International Turfgrass Society Research Journal Volume 11, 2009

SEASONAL ECOLOGY OF THE EUROPEAN CRANE FLY < TIPULA PALUDOSA) AND SPECIES DIVERSITY OF THE FAMILY

TIPULIDAE ON GOLF COURSES IN QUÉBEC, CANADA

Elisabeth Tasehereau, Louis Simard*, Jacques Brodeur, Jon Gelhaus, Guy Bélair, and Julie Dionne

ABSTRACT

The European crane fly (ECF), Tipula paludosa Meigen (Diptera: Tipulidae), has been reported in several new sites in North America recently, and has been described as an insect pest on golf courses in several areas. This study was conducted from 2003 and 2004 on four golf courses located in the Québec City area (Canada) with the objectives to identity Tipulidae assemblages to species level and to determine the spatial distribution and temporal occurrence of the ECF. Larvae, pupae and adults were scouted weekly from May to early Oct. A total of 35 species of Tipulidae,' representing four genera, were identified. Two new species were recorded for Québec, Nephrotoma cornicina L., and the Marsh crane fly Tipula oleracea L. ECF was the predominant species found on all sites, accounting for 43-92% of the total number of specimens collected at each golf course. ECF completed one generation per year. In our study, the fourth larval instar was sampled from mid-May to early Sept and adult peak emergence occurred during mid-Sept. Larval density varied among golf course management areas, with larvae being uncommon on tees and greens and most abundant on roughs. A principal component analysis using varimax rotation showed that larval abundance was positively related to silt, clay, Ca, Cu, K, and Mg, and negatively related to sand and uncompressed thatch thickness. This study indicates that the ECF is currently the only Tipulidae species causing turfgrass damage on golf courses in Québec.

Abbreviations: ANSP Academy of Natural Sciences of Philadelphia; ECF, European crane fly; F, fairway; G, green; GC, golf course; R, rough bordering fairway; GShigh, highest portion of green surrounds; GSlow lowest portion of green surrounds; TShigh, highest portion of tee surrounds; TSlow, lowest portion of tee surrounds; and T, tee.

Keywords: insect pest, Nephrotoma cornicina, spatial distribution, Tipula oleracea, turfgrass.

Elisabeth Tasehereau, Centre de Recherche en Horticulture, Département de phytologie, Université Laval, Québec, Québec, G1K 7P4, Canada. Louis Simard* and Guy Bélair, Horticulture Research and Development Centre, Agriculture and Agri-Food Canada, 430 Gouin bldv, St-Jean-sur-Richelieu, Québec, J3B 3E6, Canada. Jaques Brodeur, Institut de recherche en biologie végétale, Département de sciences biologiques, Université de Montréal, Montréal, Québec, H1X 2B2, Canada. Jon Gelhaus, Department of Entomology, Academy of Natural Sciences, Philadelphia, PA, 19103-1195, USA. Julie Dionne, Royal Canadian Golf Association, Golf House, 1333 Dorval Drive, Oakville, Ontario, L6M 4X7, Canada. Corresponding author: (simardl @agr. gc. ca).

INTRODUCTION

Worldwide the family Tipulidae (Diptera) is composed of 4,375 species and sub-species, including 208 species in Canada (Oosterbroek, 2007). They colonize a wide variety of habitats ranging from strictly aquatic to drier terrestrial environments (Alexander and Byers, 1981). Most studies on Tipulidae diversity have characterized communities of natural ecosystems (Coulson, 1959; Freeman, 1968; Young, 1978; Harper and Lauzon, 1985; Gelhaus and Podenas, 2006) but little information is available from managed habitats. Some species of Tipulidae are considered as pests in agricultural and horticultural systems. For example, the European crane fly (ECF), Tipula paludosa Meigen, and the Marsh crane fly, T. oleracea L., may cause damage to several crops including grass, spring cereals, potatoes, berries, maize, brassica crops and clover (Blackshaw and Coll, 1999).

