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Keywords:

  • Bombus;
  • Conopidae;
  • foraging;
  • mortality;
  • parasitoid;
  • Phoridae

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Abstract 1. Phorid (Diptera, Phoridae) and conopid (Diptera, Conopidae) parasitism among four North American bumble-bee (Hymenoptera, Apidae) species was investigated. Male bumble-bees experienced a significantly higher incidence of parasitism by the phorid, Apocephalus borealis Brues, and a significantly lower incidence of parasitism by the conopid, Physocephala texana Williston, than did workers.

2. The incidence of parasitism by A. borealis and P. texana varied between bumble-bee sexes and species in patterns that did not reflect differences in relative host abundance. Differences in foraging behaviour between bumble-bee workers and males, as well as between species, may explain these results.

3. Bumble-bee workers and males parasitised by A. borealis had significantly shorter lifespans than unparasitised bees. Based on previous estimates of bumble-bee mortality, A. borealis parasitism may reduce worker lifespans by up to 70%. In contrast, the mortality rate of bees parasitised by P. texana was not significantly different from that of unparasitised bees.

4. These results contrast with previous work highlighting the importance of conopid parasitism to bumble-bee populations, and suggest that phorid parasitism may impose greater costs to bumble-bees than does conopid parasitism in local populations.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Parasitoids can influence or regulate host populations (Beddington et al., 1978; Hassell, 1986; Godfray, 1994), thereby affecting the structure of ecological communities (Freeland, 1983; Lawton, 1986; Price et al., 1986). Such community effects may be highly variable as parasitism risk can differ both intra- and inter-specifically among hosts when co-existing hosts differ in quality or susceptibility to parasitoids. For example, differential parasitism risk among host species arising from parasitoid host preference may determine the outcome of competitive interactions between hosts for limited resources (Feener, 1981; Orr et al., 1995). Conversely, differential parasitism risk within host populations may stabilise host–parasitoid population dynamics if parasitism is sufficiently aggregated in space or time (Münster-Swendsen & Nachman, 1978; Chesson & Murdoch, 1986; Walde & Murdoch, 1988).

Parasitoid conopid and phorid flies attack bumble-bees (Bombus), inserting eggs on or within a bee's body. Such attacks probably occur while bees are foraging at flowers. Conopid larvae develop one per host by feeding on internal tissue and haemolymph, eventually killing the host (Pouvreau, 1974; Schmid-Hempel & Schmid-Hempel, 1988; Müller et al., 1996). By increasing worker mortality (Schmid-Hempel & Schmid-Hempel, 1988, 1989, 1990) and altering foraging behaviour (Heinrich & Heinrich, 1983; Schmid-Hempel & Schmid-Hempel, 1990; Müller & Schmid- Hempel, 1993), conopid parasitism may reduce the size of bumble-bee colonies and investment in reproductive offspring, as well as skewing host population sex ratios (Müller & Schmid-Hempel, 1992a; MacFarlane et al., 1995). Although conopid parasitoids commonly attack bumble-bees in Europe, where incidences of parasitism range between 30 and 70% (Schmid-Hempel et al., 1990), little is known about their infestation of bumble-bees in North America.

The phorid fly, Apocephalus borealis Brues (Diptera, Phoridae), is also known to parasitise bumble-bees (Brown, 1993; Disney, 1994); multiple larvae develop in each host and feed primarily on thoracic flight muscle (Ennik, 1973; Disney, 1994). De Prins and Disney (unpublished; cited by Disney, 1994) found an incidence of infestation of 10% in B. vosnesenskii from western North America, and incidences of 5% are known from bumble-bees in eastern North America (C. Cormier and D. McCorquodale, pers. comm.). Despite the broad distribution of A. borealis throughout North America (Brown, 1993), virtually nothing is known about its biology and association with bumble-bees.

