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The Reindeer Oestrids Hypoderma tarandi and Cephenemyia trompe (Diptera: Oestridae): Batesian Mimics of Bumblebees (Hymenoptera: Apidae: Bombus spp.)? Arne C. Nilssen,1,4 John R. Anderson,2,3 and Robert Bergersen1 Accepted November 23, 1999; revised December 16, 1999

The color pattern (two areas on each of 20 transverse bands along the dorsal surface of the body) in two reindeer oestrids, Hypoderma tarandi and Cephenemyia trompe (Diptera: Oestridae), was analyzed and compared with that of different bumblebee species found in an oestrid study area in northern Norway. A clustering analysis and multidimensional scaling analysis of the resulting matrix of pairwise similarity coefficients indicated that Bombus lapponicus, B. alpinus, and B. monticola (Hymenoptera: Bombinae) comprise ¨ a Mullerian guild whose members serve as Batesian models for H. tarandi, ¨ and that B. pratorum, B. jonellus, and B. lucorum comprise a Mullerian guild whose members may serve as Batesian models for C. trompe. The oestrid mimics also resemble their models in size. KEY WORDS: mimicry; bumblebee; Bombus; Cephenemyia trompe; Hypoderma tarandi.

INTRODUCTION Mimicry exists when two or more species, which may not be closely related, come to resemble each other in some respects and at least one species 1Zoology

Department, Tromsø Museum, University of Tromsø, N-9037 Tromsø, Norway. of Insect Biology, University of California, Berkeley, California 94720. 3Present address: 1283 NW Trenton, Bend, Oregon 97701. 4To whom correspondence should be addressed at Zoology Department, Tromsø Museum, University of Tromsø, N-9037 Tromsø, Norway; e-mail: [email protected]. 2Division

307 C 0892-7553/00/0500-0307$18.00/0 ° 2000 Plenum Publishing Corporation

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benefits from the resemblance (Friedlander, 1976). In Batesian mimicry, the benefited species is palatable and harmless, but is protected from predators by virtue of its similarity to a distasteful or harmful species. The protected species is known as a mimic, and the one that it imitates is called the model (Rettenmeyer, 1970). In Mullerian ¨ mimicry, two or more distasteful/ harmful species resemble one another; the benefits work through enhanced predator learning when the proportion of distasteful species increases (e.g., Rettenmeyer, 1970). Many harmful, distasteful, or poisonous insects advertise their unpalatability by having a conspicuous pattern of coloration. Such species are referred to as being aposematic, and this phenomenon is considered to be a warning signal that can be learned by predators (Waldbauer, 1988). In Batesian mimicry, mimics have evolved external features (sometimes also behavioral elements) that resemble aposematic characters. Potential predators are unable to detect the difference, and the mimic is protected (even if perfectly suitable as food). Protection associated with mimicry is based on the fact that predators can learn to avoid the colors of the distasteful/dangerous prey, even if unlearned responses are also possible (Waldbauer, 1988; Guilford, 1990; Alatalo and Mappes, 1996). In Batesian mimicry, a model can tolerate only a certain proportion of mimics. If there are too many mimics, they will be taken by predators that forget to associate inedibility or harmfulness with the aposematic pattern and subsequently also destroy some individuals of the model species. Brower (1960) found, however, that if as few as 30% of the prey were models, a significant amount of protection from predation would occur (see also Nonacs, 1985). Since the first description of mimicry (Bates, 1862), many mimicry complexes have been recognized (e.g., Owen, 1980; Brower, 1988). Among the many examples, bumblebees are obvious models since their venomous stings give them considerable protection (Friedlander, 1976; Patent, 1978; Owen, 1980; Plowright and Owen, 1980). Among others, the following Diptera have been reported as mimics of various bumblebees: Bombylius major (Bombyliidae), Mallophora bomboides (Asilidae), Mesembrina spp. (Muscidae), and Merodon equestris, Mallota bautias, and Volucella bombylans (Syrphidae) (Owen, 1980; Evans and Waldbauer, 1982; Thorp et al., 1983). In these examples of Batesian mimicry, the dense pile over the entire body of the mimic is colored to resemble a certain species of bumblebee, especially the details of pile coloration (Plowright and Owen, 1980, and references therein). Brower et al. (1960) and Evans and Waldbauer (1982) showed through various experiments that these resemblances are selectively advantageous and that such flies are indeed Batesian mimics of bumblebees. Bumblebees are even Batesian models for beetles (Thorp et al., 1983; Fisher and Tuckerman,

