Diapause Recruitment and Survival of Overwintering Haematobia ...

POPULATION ECOLOGY

Diapause Recruitment and Survival of Overwintering Haematobia irritans (Diptera: Muscidae) T. J. LYSYK

AND

R. D. MOON

Agriculture and Agri-Food Canada, Lethbridge Research Centre, Lethbridge, AB, Canada T1J 4B1 and Department of Entomology, University of Minnesota, St. Paul, MN 55108

Environ. Entomol. 30(6): 1090Ð1097 (2001)

ABSTRACT A Þeld study was conducted in Alberta to examine the dynamics of diapause recruitment and survival among overwintering horn ßies, Hematobia irritans (L.). Cohorts of eggs were reared in experimental manure pats created at weekly intervals from July into September in three successive years. Nondiapausing adults emerged 16 Ð 47 d after pats were created in July and August, but few emerged when pat temperatures fell below 15⬚C. Survival to fall emergence varied with date, but was only weakly related to pat temperature. The proportion of pupae in diapause reached 1.0 in August each year. Overwintering survival of diapausing pupae varied from 0 to 85% among dates and years, and showed a curvilinear relationship with temperature during the ßyÕs diapause sensitive period. Thus, ßies that emerged in a given spring arose from oviposition during a 3- to 6-wk interval in the preceding fall. KEY WORDS horn ßy, diapause, temperature, overwintering survival, population dynamics

ADULT HORN FLIES, Hematobia irritans (L.), live and feed on grazing cattle during the summer, when reproduction is continuous and generations overlap. Females oviposit on fresh manure pats, and larvae develop synchronously within each pat, and ultimately pupate in the pat and underlying soil. In fall, development from the egg to adult is interrupted when a facultative pupal diapause intervenes, creating a reservoir of overwintering pupae beneath their natal pats. Understanding the dynamics of overwintering recruitment may lead to development of a diapausebased control strategy for this insect (Kunz and Miller 1985). Temporal patterns in diapause induction have been studied in Missouri (Thomas et al. 1987), in Arkansas (Klein and Lancaster 1992), in Mississippi (Hoelscher and Combs 1971), and in Texas (Kunz et al. 1972); and overwintering survival has been measured in Texas (Thomas and Kunz 1986). The purpose of the current study was to evaluate the component dynamics of diapause induction and overwintering survival under Þeld conditions in Alberta, near the northern limit of the horn ßyÕs distribution in North America. Materials and Methods Horn Flies. Cohorts of horn ßies were reared from eggs in experimental pats created at weekly intervals from July though September at the Lethbridge Research Center (49⬚ 42⬘ N, 112⬚ 50⬘ W) in Alberta. In 1991, horn ßy adults were swept from cattle in a chute, placed into a 500 ml Erlenmeyer ßask, the ßask stoppered, and held at 30⬚C in the dark for 30 Ð 60 min.

Eggs laid on the sides of the ßask were collected and rinsed with tap water. Eggs used in 1992 and 1993 were obtained from a laboratory colony of ßies maintained at Lethbridge Research Center using techniques previously described (Lysyk 1991). This colony had been started with wild ßies in 1989, and supplemented with wild ßies in 1990 and 1991. Experimental Design. Horn ßy survival during the fall, fall emergence, proportion of pupae in diapause, and overwintering survival were measured using sets of artiÞcial pats placed in a pasture at Lethbridge Research Center at weekly intervals from 21 August to 19 September 1991, 27 July to 28 September 1992, and 4 August to 21 September 1993. Techniques were similar to those used previously (Lysyk 1992, 1999). On each date, 10 cohorts of developing ßies were created by placing 1Ð2 kg units of previously thawed manure on 3 cm sand in round plastic tubs. Horn ßy eggs were measured volumetrically (1 ml ⫽ 6000 eggs) and divided into 10 equal aliquots by volume. Pats were inoculated with 75Ð300 newly laid horn ßy eggs depending on availability, and the tubs containing the pats were buried 3 cm in an outdoor, sand-Þlled wooden box (1.2 by 2.4 m). Pats were placed outdoors immediately after inoculation in 1991 and 1992, but were held indoors for 24 h at 25⬚C in 1993 to increase egg hatch. Once outside, each pat was covered with a mesh net to exclude other insects and capture emerging adult horn ßies. Temperatures were recorded in the center of one pat per set using a CR21 datalogger (Campbell ScientiÞc, Logan, UT) in 1991; and a CR10 datalogger in 1992 and 1993. In 1991, pat temperatures were recorded as 4-h averages and were discontinued 01 November. In 1992 and 1993 pat temperatures were

