Phenology of the Dalmatian Toadflax Biological Control Agent Mecinus janthiniformis (Coleoptera: Curculionidae) in Utah

Phenology of the Dalmatian Toadflax Biological Control Agent Mecinus janthiniformis (Coleoptera:... Abstract The phenology of the stem-mining weevil Mecinus janthiniformis Toševski and Caldara (Coleoptera: Curculionidae) as adults attacking Dalmatian toadflax, Linaria dalmatica (L.) Miller (Plantaginaceae), was studied in 2014–2015 at two low elevation sites in northern Utah. The seasonal pattern of adult weevil abundance on the host plant at the two sites was most similar between years when described by degree-day accumulation, versus calendar date. Repeated censusing over the growing season revealed that males appeared first and subsequently peaked in abundance on the host plant earlier than females did, such that the adult population was dominated by males early in the season and by females late in the season. Peak female abundance on the host plant occurred at the time when Dalmatian toadflax stems reached their maximum height and density and when they began flowering widely. Maximum toadflax stem heights and densities, and flowering activity, were markedly reduced in 2015 compared to 2014. In contrast to these host plant parameters that vary between years, degree-day accumulation can be used readily for timing collection and survey efforts for adult weevils and female adult weevils in particular. Use of degree-day accumulation can thereby facilitate implementation of redistribution and monitoring programs for M. janthiniformis as a biological control agent of Dalmatian toadflax. Invasive weeds pose major management challenges in agriculture and native plant communities throughout the world. In agroecosystems, including rangelands, invasive weeds disrupt ecosystem services by outcompeting and ultimately displacing desirable vegetation, such as crops and forage plants, leading to severe economic loss and habitat degradation (Louda and Masters 1993, Di Tomaso 2000, Pimentel et al. 2005, Paini et al. 2016). Invasions of new geographic areas by these species can lead to reduced functional and species diversity and potentially undesirable novel ecosystems (Mack et al. 2000, Sala et al. 2000, Belnap et al. 2012). Dalmatian toadflax, Linaria dalmatica (L.) Miller (Plantaginaceae), is now one such significant invasive weed in North America (Duncan et al. 2004, Sing and Peterson 2011). First introduced as an ornamental from Eurasia in the 19th century (Sing et al. 2016), Dalmatian toadflax has subsequently invaded thousands of hectares of disturbed range and agricultural land in western North America, and it continues to spread into the southwest (Robocker 1974, Jeanneret and Schroeder 1992, Vujnovic and Wein 1997, Dodge et al. 2008, USDA 2014). The weed is a herbaceous perennial with tall erect stems that germinate in early spring and can flower at any time throughout the summer (Sing et al. 2016). It is highly competitive in many plant communities and reduces the quality of rangeland forage by displacing native and forage plants in mountain grasslands, valleys, and foothills between 1,300 and 3,100 m in elevation (Pyke 2000, Zouhar 2003). Dalmatian toadflax is not easily controlled by chemical and mechanical methods (Vujnovic and Wein 1997) and has hence been a target species for biological control. Among a number of insect biocontrol agents introduced against the weed (Sing et al. 2016), the stem-mining weevil Mecinus janthiniformis Toševski and Caldara (Coleoptera: Curculionidae) has proved especially promising. This agent is not readily morphologically distinguishable from its close relative, the yellow toadflax stem-mining weevil Mecinus janthinus Germar, and as a result, both species were introduced in shipments of M. janthinus s.l. to North America, with the first approved releases occurring in British Columbia in 1991 (Jeanneret and Schroeder 1992, USDA-APHIS 1996, De Clerck-Floate and Harris 2002, De Clerck-Floate and Miller 2002). Mecinus janthiniformis was subsequently characterized as a morphologically, genetically, and ecologically distinct species from M. janthinus s.s., associated only with Dalmatian toadflax in the native range (Toševski et al. 2011, 2013). It has become well-established in western North America and has substantially reduced populations of Dalmatian toadflax, particularly in the northwest (Sing et al. 2008, Van Hezewijk et al. 2010, Schat et al. 2011, Jamieson et al. 2012, Goulet et al. 2013, Park 2013, Cariveau and Norton 2014, Weed and Schwarzländer 2014). Adults of the univoltine M. janthiniformis overwinter in toadflax stems and emerge the following spring to mate on the host plant and lay eggs inside new, growing stems where the larvae develop before pupating in late summer (Jeanneret and Schroeder 1992, McClay and De Clerck-Floate 2002). Control of Dalmatian toadflax populations likely arises from the adverse effects due to internal larval mining of stems and external adult feeding (De Clerck-Floate and Harris 2002, Carney 2003). Multiple releases of M. janthiniformis have been made in recent years against Dalmatian toadflax in Utah. The present study was undertaken in northern Utah to characterize the phenology of adults of the weevil as found on Dalmatian toadflax stems during the spring and summer, with the broad goal of supporting biocontrol practitioners in timing their efforts to census and collect weevils for purposes of monitoring and redistribution. In particular, the objectives of the study were to determine the seasonal timing of host use by adult weevils 1) as assessed both by calendar date and by degree-day accumulation, 2) as considered individually for male versus female adult weevils, and 3) as viewed in the context of the seasonal development of the host plant population. Methods and Materials Populations of Dalmatian toadflax and the weevil were evaluated at three 1,300–1,400 m sites in Tooele County, Utah, between 2014 and 2015. These low elevation sites were characterized by hot, dry summers and mild winters. Daily snowfall from November to March (2013–2014 and 2014–2015) averaged 4–6 mm (and ranged up to 150 mm). This resulted in maximum accumulated snow depths of 330 mm in December in both 2013 and 2014. Periodic rainfall during spring and summer months in 2014 and 2015 averaged 5–6 mm per event (maximum 30 mm). The weevil had been released at the sites beginning in 2006. Dalmatian toadflax grew at high density at these sites among a mixture of grasses (including introduced Bromus tectorum L., Poa bulbosa L., and Thinopyrum intermedium Barkworth and Dewey, as well as native species), herbaceous forbs (including Tragopogon dubius Scop, Verbascum virgatum Stokes, Sphaeralcea spp., Calochortus nuttallii Watson., Medicago sativa L., and Grindelia squarrosa Pursh) and scattered shrubs (Artemisia spp., Ericameria spp., and Gutierrezia spp.). The three sites were located within 12 km of each other, along well-used roads, and were disturbed from heavy grazing in past years thereby facilitating colonization and establishment of Dalmatian toadflax. Population Census Populations of M. janthiniformis and Dalmatian toadflax were censused at two sites throughout the 2014–2015 growing seasons using different sampling strategies. Repeated censuses were taken at a single location marked by a central post (where weevils had been released) at Lake Point, a west-facing and relatively flat 2 ha site named for the nearby town (40°41ʹ56.6″N 112°15ʹ19.1″W). At Pine Canyon, a west-facing 16 ha tract of open land managed by the Bureau of Land Management (40°34ʹ25.3″N 112°14ʹ56.0″W), repeated censuses were taken at four locations marked by posts oriented along a linear, 500-m transect (weevil releases had been made only at the easternmost post). Weevil abundance was measured at both sites on 1–2 d per week from 10 April to 8 July in 2014 and on 1–4 d per week from 21 March to 29 June in 2015. Population density was estimated on each sampling occasion in 2014 by counting the number of adult weevils occurring on each of 40 individual stems 25 cm or more in height at Lake Point and at each of the four locations at Pine Canyon. Plant characteristics, including stem height (strongly correlated with stem diameter; Carney 