Temperature and Relative Humidity Effects on Postdiapause Larval ...

PHYSIOLOGICAL ECOLOGY

Temperature and Relative Humidity Effects on Postdiapause Larval Development and Adult Emergence in Three Populations of Wheat Stem Sawfly (Hymenoptera: Cephidae) JOEL PEREZ-MENDOZA1

AND

DAVID K. WEAVER

Department of Land Resources and Environmental Sciences, Montana State University, Bozeman, MT 59717

Environ. Entomol. 35(5): 1222Ð1231 (2006)

ABSTRACT Postdiapause larval development and adult emergence of the wheat stem sawßy, Cephus cinctus Norton (Hymenoptera: Cephidae), were studied in three Þeld populations collected at Amsterdam, Conrad, and Opheim, MT, at 10, 15, 20, 25, 30, and 35⬚C and at 43, 54 Ð 62, and 75Ð76% RH under laboratory conditions. No development beyond the larval stage occurred at either 10 or 35⬚C at any relative humidity. At 10⬚C, ⬎75% of the larvae remained alive, but quiescent, whereas at 35⬚C, ⬇50% of the larvae probably re-entered diapause. Temperature and population were the main factors affecting development time and adult emergence. The shortest development times occurred at temperatures of 20⬚C and higher, but development time increased sharply at 15⬚C. Adult emergence was highest at 20 and 25⬚C for the two populations collected at Amsterdam and Conrad (western Montana) and was highest at 15 and 20⬚C for the population collected at Opheim (eastern Montana). Emerged females were twice as heavy as males. Temperature and relative humidity did not affect weight, but emerged adults from the populations collected at Amsterdam and Conrad were heavier than adults emerged from the population collected at Opheim. Sex ratio of emerging adults was female biased and was strongly affected by population. The optimal conditions for larvalÐadult development of C. cinctus lie between 20 and 25⬚C and 60 Ð75% RH. This data will be used to predict adult emergence and forecast the onset of the adult ßight period in Montana wheat Þelds. KEY WORDS Cephus cinctus, postdiapause development, temperature, relative humidity, population

The wheat stem sawßy, Cephus cinctus Norton (Hymenoptera: Cephidae), is a chronic, severe pest of wheat, Triticum aestivum L., in the northern Great Plains of the United States and in the Canadian Prairies (Ainslie 1920, Holmes 1982, Morrill and Kushnak 1996). Female sawßies deposit their eggs inside the stems of wheat plants where the larvae feed and complete development (Holmes 1975). The mature larvae cut the stems near ground level in late summer and survive the winter inside the basal portion of these cut stems (also called “stubs,” which are the lower portions of cut stems containing prepupae) below ground level near the soil surface (Ainslie 1929). At this time, the larva is mature, has completed feeding, emptied the gut, and lined the stub with a hibernaculum (Salt 1947, Villacorta et al. 1971). Overwintered larvae excised from hibernacula maintain a characteristic Sshape in diapause that persists until development is resumed, when the immature straightens out to pupate (Salt 1947). Larvae enter this obligatory diapause in the fall. Diapause is terminated by a prolonged exposure to low temperatures near the soil surface over the winter, and by spring they are ready for 1

Corresponding author, e-mail: [email protected].

further physiological development when conditions warm and are favorable (Salt 1946). Unlike many insects, the wheat stem sawßy is able to re-enter diapause in the spring under unfavorable weather conditions (Salt 1947). Weather conditions also have a direct effect on the life cycle of wheat stem sawßy, with either cold and wet, or hot and dry conditions retarding the breaking of diapause and/or further development in the Þeld (Seamans 1945, Salt 1946). The effect of temperature, moisture, and light intensity on termination of diapause has been studied in detail in previous studies (Salt 1946, 1947, Church 1955, Villacorta et al. 1972). However, information on the effects of temperature, relative humidity, differing populations, and their combined effects on postdiapause development, adult emergence, and re-entry into diapause has received limited study for this species. This information would be especially useful as a component in forecasting adult emergence in the Þeld, which is of considerable value for developing integrated pest management (IPM) strategies. Therefore, the purpose of this study was to assess the variability in the duration of postdiapause larval development and the rate of adult emergence of wheat stem sawßy collected from three

0046-225X/06/1222Ð1231$04.00/0 䉷 2006 Entomological Society of America

October 2006 PEREZ-MENDOZA ET AL.: WHEAT STEM SAWFLY POSTDIAPAUSE DEVELOPMENT AND EMERGENCE 1223

Fig. 1. Geographic locations in Montana where wheat stem sawßy populations were collected, showing the distances between sampled Þelds.

