantly lower average green heights-of-cut (2.84 mm) than the susceptible courses (3.05 mm; n = 280; U = 4394.5; P = 0.001). Two-thirds of “resistant” courses but only 42% of susceptible courses had annual maintenance budgets greater than US$750,000 (18-hole equivalent). It is not surprising that, given the higher maintenance budgets at “resistant” courses, the average annual insecticide budget of “resistant” courses was more than double that of the susceptible courses (US$19,241 vs. US$8,361 annually). This statistic is understandable given that the total area damaged by L. maculicollis on “resistant” courses is more than double that of susceptible populations for most site categories, including fairways (8.3 vs. 3.4 damaged), which account for much of the managed turf area on golf courses. Greater insecticide budgets on “resistant” courses may also be explained by the significantly greater frequency of L. maculicollis applications (5.8 vs. 3.5 per year; n = 261; U = 2666, P < 0.001). More than 40% of “resistant” courses but only 10% of susceptible courses reported making more than 5 applications per year. Additionally, 18% of “resistant” courses reported making 10 or more applications to control L. maculicollis.

Chemical selection differed greatly between the two types of L. maculicollis populations (Fig. 5). Larvicides, especially chlorantraniliprole, indoxacarb (Provaunt), spinosad (Conserve), and trichlorfon (Dylox) tended to be used more on courses with “resistant” than courses with susceptible populations. Most (93%) superintendents of courses with “resistant” populations used chlorpyrifos in adult management. However, a relatively high percentage of respondents (64%) still used pyrethroids. The number of annual pyrethroid applications on the golf course with “resistant” was not significantly different from susceptible courses (n = 256; U= 4668.5, P = 0.30). “Resistant” courses were also much more likely than susceptible courses to select older broad-spectrum insecticides like trichlorfon (67% vs. 34% for susceptible courses) or carbaryl (e.g., Sevin; 21% vs. 11%).

Fig. 5.

Comparison between pyrethroid-susceptible and "resistant" courses chemical insecticide use.

Fig. 5.

Comparison between pyrethroid-susceptible and "resistant" courses chemical insecticide use.

### Integrated Pest Management

Pest control decisions for golf courses are based on aesthetics, playability, and avoidance of damage; hence, strong emphasis is placed on preventive chemical control of insects, diseases, and weeds. Turfgrass managers nevertheless can incorporate many aspects of integrated pest management (IPM) into their management of L. maculicollis, including monitoring, reducing chemically treated areas, use of relatively resistant turfgrasses, and the application of curative controls (e.g., larvicides) to at-risk areas on the course. Most (73%) responders indicated that they “always” or “sometimes” employ spot treating as a means of controlling L. maculicollis. Only 16% indicated that they never spot treat. A greater than average number of responses from the DE-MD-VA region (40%) indicated that those superintendents "never" employ spot treatments. This is surprising, given the relatively short history of damaging populations in the region, and the lower amounts of P. annua present on those golf courses.

#### Poa annua Removal

Poaannua is believed to be the preferred host plant of L. maculicollis (Kostromytska and Koppenhöfer 2014). The adults lay more eggs in P. annua and gain fitness advantages in this host, such as reduced days to development and larval weight gain (Rothwell 2003; Kostromytska and Koppenhöfer 2014). The pest can also develop in and damage A. stolonifera, even in mixed stands where P. annua is not limiting, although A. stolonifera is more tolerant and requires greater larval densities than P. annua before damage becomes visible (McGraw and Koppenhöfer 2009, Kostromytska and Koppenhöfer 2016). Therefore, promoting A. stolonifera in mixed stands should help to reduce damage and need for insecticide applications. However, only 54% of responders indicated that they tried to reduce the amount of P. annua on the course as a means to reducing L. maculicollis damage. Many of the courses, especially older courses in the New York City metropolitan area, have large percentages of P. annua in most playing surfaces. Although re-grassing the course to reduce weevil damage may not be a viable strategy for such courses, promoting A. stolonifera over P. annua through selective cultural methods and plant growth regulators may be a viable option.