2003, Willden 2017) and the number of open flowers, were recorded concurrently. Five stems were selected blindly (i.e., haphazardly without bias as to height, flowering condition, or other aspects) along each of eight transects that radiated outward from each marker post (one at Lake Point, and four at Pine Canyon) in the cardinal and ordinal directions. The first stem was selected as the nearest stem beyond the first sampling point, set at 2 m along the transect. The next sampling point was set at 2 m beyond the first selected stem, and again the nearest stem beyond the sampling point was selected. This process was repeated until either five stems along the transect had been selected or an end point at 20 m from the post had been reached. When fewer than five stems were selected along one or more transects at a post, stems were selected also along additional transects, using the same procedures, to bring the total to 40 stems sampled. These additional transects radiated out from the post to bisect the 45° angles defined by the first eight transects. Similar censusing was conducted in 2015 with larger sample sizes and included stems ≥15 cm in height. On each sampling occasion, 100 stems were sampled at Lake Point and 50 stems were sampled at each of the four locations (for a total of 200 stems) at Pine Canyon. In addition, weevils were sexed as encountered with 10 × 23-mm hand lenses, using morphological characters as described below. When large numbers of weevils were encountered on a stem (usually > 5 per plant), individuals were collected in vials and then returned to the plant after sexing. Collecting and Sexing Weevil Adults Adults of M. janthiniformis were collected en masse at the Lake Point site in 2014 and 2015 to determine the sex ratio of populations present at different times of the growing season. To avoid disturbing the area used for population censuses, collections were made in a dense patch of toadflax 100 m south of the Lake Point post (40°41ʹ53.1″N 112°15ʹ17.9″W). Mass collections of weevil adults were also made in 2014 at a second site, owned by Kennecott Utah Copper Mining Company, on a north-facing slope just southeast of Gate 19 on the Kennecott property (40°42ʹ52.2″N 112°14ʹ01.5″W). Weevil adults were collected 1–3 times per week at each of the two sites between 10 April and 30 June in 2014, and 1–4 times per week at Lake Point between 29 March and 29 June in 2015. Up to 200 adult weevils were collected within a 100 m2 area at each site on each occasion in 2014. Individuals were collected indiscriminately from blindly selected stems and were stored in collecting vials until sexed. Early and late in the season in 2014, collections of weevils were sexed in the field with hand lenses, using rostral and profemural characteristics described by Schat et al. (2007) and Carney et al. (2004), respectively. In mid-season 2014 when weevil density was high, 50–100 individuals were brought to the lab to be sexed under the microscope. In 2015, a maximum of 100 weevils were collected on each occasion, and all individuals were sexed in the lab. In both 2014 and 2015, individuals brought to the lab for sexing were typically frozen until sexing could be conducted. Sexing data at the two sites in 2014 were combined following an initial χ2 analysis which concluded that the two sites did not differ significantly in sex ratio patterns over the season. Because additional χ2 analysis revealed highly significant change in sex ratio from early to late in the season (before mid-April versus after mid-June) in each year, the numbers of males and females within mass collections of adults were compared by χ2 analyses for individual time periods in 2014 (Lake Point and Kennecott Gate 19 data combined) and independently in 2015 (data from Lake Point). Data from individual sampling dates were pooled into six time periods for each year (1 March–14 April, 15–30 April, 1–15 May, 16–31 May, 1–15 June, and 16–30 June). χ2 analyses of sex ratios (as well as all other statistical analyses noted below) were conducted using SAS 9.3 (SAS Institute 2009). Plant Density Census After taking the population census (as described above), plant density was measured at Lake Point and Pine Canyon during both 2014 (measured weekly) and 2015 (measured 1–4 times per week) by placing 0.1 m2 rings along transects radiating from marker posts at each site (one post at Lake Point and four posts at Pine Canyon). Data recorded for each ring included the number of stems ≥15 cm in height and the height of the tallest stem. Rings were placed in front of the forward foot upon walking 4 m along each transect. In 2014, eight transects were sampled starting at each center post and extending outward in each of the cardinal and ordinal directions. Five ring samples were taken every 4 m along each transect resulting in 40 ring samples total for each post. Two additional transects were added to the census in early August 2015 by sampling along 10 rather than eight rays outward from each post (i.e., a ray pointing north, with adjacent rays forming angles of 36°), resulting in 50 ring samples for each post. Data taken before this time in 2015 were recorded along eight transects. Data collected at individual posts at Pine Canyon on each sampling date for 2014 and 2015 were pooled prior to analysis, as population dynamics of Dalmatian toadflax (and of M. janthiniformis, as considered below) were similar among the posts each year. Paired t-tests were used to compare four plant characteristics: 1) height of the tallest stem per 0.1 m2, 2) density in 0.1 m2, 3) the mean number of flowers per stem in population censuses, and 4) the mean height of stems in population censuses, as measured on similar dates during 2014 and 2015. Data for each individual test included measurements for each of the 8–9 sampling dates in 2014 and the closest corresponding date in 2015. Degree-Day Modeling Archival weather data used in degree-day models were obtained from the Utah Climate Center Tooele weather station from 1 January to 31 August for each year (station ID: USC00428771; [Utah Climate Center]). A single-sign degree-day model for adult weevil phenology was generated using daily minimum and maximum temperatures (University of California, Integrated Pest Management). A lower threshold temperature of 8.9°C was selected based on similar field studies of other Coleoptera (Casagrande et al. 1977, Peterson and Meyer 1995), with an upper horizontal cutoff at 28.7°C, set at 19.8°C above the base temperature as an appropriate general approximation for insect development (Dixon et al. 2009, Jones et al. 2016). This model was used to examine seasonal patterns of adult weevil abundance on the host plant as a function of degree-days accumulated, and yielded very similar seasonal patterns to a simple maximum-minimum temperature model with the same base temperature but no upper horizontal cutoff (Arnold 1960). Hence, results from only the single sine model are given below. A highly significant equation obtained from regressing percentage males against degree-day accumulation for mass collections of adults in 2014 (presented in Fig. 3) was used to estimate the percentages and absolute numbers of adult males and females per host plant stem in population censuses in 2014 (when adults were not distinguished by sex during censuses). Similar estimations were not necessary in 2015, when all individuals encountered in the population census were sexed. Linear regressions of the percentage of weevil adults in mass collections that were males, as a function of the degree-day accumulation or calendar date, were used to estimate the number of degree-days accumulated when an equal (1:1) sex ratio occurred in 2014 and 2015. A paired t-test was used to compare degree-day accumulations for males versus females at peak density. The number of degree-days accumulated for males and for females was compared for each site in each year, resulting in four pairs of degree-day accumulations (for males vs females) in the analysis. Results Seasonal patterns of weevil abundance on Dalmatian toadflax stems were generally similar at both sites in both years, with weevils emerging at low densities by mid-April, increasing to peak abundance in May, and decreasing in numbers thereafter until