The ECF is native to Western Europe, where it is recognized as the second most widespread pest problem on golf courses throughout Europe (Mann, 2004). In North America, ECF was first observed in 1880 in Newfoundland, Canada (Alexander, 1962). The species was later reported in different areas across Canada and United States: Nova Scotia, 1955; British Columbia, 1965; Washington State, 1966; Oregon, 1984; Ontario, 1996; California, 1999; Québec, 2002; New York, 2004, and Michigan, 2006 (Fox, 1957; Wilkinson and MacCarthy, 1967; Vittum et al., 1999; Charbonneau, 2002; Umble and Rao, 2004; Gelhaus, 2006; Peck et al., 2006; Simard et al., 2006). These recent observations, along with the increasing damage reported by turfgrass managers confirmed that this species is becoming an important pest in several areas in North America.

ECF larvae, commonly called leatherjackets, feed on leaves, crowns, and roots of cool-season turfgrasses (Vittum et al., 1999). Damage is observed mainly in spring and appears as bare patches often looking like ball marks on golf course tees and greens. On golf course fairways and roughs, high ECF populations often reduce turfgrass density. ECF larvae are also considered a nuisance on golf courses because they can disrupt the playing surface when they are tunneling and dispersing. Moreover, birds and small mammals can make holes on the playing surface, further disrupting play. ECF adults do not feed and thereby do not cause damage to the turf.

In Europe and North America, ECF is univoltine and completes 4 larval stages (Laughlin, 1967; Jackson and Campbell, 1975). In Canada, little information is available on the seasonal ecology of the ECF. In Québec, Simard et al. (2006) reported the presence of ECF larvae from mid-May until the end of Aug and adult flight from the end of Aug to mid-Sept.

Factors regulating ECF larval populations have been studied primarily in agroecosystems (Jackson and Campbell, 1975; McCracken et al., 1995; Blackshaw and Coll, 1999). Soil condition is one of the major density-independent factors affecting larval abundance and oviposition. ECF eggs and larvae are susceptible to desiccation but also to soil flooding, suggesting that soil parameters influencing moisture content and water tension play a role in sustaining or suppressing ECF populations (Meats, 1970; Blackshaw and Coll, 1999). Soil parameters and thatch thickness vary considerably among and within golf courses and could influence larval survival and abundance.

Table 1. Number of core and grid samples per golf course collected weekly on eight different hole sections together with the dimension of the sampling area in each section. The number of samples per section depends on the dimension of the hole section.

Section Year Number of cores (10.8-cm diam.) Area ± SE (m2)

Green surrounds (GShigh) 2003, 2004 12 179+17 Green surrounds (GSlow) 2003, 2004 20f 298 ±56 Fairway (F) 2003 24 253 ± 9 Rough (R) 2003, 2004 32 438 ± 25 Tee surrounds (TShigh) 2003 12J 175 ±60 Tee surrounds (TSlow) 2003 20$ 286 ± 69 Green (G) 2003 20 393 ± 33 Tee (T) 2003 10Í 208±100

t Fifteen cores were collected in GSlow at GC4 (Saint-Michel-de-Bellechasse) because in this section the surface was restricted by bunkers.

t At GC1 (Cap-Rouge), a reduced number of samples were collected because the tee section was smaller than the other golf courses: 9 cores in TShigh, 15 cores in TSlow and 5 grids in T.

The specific objectives of our study were to: (i) describe to species level Tipulidae assemblages on golf courses in Québec; (ii) characterize the ECF seasonal ecology on golf courses in Québec; (iii) determine the ECF spatial distribution in relation to different golf course management areas; and (iv) measure correlations between soil parameters, uncompressed thatch thickness, and larval abundance.

MATERIALS AND METHODS

This study was conducted in 2003 and 2004 on four golf courses located in the Québec City area, Canada: GC1 = Cap-Rouge (46°49'N, 71°13'W), GC2 = Lévis (46°48'N, 71°11'W), GC3 = Boischatel (46°54'N, 71°09'W), and GC4 = Saint-Michel-de-Bellechasse (46°52'N; 70°55'W). Experimental sites were selected based on a history of ECF infestation (Simard et al., 2006). During this project, superintendents followed typical turfgrass management practices. An insecticide (Sevin XLR®, carbaryl) was applied once to control ECF on all greens at GC2 and GC4 in June 2003.