Þeld locations (referred to as “population” hereafter), each from a different wheat variety, over the range of temperatures and relative humidities that support survival and development of this species. In addition, we report on sex ratio, weight of emerged adults, and the proportion of individuals that maintain or re-enter diapause. These populations may be affected by different genetic backgrounds and by different host varieties. In this study, we only address the effects of the two abiotic factors on sawßy development in these populations. Materials and Methods Insect Collection. Infested, overwintered, wheat stem sawßy-cut stems (stubs) containing postdiapause larvae were collected from Conrad (latitude: 48.17 N, longitude: 111.95 W), Amsterdam (latitude: 45.75 N, longitude: 111.31 W), and Opheim, MT (latitude: 48.50 N, longitude: 106.19 W; Fig. 1) in late March 2005. The stubs collected at Conrad and at Amsterdam were from the hollow-stem spring wheat varieties ÔReederÕ and ÔMcNealÕ (Lanning et al. 1994), which are susceptible to sawßy damage and were from heavily infested Þelds. ÔReederÕ was released by North Dakota State University in 1995. The stubs collected at Opheim were from the solid-stem spring wheat variety ÔErnestÕ, which is partially resistant to sawßy damage. ÔErnestÕ was released by North Dakota State University in 1999. Therefore, stubs were scarcer at Opheim because of the lesser amount of sawßy damage. Stubs were removed from the Þelds with a shovel and taken to the laboratory. Uninfested residue was separated from the stubs, which were rinsed to remove the soil and spotted dry with a paper towel. Only intact stubs with live insets were selected, whereas stubs with dead insects (damaged or broken) were discarded. We dissected ⬇100 of these stubs in each population to check overwintering mortality, but we didnÕt Þnd dead insects inside the stubs. Therefore, we are assuming that we started the experiment with a very low level of mortality. Lots of 100 were stored at 4 ⫾ 1⬚C for 21 d in plastic Ziploc brand bags (Johnson & Son, Racine, WI) to homogenize and attenuate the developmental

trajectory of the insects from the three populations before the initiation of the experiment. Experimental Design. The studies were conducted in growth chambers at six temperatures (10, 15, 20, 25, 30, and 35⬚C) over three saturated salt solutions, potassium carbonate (K2CO3), sodium bromide (NaBr), and sodium chloride (NaCl). These salt solutions maintain relative humidities of 43, 54 Ð 62, and 75Ð76%, respectively, over the range of temperatures used in this study (Greenspan 1977). Either relative humidity or moisture content could be used as a classiÞcation factor because they are mathematically related (Throne 1994). We used relative humidity as a classiÞcation factor because it is a calculated parameter and can be obtained from tabulated values in Greenspan (1977). The experiments were conducted at constant photoperiod of 12:12 (L:D) h. Groups of 25 stubs were placed in each of 216 (18 environmental conditions by three populations by four replications) Ziploc plastic containers (Johnson & Son) (5 cm high by 14 cm long and wide) modiÞed with 64-␮m mesh, nylon screen covering an 8-cm hole in the lid and in the base to allow for air exchange and moisture equilibration. These containers, in groups of two (one for each population), were placed inside 108 polystyrene storage boxes with sliding lids (13.2 cm high by 40 cm long by 22 cm wide; McMaster-CARR, Santa Fe Springs, CA), containing perforated ßoors supported at 1.5 cm above the actual ßoor. Each box contained a speciÞc saturated salt solution below the perforated ßoor to maintain relative humidity. Each box was sealed with plastic wrap (Glad PressÕn Seal; The Glad Products Co., Oakland, CA) and distributed among one of six environmental chambers (18 boxes by each chamber) maintained at the appropriate temperature. Beginning 1 wk after the stubs were transferred to environmental chambers, infested stubs were examined daily until all adults had emerged. After emergence ceased, at ⬇60 d after being transferred to the environmental chambers, stubs from which no adults emerged were dissected to determine the stage of any living or dead sawßy. If the insect appeared to be alive (intact, undessicated larva, with the characteristic S-shape), we considered these in-

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Table 1. Test statistics from the general linear models procedure (PROC GLM) testing for effects of temperature, relative humidity, sex, and population on variation in postdiapause development and variation in the proportion of adult emergence of C. cinctus Parameter

Source of variation

df

F-value

Pr ⬎ F

Postdiapause development

Temperature (Temp.) Relative humidity (RH) Population (Pop.) Sex Temp. ⫻ RH Temp. ⫻ sex Temp. ⫻ pop. RH ⫻ pop RH ⫻ sex Sex ⫻ pop. Temp. ⫻ RH ⫻ sex Temp. ⫻ RH ⫻ pop. Temp. ⫻ Sex ⫻ pop. RH ⫻ Sex ⫻ pop. Temp. ⫻ RH ⫻ sex ⫻ pop. Temperature Relative humidity Population Temp. ⫻ pop. Temp. ⫻ RH RH ⫻ pop. Temp. ⫻ RH ⫻ pop.