Conopid parasitism frequently differs among bumble-bee species, sexes, and among conspecific nectar and pollen collectors in proportions that do not reflect differences in relative abundance (Schmid-Hempel et al., 1990; Schmid-Hempel & Schmid-Hempel, 1996a). Such non-random patterns of infestation suggest that conopids may be an important selective agent on the life-history traits of bumble-bees. Although differences in the incidence of parasitism between conspecific nectar and pollen collectors have been explained primarily by behavioural changes in bumble-bee foraging induced by parasitism (Schmid-Hempel & Schmid-Hempel, 1991), inter-sexual and inter-specific differences in parasitism are largely uninvestigated. For example, male bumble-bees consistently experience a lower incidence of conopid parasitism than do workers (MacFarlane & Pengelly, 1974; Schmid-Hempel & Schmid-Hempel, 1988; Maeta & MacFarlane, 1993). Further, conopid parasitism may be less common among bumble-bee species with more specialised flower visiting habits (Maeta & MacFarlane, 1993).

The purpose of the work reported here was twofold: to investigate the local prevalence (proportion of bees infected) and associated host mortality of conopid and phorid parasitoids of bumble-bees, and to determine whether intra- and inter-specific differences in conopid and phorid prevalence occur among co-existing bumble-bee species. The relative importance of a bumble-bee's species, sex, size, and resource (pollen and nectar) collection to their risk of parasitism was investigated.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Data collection

The bumble-bee fauna at the study site near Barrier Lake, in southern Alberta, Canada (51°01′N, 115°04′W) includes 17 species of Bombus and three species of the socially parasitic Psithyrus. Collecting efforts focused primarily on Bombus workers and males during summer 1998 and 1999. Here data are presented on only the four most abundant species, B. bifarius Cresson, B. occidentalis Greene, B. flavifrons Cresson, and B. californicus Smith. During 1998, sampling took place from 5 May to 20 August, and during 1999 from 4 June to 2 September. Because queens were rarely infested with dipteran endoparasitoids in 1998 (< 5%, n = 75), they were not collected in 1999 to avoid unnecessary removal of queens from the population. Samples were taken every 7–14 days depending on weather conditions. Two or three observers walked various paths within the study site, capturing all visible foraging workers and males using sweep nets and storing them in individual 7-dram vials for live transfer to the laboratory. Samples were taken during both the morning and afternoon of each collecting period. Bees were captured on a variety of plant species to avoid any bias in bee species composition resulting from bee foraging preferences.

After capture, bees were transported to the laboratory where they were housed individually in 7-dram vials and provided with sugar water ad libitum (60:40 distilled water : sugar). Bees were sexed and identified to species and, in the case of workers, classified as either pollen or nectar collectors based on the presence or absence of pollen in their corbiculae. After a bee died, the residual lifespan (number of days each bee remained alive from the day of capture) was recorded. The right forewing was removed and measured (proximal end of median plate to distal end of radial cell) as an indicator of bee body size (Harder, 1982). Bees were dissected to determine whether any parasitoids were present. Bees containing parasitoid larvae were left undisturbed for several days to allow larvae to complete development and, in the case of phorids, emerge from the host. Conopid puparia were removed from their host and held at ≈ 5 °C for several months then placed at room temperature (≈ 21 °C) with a constant light–dark cycle (LD 16:8 h) until adults emerged (≈ 1 month later). Phorid puparia were held at room temperature in vials with moist cotton until adults emerged (≈ 3 weeks later). All conopids were Physocephala texana Williston (based on Camras, 1996); all phorids were Apocephalus (Mesophora) borealis Brues (B. V. Brown, pers. comm.).

Statistical analyses

Residual lifespans were compared between parasitised and unparasitised bees using the Wilcoxon two-sample test (Proc NPAR1WAY; SAS Institute, 1998) because the probability of death was not constant. Bees often died within 1 day of capture, presumably from stress-related factors associated with capture. These bees were excluded from survivorship analyses to minimise the mortality effects arising from the collecting procedure. Removal of this age class did not affect statistical conclusions. No B. californicus collected during 1998–1999 contained conopid larvae so this species was removed from survival analyses pertaining to conopid parasitism. Residual lifespans were very similar between bumble-bee species and years so data were pooled among species and years for all survival analyses.