disappearing altogether by the end of June (Fig. 1). Weevil numbers on the host plant rose much more rapidly, however, in late April in 2015 than in 2014, as associated with more rapid gain in degree-days during this period than in 2014 (Fig. 2). Peak weevil abundance was recorded on 21 May and 27 May in 2014, and on 29 May and 18 May in 2015, at Lake Point and Pine Canyon, respectively (Fig. 1). Fig. 1. View largeDownload slide Mean daily count of Mecinus janthiniformis adults per Dalmatian toadflax stem at Lake Pointa and Pine Canyonb over the 2014c and 2015d growing seasons. aCensus taken at a single sample point. bCensus taken at 4 sample points along 500 m transect. cMean daily count number of adult weevils occurring on 40 Dalmatian toadflax stems ≥ 25 cm tall. dMean daily count of adult weevils occurring on 100 (Lake Point) or 50 (at each of four Pine Canyon sites) Dalmatian toadflax stems ≥ 15 cm tall. Fig. 1. View largeDownload slide Mean daily count of Mecinus janthiniformis adults per Dalmatian toadflax stem at Lake Pointa and Pine Canyonb over the 2014c and 2015d growing seasons. aCensus taken at a single sample point. bCensus taken at 4 sample points along 500 m transect. cMean daily count number of adult weevils occurring on 40 Dalmatian toadflax stems ≥ 25 cm tall. dMean daily count of adult weevils occurring on 100 (Lake Point) or 50 (at each of four Pine Canyon sites) Dalmatian toadflax stems ≥ 15 cm tall. Fig. 2. View largeDownload slide Degree-day accumulation (as determined using the single sine method with a critical base temperature of 8.9°C and a cutoff threshold of 28.7°C) in 2014 and 2015. Day of year 200 corresponds to 8 July. Fig. 2. View largeDownload slide Degree-day accumulation (as determined using the single sine method with a critical base temperature of 8.9°C and a cutoff threshold of 28.7°C) in 2014 and 2015. Day of year 200 corresponds to 8 July. Weevils remained at high densities for a longer period (i.e., throughout May) in 2015 than in 2014. Following the occurrence of peak population density in late May, the decline in adult abundance during June was more gradual in 2015 than in 2014, especially at Lake Point (Fig. 1), corresponding with less rapid gain in degree-days in June in 2015 than in 2014 (Fig. 2). Despite the differences in the seasonal timing of heat gain in 2014 and 2015, overall heat gain in the 2 yr was very similar from January to the end of June when M. janthiniformis adults were no longer found on the stems (Fig. 2). In both 2014 and 2015, almost all individuals found on the host plant in early spring were males, whereas most individuals after the population had peaked were females. Males were significantly more abundant than females through the end of May in 2014 and through the first half of May in 2015, while females were significantly more abundant than males during late June 2014 and throughout June in 2015 (Table 1). Males and females did not differ in abundance during early June 2014 or in late May 2015 (Table 1). Table 1. P Values for χ2 tests to compare the numbers of adult male and female weevils collected altogether during different time periods in 2014 (Kennecott and Lake Point collections combined) in 2015 (at lake point) Dates  2014  2015  N  P value  N  P value  Mar 1–April 14  Male: 40 Female: 9  <0.0001  Male: 58 Female: 14  <0.0001  Apr 15–April 30  Male: 113 Female: 17  <0.0001  Male: 378 Female: 61  <0.0001  May 1–May 15  Male: 738 Female: 212  <0.0001  Male: 636 Female: 291  <0.0001  May 16–May 31  Male: 499 Female: 404  0.0016  Male: 494 Female: 453  0.1828  June 1–June 15  Male: 382 Female: 427  0.1136  Male: 302 Female: 409  <0.0001  June 16–June 30  Male: 247 Female: 553  <0.0001  Male: 48 Female: 157  <0.0001  Dates  2014  2015  N  P value  N  P value  Mar 1–April 14  Male: 40 Female: 9  <0.0001  Male: 58 Female: 14  <0.0001  Apr 15–April 30  Male: 113 Female: 17  <0.0001  Male: 378 Female: 61  <0.0001  May 1–May 15  Male: 738 Female: 212  <0.0001  Male: 636 Female: 291  <0.0001  May 16–May 31  Male: 499 Female: 404  0.0016  Male: 494 Female: 453  0.1828  June 1–June 15  Male: 382 Female: 427  0.1136  Male: 302 Female: 409  <0.0001  June 16–June 30  Male: 247 Female: 553  <0.0001  Male: 48 Female: 157  <0.0001  View Large In both years, there was a steady decrease in the percentage of males on host plant stems as degree-days accumulated and females began to emerge (Fig. 3). The percentage of males similarly decreased with calendar date (F1,18 = 168.20; R2 = 0.90, P < 0.0001 for 2014, and F1,36 = 240.49; R2 = 0.88, P < 0.0001 for 2015). From the equations obtained in the linear regression, the sex ratio (males:females) was estimated at 1:1 at 463 degree-days in 2014 (1 June) and at 410 degree-days (25 May) in 2015. Fig. 3. View largeDownload slide The percentage of adult weevils occurring on toadflax stems that were males, versus degree-day accumulation during the spring and early summer in 2014 (F1,18 = 226.20, R2 = 0.93, P < 0.001; y = −0.1022 x + 97.33) and 2015 (F1,36 = 383.38, R2 = 0.92, P < 0.001; y = −0.1446 x + 109.48). Fig. 3. View largeDownload slide The percentage of adult weevils occurring on toadflax stems that were males, versus degree-day accumulation during the spring and early summer in 2014 (F1,18 = 226.20, R2 = 0.93, P < 0.001; y = −0.1022 x + 97.33) and 2015 (F1,36 = 383.38, R2 = 0.92, P < 0.001; y = −0.1446 x + 109.48). Populations of both male and female weevils increased rapidly with degree-day accumulation in the early spring (Fig. 4). Males reached their peak-population density at fewer degree-day accumulations than females did at both sites and in both 2014 and 2015 (paired t-test comparison of degree-day accumulations for males vs females at peak density for both sites in both years: t1, 3 = 5.65, P = 0.011). Males attained peak numbers at very similar degree-day accumulations at both sites in each year (with the peak occurring between 255 and 270 degree-days). Females peaked in abundance at fairly consistent but slightly more variable degree-day accumulations, with the peak occurring between 307 and 373 degree-days (Fig. 4). Numbers of both males and females declined gradually after peak abundance was observed with continuing degree-day accumulation (Fig. 4). Males peaked in abundance on the host plant several days before females at both sites in 2014 but 18 d (Pine Canyon) and 24 d (Lake Point) before females in 2015. Relatively high numbers of males still persisted on the host plant, however, when females became most abundant in 2015 (Fig. 4). Fig. 4. View largeDownload slide Percent of maximum number of adult Mecinus janthiniformis males (left) and females (right) versus degree-day accumulation at Lake Point (top) and Pine Canyon (bottom). Degree-day at annual maximum is indicated (2014 italicized). Fig. 4. View largeDownload slide Percent of maximum number of adult Mecinus janthiniformis males (left) and females (right) versus degree-day accumulation at Lake Point (top) and Pine Canyon (bottom). Degree-day at annual maximum is indicated (2014 italicized). Toadflax stems grew rapidly during the spring in both years (Fig. 5). By late May to early June, when 300–400 degree-days had accumulated and when peak numbers of female weevils were found on the host plant, stems had reached their maximum height and density (Fig. 5; arrows indicate peak female density). The first flush of flowering also occurred in late May to early June, but the sporadic nature of flowering among individual stems resulted in unclear trends in flowering per stem throughout the remainder of the season (Fig. 5). Fig. 5. View largeDownload slide Dalmatian toadflax tallest stem (cm), total stem density, and mean flowers per stem at Lake Point (A–C) and Pine Canyon (D–F) versus degree-day accumulation, 2014 and 2015. Peak female weevil abundance indicated by arrows (2014—unfilled, 2015—filled). Fig. 5. View largeDownload slide Dalmatian toadflax tallest stem (cm), total stem density, and mean flowers per stem at Lake Point (A–C) and Pine Canyon (D–F) versus degree-day accumulation, 2014 and 2015. Peak female weevil abundance indicated by arrows (2014—unfilled, 2015—filled). The tallest stems at both sites, as recorded in ring sample censusing, were significantly shorter in 2015 than in 2014 (Fig. 5A and D; paired t-test for mean tallest stem height on the same or nearly the same sampling dates in 2014 and 2015: t8 = 8.94, P < 0.0001 at Lake Point and t7 = 4.95, P = 0.002 at Pine Canyon). The mean heights of stems surveyed during the population censuses similarly reflected that the stems were significantly shorter in 2015 than in 2014 (paired t-test: t20 = 22.35, P < 0.0001 at Lake Point and t20 = 16.31, P < 0.0001 at Pine Canyon). For example, the mean height of stems when females reached peak abundance decreased from 39.6 ± 1.8 cm (x ± SE) in 2014 to 21.8 ± 1.3 cm in 2015 at Lake Point and similarly from 41.6 ± 1.0 cm to 20.1 ± 0.7 cm at Pine Canyon. A similar decrease in stem density from 2014 to 2015 occurred at each of the two sites (Fig 5B and E; paired t-test for mean stem density per matched sampling date in 2014 and 2015: t8 = 12.62, P < 0.0001 at Lake Point and t7 = 17.88, P < 0.0001 at Pine Canyon). Flowering also was greatly reduced in 2015 versus in 2014 (Fig. 5C and F; paired t-test for mean number of flowers per matched sampling dates in 2014 and 2015: t20= 3.98, P < 0.001 at Lake Point and t20 = 3.89, P < 0.001 at Pine Canyon). Discussion By calendar date, phenology of M. janthiniformis adults in northern Utah is similar to the weevil’s phenology both in its native region (former Yugoslavia; Jeanneret and Schroeder 1992, Toševski et al. 2011) and in other regions of western North America to which it has been introduced (De Clerck-Floate and Harris 2002, De Clerck-Floate and Miller 2002, Carney 2003, Jamieson et al. 2012, Sing et al. 2016). In particular, adult weevils began emerging from overwintered stems by late March in Utah, peaked in abundance in mid-May to late May, and had completely disappeared from the stems by July, as recorded elsewhere (Jeanneret and Schroeder 1992, Toševski et al. 2011, Sing et al. 2016). Differences between 2014 and 2015 in calendar-dating of adult phenology in northern Utah, including weevil emergence in the early spring and population decline on the host plant later in the summer, were largely accounted for by degree-day modeling of weevil phenology that reflected seasonal differences in heat accumulation between the 2 yr. Thus, as often is the case (e.g., Allen 1976, Zalom et al. 1983, Herms 2004, Sridhar and Reddy 2013), degree-day modeling enabled greater precision in describing phenology of M. janthiniformis adult use of the host plant versus simple calendar dating. Adult males and females of M. janthiniformis differed in phenology in the present study, with males appearing earlier in the spring on the host plant than females. Protandry (the earlier emergence of males) occurs commonly in insects (Thornhill and Alcock 1983, Morbey and Ydenberg 2001) and may reflect selective advantage for early emerging males in mating with unmated females (Lehmann 2012, Morbey et al. 2012). Protandry has not been described previously for M. janthiniformis adults; however, Carney (2003) also reported female-biased sex ratios of adult weevils in the latter part of their emergence period (late June) in British Columbia. Protandry can pose challenges for biological control management practices if collections of source populations occur too early in the season, when the majority of emerged or active individuals are males (Heimpel and Lundgren 2000). Because the sexes of M. janthiniformis differed in their phenology, it is beneficial to consider them individually when determining the best time to collect adult weevils for redistribution. Generally, optimal sex ratios for redistribution range from 1:1 to female biased, and models that accurately predict varying sex ratio over the season can be very helpful in this regard (Tabadkani et al. 2013). In this study, the sex ratio of adult M. janthiniformis weevils on Dalmatian toadflax stems was close to 1:1 between 410 and 460 degree-days (between 320 and 370 degree-days as based on a simple maximum-minimum temperature model without an upper cutoff;) or from late May to early June, before becoming female-biased thereafter. In 2014, relatively few degree-days separated the points in the season when male and female numbers peaked on the host plant. Greater numbers of degree-days separated these points in 2015, but even so, males still occurred in high density when females reached peak abundance. Given that densities of both sexes combined began to decline in June, collecting adults for redistribution in mid to late May at our sites when females peak in numbers (and females have commenced ovipositing; Jeanneret and Schroeder 1992, Toševski et al. 2011) would appear to be the ideal time for such efforts. It would be especially advantageous to use degree-day accumulation to time weevil collections in mid to late May, as the differing calendar-based phenologies in 2014 and 2015 at our study sites pose challenges in using date alone to determine optimal times to collect large numbers of gravid females. Using degree-day accumulation would also be advantageous to conduct field surveys among years. Such surveys could be based on sampling weevil populations annually at a consistent stage in their phenology, in monitoring programs for assessing the long-term outcome of biocontrol releases. In the present study, female M. janthiniformis peaked in abundance on the host plants each year around the time that Dalmatian toadflax stems as a population reached full maturity, i.e., when the stems reached their maximum height and density and when they began flowering widely. Comparison of Dalmatian toadflax populations between 2014 and 2015, however, illustrates the challenges of using the phenology of stem height, density, and flowering to guide collection and monitoring efforts for M. janthiniformis. Maximum heights and densities of toadflax stems attained were much lower in 2015 than in 2014; given this variation, it would be difficult to determine except in retrospect when such maxima had been reached in the late spring in a given year, in the absence of additional information on degree-day accumulation. Similarly, large differences between years occurred in toadflax flowering activity in this study. In particular, very few flowers were produced over the growing season at Lake Point, and almost none were produced at Pine Canyon, in 2015. Such low flowering activity could make it difficult during the spring to determine when initiation of widespread (even if limited) flowering was occurring. The challenges of using these aspects of host plant phenology underscore the advantage of using degree-day accumulation to time monitoring and collecting efforts for adult weevils on stems of Dalmatian toadflax. In summary, seasonal patterns reported here of adult weevil abundance on Dalmatian toadflax stems, which were in line with patterns reported from both Europe and elsewhere in North America, were most similar between years when described by degree-day accumulation versus calendar date. Degree-day accumulation can be used for optimally timing collection and survey efforts for adult weevils on Dalmatian toadflax stems. Such timing will be aided further by using the sex-specific results of degree-day modeling in the present study, as male and female adult weevils differed predictably from each other in their phenology, with males arriving earliest in the spring on the host plant. The results from this study therefore will be of value to practitioners of biological control as they seek to implement monitoring and redistribution programs for M. janthiniformis as a biocontrol agent of Dalmatian toadflax. Acknowledgments We thank A. Mendenhall (USDA APHIS) for helping us to initiate this study and providing information on M, janthiniformis releases; J. Anderson, D. Christiensen, R. Ghabayen, J. Gonzalez, and D. Wright for assistance with field work; D. Alston, C. Ransom, R. Whitesides, and two anonymous reviewers for very helpful comments on the MS; and the USDI BLM, USDA APHIS, and Utah Agricultural Experiment Station for financial support. References Cited Allen, J. C. 1976. A modified sine wave method for calculating degree days. Environ. Entomol . 5: 388‒ 396. Google Scholar CrossRef Search ADS   Arnold, C. Y. 1960. Maximum-minimum temperatures as a basis for computing heat units. Proc. Am. Soc. Hort. Sci . 76: 682‒ 692. Belnap, J., Ludwig J. A., Wilcox B. P., Betancourt J. L., Dean W. R. J., Hoffmann B. D., and Milton S. J.. 2012. Introduced and invasive species in novel rangeland ecosystems: friends or foes? Range Ecol. Manage . 65: 569‒ 578. Google Scholar CrossRef Search ADS   Cariveau, D. 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(http://www.fs.fed.us/database/ feis/plants/forb/linspp) (accessed 27 October 2016). © The Author(s) 2017. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Environmental Entomology Oxford University Press