#### Monitoring Practices

Superintendents regularly employ scouting techniques to estimate L. maculicollis population densities or determine presence (Table 5). Most (90%) responders indicated they regularly use two or more monitoring techniques, and 80% used three or more. Only 5.1% indicated that they do not regularly monitor. Most Sampling practices can be broken down into two categories: passive (scouting practices that require little manual effort) and active (monitoring practices that estimate pest density). A low percent of superintendents reported solely using one type of technique. Roughly 9% indicated the use of only active means to determine population density, and a similar number (8%) indicated using solely passive monitoring techniques (plant phenology, growing degree days). The remaining 79% of responses indicated the use of both types of monitoring techniques. Passive techniques were favored, even by responders using multiple means of assessing populations. Weevil Trak, Syngenta’s proprietary monitoring system that gauges population activity and development across the region from growing degree-days and soil and vacuum samples on courses within a region (conducted by University personnel and consultants), used by 72% of responders, was the most popular means of monitoring L. maculicollis populations. Smaller percentages of responders used other passive techniques such as monitoring plant phenology (65%) and calculating growing degree days (45%). More active means of population assessment included checking mower baskets for adults (61%) and taking soil cores (56%) to observe stages. Other active measures that were less popular were the use soap flushes (40%), traps (e.g., linear pitfall traps) (28%), salt flushes (11%), and vacuum sampling (6%).

Table 5.

Scouting methods employed by golf course superintendents in determining L.maculicollis population development or density

Scouting technique No. of responses
Weevil Trak 200 72
Plant phenology 181 65
Soil coring 155 56
Growing DD 124 45
Soap flushes 111 40
Traps 79 28
Salt flushes 30 11
Vacuuming 17
Scouting technique No. of responses
Weevil Trak 200 72
Plant phenology 181 65
Soil coring 155 56
Growing DD 124 45
Soap flushes 111 40
Traps 79 28
Salt flushes 30 11
Vacuuming 17

#### Information Sources and Influences

Most responders indicated that they use multiple sources including Colleagues (82%), Sales/distributors (80%), and University personnel (78%) for information on L. maculicollis management (Table 6). Specific “Other” responses (9%) included Syngenta’s Weevil Trak, consultants, and United States Golf Association’s Turf Advisory Service.

Table 6.

Sources of information used by superintendents managing L.maculicollis populations and the relative influence on decision-making or management philosophy

Regiona Where do you get information/help in controlling pests or formulating your insect control program? (%)

Who has the greatest influence on your management philosophy? (%)

Colleagues Sales/distributors University Internet Other Colleagues Sales/distributors University Self Consultant
All Regions 82 80 78 38 31 21 43
Northern Periphery 92 92 77 15 15 46
MA 88 82 91 39 26 13 55
CT 76 80 84 24 16 16 44
NY 80 60 71 38 13 27 13 48 10
Long Island 85 60 80 30 10 35 45
Upstate NY 73 58 58 38 19 15 15 31
NJ 75 81 81 25 13 25 50
PA 77 82 78 39 37 24 35
Eastern PA 79 82 76 47 50 25
Western PA 77 87 77 27 10 34 28 31
DE-MD-VA 88 85 71 56 17 44 15 35
Western Periphery 75 94 56 25 13 56 19
Regiona Where do you get information/help in controlling pests or formulating your insect control program? (%)

Who has the greatest influence on your management philosophy? (%)

Colleagues Sales/distributors University Internet Other Colleagues Sales/distributors University Self Consultant
All Regions 82 80 78 38 31 21 43
Northern Periphery 92 92 77 15 15 46
MA 88 82 91 39 26 13 55
CT 76 80 84 24 16 16 44
NY 80 60 71 38 13 27 13 48 10
Long Island 85 60 80 30 10 35 45
Upstate NY 73 58 58 38 19 15 15 31
NJ 75 81 81 25 13 25 50
PA 77 82 78 39 37 24 35
Eastern PA 79 82 76 47 50 25
Western PA 77 87 77 27 10 34 28 31
DE-MD-VA 88 85 71 56 17 44 15 35
Western Periphery 75 94 56 25 13 56 19
a

Abbreviations see Table 1.

When asked which source has the greatest influence on their decision-making, responders indicated University personnel (43%) followed by Colleagues (31%). There was a positive correlation between percentages of those using University information and those indicating that to be their most influential source (Pearsons = 0.58; P = 0.07). Colleagues had the greatest influence on management decisions in Eastern PA (50%), VA (46%), as well as the DE-MD-VA region (44%). We cannot ascertain as to why reliance on peers is so high in these areas, though it may reflect the relatively recent history of L. maculicollis damage there, coupled with there being relatively few University personnel dedicated to turfgrass entomology in that region.