The prevalence of conopid and phorid parasitism did not differ significantly between years for workers or males so data were pooled for both sampling years to obtain average prevalences. Comparisons of parasitoid prevalence between host sexes, species, pollen and nectar collectors, years, and by host size were performed using logistic regression (McCullagh & Nelder, 1989) (Proc GENMOD; SAS Institute, 1998). The best model was chosen by starting from a saturated model then removing all main effects and interactions with non-significant (α = 0.05) effects. In each case, parasitism (yes or no) was the response variable, and host sex, species, pollen collection, and host size were explanatory variables. The experiment-wise type I error rate was adjusted for post hoc comparisons using the Dunn–Šidák method (Sokal & Rohlf, 1995).

The incidence of multiparasitism was analysed with 2 × 2 contingency tables utilising the G-test of independence (Sokal & Rohlf, 1995).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Phorid and conopid parasitism of bumble-bees was markedly seasonal, occurring only in mid to late summer. The duration of phorid activity typically encompassed that of conopids, both starting earlier and ending later in the season (Fig. 1a). Phorid prevalence was typically higher than that of conopids, particularly during their peak in mid summer (Fig. 1b).

image

Figure 1.  (a) Seasonal phenology of four Bombus species (workers and males combined) during 1998. Bars indicate duration of phorid and conopid activity. Sample sizes are indicated in parentheses. (b) Incidence of conopid and phorid parasitism for bumble-bees (workers and males combined) during 1998; horizontal bars indicate approximate observed flight times of workers (total length of bar) and males (shaded) of two representative species of Bombus.

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The prevalence of multiparasitism (both phorid and conopid larvae occurring in a single bee) was rare and did not differ significantly between workers and males (mean ± SE, workers: 1.20 ± 0.32%, n = 831; males: 0.90 ± 0.74%, n = 111; G = 0.083, d.f. = 1, P = NS). Phorid and conopid parasitism occurred independently so that parasitism by either phorids or conopids did not predispose hosts to multiparasitism (workers: G = 0.01, d.f. = 1, P = NS; males: G = 0.66, d.f. = 1, P = NS).

Phorid parasitism

Differences among host sexes and species

Male bumble-bees experienced a significantly higher incidence of phorid parasitism than did workers (G = 11.57, d.f. = 1, P < 0.001; Fig. 2). Further, males contained significantly more phorid larvae than did workers (mean number of larvae, 95% CI; males: 11.50, CI 9.35–13.65; workers: 6.57, CI 5.82–7.32; Kruskal–Wallis, χ2 = 20.05, d.f. = 1, P < 0.001).

image

Figure 2.  Mean (± 95% CI) incidence of phorid and conopid parasitism among worker and male Bombus, 1998–1999 data pooled. Different letters indicate significant differences at P < 0.05 (see text for statistics). Sample sizes are indicated in parentheses.

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Among workers, phorid prevalence differed among bumble-bee species but not between years. In particular, phorid prevalence was significantly higher among B. occidentalis than among either B. flavifrons or B. californicus (B. occidentalis vs. B. flavifrons, G = 12.06, d.f. = 1, P < 0.001; B. occidentalis vs. B. californicus, G = 11.70, d.f. = 1, P < 0.001; Fig. 3a), and significantly higher among B. bifarius than among B. californicus (G = 5.86, d.f. = 1, P < 0.05; Fig. 3a). Phorid prevalence did not, however, differ significantly between B. bifarius and B. occidentalis (G = 2.44, d.f. = 1, P = NS; Fig. 3a), B. flavifrons and B. californicus (G = 0.97, d.f. = 1, P = NS; Fig. 3a) or B. bifarius and B. flavifrons (G = 4.87, d.f. = 1, P = NS; Fig. 3a). Observed differences in phorid prevalence among bee species were consistent between years, as shown by the absence of a significant species × year interaction (G = 4.23, d.f. = 1, P = NS). Within bee species, phorid prevalence varied considerably, particularly in B. bifarius (range 3–67%) and B. occidentalis (13–56%), but less so in B. flavifrons (10–25%) and B. californicus (5–20%). The observed patterns of phorid prevalence among heterospecific bumble-bee workers were not explainable in terms of differences in host species abundance, e.g. more abundant host species experiencing higher incidences of parasitism. The proportion each bee species comprised out of the total catch for each sampling day correlated negatively with phorid prevalence (Spearman's r = −0.64, n = 17, P < 0.01). The negative correlation between bee species abundance and phorid prevalence probably results from relatively high phorid prevalence among B. bifarius and B. occidentalis despite the relative scarcity of these species late in the summer (Fig. 1a).