3 2 2 1 6 3 6 4 2 2 6 12 6 4 12 3 2 2 6 6 4 12

1,257.4 4.4 447.2 14.4 13.8 3.8 44.3 5.0 0.5 1.0 0.1 7.7 2.2 1.2 0.9 20.5 1.5 26.6 4.8 2.0 1.0 0.9

⬍0.0001a 0.0126a ⬍0.0001a 0.0002a ⬍0.0001a 0.0096a ⬍0.0001a 0.0005a 0.6277 0.3540 0.9913 ⬍0.0001a 0.0396a 0.3108 0.5046 ⬍0.0001a 0.2322 ⬍0.0001a 0.0002a 0.0692 0.4391 0.5679

Adult emergence

a

SigniÞcant variables at P ⬍ 0.05.

pause larvae and at newly emerged adult stages, so we analyzed larval and adult mortality separately, as well as overall mortality. In addition, we used the SLICE option of PROC GLM to test simple effects (SAS Institute 2001). Effects of environmental conditions on sex ratio were analyzed as the proportion of females. Deviations in sex ratio of the emerging adults from 1:1 were analyzed using a t-test (Zar 1999). Variances were not homogeneous for response variables, except for the sex ratio of emerged adults. No adults emerged at 10 and 35⬚C, so variance was 0. Zero variances could not be homogenized with variances at other temperatures, so adult emergence data for 10 and 35⬚C were excluded from the general linear model analyses. The arcsine-square-root transformation was used to homogenize variances of adult emergence data before analysis. Data for overall mortality, larval and adult mortality, and proportion of individuals in diapause were arcsine-square root transformed before analysis. Postdiapause development times were log-

dividuals either as having re-entered diapause or as having never broken diapause. If the insect was dead (presence of a desiccated or moldy cadaver), the developmental stage of the cadaver was recorded. Duration of postdiapause larval development, the proportion of individuals that emerged as adults (hereafter referred to as adult emergence), the proportion of individuals that reentered or remained in diapause (hereafter referred to as individuals in diapause), the proportion of insect mortality, and the sex ratio and weight of emerged adults were determined from these data. Data Analysis. Differences in postdiapause development, adult emergence, insect mortality, weight of emerged adults, and sex ratio, as well as the proportion of individuals in diapause, were analyzed as a function of both biotic and abiotic factors (population, temperature, and relative humidity) using a general linear models procedure (PROC GLM; SAS Institute 2001). Insect mortality inside the stubs occurred at postdia-

Table 2. Mean 关ⴞSEM (n)兴 duration days of postdiapause development from larva to adult of C. cinctus in three field populations at indicated temperatures and relative humidities Population Conrad

Opheim

Amsterdam

Temperature (⬚C) 15 20 25 30 15 20 25 30 15 20 25 30

Percent relative humidity 43

53Ð 61

75Ð76

41.3 ⫾ 1.6 (06) 23.5 ⫾ 0.4 (44) 17.7 ⫾ 0.2 (69) 19.3 ⫾ 0.5 (35) 45.3 ⫾ 0.6 (11) 33.7 ⫾ 1.2 (15) 27.6 ⫾ 2.1 (05) 23.6 ⫾ 1.5 (05) 39.2 ⫾ 0.3 (52) 22.0 ⫾ 0.5 (61) 19.5 ⫾ 0.3 (56) 17.9 ⫾ 0.3 (42)

40.9 ⫾ 0.5 (28) 22.1 ⫾ 0.2 (64) 19.6 ⫾ 0.2 (70) 18.3 ⫾ 0.4 (19) 46.5 ⫾ 0.5 (24) 37.5 ⫾ 1,0 (31) 34.7 ⫾ 1.2 (15) 22.5 ⫾ 0.2 (10) 39.7 ⫾ 0.3 (50) 23.8 ⫾ 0.5 (59) 19.5 ⫾ 0.2 (79) 16.5 ⫾ 0.5 ((4)

43.3 ⫾ 0.7 (31) 22.2 ⫾ 0.3 (59) 16.1 ⫾ 0.4 (56) 16.6 ⫾ 0.3 (30) 44.4 ⫾ 0.5 (26) 32.5 ⫾ 1.0 (42) 28.2 ⫾ 9.8 (15) 31.2 ⫾ 0.2 (06) 44.5 ⫾ 0.7 (40) 22.0 ⫾ 0.4 (76) 18.7 ⫾ 0.2 (81) 16.8 ⫾ 0.6 (06)