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LYSYK AND MOON: DYNAMICS OF OVERWINTERING IN HORN FLIES

recorded as 1-h averages, and were recorded throughout the winter and subsequent spring. Maximum, minimum, and daily average pat temperatures were calculated. Daily maximum and minimum air temperatures were obtained from a nearby weather station. The average winter pat temperature for the period 01 NovemberÐ30 March was calculated directly from daily pat temperatures recorded in the winters of 1992Ð1993 and 1993Ð 1994. Because winter pat temperatures were not recorded in 1991Ð1992, average daily pat temperatures for 1 November 1991Ð30 March 1992 were calculated from average daily air temperatures using the relationship presented in Lysyk (1999; Table 4), and these used to calculate average winter pat temperature. All pats were examined daily throughout the fall to collect and count emerged adults. After emergence had ceased, beginning in mid-October, Þve pats per set were retrieved, and their pupae were extracted by ßotation, counted, and dissected to determine the number in diapause. These were designated as “fall pats.” The remaining Þve pats in each set, designated as “spring pats,” were left in the Þeld throughout the winter to determine the number of horn ßies that emerged in the following spring (Lysyk 1999). The elapsed time from oviposition to 50% emergence in fall was calculated for each set of pats. Corresponding mean air temperatures (Tair) and mean pat temperatures while the immatures were developing (Tid) were calculated from temperatures recorded between times of oviposition and median emergence, or 50 d (in the cases where none emerged). Physiological age from oviposition onward was calculated for each cohort using a temperature driven, rate-summation model for eggÐadult development (Lysyk 1992). Mean pat temperature during the diapause sensitive period (Tsp) (physiological age ⫽ 0.1Ð 0.82; Lysyk and Moon 1994) was also calculated for each cohort. Horn Fly Population Dynamics. For each set of fall pats, fall survival was estimated for each pat as (total ßies emerged ⫹ viable pupae)/(number of eggs). Fall emergence was estimated for each fall and spring pat as (total ßies emerged in fall)/(number of eggs). The proportion of pupae in diapause was estimated for each fall pat as (number of viable pupae)/(number of emerged ßies ⫹ number of viable pupae). Overwintering survival was estimated for the Þve spring pats combined as (total number of ßies emerged in spring)/(total number of diapausing pupae in corresponding Þve fall pats), and variance within each set was calculated as the variance of a proportion. Survival to spring emergence was calculated for each spring pat as (total ßies emerged in spring)/(number of eggs). This variable combined fall survival, proportion that diapaused, and overwintering survival, and indicated the proportion of eggs laid on a given date in the fall that ultimately emerged as adults the following spring. Analysis of variance (ANOVA) was used to determine if levels of fall survival, proportion diapause, and spring emergence varied signiÞcantly among the weeks in each year, and means were separated using Fisher least signiÞcant difference (LSD). The mean and variance of fall survival, fall emergence, propor-