image

Figure 3.  Mean (± 95% CI) incidence of phorid parasitism among bumble-bee species for pollen- and nectar-collecting workers (a) combined and (b) separately. 1998–1999 data pooled. Different letters indicate significant differences at P < 0.05 (see text for statistics). In (b), lower case letters indicate comparisons among nectar collectors, upper case among pollen collectors. *Indicates within-species differences at P < 0.05 (see text for statistics). Sample sizes are indicated in parentheses.

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Differences among pollen and nectar collectors

The incidence of phorid parasitism differed among host species for pollen-collecting workers but not for nectar-collecting workers. Among pollen collectors, B. occidentalis experienced significantly higher parasitism than B. bifarius, B. flavifrons, and B. californicus (B. occidentalis vs. B. bifarius, G = 8.75, d.f. = 1, P < 0.01; vs. B. flavifrons, G = 17.78, d.f. = 1, P < 0.001; vs. B. californicus, G = 14.23, d.f. = 1, P < 0.001; Fig. 3b). The incidence of phorid parasitism did not differ among host species for nectar collectors (all P = NS; Fig. 3b). Within bee species, phorid parasitism was significantly more common among pollen collectors than among nectar collectors for B. occidentalis (G = 9.71, d.f. = 1, P < 0.01; Fig. 3b) but not for B. bifarius, B. flavifrons, or B. californicus (all P = NS; Fig. 3b).

Differences according to host size

During 1998 and 1999, changes in the mean body size of workers over the sampling period did not differ between phorid parasitised and unparasitised bees for any of the bumble-bee species. Bombus bifarius workers parasitised by phorids were larger than unparasitised conspecifics during 1998 (G = 6.06, d.f. = 1, P < 0.05). In 1999, phorid parasitised B. californicus workers were significantly smaller than unparasitised conspecifics (G = 6.05, d.f. = 1, P < 0.05). Otherwise, there were no significant size differences in either 1998 or 1999 between phorid parasitised and unparasitised workers (all P = NS).

Host mortality

Unparasitised workers survived an average (± SE) of 11.22 ± 0.37 days (n = 599) after capture, considerably longer than those parasitised by phorids: 3.69 ± 0.12 days (n = 91) (z = −8.48, P < 0.001; Fig. 4a). Unparasitised males survived an average (± SE) of 13.03 ± 0.80 days (n = 101) after capture, also significantly longer than those parasitised by phorids, 4.02 ± 0.24 days (n = 32) (z = −6.50, P < 0.001; Fig. 4b). Among parasitised bees, residual lifespan correlated negatively with number of larvae per bee in males (Spearman's r = − 0.44, P < 0.05) but not in workers (Spearman's r = − 0.14, P = NS).

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Figure 4.  (a) Survivorship curves for phorid and conopid parasitised and unparasitised Bombus workers 1998–1999 data pooled. (b) Survivorship curves for phorid parasitised and unparasitised Bombus males 1998–1999 data pooled.