Sales people/distributors were the main source of information for 21% of the surveyed superintendents. Their influence was greatest in Western “Peripheral” states/regions (56%) and PA (24%), perhaps reflecting lack of dedicated University turf entomology programs in the recent past in PA. A small percentage of responses indicated “consultant” (3%) and “self” (3%) as having the greatest influence on management decisions. Consultants were most influential in the decision-making process in NY (10%) and in the Northern “Peripheral” states/provinces (8%). These low values likely reflect the relatively few turfgrass consulting and scouting services available across the region.

#### Changes to Management Programs

More than half (54%) of the surveyed superintendents indicated that they made changes based on presentations or recommendations made by University researchers and staff. Two thirds of all responses from NJ and NY (including 75% from Long Island) indicated changes were made based on information from University personnel. Lowest frequency of impact from University personnel was observed in responses collected from DE-MD-VA (32%) and western PA (24%).

Most turf managers (94%) who answered the question about changes described those changes in the fill-in-the-blank section of the survey. Most changes made were related to chemical management. Timing of controls (43%), chemical selection (39%), and chemical rotations (23%) were the predominant responses given. Some responders (17%) noted that they moved away from pyrethroids or chemical insecticides (in general) based on recommendations from University research or recommendations. Less common answers dealt with general IPM recommendations, such as learning about scouting techniques (8%), reducing sprayed areas (2%), alternative controls (2%), and reducing P. annua populations (1%).

## CONCLUSIONS

This survey provides a broad framework for understanding the importance and spread of L. maculicollis as a golf course pest, the spread and severity of insecticide resistance, and the need for expanded extension efforts to communicate best management practices for the pest. With 90% of respondents indicating damaging densities on their courses with on average about one third of fairways, tees, and greens/collars affected, the weevil clearly is a tremendous problem in the region. Resistance is already widespread, with 20% of responders throughout region (regionally up to 55%) suspecting or having confirmed resistance. Since resistance may not be recognized until resistance ratios (RR50) reach or pass about 30 (for pyrethroids; A. M. Koppenhöfer, unpublished data), there are likely many more courses that will develop insecticide-resistant populations in the near future.

Despite reports of pyrethroid resistance, pyrethroids are still the most widely used insecticide class for the weevil's management, followed by another adulticide, chlorpyrifos. While "resistant" courses have made significant changes in insecticide use, particularly greater adoption of larvicides and switching to chlorpyrifos as the primary adulticide, 64% of those courses still used pyrethroids. Greater changes in types of insecticides used are likely being held back by a combination of risk-averseness, dominance of preventive approaches by superintendents, and the much lower cost of adulticides compared to the more effective larvicides. However, few classes of insecticides are effective in controlling adult weevils, and the ability for those classes to control pyrethroid-resistant L. maculicollis populations is questionable, as highly pyrethroid-resistant populations show already increased tolerance if not resistance to all of them (Koppenhöfer et al. 2012). Our findings highlight the need for novel approaches for controlling adults. Registration of a new highly effective larvicide (cyantraniliprole, Ference) in 2015 (after this survey was conducted) is likely to increase larvicide use, at least against "resistant" populations. Unfortunately, larvicides are generally much more expensive than adulticides, and therefore are cost-prohibitive for many facilities.

Nearly all superintendents who deal with L. maculicollis monitor weevil populations, but the most widely used methods only help with timing of management as opposed to estimating population densities. However, 56% of respondents used soil cores to scout for larval stages, which is the most direct and likely most precise method to assess need for treatments. If more courses move away from primary reliance on adulticides, monitoring of larvae will become more important, which could in turn reduce total insecticide use. Because highly resistant weevil population are also more tolerant if not resistant to most of the currently available larvicides (Koppenhöfer et al. 2012), superintendents will also have to start relying more on biorational insecticides and cultural means to manage weevil populations. Alternatives based on azadirachtin, Bacillus thuringiensis, and entomopathogenic nematodes are being studied, and some of them may offer viable alternatives (B. A. McGraw and A. M. Koppenhöfer, unpublished data). Such options may become increasingly used, at least on courses with resistant L. maculicollis populations, or ones in localities (e.g., Long Island, NY) having special restrictions on insecticide use.

