How many monarchs in natural populations are infected with O. elektroscirrha?

(Continued)

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RESULTS

Comparison of assessment techniques

Parasite loads derived from the tape method of disease assessment were correlated highly with loads assessed using the hemacytometer technique (Fig. 2). Examination of this relationship indicates that a sigmoid (3^rd order polynomial) curve best describes the correspondence between the tape and hemacytometer spore counts (Table 1). This nonlinear curve suggests that parasite load categories based on the tape method recognize more variation in low parasite loads than the hemacytometer technique, but may underestimate the large difference in hemacytometer counts between parasite load classes 3 and 4. From a pragmatic perspective, major differences between the two techniques are the increased time and the destructive sampling required by the hemacytometer method. All data described below are based on parasite load categories using the tape method.

Fig. 2. Relationship between the log₁₀ of hemacytometer spore counts and the measure of parasite load class using the tape method of disease assessment. This relationship was best described by a 3^rd order polynomial regression curve (log₁₀ (spore count) = b ₀ + b ₁X + b ₂X² + b ₃X³ + e, where X = parasite load class and coefficients are as follows: b ₀ = 0.171, b ₁ = -1.861, b ₂ = 1.190, and b ₃ = -0.124). Error bars represent 95% confidence intervals. Sample sizes are: class 0: 37, class 1: 11, class 2: 25, class 3: 34, class 4: 43, class 5: 76.

Recent and historical variation in parasite prevalence among North American monarchs

Monarch populations within North America show large differences in the proportion of adults with different parasite loads. In the eastern migratory population, very few adults were infected with any number of O. elektroscirrha spores (Fig. 3a), whereas most adults in the western migratory population showed intermediate or high parasite loads (Fig. 3b). All of the monarchs captured in a continuously breeding population near Miami, Florida had O. elektroscirrha spores, and most of these adults were heavily infected (Fig. 3c).

Fig. 3. Representative sample of the frequency distribution of parasite loads in three North American monarch populations: (a) eastern migratory population, (b) western migratory population, (c) southern Florida population. See text for description of parasite load classes. c ² -analysis of the association between infection class (0-5) and population (a-c) shows that differences in the distribution of parasite loads are highly significant (c ² = 1087.5, d.f. = 10, p < 0.001).

Examination of butterflies in past collections suggests that population differences in the prevalence of heavily infected monarchs have persisted over time (Fig. 4), although changes in prevalence may have occurred during the large time intervals between samples. Across all years, the prevalence of heavily infected monarchs in the eastern migratory population was less than 8%, and this prevalence was highest during the years 1977-1981. The prevalence of heavy infection in the western migratory population was approximately 30% for each of the 4 years sampled. It is important to note however that more than 10 years separate two of the western samples. In the southern Florida population, prevalence varied among years but was always higher than 70%.

Fig. 4. Prevalence of heavily infected adults (parasite load classes 4 and 5) over time for each of three North American monarch populations. Sample sizes, locations, and dates are shown in Appendix A.

Short-term temporal and spatial variation in parasite prevalence in North American monarchs

Eastern migratory population. To examine whether the frequency of high and low parasite loads varied with seasonal host behavior in eastern North America, I divided samples collected from 1993 to 1997 into the following three categories: breeding, migrating south, and overwintering (Appendix B). Although the prevalence of heavily infected adults varied among sampling dates, no association between behavior category and the proportion of adults with high parasite loads was evident (Fig. 5). However, behavior category did have a significant effect on the proportion of monarchs with low parasite loads. The proportion of adults with low parasite loads was lowest among summer breeding monarchs and highest among those captured overwintering (Fig. 5). This indicated that the prevalence of low parasite loads increased throughout the monarchs’ annual cycle.

Fig. 5. Variation in parasite prevalence among adults in the eastern migratory population as a function of behavior at time of capture. Yellow line plots the prevalence of heavy infection (classes 4 and 5), and green line shows the proportion of adults with low parasite loads (classes 1, 2, and 3). Points represent weighted averages for samples collected from 1993 to 1997. Error bars represent 95% confidence intervals based on total number of butterflies combined across years. Sample sizes, dates, and locations are shown in Appendix B.

During one overwintering season (1993-94), adults were obtained from 7 separate colonies in Central Mexico for each month (November - March). These samples were divided into three overwintering phases: early (November), middle (December, January), and late (February, March). The proportion of heavily infected adults was very small and remained nearly constant throughout the overwintering period, but the proportion of adults with low parasite loads increased between the early and middle overwintering phases (Table 1; Fig. 6a).

Table 1. Temporal and spatial variation in the prevalence of monarchs with high and low parasite loads during the 1993-94 overwintering season in Central Mexico. For locations, see Calvert & Brower (1986) and Alonso (1996). Sample sizes range from 100 to 200 individuals per site per phase. Early, middle, and late phases are described in the text. Proportions represent the number of monarchs with either low (class 1, 2, and 3) or high (class 4 and 5) parasite loads over the total number of butterflies sampled. (The proportion of monarchs with no parasites is not shown.)