Phenology of the Dalmatian Toadflax Biological Control Agent Mecinus janthiniformis (Coleoptera: Curculionidae) in Utah

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Abstract

Abstract The phenology of the stem-mining weevil Mecinus janthiniformis Toševski and Caldara (Coleoptera: Curculionidae) as adults attacking Dalmatian toadflax, Linaria dalmatica (L.) Miller (Plantaginaceae), was studied in 2014–2015 at two low elevation sites in northern Utah. The seasonal pattern of adult weevil abundance on the host plant at the two sites was most similar between years when described by degree-day accumulation, versus calendar date. Repeated censusing over the growing season revealed that males appeared first and subsequently peaked in abundance on the host plant earlier than females did, such that the adult population was dominated by males early in the season and by females late in the season. Peak female abundance on the host plant occurred at the time when Dalmatian toadflax stems reached their maximum height and density and when they began flowering widely. Maximum toadflax stem heights and densities, and flowering activity, were markedly reduced in 2015 compared to 2014. In contrast to these host plant parameters that vary between years, degree-day accumulation can be used readily for timing collection and survey efforts for adult weevils and female adult weevils in particular. Use of degree-day accumulation can thereby facilitate implementation of redistribution and monitoring programs for M. janthiniformis as a biological control agent of Dalmatian toadflax. Invasive weeds pose major management challenges in agriculture and native plant communities throughout the world. In agroecosystems, including rangelands, invasive weeds disrupt ecosystem services by outcompeting and ultimately displacing desirable vegetation, such as crops and forage plants, leading to severe economic loss and habitat degradation (Louda and Masters 1993, Di Tomaso 2000, Pimentel et al. 2005, Paini et al. 2016). Invasions of new geographic areas by these species can lead to reduced functional and species diversity and potentially undesirable novel ecosystems (Mack et al. 2000, Sala et al. 2000, Belnap et al. 2012). Dalmatian toadflax, Linaria dalmatica (L.) Miller (Plantaginaceae), is now one such significant invasive weed in North America (Duncan et al. 2004, Sing and Peterson 2011). First introduced as an ornamental from Eurasia in the 19th century (Sing et al. 2016), Dalmatian toadflax has subsequently invaded thousands of hectares of disturbed range and agricultural land in western North America, and it continues to spread into the southwest (Robocker 1974, Jeanneret and Schroeder 1992, Vujnovic and Wein 1997, Dodge et al. 2008, USDA 2014). The weed is a herbaceous perennial with tall erect stems that germinate in early spring and can flower at any time throughout the summer (Sing et al. 2016). It is highly competitive in many plant communities and reduces the quality of rangeland forage by displacing native and forage plants in mountain grasslands, valleys, and foothills between 1,300 and 3,100 m in elevation (Pyke 2000, Zouhar 2003). Dalmatian toadflax is not easily controlled by chemical and mechanical methods (Vujnovic and Wein 1997) and has hence been a target species for biological control. Among a number of insect biocontrol agents introduced against the weed (Sing et al. 2016), the stem-mining weevil Mecinus janthiniformis Toševski and Caldara (Coleoptera: Curculionidae) has proved especially promising. This agent is not readily morphologically distinguishable from its close relative, the yellow toadflax stem-mining weevil Mecinus janthinus Germar, and as a result, both species were introduced in shipments of M. janthinus s.l. to North America, with the first approved releases occurring in British Columbia in 1991 (Jeanneret and Schroeder 1992, USDA-APHIS 1996, De Clerck-Floate and Harris 2002, De Clerck-Floate and Miller 2002). Mecinus janthiniformis was subsequently characterized as a morphologically, genetically, and ecologically distinct species from M. janthinus s.s., associated only with Dalmatian toadflax in the native range (Toševski et al. 2011, 2013). It has become well-established in western North America and has substantially reduced populations of Dalmatian toadflax, particularly in the northwest (Sing et al. 2008, Van Hezewijk et al. 2010, Schat et al. 2011, Jamieson et al. 2012, Goulet et al. 2013, Park 2013, Cariveau and Norton 2014, Weed and Schwarzländer 2014). Adults of the univoltine M. janthiniformis overwinter in toadflax stems and emerge the following spring to mate on the host plant and lay eggs inside new, growing stems where the larvae develop before pupating in late summer (Jeanneret and Schroeder 1992, McClay and De Clerck-Floate 2002). Control of Dalmatian toadflax populations likely arises from the adverse effects due to internal larval mining of stems and external adult feeding (De Clerck-Floate and Harris 2002, Carney 2003). Multiple releases of M. janthiniformis have been made in recent years against Dalmatian toadflax in Utah. The present study was undertaken in northern Utah to characterize the phenology of adults of the weevil as found on Dalmatian toadflax stems during the spring and summer, with the broad goal of supporting biocontrol practitioners in timing their efforts to census and collect weevils for purposes of monitoring and redistribution. In particular, the objectives of the study were to determine the seasonal timing of host use by adult weevils 1) as assessed both by calendar date and by degree-day accumulation, 2) as considered individually for male versus female adult weevils, and 3) as viewed in the context of the seasonal development of the host plant population. Methods and Materials Populations of Dalmatian toadflax and the weevil were evaluated at three 1,300–1,400 m sites in Tooele County, Utah, between 2014 and 2015. These low elevation sites were characterized by hot, dry summers and mild winters. Daily snowfall from November to March (2013–2014 and 2014–2015) averaged 4–6 mm (and ranged up to 150 mm). This resulted in maximum accumulated snow depths of 330 mm in December in both 2013 and 2014. Periodic rainfall during spring and summer months in 2014 and 2015 averaged 5–6 mm per event (maximum 30 mm). The weevil had been released at the sites beginning in 2006. Dalmatian toadflax grew at high density at these sites among a mixture of grasses (including introduced Bromus tectorum L., Poa bulbosa L., and Thinopyrum intermedium Barkworth and Dewey, as well as native species), herbaceous forbs (including Tragopogon dubius Scop, Verbascum virgatum Stokes, Sphaeralcea spp., Calochortus nuttallii Watson., Medicago sativa L., and Grindelia squarrosa Pursh) and scattered shrubs (Artemisia spp., Ericameria spp., and Gutierrezia spp.). The three sites were located within 12 km of each other, along well-used roads, and were disturbed from heavy grazing in past years thereby facilitating colonization and establishment of Dalmatian toadflax. Population Census Populations of M. janthiniformis and Dalmatian toadflax were censused at two sites throughout the 2014–2015 growing seasons using different sampling strategies. Repeated censuses were taken at a single location marked by a central post (where weevils had been released) at Lake Point, a west-facing and relatively flat 2 ha site named for the nearby town (40°41ʹ56.6″N 112°15ʹ19.1″W). At Pine Canyon, a west-facing 16 ha tract of open land managed by the Bureau of Land Management (40°34ʹ25.3″N 112°14ʹ56.0″W), repeated censuses were taken at four locations marked by posts oriented along a linear, 500-m transect (weevil releases had been made