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tion in diapause, and survival to spring emergence were calculated for each set, and the relationships between the mean and variance of each variable were examined separately using TaylorÕs power law to select a transformation that would best stabilize variances among the sets. Two-way ANOVA was used to determine if fall emergence varied among weeks and pat types (“fall” versus “spring”), and means were separated using Fisher LSD. Lack of signiÞcant effects for pat type and cohort * type was interpreted to indicate that valid estimates of overwintering survival were made based on the number of pupae determined from fall pats and adult emergence determined from the spring pats. A chi-square test was used to determine if overwintering survival was consistent among cohorts within years, as well as to test if overall overwintering survival for pooled cohorts varied among years. Linear regression was used to assess the relation between fall survival and Tid, and quadratic regression weighted by the number of diapausing pupae was used to determine the relation between overwintering survival and Tsp. The relations were also tested for homogeneity among years. Contribution to Spring Population. Estimates of survival to spring emergence were combined with previously published estimates of ßy density on a nearby herd (Lysyk, 2000) to characterize the recruitment interval for offspring ßies that would have emerged in the following springs. For each week, the number of eggs laid by ßies on the herd was estimated as (mean number of ßies per animal during the week) * (0.5 females per ßy) * (8.7 eggs per female per day) (Lysyk 1991). The contribution of those eggs to the subsequent spring population was adjusted for overwintering survival by multiplying by mean level of survival observed in the matching set of spring pats.

Results and Discussion Temperature Patterns. Air temperatures and pat temperatures declined throughout the experimental periods each year, but were generally warmer in 1991 than in 1992 and 1993 (Fig. 1). Pat temperatures remained above 15⬚C until mid September in 1991, but dropped below 15⬚C in mid-August in 1992 and 1993. Horn ßies emerged from the experimental pats when corresponding pat temperatures averaged ⬎15⬚C while eggs and larvae were developing. As temperatures declined each year, time to 50% emergence increased from 16 to 31, 16 Ð 47, and 18 to 41 d in 1991, 1992, and 1993, respectively. Observed developmental times averaged (⫾SD) 22.9 (⫾7.9) d and were similar to the average 23.4 (⫾7.9) d predicted by the ratesummation model (Fig. 1). Horn Fly Population Dynamics. Total numbers of eggs, numbers of adults that emerged in fall, numbers of diapausing pupae, and numbers of adults that emerged in spring from each set of pats are shown in Table 1. The numbers of insects observed in the different sets ranged from 31Ð 883 in 1991; 3Ð783 in 1992; and 211Ð1,779 in 1993.

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Fig. 1. Mean (solid line), maximum (upper dotted line), and minimum (lower dotted line) daily air and pat temperatures during 1991Ð1993. Horn ßy development in each cohort is indicated in lower panels. For each cohort, solid squares denote dates of 50% emergence, open squares simulated times of 50% eclosion, dotted lines where no fall emergence occurred.

Fall Survival. TaylorÕs regression of set variances and means was ln(variance) ⫽ -3.04 ⫹ 1.27ln(mean) (SEslope ⫽ 0.15; t ⫽ 8.6, df ⫽ 24, P ⬍ 0.0001, r2 ⫽ 0.75), so levels of fall survival were transformed to y0.36 before ANOVA. Fall survival varied signiÞcantly among cohorts in each year (Table 2). During 1991, the arithmetic mean of fall survival ranged from 0.016 ⫾ 0.006 Ð 0.52 ⫾ 0.15, increased with oviposition date from late July to early August, peaked in mid-August, and was relatively constant throughout the remainder of the experimental period, with the exception of a single low value in mid-September Table 1. Alberta

Totals of emerged and diapausing horn flies recovered from experimental manure pats reared in the field at Lethbridge, 1991

Date

Total eggs

31/07 07/08 14/08 21/08 28/08 04/09 11/09 19/09

1,200 1,500 1,800 2,100 1,950 3,000 2,700 750

(Fig. 2A). In 1992, fall survival ranged from 0.28 ⫾ 0.03 on 31 August to 0.002 ⫾ 0.001 on 14 September and was lowest from early September on (Fig. 2A). In 1993, fall survival ranged from 0.73 ⫾ 0.04 on 11 August to 0.01 ⫾ 0.03 on 7 September and was similar among the remaining cohorts (Fig. 2A). Thomas and Morgan (1972) and Miller (1977) estimated 41Ð 45% and 14% immature survival in protected pats, and their values were within the ranges observed in the current study. Fall survival varied among years, but was only weakly related to pat temperatures during develop-