ECF sampling For each golf course, the same hole

was scouted weekly from May to early Oct in 2003 and 2004, except for GC4 where no

sampling was done in 2004. Golf holes were divided in 8 sections, or management areas: green (G), tee (T), highest portion of green surrounds (GShigh), lowest portion of green surrounds (GSlow), fairway (F), rough bordering fairway (R), highest portion of tee surrounds (TShigh), and lowest portion of tee surrounds (TSlow). In 2003, all sections were scouted to characterize the distribution of ECF larvae on golf courses. Seasonal development was characterized in 2003 and 2004 by scouting only sections with substantial ECF populations (GShigh, GSlow and R sections).

A golf course hole cutter (10.8-cm diam.) was used for sampling larvae and pupae in thatch and soil to a depth of 7.7 cm. Cores were broken up and insects were counted directly on the site. On greens and tees, a non-destructive method was used. Larvae and pupae at the surface of greens and tees were counted early in the morning before mowing,

2 using a 0.25 m grid (Majeau et al., 2000). Table 1 shows the numbers of grids and cores randomly sampled on each section. Sampling was interrupted during the second and the third weeks of Sept because a previous study (Simard et al., 2006) showed that there were no larvae and pupae during this period in the Québec City area.

An ultraviolet light trap (BioQuip Products Inc®, Rancho Dominguez, California, United States) equipped with a 5 cm x 5 cm insecticide plaque (Vapona® No-Pest® Strip, Marysville, Ohio, United States) was installed on the ground at each golf course to sample ECF adults. The environment surrounding the light trap varied at each golf course. At GC1, the light trap was surrounded by woodland patches; at GC2, it was placed between two ponds; at GC3, it was located in an open area (between two fairways) ca. 500 m from a partially submerged stream; and at GC4, it was placed in an open area surrounded by the club house, the driving range and within 500 m of a stream. Light was activated at dark by a photoelectric switch. Insect captures were collected each week from mid-May to the beginning of Oct.

Larvae, pupae and adults were brought back to the laboratory and preserved in a solution of ethyl alcohol, glycerin, acetic acid, and distilled water (8/1/1/5, v/v/v/v) (Loiselle and LePrince, 1987). Tipulidae larvae were identified by Dr. Sujaya Rao, Oregon State University, using mitochondrial cytB sequences (Rao et al., 2006). Head width (distance between antennae) and length of the antennae were measured for all larvae collected in GShigh, GSlow and R sections to determine larval instars. For these sections, a total of 1936 head capsules and antennae were measured in 2003 and 2004 using a dissecting microscope at 3x magnification equipped with Motic Images 2000 1.3 ® (Motic Instruments Inc., Richmond, BC, Canada) and larval stages were determined according to Pritchard (1982).

Adults were identified to species and sex. Initial identifications were made by Dr. Pierre-Paul Harper from the University of Montréal and then confirmed by Dr. Jon Gelhaus. Identification was made using

keys from Alexander (1942) and various papers updating portions of those keys, as well as comparing specimens to those in the reference collection at the Academy of Natural Sciences at Philadelphia (ANSP). Species identifications for crane flies are most definitive when based on male specimens; species designations left at "sp." are generally unassociated female specimens in groups in which the female stage is not clearly identifiable (e.g., Tipula [Beringotipula]) or the specimen was in poor condition, precluding a definitive identification. Species classification was derived by consulting Oosterbroek (2007). Larval habitat designations were taken from Young and Gelhaus (2000) or developed through surveying the literature (such as Gelhaus, 1986) and/or unpublished rearing and collection notes of author Gelhaus. Voucher specimens are housed at ANSP and at the Collection d'insectes du Québec of the Ministère des Ressources naturelles et de la faune du Québec.

Soil characterization In July 2003, each section of the 4

golf courses was sampled using a 2.2-cm diam. x 15-cm deep soil probe. A total of 112 samples (approximately 250 ml of soil) was taken as followed: G = 2; GShigh = 4; GSlow = 4 (except 3 at GC4); F = 4; R = 5 (except 6 and 4 at GC1 and GC2, respectively); T = 2 (except 1 at GC1 and GC4); TShigh = 4; and TSlow 4 (except 3 at GC1). Soil analyses were done at the chemistry laboratory of the Horticultural Research and Development Centre (Agriculture and Agri-Food Canada at St-Jean-sur-Richelieu, Québec, Canada). Available Al, Ca, Cu, Fe, K, Mg, Mn, P and Zn were determined following the Mehlich III extraction method and total N contents was measured using a modified Kjeldahl method (Isaac and Johnson, 1976). Soil pH (CaCl2) and organic matter content (%, w/w dry) were also assessed. The particle size

distribution was done using the Bouyoueos hydrometer method (ASTM-type 152H). Furthermore, the uncompressed thatch thickness was measured with a ruler for each golf course (20 samples / section).