only at the easternmost post). Weevil abundance was measured at both sites on 1–2 d per week from 10 April to 8 July in 2014 and on 1–4 d per week from 21 March to 29 June in 2015. Population density was estimated on each sampling occasion in 2014 by counting the number of adult weevils occurring on each of 40 individual stems 25 cm or more in height at Lake Point and at each of the four locations at Pine Canyon. Plant characteristics, including stem height (strongly correlated with stem diameter; Carney 2003, Willden 2017) and the number of open flowers, were recorded concurrently. Five stems were selected blindly (i.e., haphazardly without bias as to height, flowering condition, or other aspects) along each of eight transects that radiated outward from each marker post (one at Lake Point, and four at Pine Canyon) in the cardinal and ordinal directions. The first stem was selected as the nearest stem beyond the first sampling point, set at 2 m along the transect. The next sampling point was set at 2 m beyond the first selected stem, and again the nearest stem beyond the sampling point was selected. This process was repeated until either five stems along the transect had been selected or an end point at 20 m from the post had been reached. When fewer than five stems were selected along one or more transects at a post, stems were selected also along additional transects, using the same procedures, to bring the total to 40 stems sampled. These additional transects radiated out from the post to bisect the 45° angles defined by the first eight transects. Similar censusing was conducted in 2015 with larger sample sizes and included stems ≥15 cm in height. On each sampling occasion, 100 stems were sampled at Lake Point and 50 stems were sampled at each of the four locations (for a total of 200 stems) at Pine Canyon. In addition, weevils were sexed as encountered with 10 × 23-mm hand lenses, using morphological characters as described below. When large numbers of weevils were encountered on a stem (usually > 5 per plant), individuals were collected in vials and then returned to the plant after sexing. Collecting and Sexing Weevil Adults Adults of M. janthiniformis were collected en masse at the Lake Point site in 2014 and 2015 to determine the sex ratio of populations present at different times of the growing season. To avoid disturbing the area used for population censuses, collections were made in a dense patch of toadflax 100 m south of the Lake Point post (40°41ʹ53.1″N 112°15ʹ17.9″W). Mass collections of weevil adults were also made in 2014 at a second site, owned by Kennecott Utah Copper Mining Company, on a north-facing slope just southeast of Gate 19 on the Kennecott property (40°42ʹ52.2″N 112°14ʹ01.5″W). Weevil adults were collected 1–3 times per week at each of the two sites between 10 April and 30 June in 2014, and 1–4 times per week at Lake Point between 29 March and 29 June in 2015. Up to 200 adult weevils were collected within a 100 m2 area at each site on each occasion in 2014. Individuals were collected indiscriminately from blindly selected stems and were stored in collecting vials until sexed. Early and late in the season in 2014, collections of weevils were sexed in the field with hand lenses, using rostral and profemural characteristics described by Schat et al. (2007) and Carney et al. (2004), respectively. In mid-season 2014 when weevil density was high, 50–100 individuals were brought to the lab to be sexed under the microscope. In 2015, a maximum of 100 weevils were collected on each occasion, and all individuals were sexed in the lab. In both 2014 and 2015, individuals brought to the lab for sexing were typically frozen until sexing could be conducted. Sexing data at the two sites in 2014 were combined following an initial χ2 analysis which concluded that the two sites did not differ significantly in sex ratio patterns over the season. Because additional χ2 analysis revealed highly significant change in sex ratio from early to late in the season (before mid-April versus after mid-June) in each year, the numbers of males and females within mass collections of adults were compared by χ2 analyses for individual time periods in 2014 (Lake Point and Kennecott Gate 19 data combined) and independently in 2015 (data from Lake Point). Data from individual sampling dates were pooled into six time periods for each year (1 March–14 April, 15–30 April, 1–15 May, 16–31 May, 1–15 June, and 16–30 June). χ2 analyses of sex ratios (as well as all other statistical analyses noted below) were conducted using SAS 9.3 (SAS Institute 2009). Plant Density Census After taking the population census (as described above), plant density was measured at Lake Point and Pine Canyon during both 2014 (measured weekly) and 2015 (measured 1–4 times per week) by placing 0.1 m2 rings along transects radiating from marker posts at each site (one post at Lake Point and four posts at Pine Canyon). Data recorded for each ring included the number of stems ≥15 cm in height and the height of the tallest stem. Rings were placed in front of the forward foot upon walking 4 m along each transect. In 2014, eight transects were sampled starting at each center post and extending outward in each of the cardinal and ordinal directions. Five ring samples were taken every 4 m along each transect resulting in 40 ring samples total for each post. Two additional transects were added to the census in early August 2015 by sampling along 10 rather than eight rays outward from each post (i.e., a ray pointing north, with adjacent rays forming angles of 36°), resulting in 50 ring samples for each post. Data taken before this time in 2015 were recorded along eight transects. Data collected at individual posts at Pine Canyon on each sampling date for 2014 and 2015 were pooled prior to analysis, as population dynamics of Dalmatian toadflax (and of M. janthiniformis, as considered below) were similar among the posts each year. Paired t-tests were used to compare four plant characteristics: 1) height of the tallest stem per 0.1 m2, 2) density in 0.1 m2, 3) the mean number of flowers per stem in population censuses, and 4) the mean height of stems in population censuses, as measured on similar dates during 2014 and 2015. Data for each individual test included measurements for each of the 8–9 sampling dates in 2014 and the closest corresponding date in 2015. Degree-Day Modeling Archival weather data used in degree-day models were obtained from the Utah Climate Center Tooele weather station from 1 January to 31 August for each year (station ID: USC00428771; [Utah Climate Center]). A single-sign degree-day model for adult weevil phenology was generated using daily minimum and maximum temperatures (University of California, Integrated Pest Management). A lower threshold temperature of 8.9°C was selected based on similar field studies of other Coleoptera (Casagrande et al. 1977, Peterson and Meyer 1995), with an upper horizontal cutoff at 28.7°C, set at 19.8°C above the base temperature as an appropriate general approximation for insect development (Dixon et al. 2009, Jones et al. 2016). This model was used to examine seasonal patterns of adult weevil abundance on the host plant as a function of degree-days accumulated, and yielded very similar seasonal patterns to a simple maximum-minimum temperature model with the same base temperature but no upper horizontal cutoff (Arnold 1960). Hence, results from only the single sine model are given below. A highly significant equation obtained from regressing percentage males against degree-day accumulation for mass collections of adults in 2014 (presented in Fig. 3) was used to estimate the percentages and absolute numbers of adult males and females per host plant stem in population censuses in 2014 (when adults were not distinguished by sex during censuses). Similar estimations were not necessary in 2015, when all individuals encountered in the population census were sexed. Linear regressions of the percentage of weevil adults in mass collections that were males, as a function of the degree-day accumulation or calendar date, were used to estimate the number of degree-days accumulated when an equal (1:1) sex ratio occurred in 2014 and 2015. A paired t-test was used to compare degree-day