Fall pats

1992 Spring pats

Fall Diap. Fall Spring Date adults pupae adults adults 66 117 463 177 172 0 0 0

0 10 6 221 106 416 22 119

64 140 414 236 283 1 0 0

0 2 0 90 90 193 9 39

27/07 03/08 10/08 17/08 24/08 31/08 08/09 14/09 21/09 28/09

Total eggs 3,000 3,000 3,000 3,000 3,000 3,000 3,000 3,000 3,000 3,000

Fall pats

1993 Spring pats

Fall Diap. Fall Spring adults pupae adults adults 41 200 189 68 1 56 0 0 0 0

128 185 33 172 70 363 36 3 214 27

61 269 285 225 1 1 0 0 0 0

71 129 12 53 21 176 0 0 3 0

date

Total eggs

04/08 11/08 18/08 25/08 01/09 07/09 14/09 21/09

3,000 3,000 3,000 3,000 3,000 3,000 3,000 3,000

Fall pats

Spring pats

Fall Diap. Fall Spring adults pupae adults adults 208 332 10 11 0 0 0 0

546 756 787 551 620 149 498 697

215 273 16 21 0 0 0 0

Total number of eggs was divided evenly among 10 pats, Þve of which were sampled in the same fall, and Þve the following spring.

61 414 320 145 231 62 84 35

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Table 2. Results of significance tests to assess differences in horn fly survival, emergence, and diapause among cohort dates and pat types in 1991, 1992, and 1993 Source

Statistic

Fall survival Cohort Fall emergence Cohort Type C*T Proportion diapause Cohort Spring emergence Cohort Overwintering survival Cohort

1991

1992

1993

Value

df

P

Value

df

P

Value

df

P

F

10.4

7, 32

⬍0.0001

12.4

9, 40

⬍0.0001

16.7

7, 32

⬍0.0001

F F F

46.8 0.3 0.1

7, 64 1, 64 7, 64

⬍0.0001 ⬎0.58 ⬎0.99

70.4 2.4 1.9

9, 80 1, 80 9, 80

⬍0.0001 ⬎0.11 ⬎0.06

119.7 0.1 0.4

7, 64 1, 64 7, 64

⬍0.0001 ⬎0.96 ⬎0.91

F

43

7, 32

⬍0.0001

14.4

9, 34

⬍0.0001

34.1

7, 32

⬍0.0001

7, 32

⬍0.0001

14.4

9, 40

⬍0.0001

6.4

7, 32

⬍0.0001

6

⬍0.0001

281.0

9

⬍0.0001

639.1

8

⬍0.0001

F

9.9

X2

82.9

ment (Fig. 2B). Regression analysis indicated that the slopes of the relation between fall survival and temperature were similar among years (F ⫽ 2.3; df ⫽ 2, 124; P ⬎ 0.10), but that the intercepts varied signiÞcantly among years (F ⫽ 33.9; df ⫽ 2, 124; P ⬍ 0.0001). Fall survival increased slightly with increasing temperature, but temperature alone accounted for only 14% of the variation in fall survival, whereas variation in the intercepts among years accounted for 34% of the variation. The higher intercept in 1993 reßected overall greater survival that year, probably resulting from the pats being held indoors for 24 h to improve egg hatch. Miller (1977) found that exclusion of other insects explained 64% of the variation in horn ßy immature survival, and that addition of temperature and moisture accounted for an additional 10%, so it seems unlikely that temperature during autumn plays a major role in determining fall survival. We determined potential error in calculating survival by using volumetric determination of the number of eggs per pat. Fall survival was recalculated for each pat assuming that the actual number of eggs per pat varied by ⫾ 10% of the number of eggs determined volumetrically. These calculations indicated that the potential error due to volumetric determination was small. Underestimating the number of eggs per pat by 10% would have resulted in survival being overestimated by an average (⫾SD) of 0.02 (⫾0.02), while overestimating the number of eggs would have resulted in underestimating survival by an average of 0.03 (⫾0.02). Fall Emergence. A total of 2,123, 1,397, and 1,086 ßies emerged from fall pats in 1991, 1992, and 1993, respectively (Table 1). The relationship between the mean and variance in fall emergence was ln(variance) ⫽ ⫺2.45 ⫹ 1.45 ln(mean) (SEslope ⫽ 0.08, t ⫽ 17.4, df ⫽ 29, P ⬍ 0.0001; r2 ⫽ 0.91), so fall emergence was transformed to y0.28 before further analysis. Fall emergence varied signiÞcantly among cohorts each year, but was similar between pats sampled in fall and spring (Table 2), and there were also no signiÞcant pat type * cohort interaction. In 1991, ßies emerged from eggs laid up to 28 August, and only a single ßy emerged from