October 2006 PEREZ-MENDOZA ET AL.: WHEAT STEM SAWFLY POSTDIAPAUSE DEVELOPMENT AND EMERGENCE 1225 transformed, and data for the weight of emerged adults were square rootÐtransformed before analysis. Untransformed data are reported to simplify interpretation. A number of different equation forms were Þt to the data using TableCurve 2D (SYSTAT 2002). Selection of an equation to describe the data was based on the magnitude and the pattern of residuals, lack-of-Þt tests, and R2 values (Draper and Smith 1981). We also ensured that the shape of the curve was biologically reasonable for describing the data. Adult emergence data from 10 and 35⬚C were used for curve-Þtting equations We did not examine the behavior of the equations beyond the range of conditions at which we measured responses, and we do not recommend using the equations to extrapolate beyond the data range reported. Results Postdiapause Development and Adult Emergence. The duration of postdiapause development varied with temperature, relative humidity, population, and sex of emerging adults (Table 1). The interactions for temperature by relative humidity, temperature by sex, temperature by population, relative humidity by population, temperature by relative humidity by population, and temperature by sex by population were also signiÞcant, but the interactions for relative humidity by sex, sex by population, temperature by relative humidity by sex, relative humidity by sex by population, and temperature by relative humidity by sex by population were not signiÞcant (Table 1). The shortest development times occurred at 25 and 30⬚C, and development times increased as temperature decreased below 20⬚C (Table 2). Development times tended to be greater in the insect population collected from the solid-stem wheat variety ÔErnestÕ at Opheim across all the temperatures compared with the two different insect populations collected from the hollow-stem varieties ÔReederÕ at Conrad and ÔMcNealÕ at Amsterdam (Table 2). Males emerged earlier than females in the three populations. The SLICE option of PROC GLM showed that relative humidity and sex have only a small effect on postdiapause development, and only at 20 and 25⬚C, so we did not include relative humidity and sex in the model. Because the interaction for temperature by population was signiÞcant, we described postdiapause development time as a function of temperature for each population (Fig. 2; Table 3). The proportion of adult emergence varied with temperature and population but not with relative humidity (Table 1). The interaction for temperature by population was also signiÞcant, but the interactions for temperature by relative humidity, population by relative humidity, and temperature by population by relative humidity were not signiÞcant (Table 1). Because the interaction between temperature and population was signiÞcant, we described adult emergence as a function of temperature for each population (Fig. 3; Table 3). Adult emergence was lower at the transition temperatures of 15 and 30⬚C and was much

Fig. 2. Relationship between developmental period from postdiapause larva to adult emergence and temperature for C. cinctus from three Þeld populations. Solid lines are from equations in Table 3.

lower across the temperatures tested in the insects developing in the solid-stem wheat variety ÔErnestÕ collected at Opheim (Table 4). Proportion of Individuals in Diapause and Insect Mortality. The proportion of insects that remained in or re-entered diapause varied with temperature and population but not with relative humidity (Table 5). The interaction for temperature by population was also signiÞcant, but the interactions for temperature by relative humidity, population by relative humidity,

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Table 3. Equations and test statistics describing effects of temperature on adult emergence and developmental duration of postdiapause immature C. cinctus from three field populations Equation parameters ⫾ SE

Fita

Lack of Þt

Life history parameter /population

a

b

c

R2

Max. R2

F

df

P

Emergence/Conradb Emergence/Opheimc Emergence/Amsterdamb Duration/Conradd Duration/Opheime Duration/Amsterdamf

1.4766 ⫾ 0.09 ⫺25.51 ⫾ 6.65 1.3521 ⫾ 0.05 53.21 ⫾ 5.12 50.38 ⫾ 5.07 32.67 ⫾ 4.51

1.28 by 10⫺13 ⫾ 4.6 by 10⫺14 157.61 ⫾ 43.4 4.10 by 10⫺13 ⫾ 1.3 by 10⫺13 ⫺1952.79 ⫾ 213.8 ⫺0.8177 ⫾ 0.20 ⫺9600.44 ⫾ 1690.8

6.6778 ⫾ 2.66 ⫺955.05 ⫾ 269.7 2579080 ⫾ 642427 26705.8 ⫾ 2107 2.33 by 10⫹07 ⫾ 8.46 by 10⫹06 38961.8 ⫾ 5600.4

0.90 0.76 0.95 0.99 0.85 0.98

0.93 0.82 0.97 0.99 0.85 0.98

1.8 1.3 1.3 0.12 0.001 3.9

3,12 3,12 3,12 1,20 1,20 1,20

0.20 0.33 0.31 0.74 0.97 0.06

a 2 R is the amount of variation explained by the given equation; max R2 indicates the max amount of variation that any equation Þt to the data could explain, given the pure error in the data (Draper and Smith 1981). b Equation is y⫺1 ⫽ a ⫹ bex ⫹ cex, where x ⫽ temperature (⬚C) and y ⫽ adult emergence. c Equation is ln(y) ⫽ a ⫹ b/x 0.5 ⫹ c/x 1.5, where x ⫽ temperature (⬚C) and y ⫽ adult emergence. d Equation is y ⫽ a ⫹ b/x ⫹ c/x2, where x ⫽ temperature (⬚C) and y ⫽ duration from postdiapause larvae to adult emergence (days). e Equation is y ⫽ a ⫹ bx ⫹ ce⫺x, where x ⫽ temperature (⬚C) and y ⫽ duration from postdiapause larvae to adult emergence (days). f Equation is y ⫽ a ⫹ b/x 1.5 ⫹ c/x2, where x ⫽ temperature (⬚C) and y ⫽ duration from postdiapause larvae to adult emergence (days).

