Dasineura oxycoccana Johnson (Diptera: Cecidomyiidae) is an economically significant pest of cranberry, Vaccinium macrocarpon Aiton (Ericaceae), and highbush blueberry species, including V. corymbosum L., V. corymbosum L. × V. darrowi Camp., and V. virgatum Aiton (all Ericaceae) (Dernisky et al. 2005; Fitzpatrick 2009; Liburd & Averill 2016; Rhodes et al. 2014). Host-associated populations of D. oxycoccana from cranberry (cranberry tipworm) and blueberry (blueberry gall midge) (Cook et al. 2012) are genetically distinct (Mathur et al. 2012), produce different pheromones (Fitzpatrick et al. 2013) and do not interbreed (Cook et al. 2011). The overwintering stage of cecidomyiids is usually the full-grown larva that uses a spatula structure on the prothorax to dig into soil before entering diapause (Gagne 1989). Cranberry tipworm larvae overwinter in leaf litter and soil below the mat of cranberry vines (Eck 1990). Pupation is presumed to occur in early spring before adults emerge, mate, and lay eggs in the apex of growing cranberry shoots. Oviposition begins as cranberry shoots elongate in early spring (Cockfield & Mahr 1994) and increases steadily until mid- or late Jul when fruit have formed and plants are setting buds for the following year (Cook et al. 2012). Eggs laid in early spring are progeny of overwintered individuals. It is not known if eggs laid later in the season are progeny of overwintered or subsequent generations. If cranberry tipworm adults have a prolonged period of emergence from overwintering, as do adults of the swede midge, Contarinia nasturtii (Kieffer) (Diptera: Cecidomyiidae) (Des Marteaux et al. 2015), then a proportion of eggs laid throughout the growing season would originate from overwintered females.
To test the hypothesis that overwintered cranberry tipworms emerge as adults during a prolonged period through spring and summer, we designed an emergence trap similar to the bucket traps evaluated in blueberries (Roubos & Liburd 2010; Hahn & Isaacs 2012; Rhodes et al. 2014), but with some notable differences. Our buckettype emergence trap can be seated snugly onto the soil without damaging the mat of intertwined woody cranberry vines while allowing penetration of rain and irrigation water. Here we describe trap design, report seasonal emergence of overwintered cranberry tipworms, and compare temperature inside and outside the trap during the growing season. In addition, we discovered that our emergence trap detected overwintered hymenopteran parasitoids from the soil beneath infested cranberry plants.
The emergence trap was constructed from 2 white 2.3 L buckets of high density polyethylene (Snap on Lid Pails; Pro-Western Plastics Ltd., St. Albert, Alberta, Canada) (Fig. 1). In order to create a cylinder 16 cm high, the bottom of 1 bucket (the support bucket) was removed with a power saw. The lower edge of the support bucket was fitted with 3 pegs (15 cm long) of plastic-coated wire (0.3 cm diam) spaced equidistantly and attached with cable ties through holes 2.5 cm above the lower rim. A pleated skirt (15 cm long) of black landscape fabric (Vigoro Polyethylene Weed Barrier; Home Depot Inc., Chilliwack, British Columbia, Canada) was attached with weatherproof sealant and black weatherproof electrical tape to the outer surface of the support bucket, 2.5 cm above the lower rim. The second (inner) bucket was cut to create a bottomless cylinder 10 cm high. A circular opening (10 cm diam) was cut in the center of the lid (16 cm diam) of the inner bucket. The opening was covered with a circle (13 cm diam) of white no-seeum mesh (7250NSW; BioQuip Products, Rancho Dominguez, California, USA) glued at the perimeter to the underside of the lid. To hold a double-sided yellow sticky card trap (Silvalure Catch-It Yellow; Terra-Link, Abbotsford, British Columbia, Canada) inside the inner bucket, a length of wooden dowel (0.5 diam × 16.5 cm long) was positioned 1 cm below the top rim and glued at the ends into holes (0.5 cm) cut into the plastic. A 2.5 cm foldback binder clip (Lyreco; Grand & Toy, Vaughan, Ontario, Canada) was clipped around the dowel and oriented so that the handles could be gripped through the no-see-um mesh to attach or release the yellow sticky card.
The trap was assembled by sliding the inner bucket, with the yellow sticky card attached to the clip on the dowel in the lid, into the support bucket (Fig. 1). The trap (20 cm high, 16 cm diam [top], 13 cm diam [bottom]) was seated into the cranberry field by pushing the 3 pegs on the support bucket into soil exposed by parting the cranberry vines, then pushing square-top landscape staples into the fabric skirt to seal the lower rim of the support bucket to the soil. The circular lower rim of the trap enclosed 135 cm2 of soil. Traps were checked weekly by sliding the inner bucket out of the support bucket and squeezing the clip handles to release the used yellow sticky card before installing a fresh one.