all of the September cohorts (Table 1; Fig. 3). In 1992, fall emergence occurred from eggs laid as late as 17 August, was greatly reduced from the 24 Ð31 August, and did not occur from the 8 September or later (Fig. 3). In 1993, fall emergence occurred from 4 to 11 August was greatly reduced from 18 to 25 August, and was nil from 1 September (day 244) or later (Fig. 4). In Texas, horn ßies emerged from eggs laid as late as October, but not from November (Kunz et al. 1972, Kunz and Cunningham 1977). In Mississippi and Arkansas, emergence in the fall ceased in pats from mid-October onward (Hoelscher and Combs 1971, Klein and Lancaster 1992). Thus, fall emergence ceased 1Ð2 mo earlier in Lethbridge than in the southern localities. Proportion in Diapause. The relationship between the variance and mean of the proportion in diapause was not signiÞcant (F ⫽ 0.2; df ⫽ 1, 12; P ⬎ 0.65), so no transformation was applied. The temporal pattern in proportion of ßies in diapause varied signiÞcantly among cohorts and years (Table 2; Fig. 4). In 1991, diapause was Þrst observed in pupae from eggs laid on 7 August and increased steadily to 1.0 by 4 September (Fig. 4). In 1992, a high incidence of diapause (⬎0.70) occurred in the 27 July cohort, but decreased until 10 August, then increased to nearly 1.0 by 24 August and thereafter. In 1993, the proportion in diapause was ⬇0.70 in the 4 and 11 August cohorts, and was ⬎0.97 thereafter. Depner (1961) observed Þrst diapause in pupae from eggs laid in late July to mid-August in Alberta. In contrast, diapause occurred later in other locations, beginning in pats formed in early to midSeptember in Missouri (Thomas et al. 1987), mid- to late-September in Arkansas (Klein and Lancaster 1992) and Mississippi (Hoelscher and Combs 1971), and early to mid-October in Texas (Kunz et al. 1972; Kunz and Cunningham 1977; Thomas and Kunz 1986). Combined with the present data, there appears to be a clear N-S gradient in date of diapause induction. Overwintering Survival. Overwintering survival was signiÞcantly different among cohorts each year (Table 2; Fig. 5A), ranging from 0 to 0.85, 0 to 0.70, and 0.05 to 0.55 in 1991, 1992, and 1993. In 1991, overwintering

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Fig. 2. (A) Mean fall survival ⫾SE from egg to pupa of horn ßies in artiÞcial pats placed in the Þeld, n ⫽ 5 pats per point. (B) Relationship between mean fall survival ⫾SE and mean pat temperature during development of immature horn ßies, n ⫽ 5 pats. The relationship between transformed fall survival (y) and mean pat temperature (Tid) during the immature developmental period was y ⫽ 0.5036 (⫾0.0529) ⫹ 0.0145 (⫾0.0031)Tid - 0.2018 (⫾0.0413)X1 - 0.3104 (⫾0.0384)X2 (F ⫽ 32.9; df ⫽ 3, 126; P ⬍ 0.0001; r2 ⫽ 0.44), where X1 ⫽ 1 if the year was 1992 and 0 otherwise, and X2 ⫽ 1 if the year was 1993 and 0 otherwise. 1991 (F) solid line, 1992 (‚) dashed line, 1993 (䡺) dotted line.