Statistical analysis Densities of ECF larvae (average

larvae/m2) collected from SG sections (GShigh and GSlow) were compared by two-way ANOVA between golf courses and years using the procedure PROC MIXED (SAS Institute, 1999). Considering the significant interaction (Year x GC), the abundance was then analyzed with PROC GLM followed by protected least significant difference (LSD) to compare means within year (SAS Institute Ine, 1999). SG sections were selected to compare ECF abundance because no insecticide was applied to those areas. Ten weeks of sampling from mid-June to mid-Aug. in 2003 and in 2004 were used as replicates because only one site per section was scouted at each golf course. We considered that ECF larvae are inactive during this period and are waiting in their burrows before pupation as described by Laughlin (1967). Durbin-Watson test confirmed that error terms were not positively or negatively auto-correlated.

Densities of ECF larvae (average larvae/m2) found in fairways and roughs were also compared by two-way ANOVA between sections and golf courses (PROC GLM, SAS Institute Ine, 1999). Green (G) and tee (T) sections were not included in this analysis because the scouting method was different from other management areas. Considering the significant interaction (Section x GC), the abundance was then analyzed with PROC GLM followed by protected least significant difference (LSD) to compare means within golf course (SAS Institute Ine, 1999). As mentioned previously, 10 wk of sampling from mid-June to mid-Aug in 2003 were used as

replicates because only one site per section was scouted at each golf course. Data contained many zeros, which generated heterogeneity of variance. To respect the postulate of homogeneity of variance, density data were transformed in categories (0 larva/m2 = 0 and 1 larva/m2 or more = 1) for modeling the probability of presence (the probability to observe at least one larva). These probabilities were arcsin transformed to normalize data. Type I error rate was set at a = 0.05 for all analyses.

A principal component analysis followed by a varimax rotation (PROC FACTOR, SAS Institute Inc, 1999) was performed on the average number of ECF larva/m2 (10 wk of sampling from mid-June to mid-Aug in 2003) in relationship with the corresponding sand, silt, clay, Al, Ca, Cu, Fe, K, Mg, Mn, N, P, Zn, organic matter, uncompressed thatch thickness, and pH results. Only the varimax rotated components with eigenvalues >1 and involving high saturation with ECF larvae were retained. Absolute values >0.40 were considered statistically significant.

RESULTS

Species diversity Adult specimens collected in 2003

and 2004 provided a description of the Tipulidae community occurring on golf courses in Québec. A total of 1,704 adults were collected over 2 yr. Table 2 shows the list of species identified, their abundance per golf course, the period when adults were caught in light traps, and the type of habitats associated with the larvae as described by Young and Gelhaus (2000).

A total of 35 species of Tipulidae representing four genera were identified (Table 2). Nephrotoma cornicina, and T. oleracea were new records for Québec. Species richness varied among golf courses

Table 2. List of species of the family Tipulidae identified on four golf courses of Québec City area during 2003 and 2004. Abundance refers to the total number of adults collected in light traps over both years

Abundance Golf coursesf

Species GC1 GC2 GC3 GC4 MonthsJ Habitats* Angarotipula illustris Doane 3 A Aq Dolichopeza (Oropeza) sp. 1 J Dolichopeza venosa Johnson 1 J T-Fo Nephrotoma cornicino Linnaeus 15 6 J A T-Fo / Tu Nephrotoma euceroides Alexander 5 9 J J T-Fo Nephrotoma ferruginea Fabricáis 7 13 2 1 J A S T-Tu / Fo Nephrotoma lugens Loew 1 J __ Nephrotoma sp. 1 1 J Nephrotoma sp. 2 2 J J Típula (Beringotipula) borealis Walker 1 J SAq Tipula (Beringotipula) latipennis Loew 1 J —