Our survey suggests that most superintendents already rely on University personnel for information about L. maculicollis management, and that University-based advice has the greatest impact on their management philosophy. Not surprisingly, the influence of University personnel tends to be highest in areas having entomologists dedicated to the problem, and in areas with a longer history of weevil problems. Efforts by University personnel to extend information regarding resistance management and use of alternatives to synthetic insecticides need to increase. Information gathered from this survey along with ongoing research on these alternatives should help toward this goal.

## References Cited

Clavet
C. D.
Requintina
E. D.
Jr.
Ramoutar
D.
Alm
S. R.
.
2010
.
Susceptibility of Listronotus maculicollis (Coleoptera: Curculionidae) adults from southern New England golf courses to chlorpyrifos
.
Florida Entomologist

93
:
630
632
.
(GCSAA) Golf Course Superintendents Association of America
.
2007
. Golf Course Environmental Profile: property profile and environmental stewardship of Golf Courses, vol. 1, Lawrence, KS.
.
2015
. Golf facilities in Canada 2015: The definitive report of golf facilities and development in Canada, Acton, Ontario.
Koppenhöfer
A. M.
Alm
S. R.
Cowles
R. A.
McGraw
B. A.
Swier
S.
Vittum
P. J.
.
2012
.
Controlling annual bluegrass weevil: optimal timing and rates
.
Golf Course Management

March: 98
104
.
Kostromytska
O. S.
Koppenhöfer
A. M.
.
2014
.
Ovipositional preferences and larval survival of annual bluegrass weevil, Listronotus maculicollis, on Poa annua and selected bentgrasses (Agrostis spp.)
.
Entomologia Experimentalis et Applicata

152
:
108
119
.
Kostromytska
O. S.
Koppenhöfer
A. M.
.
2016
.
Responses of Poa annua and three bentgrass species (Agrostis spp.) to adult and larval feeding of annual bluegrass weevil, Listronotus maculicollis (Coleoptera: Curculionidae)
.
Bulletin of Entomological Research
. (in press).
McGraw
B. A.
Koppenhöfer
A. M.
.
2007
. Biology and management of the annual bluegrass weevil, Listronotus maculicollis, pp.
335
350
. In
Pessarakli
M.
(ed.),
The handbook of turfgrass physiology and management
.
Taylor and Francis
,
Boca Raton, FL
.
McGraw
B. A.
Koppenhöfer
A. M.
.
2009
.
Development of binomial sequential sampling plans for forecasting Listronotus maculicollis (Coleoptera: Curculionidae) larvae based on the relationship to adult counts and turfgrass damage
.
Journal of Economic Entomology

102
:
1325
1335
.
O’Brien
C. W.
Wibmer
G. J.
.
1982
.
Annotated checklist of the weevils (Curculionidae sensu lato) of North America, Central America, and the West Indies (Coleoptera: Curculionoidea)
.
Memoirs of the American Entomological Institute

34
:
1
382
.
Ramoutar
D.
Alm
S. R.
Cowles
R. S.
.
2009a
.
Pyrethroid resistance in populations of Listronotus maculicollis (Coleoptera: Curculionidae) from southern New England golf courses
.
Journal of Economic Entomology

102
:
388
392
.
Ramoutar
D.
Cowles
R. S.
Alm
S. R.
.
2009b
.
Pyrethroid resistance mediated by enzyme detoxification in Listronotus maculicollis Kirby, (Coleoptera: Curculionidae) from Connecticut
.
Journal of Economic Entomology

102
:
1203
1208
.
Rothwell
N. L.
2003
. Investigation into Listronotus maculicollis (Coleoptera: Curculionidae), a pest of highly maintained turfgrass. Ph.D. thesis. University of Massachusetts, Amherst, MA.
Vittum
P. J.
Villani
M. G.
Tashiro
H.
.
1999
. Annual bluegrass weevil, pp.
230
242
. In
Vittum
P. J.
Villani
M. G.
Tashiro
H.
(eds.),
Turfgrass insects of the United States and Canada
.
Cornell University Press
,
Ithaca, NY
.
Vittum
P. J.
2012
. Annual bluegrass weevil, pp.
9
11
. In
Brandenburg
R. L.
Freeman
C. P.
(eds.),
Handbook of turfgrass insects
,
2nd ed
.
Entomological Society of America
,
Lanham, MD
.

## Author notes

Subject Editor: Danesha Carley