and temperature by population by relative humidity were not signiÞcant. The SLICE option of PROC GLM showed that population has a signiÞcant effect on the proportion of insects that remained in or re-entered diapause at 15, 20, 25, and 30⬚C but not at 10 and 35⬚C. A high proportion of wheat stem sawßy larvae exposed at these extreme temperatures (10 and 35⬚C) tended to remain in or re-enter diapause regardless of population (Table 4). Insects that failed to break diapause or that re-entered diapause were observed among those populations collected at Conrad and Amsterdam only at 10 and 35⬚C. However, this response was common for insects collected at Opheim at all tested temperatures (Table 4). Insect mortality inside the stubs occurred predominantly at two life stages: larvae and newly eclosed adults. Newly eclosed adults were sometimes unable to chew an emergence hole through the frass plug at the apex of the stub and subsequently died. Therefore, we analyzed overall insect mortality, as well as postdiapause larval and unemerged adult mortalities separately. Overall mortality varied with temperature and population but not with relative humidity. The interactions for temperature by population and temperature by relative humidity were also signiÞcant, but the interactions for population by relative humidity, and temperature by population by relative humidity were not signiÞcant. The SLICE option of PROC GLM showed that relative humidity had a signiÞcant effect on overall mortality only at 25 and 30⬚C, whereas population had a signiÞcant effect on overall mortality at 15, 20, 25, and 30⬚C. Mortality occurred at all temperatures and in the three populations tested. However, mortality tended to be higher for insects developing at 15 and 30⬚C (Table 4). The proportion of postdiapause larval mortality (Table 4) varied with temperature and population but not with relative humidity. The interaction of temperature by population was also signiÞcant, but the interactions for temperature by relative humidity, population by relative humidity, and temperature by population by relative humidity were not signiÞcant. The SLICE option of PROC GLM showed that relative humidity had a signiÞcant effect on larval mortality

only at 30⬚C, whereas population had a signiÞcant effect on larval mortality at 15, 20, 25, and 30⬚C. Larval mortality occurred at all temperatures tested. However, mortality tended to be higher for insects developing in the stubs collected in the solid-stem variety ÔErnestÕ at Opheim (Table 4). The proportion of dead adults inside the stems (Table 4) varied with temperature and population but not with relative humidity. The interaction for temperature by population was also signiÞcant, but the interactions for temperature by relative humidity, population by relative humidity, and temperature by population by relative humidity were not signiÞcant. The SLICE option of PROC GLM showed that temperature had a signiÞcant effect on adult mortality only in the insect populations collected at Conrad and Amsterdam. Therefore, in contrast to larval mortality, most adult mortality occurred in the stubs collected at those locations and tended to be higher at 15 and 20⬚C (Table 4). Weight of Emerged Adults. Weight of emerged adults (Table 6) varied with sex and population but not with temperature or relative humidity. The interaction of sex by population was also signiÞcant, but the interactions for temperature by relative humidity, temperature by sex, temperature by population, relative humidity by sex, relative humidity by population, temperature by relative humidity by sex, temperature by relative humidity by population, temperature by sex by population, relative humidity by sex by variety, and temperature by relative humidity by sex by population were not signiÞcant. Emerged females (8.58 ⫾ 0.40 mg) across all treatment combinations were more than two-fold heavier than emerged males (4.19 ⫾ 0.16 mg). Both males (5.2 ⫾ 0.2 mg) and females (11.0 ⫾ 0.2 mg) that emerged from the stubs collected at Conrad were heavier than males (3.9 ⫾ 0.1 mg) and females (8.7 ⫾ 0.1 mg) that emerged from the stubs collected at Amsterdam or the males (3.1 ⫾ 0.1 mg) and females (5.1 ⫾ 0.2 mg) that emerged from the stubs collected at Opheim. Sex Ratio. The proportion of emerged adults that were females (Table 6) varied with temperature and with population but not with relative humidity. The

October 2006 PEREZ-MENDOZA ET AL.: WHEAT STEM SAWFLY POSTDIAPAUSE DEVELOPMENT AND EMERGENCE 1227 Discussion

Fig. 3. Relationship between proportion of adults emerging from postdiapause larvae and temperature for C. cinctus from three Þeld populations. Solid lines are from equations in Table 3.

interactions of temperature by relative humidity, temperature by population, relative humidity by population, and temperature by relative humidity by population were also not signiÞcant. However, the SLICE option of PROC GLM showed that temperature had a small signiÞcant effect on sex ratio only at 30⬚C (F ⫽ 4.4; df ⫽ 2; P ⫽ 0.036) in the three populations studied. The proportion of females (0.66 ⫾ 0.02) averaged over all treatment combinations differed from 0.5 (t-test; t ⫽ 14.5; df ⫽ 70; P ⬍ 0.01; Fig. 4).