Tipula (Beringotipula) resurgens Walker 1 2 J J —

Tipula (Beringotipula) sp. 6 13 20 J A —

Tipula (Lindnerina) senega Alexander 4 J __ Tipula (Lunatipula) d. dorsimacula Walker 2 1 6 J T-Tu/Fo Tipula (Lunatipula) submaculata Loew 2 J A T-Fo Tipula (Lunatipula) valida Loew 1 J T-Fo Tipula (Platytipula) cunctans Say 1 1 S Aq Tipula (Platytipula) sp. 5 2 1 S 0 Tipula (Platytipula) spenceriana Alexander 4 1 S Aq Tipula (Pterelachisus) sp. near trivittata 1 J T-Fo Tipula (Schummelia) hermannia Alexander 1 J T-Fo Tipula (Schummelia) sp. 1 J Tipula (T. ) oleracea Linnaeus 3 A T-Tu Tipula (T. ) paludosa Meigen 417 717 62 205 A S 0 T-Tu Tipula ( Vestiplex) longiventris Loew 1 J T-Fo Tipula (Yamatotipula) caloptera Loew 1 11 J A s Aq Tipula (Yamatotipula) cayuga Alexander 1 J Aq Tipula (Yamatotipula) eluta Loew 13 A s Aq Tipula (Yamatotipula) furca Walker 12 32 20 J A s Aq Tipula (Yamatotipula) kennicotti Alexander 6 15 10 2 J A s Aq Tipula (Yamatotipula) sayi Alexander 5 1 1 2 A SAq / T-Fo Tipula (Yamatotipula) strepens Loew 4 1 2 J J A s Aq Tipula (Yamatotipula) tephrocephala Loew 2 J Aq Tipula sp. 2 1 J A

tLocations of golf courses: GC1 (Cap Rouge), GC2 (Levis), GC3 (Boischatel) and GC4 (Saint-Michel-de-Bellechasse).

XMonths of capture from May to Oct (no specimens were captured in May). * Larval habitats according to designations taken from Young and Gelhaus (2000). Abbreviations of habitats:

Aquatic (Aq), Semi-aquatic (SAq), Terrestrial -Forest (T-Fo) and Terrestrial-Turf (T-Tu).

with 10, 15, 17, and 22 species observed for GC4, GC3, GC1, and GC2, respectively. Only 4 species were found on all golf courses: Nephrotoma ferruginea, T. paludosa, T. kennicotti, and T. sayi. All except T. kennicotti are known to be associated with turf or disturbed environments. T. paludosa predominated the Tipulidae community on all sites, accounting for 43-92% of the total number of specimens collected at each golf course.

All larvae collected on golf courses were identified as T. paludosa, no larvae of any other species were detected.

ECF seasonal ecology In our study, ECF completed one

generation per year on golf courses in Québec and overwintered generally as second instars. The fourth larval instar was sampled from mid-May to early Sept and adult peak emergence occurred during mid-

Fig. 1. European crane fly seasonal development on four golf courses in the Québec City area in 2003 and 2004. Locations of golf courses: GC1 (Cap Rouge), GC2 (Levis), GC3 (Boischatel) and GC4 (Saint-Michel-de-Bellechasse). Data presented are from highest portion of green surrounds (GShigh), lowest portion of green surrounds (GSlow) and rough bordering fairway (R).

Sept. Figure 1 illustrates the seasonal ecology of T. paludosa on the four golf courses in 2003 and 2004

Abundance and distribution In 2003 and 2004, populations of

ECF larvae in green surrounds (SG) sections varied among golf courses (F = 41.89, df = 3, P < 0.0001) and years (F = 114.41, df = 1, P < 0.0001). Larval abundance was higher in 2003 compare to 2004 for two golf courses (GC1: F = 155.92, df = 27, P < 0.0001; GC3: F = 26.60, df = 27,

P < 0.0001). The highest population of ECF was observed at GC1 throughout the study. In 2003, larval populations at this golf course were significantly higher (mean larvae/m2 ± SE; 25.9 ± 1.2) than all other golf course sampled (F = 63.33, df = 3, P< 0.0001). GC2 (7.7 ± 1.1) and GC4 (7.8 ± 0.8) had significantly lower populations than GC3 (11.9 ± 1.3). In 2004, GC1 (10.2 ± 1.3) had a significantly higher populations compared to GC2 (6.6 ± 0.7) and GC3 (5.4 ± 1.2) (F= 5.41, df = 2, P < 0.0106).