accumulations for males versus females at peak density. The number of degree-days accumulated for males and for females was compared for each site in each year, resulting in four pairs of degree-day accumulations (for males vs females) in the analysis. Results Seasonal patterns of weevil abundance on Dalmatian toadflax stems were generally similar at both sites in both years, with weevils emerging at low densities by mid-April, increasing to peak abundance in May, and decreasing in numbers thereafter until disappearing altogether by the end of June (Fig. 1). Weevil numbers on the host plant rose much more rapidly, however, in late April in 2015 than in 2014, as associated with more rapid gain in degree-days during this period than in 2014 (Fig. 2). Peak weevil abundance was recorded on 21 May and 27 May in 2014, and on 29 May and 18 May in 2015, at Lake Point and Pine Canyon, respectively (Fig. 1). Fig. 1. View largeDownload slide Mean daily count of Mecinus janthiniformis adults per Dalmatian toadflax stem at Lake Pointa and Pine Canyonb over the 2014c and 2015d growing seasons. aCensus taken at a single sample point. bCensus taken at 4 sample points along 500 m transect. cMean daily count number of adult weevils occurring on 40 Dalmatian toadflax stems ≥ 25 cm tall. dMean daily count of adult weevils occurring on 100 (Lake Point) or 50 (at each of four Pine Canyon sites) Dalmatian toadflax stems ≥ 15 cm tall. Fig. 1. View largeDownload slide Mean daily count of Mecinus janthiniformis adults per Dalmatian toadflax stem at Lake Pointa and Pine Canyonb over the 2014c and 2015d growing seasons. aCensus taken at a single sample point. bCensus taken at 4 sample points along 500 m transect. cMean daily count number of adult weevils occurring on 40 Dalmatian toadflax stems ≥ 25 cm tall. dMean daily count of adult weevils occurring on 100 (Lake Point) or 50 (at each of four Pine Canyon sites) Dalmatian toadflax stems ≥ 15 cm tall. Fig. 2. View largeDownload slide Degree-day accumulation (as determined using the single sine method with a critical base temperature of 8.9°C and a cutoff threshold of 28.7°C) in 2014 and 2015. Day of year 200 corresponds to 8 July. Fig. 2. View largeDownload slide Degree-day accumulation (as determined using the single sine method with a critical base temperature of 8.9°C and a cutoff threshold of 28.7°C) in 2014 and 2015. Day of year 200 corresponds to 8 July. Weevils remained at high densities for a longer period (i.e., throughout May) in 2015 than in 2014. Following the occurrence of peak population density in late May, the decline in adult abundance during June was more gradual in 2015 than in 2014, especially at Lake Point (Fig. 1), corresponding with less rapid gain in degree-days in June in 2015 than in 2014 (Fig. 2). Despite the differences in the seasonal timing of heat gain in 2014 and 2015, overall heat gain in the 2 yr was very similar from January to the end of June when M. janthiniformis adults were no longer found on the stems (Fig. 2). In both 2014 and 2015, almost all individuals found on the host plant in early spring were males, whereas most individuals after the population had peaked were females. Males were significantly more abundant than females through the end of May in 2014 and through the first half of May in 2015, while females were significantly more abundant than males during late June 2014 and throughout June in 2015 (Table 1). Males and females did not differ in abundance during early June 2014 or in late May 2015 (Table 1). Table 1. P Values for χ2 tests to compare the numbers of adult male and female weevils collected altogether during different time periods in 2014 (Kennecott and Lake Point collections combined) in 2015 (at lake point) Dates  2014  2015  N  P value  N  P value  Mar 1–April 14  Male: 40 Female: 9  <0.0001  Male: 58 Female: 14  <0.0001  Apr 15–April 30  Male: 113 Female: 17  <0.0001  Male: 378 Female: 61  <0.0001  May 1–May 15  Male: 738 Female: 212  <0.0001  Male: 636 Female: 291  <0.0001  May 16–May 31  Male: 499 Female: 404  0.0016  Male: 494 Female: 453  0.1828  June 1–June 15  Male: 382 Female: 427  0.1136  Male: 302 Female: 409  <0.0001  June 16–June 30  Male: 247 Female: 553  <0.0001  Male: 48 Female: 157  <0.0001  Dates  2014  2015  N  P value  N  P value  Mar 1–April 14  Male: 40 Female: 9  <0.0001  Male: 58 Female: 14  <0.0001  Apr 15–April 30  Male: 113 Female: 17  <0.0001  Male: 378 Female: 61  <0.0001  May 1–May 15  Male: 738 Female: 212  <0.0001  Male: 636 Female: 291  <0.0001  May 16–May 31  Male: 499 Female: 404  0.0016  Male: 494 Female: 453  0.1828  June 1–June 15  Male: 382 Female: 427  0.1136  Male: 302 Female: 409  <0.0001  June 16–June 30  Male: 247 Female: 553  <0.0001  Male: 48 Female: 157  <0.0001  View Large In both years, there was a steady decrease in the percentage of males on host plant stems as degree-days accumulated and females began to emerge (Fig. 3). The percentage of males similarly decreased with calendar date (F1,18 = 168.20; R2 = 0.90, P < 0.0001 for 2014, and F1,36 = 240.49; R2 = 0.88, P < 0.0001 for 2015). From the equations obtained in the linear regression, the sex ratio (males:females) was estimated at 1:1 at 463 degree-days in 2014 (1 June) and at 410 degree-days (25 May) in 2015. Fig. 3. View largeDownload slide The percentage of adult weevils occurring on toadflax stems that were males, versus degree-day accumulation during the spring and early summer in 2014 (F1,18 = 226.20, R2 = 0.93, P < 0.001; y = −0.1022 x + 97.33) and 2015 (F1,36 = 383.38, R2 = 0.92, P < 0.001; y = −0.1446 x + 109.48). Fig. 3. View largeDownload slide The percentage of adult weevils occurring on toadflax stems that were males, versus degree-day accumulation during the spring and early summer in 2014 (F1,18 = 226.20, R2 = 0.93, P < 0.001; y = −0.1022 x + 97.33) and 2015 (F1,36 = 383.38, R2 = 0.92, P < 0.001; y = −0.1446 x + 109.48). Populations of both male and female weevils increased rapidly with degree-day accumulation in the early spring (Fig. 4). Males reached their peak-population density at fewer degree-day accumulations than females did at both sites and in both 2014 and 2015 (paired t-test comparison of degree-day accumulations for males vs females at peak density for both sites in both years: t1, 3 = 5.65, P = 0.011). Males attained peak numbers at very similar degree-day accumulations at both sites in each year (with the peak occurring between 255 and 270 degree-days). Females peaked in abundance at fairly consistent but slightly more variable degree-day accumulations, with the peak occurring between 307 and 373 degree-days (Fig. 4). Numbers of both males and females declined gradually after peak abundance was observed with continuing degree-day accumulation (Fig. 4). Males peaked in abundance on the host plant several days before females at both sites in 2014 but 18 d (Pine Canyon) and 24 d (Lake Point) before females in 2015. Relatively high numbers of males still persisted on the host plant, however, when females became most abundant in 2015 (Fig. 4). Fig. 4. View largeDownload slide Percent of maximum number of adult Mecinus janthiniformis males (left) and females (right) versus degree-day accumulation at Lake Point (top) and Pine Canyon (bottom). Degree-day at annual maximum is indicated (2014 italicized). Fig. 4. View largeDownload slide Percent of maximum number of adult Mecinus janthiniformis males (left) and females (right) versus degree-day accumulation at Lake Point (top) and Pine Canyon (bottom). Degree-day at annual maximum is indicated (2014 italicized). Toadflax stems grew rapidly during the spring in both years (Fig. 5). By late May to early June, when 300–400 degree-days had accumulated and when peak numbers of female weevils were found on the host plant, stems had reached their maximum height and density (Fig. 5; arrows indicate peak female density). The first flush of flowering also occurred in late May to early June, but the sporadic nature of flowering among individual stems resulted in unclear trends in flowering per stem throughout the remainder of the season (Fig. 5). Fig. 5. View largeDownload slide Dalmatian toadflax tallest stem (cm), total stem density, and mean flowers per stem at Lake Point (A–C) and Pine Canyon (D–F) versus degree-day