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Conopid parasitism

Differences among host species and sexes

Male bumble-bees experienced a significantly lower incidence of conopid parasitism than did workers (G = 11.86, d.f. = 1, P < 0.001; Fig. 2). Further, conopid parasitism occurred less often than phorid parasitism in males (G = 0.64, d.f. = 1, P < 0.001; Fig. 2) but not in workers (G = 0.03, d.f. = 1, P = NS; Fig. 2).

The incidence of conopid parasitism differed among bumble-bee species but not among years. No B. californicus workers were found to contain conopid larvae during 1998–1999, and their incidence of parasitism (or lack of) was significantly lower than each of the other three host species (B. californicus vs. B. bifarius, G = 8.97, d.f. = 1, P < 0.01; vs. B. occidentalis, G = 13.50, d.f. = 1, P < 0.001; vs. B. flavifrons, G = 20.03, d.f. = 1, P < 0.001; Fig. 5a). Conopid prevalence differed weakly between B. bifarius and B. flavifrons (G = 4.26, d.f. = 1, P < 0.05; Fig. 5a) whereas all other comparisons of conopid prevalence between species were non-significant (all P = NS). Conopid parasitism was too rare among males (1.8%, n = 111) to test for differences among species. Among workers, patterns of conopid prevalence among bee species were consistent between years, as shown by the absence of a significant species × year interaction (G = 0.03, d.f. = 1, P = NS). The incidence of conopid parasitism among workers varied somewhat within years, but a range of 5–20% was typical of all host species. Differences in the incidence of conopid parasitism among heterospecific bumble-bee workers were not explainable in terms of differences in host species abundance; the proportion each bee species comprised out of the total catch for each sampling day was not correlated with the incidence of conopid parasitism (Spearman's r = −0.51, n = 11, P = NS).

image

Figure 5.  Mean (± 95% CI) incidence of conopid parasitism among bumble-bee species for pollen- and nectar-collecting workers (a) combined and (b) separately. 1998–1999 data pooled. Different letters indicate significant differences at P < 0.05 (see text for statistics). In (b), no significant differences in the incidence of conopid parasitism were found among or within species between nectar collectors and pollen collectors. Sample sizes are indicated in parentheses.

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Differences among pollen and nectar collectors

The incidence of conopid parasitism did not differ significantly between host species for either pollen- or nectar-collecting workers (all P = NS; Fig. 5b). Within species, the incidence of conopid parasitism did not differ between pollen- and nectar-collecting workers for any of the host species (all P = NS; Fig. 5b).

Differences according to host size

During 1998 and 1999, changes in the mean body size of workers over the sampling period did not differ between conopid parasitised and unparasitised bees for any of the bumble-bee species. Bombus flavifrons workers parasitised by conopids were larger than unparasitised conspecifics in 1998 (G = 4.50, d.f. = 1, P < 0.05). Otherwise, there were no size differences in either year between conopid parasitised and unparasitised workers (all P = NS).

Host mortality

Surprisingly, unparasitised workers did not survive significantly longer than those parasitised by conopids [average residual lifespan (± SE), unparasitised: 11.22 ± 0.37 days (n = 599); parasitised, 9.66 ± 0.48 days (n = 65) (z = 0.42, P = NS; Fig. 4a)]. Indeed, during the first 8 days after capture, workers parasitised by conopids had a lower mortality rate than unparasitised workers. Survivorship of males parasitised by conopids was not analysed as only two collected males (one B. occidentalis and one B. flavifrons) contained conopid larvae.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

At Barrier Lake, the phorid parasitoid A. borealis probably affected bumble-bees more than the conopid parasitoid P. texana. Phorids parasitised bees during a longer period (Fig. 1a), at higher frequencies (Figs 1b and 2), and imposed greater host mortality (Fig. 4) than did conopids. The average phorid prevalence at Barrier Lake was twice the 5–10% range reported previously (Brown, 1993; Disney, 1994), peaking at nearly 50% in mid summer (Fig. 1b).