SteUoni Fig. 2. Incidence of European crane fly larvae on 4 golf courses in the Québec City area. Histograms represent the probability (+ SE) to observe at least one larva in each section of all golf courses from mid-June to mid-Aug 2003. Values followed by the same letter are not significantly different (ANOVA followed by LSD test; a = 0.05). Sections are: GShigh = highest portion of green surrounds, GSlow = lowest portion of green surrounds, F - fairway, R = rough bordering fairway, TShigh = highest portion of tee surrounds, TSlow = lowest portion of tee surrounds. Locations of golf courses: GC1 (Cap Rouge), GC2 (Lévis), GC3 (Boischatel) and GC4 (Saint-Michel-de-Bellechasse).

The probability to observe at least one larva varied between golf courses (F = 45.62, df = 3, P < 0.0001) and sections (F = 60.56, df= 5, P < 0.0001) (Fig. 2). For the SG and ST sections, larval populations were significantly more abundant in the lowest portion (GSlow or TSlow) than in the highest portion (GShigh or TShigh), except for ST section at GC3. The highest ECF larval densities recorded in 2003 and 2004 were at GC1 in rough with 150 and 126 larvae/m2, respectively. Number of ECF larvae observed on greens and tees were very low with a total number of 79 and 4 larvae collected on the four golf courses in 2003 on greens and tees, respectively.

Soil parameters The principal components involving

ECF larval abundance represented a proportion

of the variance of 5.00 for the component #1 and 1.20 for the component #5 (Table 3). The component #1 indicated that larval abundance was positively related to silt, clay, Ca, Cu, K, and Mg, and negatively related to sand and the uncompressed thatch thickness. Furthermore, the component #5 revealed that larval abundance was positively related to Mn.

DISCUSSION

We identified 35 species of Tipulidae representing 4 genera during this study. The Tipulidae species composition varied among the 4 golf courses, which could be related to the variety of potential larval habitats surrounding the golf courses. Species known from aquatic and semi-aquatic

habitats, including species exploiting stream, marsh, seep and pond habitats, were more numerous in GC2 and GC3. While 10 of the 14 species captured in GC1 are known from forested habitats, the other golf courses had only one to four of these species in the samples. GC4 had the lowest diversity in both terrestrial and aquatic species, but sampling was only conducted over 1 yr. Despite the great diversity of Tipulidae species present on golf courses as adults, including four species known to develop in turf soil, only T. paludosa larvae were found feeding on turfgrass from golf courses and potentially causing damage.

ECF completes one generation per year in Québec. As observed by Simard et al. (2006), the adult flight period extends from mid-Aug to the end of Sept. Data

Table 3. Principal components analysis of the relationships between the yearly average number of ECF larvae/m2 and soil parameters.

Component number / total number of rotated

components of eigenvalue > l f #1/5 #5/5

ECF larval count 0.47Î 0.60 Sand -0.87 -0.06 Silt 0.73 0.03 Clay 0.90 0.07 A1 0.20 -0.07 Ca 0.69 -0.10 Cu 0.62 0.17 Fe 0.25 -0.06 K 0.76 0.02 Mg 0.84 -0.04 Mn -0.11 0.83 N 0.15 0.05 P -0.24 -0.24 Zn -0.06 0.05 Organic matter 0.26 -0.09 pH 0.04 0.02 Thatch tickness -0.52 -0.17 Variance explained by rotated component 5.00 1.20

tOnly the varimax rotated components with eigenvalues >1 and involving high saturation with ECF larvae were retained.

{Absolute values >0.40 are in bold and are considered statistically significant.

collected from GC2 during 4 yr showed that the flight period is consistent from year to year (data not shown for 2006 and 2007). The estimated oviposition period in Québec occurred from late Aug to early Oct. ECF are sexually mature at emergence and both mating and oviposition occur almost immediately after female emergence (Coulson, 1962). Moreover, Jackson and Campbell (1975) observed that the ECF females had laid 95% of their eggs within 26 hr after emergence.

In Québec, ECF adults emerged 3 wk earlier than in southern Ontario, where the flight period occurs from 21 Sept to 4 Oct (Charbonneau and Dupuis, 1999). However, sampling ECF populations with sweep nets in Ontario rather than with light traps (our study) would narrow the observed window of emergence and consequently the earliest and the latest adults might not be sampled. The larval development of ECF in the Québec City area appeared to be similar to the observations reported in southern Ontario (Charbonneau and Dupuis, 1999). First and second instars of ECF were found 1 wk earlier in Québec than in Ontario. Second and third instars were recovered in spring during our study, indicating that both instars can survive winter conditions.