Western migratory population. For one overwintering season, monarchs were collected at 10 separate colonies along the coast of California for 5 months (November 1989 - March 1990). The overwintering period was again divided into early, middle, and late phases, as above. The proportion of heavily infected adults declined slightly throughout the overwintering period, and the proportion of monarchs with low parasite loads increased from early to late overwintering phases (Table 2; Fig. 6b).

Table 2. Spatial and temporal variation in disease prevalence among monarchs in western North America during the 1989-90 overwintering season (from L.P. Brower & W.H. Calvert, unpublished). Sample sizes range from 20 to 80 individuals per site per phase. Early, middle, and late phases are described in the text. Proportions represent the number of monarchs with either low (class 1, 2, and 3) or high (class 4 and 5) parasite loads over the total number sampled.

Fig. 6. Parasite prevalence in monarchs throughout early, middle, and late overwintering phases, shown as the proportion of heavily infected adults (yellow line) and those with low parasite loads (green line). (a) Eastern migratory population, from five overwintering sites in central Mexico, November 1992 to March 1994, (b) western migratory population, from seven overwintering sites along the California coast, November 1989 to March 1990. Error bars show 95% confidence intervals. See Tables 1 and 2 for a description of specific sampling locations.

In summer 1997, breeding monarchs were sampled at 12 locations throughout western North America (Appendix C). Linear regression was used to quantify how average parasite loads (based on the 0-5 scale) were affected by the distance between breeding location and the closest overwintering site, measured to the nearest kilometer (Fig. 7). The response variable was the average parasite load of adults for each breeding location, and regression analysis was weighted by the number of observations within each location due to unequal sample sizes (Weisberg 1985). Average parasite loads declined significantly with increasing distance from overwintering sites (Fig. 7; b = - 0.002, T = -2.44, p < 0.05).

Fig. 7. Geographical variation in average parasite loads among summer breeding monarchs in western North America. Distance (km) was measured between the collection site and the nearest overwintering location. Error bars show 95% confidence intervals. Sample sizes and collection sites are presented in Appendix C.

Southern Florida population. Temporal variation in parasite prevalence in southern Florida was evaluated using monarchs collected at monthly intervals between December 1994 and November 1995 (Fig. 8). Although the prevalence of heavy infection varied from month to month, these changes did not follow a consistent temporal trend. The proportion of monarchs with high parasite loads was lower in October and November than at other times of the year (Fig. 8). This coincides with the time when the larger eastern population is migrating south. The proportion of heavily infected monarchs collected nearby in Cuba in November 1995 and 1996, and in southern Florida in November 1970, were statistically similar to the November 1995 Florida sample (c ² analysis: c ² = 4.32, d.f. = 3, p = NS; Fig. 8).

Fig. 8. Prevalence of heavily infected adults (classes 4 and 5) near Miami, Florida between December 1994 and November 1995. To the right of the vertical yellow line is shown the prevalence of heavily infected adults for three other samples collected in November in Cuba and southern Florida (showing disease prevalence similar to Miami for November 1995). Error bars represent 95% confidence intervals.

Parasite prevalence in other populations

Samples of breeding monarchs collected in Australia and South America show that O. elektroscirrha has a wide geographic distribution, with infected monarchs present at all sampling locations (Fig. 9). Within Australia, monarchs from Sydney (SE Australia) showed the highest prevalence of heavy infection (0.39), while monarchs obtained farther north from Mt Crosby (near Brisbane, E Australia) had a lower prevalence of heavy infection (0.27). A sample of adults from Rockhampton (on the coast of Queensland, north of Brisbane) had the lowest prevalence of heavily infected adults (0.083). A c ² analysis of these 3 Australian populations showed that the proportions of heavily infected adults were significantly different (c ² = 6.87, d.f. = 2, p < 0.05). Monarchs from northern South America (Colombia and Venezuela) had infection levels similar to those in Rockhampton, Australia (proportion heavily infected = 0.11 and 0.17, respectively). No monarchs collected in Trinidad in 1968 were infected with spores, although this sample was very small (11 adults).

Fig. 9. Between-population comparisons of parasite prevalence for North America, South America, and Australia. Bars show the frequency of heavily infected monarchs (classes 4 and 5) with 95% confidence intervals. Sample dates and sizes for Australian and South American data are shown in Appendix A. Prevalence for the eastern migratory population in North America is for March 1996, Sierra Chincua, Mexico, prevalence for the western migratory population is combined across five overwintering colonies along the California coast in February 1997, and prevalence for the southern Florida population is pooled for December 1994-April 1995.

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