Our studies from three Þeld populations of C. cinctus with six temperature and three relative humidity combinations showed that development of postdiapause larvae and adult emergence did not occur under the more extreme temperature conditions of 10 and 35⬚C. The arrest of insect development at these temperatures was driven by two factors. The Þrst was the ability of this species to enter diapause again at high temperatures or to remain in diapause at low temperatures (Salt 1947). The second factor is the signiÞcant mortality of both immature and adult individuals inside the stubs. This is supported by data obtained by the dissection of stubs from which no adults emerged. More than 75% of the larvae inside infested stubs incubated at 10⬚C were alive but undeveloped. This suggests that these individuals may have re-entered diapause or they remained quiescent, waiting for warmer temperatures. The second scenario seems more likely as Villacorta et al. (1972) reported that temperatures of 10⬚C or less suppress postdiapause development, and sawßies can be kept in a quiescent condition for months or even years at such temperatures. Villacorta et al. (1972) also reported that the postdiapause development threshold was near 15⬚C. No adults emerged from stubs incubated for ⬎60 d at 10⬚C in a study by Lou et al. (1998). In the case of stubs incubated at 35⬚C, almost 50% of the larvae that failed to complete development probably re-entered diapause, whereas the rest died. Our results agree with previous studies showing that no postdiapause development of C. cinctus occurs when the insects are exposed to more extreme temperatures. For example, Salt (1947) reported that larval diapause is terminated by incubating the larvae for almost 3 mo at 10⬚C. However, it is necessary to transfer these individuals to higher temperatures to complete development after the diapause requirement has been met. Incubating postdiapause larvae at high temperatures (35Ð 40⬚C) for ⬎4 d caused either high mortality or reversion to diapause (Salt 1947). Church (1955) and Villacorta et al. (1971) also reported that diapause was terminated in wheat stem sawßy larvae incubated for 100 and 120 d at 10⬚C and that diapause was reinstated by incubating postdiapause larvae at 35⬚C for ⬎4 d. Temperature and population had the greatest effect on postdiapause development and adult emergence of wheat stem sawßy in this study. Although the effects of relative humidity and sex of emerged adults were sometimes statistically signiÞcant, their effects were minor, although they were usually more pronounced at extreme temperatures. This suggests that the effect of relative humidity is most important when the insect is already stressed because of adverse temperatures or development in a less suitable host. Males tended to emerge 0.6 Ð2 d earlier than females, with the greatest difference in emergence dates occurring in the population collected at Opheim. Earlier emergence of males was noted also by Holmes and Peterson (1963) and Ca´rcamo et al. (2005), whose results showed that males typically emerge 2Ð 4 d earlier than females.

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Table 4. Mean (ⴞSEM) proportion of adult emergence, larvae that re-entered diapause, and mortality of postdiapause C. cinctus from three field populations exposed to indicated constant temperatures for 60 d Population

Proportion of insect mortality

Temperature (⬚C)

Proportion of adult emergence

Proportion of larvae that re-entered diapause

Overall

Larvae

Adults

10 15 20 25 30 35 10 15 20 25 30 35 10 15 20 25 30 35

0.00 ⫾ 0.00 0.22 ⫾ 0.08 0.59 ⫾ 0.06 0.69 ⫾ 0.06 0.32 ⫾ 0.05 0.00 ⫾ 0.00 0.00 ⫾ 0.00 0.25 ⫾ 0.06 0.34 ⫾ 0.08 0.15 ⫾ 0.05 0.08 ⫾ 0.01 0.00 ⫾ 0.00 0.00 ⫾ 0.00 0.46 ⫾ 0.03 0.66 ⫾ 0.05 0.72 ⫾ 0.08 0.18 ⫾ 0.13 0.00 ⫾ 0.00

0.76 ⫾ 0.03 0.00 ⫾ 0.00 0.00 ⫾ 0.00 0.00 ⫾ 0.00 0.00 ⫾ 0.00 0.45 ⫾ 0.03 0.75 ⫾ 0.01 0.23 ⫾ 0.04 0.10 ⫾ 0.06 0.13 ⫾ 0.02 0.25 ⫾ 0.08 0.49 ⫾ 0.01 0.80 ⫾ 0.02 0.00 ⫾ 0.00 0.00 ⫾ 0.00 0.00 ⫾ 0.00 0.00 ⫾ 0.00 0.54 ⫾ 0.05

0.24 ⫾ 0.03 0.78 ⫾ 0.08 0.41 ⫾ 0.06 0.31 ⫾ 0.07 0.68 ⫾ 0.04 0.55 ⫾ 0.03 0.25 ⫾ 0.01 0.52 ⫾ 0.04 0.56 ⫾ 0.06 0.72 ⫾ 0.06 0.67 ⫾ 0.07 0.51 ⫾ 0.01 0.20 ⫾ 0.02 0.54 ⫾ 0.03 0.34 ⫾ 0.05 0.28 ⫾ 0.08 0.82 ⫾ 0.13 0.46 ⫾ 0.05

1.00 ⫾ 0.00 0.58 ⫾ 0.08 0.54 ⫾ 0.10 0.79 ⫾ 0.02 0.76 ⫾ 0.05 1.00 ⫾ 0.00 1.00 ⫾ 0.00 0.89 ⫾ 0.02 0.95 ⫾ 0.02 0.98 ⫾ 0.01 0.97 ⫾ 0.02 1.00 ⫾ 0.00 1.00 ⫾ 0.00 0.47 ⫾ 0.10 0.56 ⫾ 0.09 0.61 ⫾ 0.11 0.62 ⫾ 0.15 1.00 ⫾ 0.00

0.00 ⫾ 0.00 0.42 ⫾ 0.08 0.46 ⫾ 0.10 0.21 ⫾ 0.02 0.24 ⫾ 0.05 0.00 ⫾ 0.00 0.00 ⫾ 0.00 0.11 ⫾ 0.02 0.05 ⫾ 0.02 0.02 ⫾ 0.01 0.03 ⫾ 0.02 0.00 ⫾ 0.00 0.00 ⫾ 0.00 0.53 ⫾ 0.10 0.44 ⫾ 0.09 0.39 ⫾ 0.11 0.38 ⫾ 0.15 0.00 ⫾ 0.00