Several factors may contribute to the variation in T. paludosa larval abundance between golf courses, years, and habitat sections. Soil moisture content is known to influence survival of ECF (Blackshaw and Coll, 1999) because eggs and larvae are sensitive to desiccation (Meats, 1967ab) and also soil flooding (Meats, 1970). Pesho et al. (1981) observed lower populations of ECF larvae in forage grass fields than in irrigated turfgrass fields. ECF larvae were most abundant on green surrounds in the lowest portion (GSlow), rough (R) and tee surrounds in the lowest portion (TSlow). Overall, ECF larval abundance was higher

in the lowest sections than in the highest. These differences may be attributed to the fact that greens and tees are irrigated and the lowest portions are more susceptible to excess of water then the highest portions because of the slope. At GC4, there was no irrigation system in the fairway and ECF density was significantly lower than at the other golf courses. Precipitation probably is not a major factor influencing ECF density on golf courses that have an irrigation system. Increasing the drainage of areas where water flows and tends to accumulate, like green surrounds, could help to reduce the number of ECF moving on golf greens. Mowing height influences soil moisture and consequently would have an impact on ECF abundance on golf courses. Tall grasses contribute to maintaining lower soil temperatures, as well as to protecting soil from direct sunlight and wind (Carrow et al., 2001), and consequently to preserve soil moisture. SG, ST and R sections have a higher mowing height (44 to 65 mm) and showed higher ECF abundance while other sections with lower mowing height (green = 3 to 5 mm, tee = 7 to 9 mm, and fairway = 12 to 15 mm) had generally lower ECF populations.

Most ECF larval populations observed during this study were below the economic threshold of 269 larvae/m2 on golf courses suggested by Antonelli and Stahnke (2000). However, low populations of ECF larvae can induce turfgrass damage on golf courses on greens and tees. Furthermore, ECF predators such as birds, skunks, and raccoons often contribute to increase damage. Two golf courses sprayed insecticide on greens in early June 2003 to control ECF because larval populations were high enough to disrupt the playing surface.

Our results showed that ECF larvae were more abundant in clay and loam soils than in sandy soils. Water can percolate

through sandy soils more readily than heavier soils, so humidity on the surface of sandy soils often is lower (Carrow et al., 2001). Lower humidity enhances the probability of ECF larval desiccation. ECF larvae have been reported in all types of soil (Brindle, 1957, 1959; Coulson, 1959) but Coulson (1962) found that mineral soils are more suitable for ECF larval development because of their better capacity to raise water from water table during drought than peat soils. ECF larvae were also more abundant where thatch was not thick. An excess of thatch often repels water and thatch is difficult to wet following desiccation (Beard, 2002). Moreover, excessive thatch could interfere with oviposition of ECF females because the ovipositor might not be long enough to penetrate entirely through the thatch. ECF usually insert the tip of the abdomen into the soil, but never more than the half the length of the abdomen (Coulson, 1962). When eggs are laid in the thatch layer rather than soil they are more likely to be exposed to dry conditions.

Knowledge of the seasonal development and distribution of ECF on golf courses contributes to design and implementation of appropriate pest management strategies. This information is crucial to optimize the timing of treatment applications and to target more precisely infested areas. For instance, golf superintendents typically applied insecticides to control ECF larvae crawling on greens. However, our results showed that ECF larvae were mostly located in green surrounds so treatment strategies should target these areas. Recently, important ECF damage has been reported on golf courses and also on several crops in eastern Québec (Roy et al., 2008). At this time, the ECF is the only Tipulidae species causing turfgrass damage on golf courses in

Québec but the discovery of T. oleracea justifies further monitoring of this species.

ACKNOWLEDGEMENTS

The authors thank Vincent Brousseau, Manon Desjardins and Marie-Eve Gosselin for dedicated technical assistance, as well as all superintendents and golf courses involved in this study. We also thank Dr. Pierre-Paul Harper from the University of Montréal for initial identification of specimens and Dr. Patricia Vittum for critical review of the manuscript. The Canadian Turfgrass Research Foundation and the Royal Canadian Golf Association provided financial support for this project.

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