survival was initially low for the 7Ð14 August cohorts, peaked in the 28 August cohort, then declined thereafter. In 1992, overwintering survival was highest for the 27 JulyÐ3 August cohorts, was reduced for the next four cohorts, then negligible for the cohorts initiated in September. In 1993, overwintering survival was initially low, but increased for the 11 AugustÐ7 September cohorts, then declined. Overwintering survival had a signiÞcant (F ⫽ 11.5; df ⫽ 3, 22; P ⬍ 0.0004; r2 ⫽ 0.51) curvilinear relationship with temperature during the diapause sensitive period (Fig. 5B). The relation-

Vol. 30, no. 6

Fig. 3. Mean proportion of ßies emerged in the fall from “fall” pats (solid symbols) and “spring” pats (open symbols) by date of oviposition. n ⫽ 5 pats per type

ship was y ⫽ ⫺0.4980 ⫹ 0.1018Tsp - 0.0027Tsp2 (SEb0 ⫽ 0.5167; SEb1 ⫽ 0.0332; SEb2 ⫽ 0.0011), where y ⫽ overwintering survival and X ⫽ temperature during the diapause sensitive period. The relationship was not signiÞcantly different among years (F ⫽ 1.46; df ⫽ 6, 16; P ⬎ 0.25). Overwintering survival was low when pat temperatures were ⬍10⬚C during development, and was highest when pat temperatures were in the range 10 Ð20⬚C. Because diapause is not induced when temperatures during the sensitive period exceeded 23⬚C (Lysyk and Moon 1994), we speciÞed overwintering survival ⫽ 0 above 23⬚C. This pattern suggests that larvae produced when it is too cold will be less likely to survive the winter than larvae produced during warmer periods. Larvae produced during colder periods may not be able to become physiologically ready to overwinter.

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Fig. 4. Mean proportion of viable pupae in diapause by date of oviposition, n ⫽ 10 pats. 1991 (F) solid line, 1992 (‚) dashed line, 1993 (䡺) dotted line.

The combined overwintering survival for all cohorts within a year varied signiÞcantly among years (␹2 ⫽ 119.2, df ⫽ 2, P ⬍ 0.0001) and was 0.47, 0.38, and 0.29 during 1992, 1992, and 1993. Average pat temperatures during each winter (01 November to 30 March) showed relatively little variation among years, averaging (⫾SD) 1.0 (⫾3.9), ⫺2.6 (⫾4.5), and ⫺2.0 (⫾4.4)⬚C in 1991, 1992, and 1993. Since the relationship between overwintering survival and temperatures during the diapause sensitive period was homogenous among years, the small amount of variation in winter pat temperatures did not explain either variation in combined overwintering survival between years or the large variation in overwintering survival within each year. In previous studies, survival during diapause averaged 68, 75, and 73% when pupae were stored at ⫺5, 0.5, and 5⬚C (Lysyk 1999), a relatively small effect, providing further evidence that temperatures during diapause do not inßuence overwintering survival. Additionally, pat temperatures are considerably more stable throughout the winter compared with air temperatures (Lysyk 1999). Overwintering survival was generally believed to be quite low (Kunz and Miller 1985). Thomas and Kunz (1986) later concluded that overwintering survival was high (⬎1.0); however, their methods may have underestimated the number of overwintering pupae. Hoelscher et al. (1967) found that at least 60% of diapausing horn ßy pupae were alive when transferred from Þeld to laboratory in January and February. Our estimates suggest that overwintering survival can be quite high, but vary according to the temperatures larvae experience during immature development. Survival to Spring Emergence. The relationship between the variance and mean of survival to spring emergence was ln(variance) ⫽ ⫺2.09 ⫹ 1.47 ln(mean) (SEslope ⫽ 0.09; t ⫽ 16.4;df ⫽ 19; P ⬍ 0.0001; r2 ⫽ 0.93), so survival to spring emergence was transformed to y0.28 before further analysis. Survival to spring emer-