Phorid parasitism of bumble-bees

At Barrier Lake, phorid prevalence differed among bumble-bee species (Fig. 3a). Because bee-species abundance did not correlate positively with phorid prevalence, it seems unlikely that differences in the seasonal abundance of host species can explain the observed patterns in phorid prevalence (e.g. more abundant bee species experiencing higher prevalence). In addition, there was little evidence that host size differed consistently between phorid parasitised and unparasitised bumble-bees. Further investigation of host selection by A. borealis is in progress.

Phorid prevalence differed among pollen-collecting but not among nectar-collecting workers (Fig. 3b); however the interpretation of differences in prevalence among pollen collecting workers is hampered by a lack of information about the cause and effect relationship between parasitism and pollen collection. On the one hand, variation in parasitism between pollen and nectar collectors may arise because the risk of infection differs according to host foraging behaviour. For example, differences in pollen and nectar collecting between bumble-bee species, as well as differences in plant species preference among bumble-bee species (e.g. Brian, 1957; Liu et al., 1975; Heinrich, 1979), may contribute to these trends if A. borealis locates hosts non-randomly with respect to plant species. Alternatively, parasitism may alter the propensity of hosts to collect pollen. Schmid-Hempel and Schmid-Hempel (1991) found that fewer B. pascuorum workers harbouring late-instar conopid larvae collected pollen than did unparasitised conspecifics. If parasitism alters host behaviour such that infested bumble-bees are more or less likely to collect pollen than uninfested bees, this result should be generally consistent between host species. In this study, however, the relative incidence of parasitism for pollen and nectar collectors differed among host species (Fig. 3b), making this explanation less feasible.

Phorid parasitism reduced the survival of bumble-bees severely after capture. Bumble-bees containing phorid larvae had considerably shorter residual lifespans than unparasitised bees and, at best, survived less than half as long as worker bumble-bees survive in the field (for lifespan of field bumble-bees, see Rodd et al., 1980). Further, the residual lifespans of bees parasitised by phorids varied little within and among species and between sexes, suggesting that the rate of development of A. borealis larvae and their impact on bee lifespan is very consistent. Consequently, the observed mortality effects of phorid parasitism (Fig. 4) probably constitute real costs for bees. Based on Rodd et al.'s (1980) estimates of bumble-bee worker mortality, the results presented here suggest that phorids may reduce the average lifespan of workers by up to 70%. Although rates of male bumble-bee mortality are not known, it seems reasonable to suggest that phorids reduce the lifespan of males significantly. Phorid-induced mortality of workers may diminish the resources (pollen and nectar) gathered for colony growth. In turn, reduced colony size could ultimately decrease the number and/or quality of sexuals (males and queens) produced (Owen et al., 1980; Müller & Schmid-Hempel, 1992a,b).

The residual lifespan of parasitised males, but not workers, varied negatively with the number of A. borealis larvae. Further, males parasitised by phorids contained significantly more phorid larvae than did workers. Such a negative relationship between residual lifespan and parasitoid load may represent an increasing mortality effect at high levels of infestation (i.e. many larvae per bee) or higher levels of superparasitism (hosts containing larvae from multiple phorid females) in older bees.

Conopid parasitism of bumble-bees

Conopid prevalence among bumble-bees at Barrier Lake (Figs 2 and 3a) was less than half that reported from Europe (Schmid-Hempel & Schmid-Hempel, 1988; Schmid-Hempel et al., 1990; Shykoff & Schmid-Hempel, 1991), where conopids parasitised 5–10% of males and 20–30% of workers. Although the results presented here agree quite closely with other North American data (MacFarlane & Pengelly, 1974), more work is necessary to determine whether conopid parasitism is typically less common in North America than in Europe. At least in Europe (Schmid-Hempel & Schmid-Hempel, 1988, 1996a; Schmid-Hempel et al., 1990) and Japan (Maeta & MacFarlane, 1993), the presence of both Physocephala and Sicus conopids contributes to the higher incidence of bumble-bee parasitism than at Barrier Lake, where only Physocephala occurred. For example, Schmid-Hempel and Schmid-Hempel (1996a) found that bumble-bees in northern Switzerland were parasitised most often by Sicus ferrugineus Latreille, whereas parasitism by Physocephala rufipes Fabricius accounted for less than half of the total conopid parasitism. Indeed, greater conopid diversity in the Palaearctic than in the Nearctic has been suggested to pose a substantially greater risk to certain bee species (e.g. Megachile rotundata Fabricius) (Doroshina, 1991).