Conrad

Opheim

Amsterdam

The duration of postdiapause development was longer at low temperatures. C. cinctus can complete development at 15 and 30⬚C, but mortality is higher than at 20 and 25⬚C. Adult emergence was higher at 20 Ð25⬚C for insects collected at Conrad and at Amsterdam, whereas it was higher at 15Ð20⬚C for insects collected at Opheim. Therefore, based on these results, the maximum rate of population development of this species will occur at 20 and 25⬚C and 60 Ð75% RH. These results suggest that the hollow-stem wheat va-

rieties ÔReederÕ and ÔMcNealÕ may be more suitable for C. cinctus development, adult emergence, and weight of emerging adults than the solid-stem variety ÔErnestÕ. Postdiapause development was shorter, adult emergence was higher, and emerged adults were heavier when emerging from the hollow-stem varieties compared with the solid-stem variety. Ca´rcamo et al. (2005) reported similar differences in these biological parameters for populations collected in solid- and hollow-stem spring wheat varieties in Canada when in-

Table 5. Test statistics from the general linear models procedure (PROC GLM) testing for effects of temperature, relative humidity, and population on variation in the proportion of C. cinctus that remained in or re-entered diapause, overall mortality, and postdiapause larval and adult mortality Parameter

Source of variation

df

F-value

Pr ⬎ F

Insects that remained in or re-entered diapause

Temperature (Temp.) Relative humidity (RH) Population (Pop) Temp. ⫻ RH Temp. ⫻ pop RH ⫻ pop Temp. ⫻ RH ⫻ pop Temperature Relative humidity Population Temp. ⫻ RH Temp. ⫻ pop RH ⫻ pop Temp. ⫻ RH ⫻ pop Temperature Relative humidity Population Temp. ⫻ pop Temp. RH RH ⫻ pop Temp. ⫻ RH ⫻ pop Temperature Relative humidity Population Temp. ⫻ pop Temp. ⫻ RH RH ⫻ pop Temp. ⫻ RH ⫻ pop

5 2 2 10 10 4 20 5 2 2 10 10 4 20 5 2 2 10 10 4 20 5 2 2 10 10 4 20

438.4 1.0 88.8 1.4 13.5 2.3 1.3 30.2 1.5 4.2 2.1 7.3 0.7 1.4 40.9 1.7 47.6 5.5 1.5 2.2 1.5 30.9 1.3 46.7 5.5 1.8 1.7 1.6

⬍0.0001a 0.3653 ⬍0.0001a 0.1656 ⬍0.0001a 0.0636 0.1702 ⬍0.0001a 0.2232 0.0174a 0.0321a ⬍0.0001a 0.5903 0.1363 ⬍0.0001a 0.1917 ⬍0.0001a ⬍0.0001a 0.1367 0.0710 0.0787 ⬍0.0001a 0.2669 ⬍0.0001a ⬍0.0001a 0.0710 0.0930 0.0754

Overall insect mortality

Larval mortality

Adult mortality

a


October 2006 PEREZ-MENDOZA ET AL.: WHEAT STEM SAWFLY POSTDIAPAUSE DEVELOPMENT AND EMERGENCE 1229 Table 6. Test statistics from the general linear models procedure (PROC GLM) testing for effects of temperature, relative humidity, and population on variation in body weight of emerging adults and sex ratio of C. cinctus Parameter

Source of variation

df

F-value

Pr ⬎ F

Body weight

Temperature (Temp.) Relative humidity (RH) Population (Pop.) Sex Temp. ⫻ RH Temp. ⫻ Sex Temp. ⫻ pop. RH ⫻ pop RH ⫻ Sex Sex ⫻ pop. Temp. ⫻ RH ⫻ Sex Temp. ⫻ RH ⫻ pop. Temp. ⫻ Sex ⫻ pop. RH ⫻ Sex ⫻ pop. Temp. ⫻ RH ⫻ Sex ⫻ pop. Temperature Relative humidity Population Temp. ⫻ pop. Temp. ⫻ RH RH ⫻ pop. Temp. ⫻ RH ⫻ pop.