accumulation, 2014 and 2015. Peak female weevil abundance indicated by arrows (2014—unfilled, 2015—filled). Fig. 5. View largeDownload slide Dalmatian toadflax tallest stem (cm), total stem density, and mean flowers per stem at Lake Point (A–C) and Pine Canyon (D–F) versus degree-day accumulation, 2014 and 2015. Peak female weevil abundance indicated by arrows (2014—unfilled, 2015—filled). The tallest stems at both sites, as recorded in ring sample censusing, were significantly shorter in 2015 than in 2014 (Fig. 5A and D; paired t-test for mean tallest stem height on the same or nearly the same sampling dates in 2014 and 2015: t8 = 8.94, P < 0.0001 at Lake Point and t7 = 4.95, P = 0.002 at Pine Canyon). The mean heights of stems surveyed during the population censuses similarly reflected that the stems were significantly shorter in 2015 than in 2014 (paired t-test: t20 = 22.35, P < 0.0001 at Lake Point and t20 = 16.31, P < 0.0001 at Pine Canyon). For example, the mean height of stems when females reached peak abundance decreased from 39.6 ± 1.8 cm (x ± SE) in 2014 to 21.8 ± 1.3 cm in 2015 at Lake Point and similarly from 41.6 ± 1.0 cm to 20.1 ± 0.7 cm at Pine Canyon. A similar decrease in stem density from 2014 to 2015 occurred at each of the two sites (Fig 5B and E; paired t-test for mean stem density per matched sampling date in 2014 and 2015: t8 = 12.62, P < 0.0001 at Lake Point and t7 = 17.88, P < 0.0001 at Pine Canyon). Flowering also was greatly reduced in 2015 versus in 2014 (Fig. 5C and F; paired t-test for mean number of flowers per matched sampling dates in 2014 and 2015: t20= 3.98, P < 0.001 at Lake Point and t20 = 3.89, P < 0.001 at Pine Canyon). Discussion By calendar date, phenology of M. janthiniformis adults in northern Utah is similar to the weevil’s phenology both in its native region (former Yugoslavia; Jeanneret and Schroeder 1992, Toševski et al. 2011) and in other regions of western North America to which it has been introduced (De Clerck-Floate and Harris 2002, De Clerck-Floate and Miller 2002, Carney 2003, Jamieson et al. 2012, Sing et al. 2016). In particular, adult weevils began emerging from overwintered stems by late March in Utah, peaked in abundance in mid-May to late May, and had completely disappeared from the stems by July, as recorded elsewhere (Jeanneret and Schroeder 1992, Toševski et al. 2011, Sing et al. 2016). Differences between 2014 and 2015 in calendar-dating of adult phenology in northern Utah, including weevil emergence in the early spring and population decline on the host plant later in the summer, were largely accounted for by degree-day modeling of weevil phenology that reflected seasonal differences in heat accumulation between the 2 yr. Thus, as often is the case (e.g., Allen 1976, Zalom et al. 1983, Herms 2004, Sridhar and Reddy 2013), degree-day modeling enabled greater precision in describing phenology of M. janthiniformis adult use of the host plant versus simple calendar dating. Adult males and females of M. janthiniformis differed in phenology in the present study, with males appearing earlier in the spring on the host plant than females. Protandry (the earlier emergence of males) occurs commonly in insects (Thornhill and Alcock 1983, Morbey and Ydenberg 2001) and may reflect selective advantage for early emerging males in mating with unmated females (Lehmann 2012, Morbey et al. 2012). Protandry has not been described previously for M. janthiniformis adults; however, Carney (2003) also reported female-biased sex ratios of adult weevils in the latter part of their emergence period (late June) in British Columbia. Protandry can pose challenges for biological control management practices if collections of source populations occur too early in the season, when the majority of emerged or active individuals are males (Heimpel and Lundgren 2000). Because the sexes of M. janthiniformis differed in their phenology, it is beneficial to consider them individually when determining the best time to collect adult weevils for redistribution. Generally, optimal sex ratios for redistribution range from 1:1 to female biased, and models that accurately predict varying sex ratio over the season can be very helpful in this regard (Tabadkani et al. 2013). In this study, the sex ratio of adult M. janthiniformis weevils on Dalmatian toadflax stems was close to 1:1 between 410 and 460 degree-days (between 320 and 370 degree-days as based on a simple maximum-minimum temperature model without an upper cutoff;) or from late May to early June, before becoming female-biased thereafter. In 2014, relatively few degree-days separated the points in the season when male and female numbers peaked on the host plant. Greater numbers of degree-days separated these points in 2015, but even so, males still occurred in high density when females reached peak abundance. Given that densities of both sexes combined began to decline in June, collecting adults for redistribution in mid to late May at our sites when females peak in numbers (and females have commenced ovipositing; Jeanneret and Schroeder 1992, Toševski et al. 2011) would appear to be the ideal time for such efforts. It would be especially advantageous to use degree-day accumulation to time weevil collections in mid to late May, as the differing calendar-based phenologies in 2014 and 2015 at our study sites pose challenges in using date alone to determine optimal times to collect large numbers of gravid females. Using degree-day accumulation would also be advantageous to conduct field surveys among years. Such surveys could be based on sampling weevil populations annually at a consistent stage in their phenology, in monitoring programs for assessing the long-term outcome of biocontrol releases. In the present study, female M. janthiniformis peaked in abundance on the host plants each year around the time that Dalmatian toadflax stems as a population reached full maturity, i.e., when the stems reached their maximum height and density and when they began flowering widely. Comparison of Dalmatian toadflax populations between 2014 and 2015, however, illustrates the challenges of using the phenology of stem height, density, and flowering to guide collection and monitoring efforts for M. janthiniformis. Maximum heights and densities of toadflax stems attained were much lower in 2015 than in 2014; given this variation, it would be difficult to determine except in retrospect when such maxima had been reached in the late spring in a given year, in the absence of additional information on degree-day accumulation. Similarly, large differences between years occurred in toadflax flowering activity in this study. In particular, very few flowers were produced over the growing season at Lake Point, and almost none were produced at Pine Canyon, in 2015. Such low flowering activity could make it difficult during the spring to determine when initiation of widespread (even if limited) flowering was occurring. The challenges of using these aspects of host plant phenology underscore the advantage of using degree-day accumulation to time monitoring and collecting efforts for adult weevils on stems of Dalmatian toadflax. In summary, seasonal patterns reported here of adult weevil abundance on Dalmatian toadflax stems, which were in line with patterns reported from both Europe and elsewhere in North America, were most similar between years when described by degree-day accumulation versus calendar date. Degree-day accumulation can be used for optimally timing collection and survey efforts for adult weevils on Dalmatian toadflax stems. Such timing will be aided further by using the sex-specific results of degree-day modeling in the present study, as male and female adult weevils differed predictably from each other in their phenology, with males arriving earliest in the spring on the host plant. The results from this study therefore will be of value to practitioners of biological control as they seek to implement monitoring and redistribution programs for M. janthiniformis as a biocontrol agent of Dalmatian toadflax. Acknowledgments We thank A. 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Environmental EntomologyOxford University Press

Published: Feb 1, 2018

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