In contrast to B. bifarius, B. occidentalis, and B. flavifrons, which experienced a similar incidence of conopid parasitism, no B. californicus workers collected during 1998–1999 contained conopid larvae or eggs. Because B. californicus is a late-season bee at Barrier Lake, their relative scarcity during the period of conopid activity (Fig. 1a) may explain this result. Similarly, Schmid-Hempel and Schmid-Hempel (1988) and Schmid-Hempel et al. (1990) found particularly low incidences of conopid parasitism among B. pratorum and B. hortorum, species that are active primarily during early summer (for bumble-bee phenologies, see Prys-Jones & Corbet, 1987), prior to conopid activity; however the occurrence of conopid parasitism in B. californicus workers was still significantly lower than that among other species when considering only late summer sampling dates (1998, G = 22.84, d.f. = 1, P < 0.001; 1999, G = 8.15, d.f. = 1, P < 0.01), suggesting that host species phenology alone cannot explain this pattern.

Another explanation for the low incidence of conopid parasitism among B. californicus workers is that P. texana does not seek hosts at the plant species favoured by B. californicus. At Barrier Lake, B. californicus is a relatively long-tongued bumble-bee and foraged almost exclusively from flowers with relatively deep corollas, particularly Castilleja spp. and Trifolium pratense. In contrast, P. texana is a more catholic flower visitor, frequenting the relatively shallow flowers of composites for nectar (Freeman, 1966; Smith & Peterson, 1987). Such differences in flower-visiting habits may result in a low risk of conopid parasitism for B. californicus workers if conopids use flowers as both nectar sources and host-location sites. Indeed, Maeta and MacFarlane (1993) observed that European bumble-bee species with more specialised flower-visiting habits experience lower levels of conopid parasitism. Further, in some eastern Canadian populations, workers of the relatively long-tongued bumble-bee species, B. fervidus, experience a substantially lower incidence of conopid parasitism than other bumble-bee species (C. Cormier and D. B. McCorquodale, pers. comm.).

Surprisingly, at Barrier Lake, workers parasitised by conopids died at a similar rate to unparasitised workers (Fig. 2a). In contrast, studies in Europe have found conopid parasitism to increase bumble-bee mortality (Schmid-Hempel & Schmid-Hempel, 1988, 1989, 1991). The effect of conopid parasitism on worker survival found in this study probably differs from the results of Schmid-Hempel and Schmid-Hempel (1988, 1989, 1991) because unparasitised bees in this study had considerably shorter lifespans after capture than those in European studies. For example, the mean lifespan for unparasitised workers reported here (11.22 days) is less than half of that found by Schmid-Hempel and Schmid-Hempel (1991) (23.2 days). Despite this difference, the average residual lifespan of workers parasitised by Physocephala conopids at Barrier Lake (9.66 days) is very similar to that estimated from European studies (8.3 days; Schmid-Hempel & Schmid-Hempel, 1989) and to the estimated development time of a Physocephala conopid larva (11.4 days; Schmid-Hempel & Schmid-Hempel, 1996b). Based on these results, it appears that the mean lifespan of workers parasitised by Physocephala conopids is consistently close to previous estimates of the mean lifespan of workers in the field (13.2 days; Rodd et al., 1980). Consequently, significant worker mortality arising from conopid parasitism may not be apparent in all bumble-bee populations and is unlikely to be a general influence on bumble-bee life-history traits, such as colony investment into sexuals and population sex ratio, as suggested previously (e.g. Schmid-Hempel & Schmid-Hempel, 1988; Müller & Schmid- Hempel, 1992a,b).