3 2 2 1 6 3 6 4 2 2 6 12 6 4 12 3 2 2 6 6 4 12

0.3 2.3 109.4 355.4 0.3 0.1 1.2 0.5 0.2 15.5 0.4 0.1 0.4 0.2 0.3 4.5 3.0 6.7 0.4 2.3 0.8 0.9

0.8049 0.0994 ⬍0.0001a ⬍0.0001a 0.9361 0.9539 0.2846 0.7363 0.7906 ⬍0.0001a 0.8516 0.9998 0.8953 0.9224 0.9874 0.0253a 0.0871 0.0111a 0.8604 0.1048 0.5785 0.7136

Sex ratio

a


cubated at 20⬚C. For example, they found that adults from the hollow-stem cultivars ÔAC AvonleaÕ and ÔAC CadillacÕ emerged signiÞcantly earlier than those developing in solid-stem ÔAC EatoniaÕ. Similarly, the proportion of adult emergence in the hollow-stem varieties was more than double that in the solid-stem varieties. Finally, the hollow-stem varieties produced adults more than twice as large as those emerging from solid-stem varieties. Holmes and Peterson (1962) also reported higher mortality rates for larvae developing in the solid stem varieties ÔRescueÕ and ÔGolden BallÕ compared with the hollow-stem varieties ÔRed BobsÕ and ÔStewartÕ. The average weight of emerged males and females in our study is similar to the weight of males and females reported by Ca´rcamo et al. (2005) for sawßies reared on different wheat varieties at 20⬚C. Female-biased sex ratios of emerged adults were strongly inßuenced by population and very slightly by

Fig. 4. Mean (⫾SE) proportion of females among wheat stem sawßy adults that emerged from three Þeld populations at indicated temperatures.

the incubation temperatures. Seventy-two percent of the emerged adults from the population collected at Conrad were females compared with 65 and 62% for the insects collected at Amsterdam and Opheim, respectively. More females emerged at 20⬚C across the three population combinations. These female-biased sex ratios may by caused by the combination of several factors. First, we selected only the best stubs for this study to reduce the possibility of having stubs with dead larvae inside. Thus, more females emerged from those stubs. It is well known that the quality of the stubs in which sawßies develop has a signiÞcant effect on the sex ratio of emerging adults in this species. More females emerge from stubs with larger diameter than do males (Wall 1952, Morrill et al. 2000, Ca´rcamo et al. 2005). Second, we collected our populations from three different wheat varieties. Differences in sex ratios between solid- and hollow-stem varieties have been reported in previous studies (Farstad et al. 1949, Holmes and Peterson 1963). Ca´rcamo et al. (2005) did not Þnd cultivar effects on sex ratio in their “current cultivar study” but did Þnd effects in their “historical study.” Finally, the insects collected from the three locations may have been from populations of different genetic composition. We found numerous differences in development, adult emergence, body weight, and sex ratio of emerged adults between the population collected from solid-stem wheat at Opheim in eastern Montana and those collected from hollow-stem wheat grown near Amsterdam and Conrad in western Montana. The distance between the Þelds in which the stubs were collected is ⬎270 km from one Þeld to another. Although much of our data closely follow patterns attributed to stem-solidness in Ca´rcamo et al. (2005), earlier studies provide some evidence for different developmental parameters from eastern and western

1230


populations of the wheat stem sawßy. Lou et al. (1998) showed that sawßy populations from six sites in North Dakota developed much more slowly at 15, 20, and 25⬚C than a population collected in western Montana, near where the Amsterdam population was collected in this study. However, there is no mention of whether the populations were collected from hollow- or solidstem wheat. Holmes et al. (1957) reported differential ability of wheat stem sawßies to cut solid-stem ÔGolden BallÕ durum wheat for from the west, near Lethbridge, Alberta, when compared with those from the east, near Regina, Saskatchewan. They conducted relocation experiments with these two insect populations and concluded that genetic differences played a role in the different stem cutting abilities. Ca´rcamo et al. (2005) reported major decreases in adult emergence from a local population of wheat stem sawßy caused by stem solidness across wheat varieties, but no signiÞcant difference in developmental delays among hollow-stem and solid-stem cultivars. We report both a large decrease in emergence and a large developmental delay for the eastern population from solidstem wheat relative to the more rapid development and greater emergence for the two western populations from hollow-stem wheat. This suggests that differences in our data might be attributable to both population differences (large developmental duration differences) and to solid-stem wheat (reduced emergence and decreased size). We are conducting varietal experiments with relocated, caged populations to further address this important question, within the context of similar environments. The ideal environmental conditions for C. cinctus postdiapause development lie within the range of 20 Ð 25⬚C and 60 Ð75% RH. However, the ability of the populations of this insect to complete postdiapause development at both 15 or 30⬚C and at 43% RH on the three wheat varieties studied clearly enable this insect to infest and survive in both solid- and hollow-stem wheat cultivars under a broad range of environmental conditions that could be encountered across most crop areas in the Northern Great Plains and Canadian Prairies. These results, and those from our ongoing research, will be especially useful to predict adult emergence in the Þeld so that future IPM approaches can be synchronized with adult activity during the ßight period.

Acknowledgments We thank J. Marquez, M. Hoßand, J. Peterson, and A. Perez-Fajardo for technical support recording the emergence of adults. We also thank J. E. Throne (USDAÐARS GMPRC) for comments and suggestions on an earlier version of the manuscript. This research was supported by funds from a USDA, CSREES, Special Research grant entitled, “Novel semiochemical- and pathogen-based management strategies for wheat stem sawßy.” Additional support was provided by the Montana Wheat and Barley Committee and by the Montana Ag Experiment Station.

Vol. 35, no. 5 References Cited

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Received for publication 12 April 2006; accepted 6 July 2006.