Emergence traps were tested in 2015 on 6 cranberry farms in Pitt Meadows (49.3833°N, 122.2333°W) and Langley (49.2666°N, 122.8166°W), British Columbia, Canada. On each farm, 10 emergence traps were placed 10 to 20 m apart along 1 field edge, where cranberry plants had cupped leaves characteristic of tipworm damage from the previous year. Yellow sticky cards in the traps were retrieved weekly and examined under 20 × magnification to count cranberry tipworms and parasitoids that emerged from pupation sites in the soil.
To determine if emergence of overwintered tipworms might be accelerated by warmer temperatures inside traps, hourly temperatures inside and outside 4 traps (1 in each of 4 fields) on 1 Pitt Meadows farm were measured using HOBO Pro v2 (U23-001) temperature loggers (Onset Computer Corporation, Bourne, Massachusetts, USA) in 2016. Loggers were mounted vertically on bamboo stakes with the sensor end 5 cm above soil surface and a UV protective cap over the communication window. We recognize the limitations of using temperature loggers in this way (Terando et al. 2017). Temperature data were downloaded weekly using the HOBO Waterproof Shuttle and HOBOware (Onset Computer Corporation, Bourne, Massachusetts, USA). In 2016, we also monitored emerged tipworms in 20 traps (5 per field) on this farm (see below).
During the 17-wk test period in 2015, a total of 161 overwintered cranberry tipworms were detected in emergence traps on the 6 farms (Fig. 2). The total non-zero number of tipworms per trap per wk ranged from 1 to 7, but zero was the most frequent weekly count; thus, data distribution was non-normal (Shapiro-Wilk = 0.306; N = 919; P = 0.000; SYSTAT 13) (SYSTAT Software Inc. 2013). Emergence began in early May and continued until mid Aug (Fig. 2). More females (101) than males (61) were detected (Pearson chi-square = 9.9; df = 1; P = 0.002; SYSTAT 13). Overwintered tipworms of both sexes were detected most wk.
In 2016, 20 traps on the farm where 43% of overwintered tipworms emerged in 2015 yielded only 5 overwintered tipworms in 17 wk: 3 (0.15 per trap) in May; 1 (0.05 per trap) in early Jun; and 1 (0.05 per trap) in early Jul. This result is not due to failure of emergence traps. It is due probably to the lethal effects of post-bloom application in 2015 of registered insecticide on larvae that would have otherwise overwintered.
In both years, 2 other cecidomyiid species were detected in emergence traps. Identification to species has not been possible, but 1 is in the subfamily Porricondylinae (S.M.F. unpublished data) and probably is mycetophagous in decaying woody substrates in cranberry fields. Mean daily temperatures increased from 30 Mar to 18 Jul 2016 (Julian dates 90 to 200), ranging from 8.6 ± 0.4 to 23.1 ± 1.7 °C inside (y = 5.26 + 0.07x; r<sup>2</sup> = 0.45) and 7.7 ± 0.4 to 21.6 ± 1.7 °C outside (y = 5.18 + 0.07x; r<sup>2</sup> = 0.42) emergence traps. The daily difference in mean temperature (inside minus outside) ranged from 0.9 ± 0.2 to 1.8 ± 1.7 °C and increased (y = 0.07 + 0.005x; r2 = 0.19; SYSTAT 13) during the season. It is probable that tipworm pupae under emergence traps developed slightly faster than those outside traps.
In 2015, overwintered parasitoids (Hymenoptera) of 4 genera were detected in emergence traps: 3 Aprostocetus sp. Westwood (near Aprostocetus marylandensis [Girault]) (Eulophidae); 365 Ceraphron sp. (Ceraphronidae); 2 Inostemma sp. (Platygastridae); and 4 Platygaster sp. Latreille (Platygastridae). Parasitoids in the genera Aprostocetus and Playtgaster are known previously from cranberry (Peach et al. 2012). In related studies, parasitoids in the genera Ceraphron and Inostemma have emerged in the laboratory from field-collected cranberry shoots harboring parasitized cranberry tipworm larvae; identification to species has not been possible (S.M.F. unpublished data). Ceraphron, in particular, might parasitize other cecidomyiids detected in emergence traps. The total non-zero number of parasitoids per trap per wk ranged from 1 to 12, but zero was the most frequent weekly count, thus data distribution was non-normal (Shapiro-Wilk = 0.38; N = 923; P = 0.000; SYSTAT 13). Emergence of parasitoids began in the third wk of May and continued every wk until mid-Aug (Fig. 2).
Our results from 2015 and 2016 support the hypothesis that overwintered cranberry tipworms emerge as adults during a prolonged period through spring and summer. Overwintered tipworms add offspring to the field population even after insecticide has been applied in spring. Recently, in British Columbia, spring applications have been discontinued because post-bloom application so effectively kills larvae that would otherwise overwinter. Nevertheless, it is important to understand the potential contribution of overwintered tipworms to the pest population in general.
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