Contrary to expectation, at Barrier Lake, workers parasitised by conopids displayed a lower mortality rate than unparasitised bees during early residual lifespan classes (1–9 days). This pattern may indicate that female conopids tend to parasitise relatively young bees. Schmid-Hempel and Schmid-Hempel (1996b) estimated the developmental period of conopid larvae to be 11 days, which is very close to the average residual lifespan reported here for unparasitised bees. Consequently, only young bees are likely to live long enough for successful development of conopid larvae, favouring active selection of young bees by female conopids. Indeed, Schmid-Hempel and Schmid-Hempel (1991) estimated (via fat body condition, a correlate of bee age) that B. pascuorum workers parasitised by conopids were significantly younger than unparasitised conspecifics. Consequently, young bees parasitised by conopids may survive better shortly after capture than unparasitised bees, which on average are older.

Differences in phorid and conopid prevalence among bumble-bee workers and males

Male bumble-bees experienced consistently less parasitism by conopids than workers, both in this study (Fig. 2) and in other populations (MacFarlane & Pengelly, 1974; Schmid-Hempel & Schmid-Hempel, 1988; Maeta & MacFarlane, 1993). Interestingly, male bumble-bees at Barrier Lake experienced significantly higher rates of phorid parasitism than workers (Fig. 2); however because phorid and conopid parasitism were found to occur independently of one another, it is unlikely that such contrasting incidences of parasitism are the result of phorid larvae outcompeting conopid larvae in cases of multiparasitism. Further, similarly low rates of conopid parasitism in males have been observed at sites with comparable incidences of conopid parasitism, yet where phorids are absent (T. L. Whidden and M. C. Otterstatter, unpublished).

Alternatively, intersexual differences in the incidence of phorid and conopid parasitism may reflect differences in the ecology of worker and male bumble-bees. After leaving their parent colony, males remain in the field during both day and night, whereas workers return frequently throughout the day and typically return for the duration of the night. Because environmental hazards away from the nest probably cause most bee mortality (Brian, 1952; Sakagami & Fukuda, 1968), males should be particularly prone not only to weather (Brian, 1952, 1965) but also to predators such as crab spiders (Araneae: Thomisidae) (Morse, 1979, 1986). Consequently, males may represent low-quality hosts for conopid larvae, which require a relatively long host lifespan for development, but not so for the rapidly developing phorid larvae. Furthermore, exposure of field-dwelling males to cool night-time temperatures (compared with the warmer temperatures workers would experience inside their parent colony) may prolong the development of parasitoid larvae. If this were the case, conopid larvae might not be able to complete development in a typical male bumble-bee before it succumbed to extrinsic sources of mortality.

Prevalence of the phorid parasitoid Apocephalus borealis differed among bumble-bee species, sexes, and between pollen and nectar collectors. Male bees experienced a higher incidence of phorid parasitism than workers in all host species. Prevalence of the conopid parasitoid Physocephala texana differed by host species and sex, with male bees experiencing a significantly lower incidence of parasitism than workers. The effect of host size on the incidence of phorid and conopid parasitism was typically weak and varied between host species and years. Surprisingly, conopid-imposed host mortality was non-significant, while that of phorids was especially severe. These results suggest that while conopid parasitism may be less important locally than elsewhere (e.g. Müller & Schmid-Hempel, 1992a; Maeta & MacFarlane, 1993), phorid parasitism may place significant stress on bumble-bee populations.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We are grateful to L. D. Harder and G. Pritchard for comments on the manuscript, B. V. Brown for identifying phorid flies, and C. Cormier and D. B. McCorquodale for discussions pertaining to phorid and conopid parasitism of bumble-bees. This work was supported by grants from the Natural Sciences and Engineering Council of Canada and Mount Royal College to R. E. Owen.

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  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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Accepted 22 August 2001