Fig. 5. (A) Mean overwinter survival of horn ßy pupae by date of oviposition, n ⫽ 5 pats. (B). Relationship between mean overwintering survival in cohorts of immatures horn ßies and mean pat temperature during the diapause sensitive period, n ⫽ 5 pats. 1991 (F) solid line, 1992 (‚) dashed line, 1993 (䡺) dotted line.

gence varied signiÞcantly among cohorts each year (Table 2; Fig. 6), and was greatest for the 21 AugustÐ19 September cohorts in 1991, 27 JulyÐ3 August and 31 August cohorts in 1992, and 11 AugustÐ1 September cohorts in 1993. The distribution of survival to spring emergence over time was unimodal in 1991 and 1993, with the highest values occurring over a 5- and 4-wk period, respectively. In 1992, the distribution over time was bimodal, with the highest values occurring over a total period of at least 6 wk. Contribution to Spring Populations. Horn ßy populations on a nearby herd declined throughout the study period each year (Fig. 7). In 1991, we estimated that reproduction during the 21 AugustÐ 4 September cohorts accounted for 92% of the ßies that emerged the following spring. In 1992, reproduction during the 27 JulyÐ3 August cohorts was estimated to account for 57% of the ßies emerging next spring, with an addi-

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Fig. 6. Survival from egg to spring emergence by date of oviposition, n ⫽ 5 pats. 1991 (F) solid line, 1992 (‚) dashed line, 1993 (䡺) dotted line.

tional 30% being added by the 31 August cohort. In 1993, the 11 AugustÐ18 August cohorts were estimated to account for 73% of the ßies that emerged the following spring and reproduction from the 4 AugustÐ25 August cohorts would have accounted for 88%. In all years, reproduction by the cohorts placed out after 7 September made little contribution the spring generation even though adult ßies were present on the animals. Depending on the fall weather, reproduction during a 3- to 6-wk period accounted for the majority of the ßies that emerged in the spring. In Mississippi, 85% of the horn ßies that emerged in the spring arose from pats deposited during a 3- to 5-wk period in late September and October (Hoelscher et al. 1971). In Texas, Thomas and Kunz (1986) estimated that 61% of the overwintering population was produced during a 2-wk period in November. Manure temperatures during the fall appeared to inßuence a variety of processes in the horn ßy. As manure temperatures declined, immature developmental time increased and an increasing proportion of horn ßy pupae entered diapause. Manure temperatures during development were weakly related to survival during the fall, but overwintering survival was related quite strongly to temperatures experienced during the larval developmental period. It appears that immatures destined for diapause must develop sufÞciently to ensure survival through the winter. The relationships between temperature, development, and overwintering survival appear to be major determinants of the recruitment dynamics in fall horn ßy populations, and ultimately determine the number and timing of emerging adults in the following spring. The current results indicate that in a given year, the majority of the founding spring population in the Lethbridge area is likely to have been recruited from eggs laid during a 3- to 6-wk interval in the preceding August and early September. From a practical stand-

Fig. 7. Estimated proportion of the horn ßy population that emerged in spring (lines with points and error bars) originating from eggs laid the previous fall and matching weekly estimates of horn ßy abundance (lines without points) on a nearby herd during the fall (Lysyk 2000).

point, this means that control measures designed to reduce the overwintering reservoir in the area would be most efÞcient if their effects were to coincide with this interval, either by reducing density of ovipositing females or survival of their offspring in manure pats produced during the same interval. Because the onset and duration of the recruitment interval varied among years, efÞciency of efforts to reduce the overwintering reservoir in a given year may be improved to the extent that methods can be developed to predict the timing of diapause induction and the subsequent survival of the resulting pupae.

Acknowledgments The authors are grateful for the expert technical assistance of R. C. Lancaster and P. Coghlin, Lethbridge Research Centre. This is Lethbridge Research Centre Contribution No. 3870061. The work was supported in part by the Minnesota Agriculture Experiment Station and is a contribution to Regional Research Project S-274.

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LYSYK AND MOON: DYNAMICS OF OVERWINTERING IN HORN FLIES References Cited

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Received for publication 19 January 2001; accepted 7 August 2001.