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1986) and lepidopterans such as Hemaris spp. (Sphingidae) (Friedlander, 1976), which have lost the scales over most of the surface of their wings, an unusual feature in a lepidopteran. Several authors have noted that species of Cephenemyia and Hypoderma (Diptera: Oestridae) resemble bumblebees (e.g., Hadwen and Palmer, 1922; Bennett and Sabrosky, 1962; Zumpt, 1965; Cogan, 1973; Papavero, 1977; Thorp et al., 1983; Wood, 1987; Scholl, 1993), but aside from general anecdotal/casual comments, no one apparently has investigated to what extent these flies mimic various bumblebees. During field work with reindeer oestrids [Hypoderma (=Oedemagena) tarandi (L.) and Cephenemyia trompe (Modeer)] in northern Norway (Anderson et al., 1994; Nilssen and Anderson, 1995; Anderson and Nilssen, 1996a), we often observed bumble bees and oestrids occurring simultaneously in the same habitats. As we noted a striking resemblance between these oestrids and several bumblebee species, the objective of the present study was to determine which of the bumblebee species observed and collected might represent models for Batesian mimicry by the above oestrids.

MATERIAL AND METHODS Most field work was carried out in northern Norway in Troms County (at Vaddas, 69◦ 50’ N, 20◦ 40’ E, altitude 140–160 m) and in Finnmark County (at Suolovuopmi, 69◦ 40’ N, 23◦ 30’ E, altitude 440–520 m) from 1983 to 1995. Collection sites included areas both below and above the tree limit. The forest habitats consist primarily of mountain birch (Betula pubescens ssp. tortuosa), with individual trees as tall as 5–6 m, with the field layer being a mixture of dwarf birch (Betula nana) and juniper (Juniper communis) in dry locations, and willows (Salix spp.) in moist places. Dry heaths are dominated by bilberry (Vaccinium myrtillus) and crowberry (Empetrum nigrum). The climate is subarctic and of a continental type (Bruun, 1967), and mean temperatures for May, June, July, August, and September (at Suolovuopmi) were 2.1, 8.4, 11.4, 8.9, and 4.7◦ C, respectively (data from The Weather Bureau of Northern Norway, Tromsø). Oestrid flies were captured by flight traps baited with carbon dioxide (Anderson and Nilssen, 1996a), netted near reindeer or people, or netted while studying their mating behavior (Anderson et al., 1994; Nilssen and Anderson, 1995). Bumblebees were obtained by saving representative samples of species captured in the traps, and by netting specimens seen in the terrain while servicing the flight traps or seen during our studies at mating places. Collected specimens were frozen and later pinned for identification (Anderson and Nilssen, 1996a). At oestrid mating places we sporadically compared the

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densities of oestrids with bumblebees. In the field, possible avian predators and their behavior were noted, and two H. tarandi females were glued to rocks on 9 August to see if they were attractive to birds. Information about the flight season of bumble bees is reported by Løken (1973). Taxonomy and nomenclature for bumblebees follows Løken (1973, 1984, 1985). For identification of Bombus lapponicus and B. monticola, the redescription in Svensson (1979) was used. Svensson (1979) used Pyrobombus as the generic name, but we follow Løken (1985) in using Bombus. We follow the recommendation in Williams (1994) that Psithyrus should be included in Bombus. In the study, the dorsal color pattern of the different social Bombus species was compared with that of the two oestrid species. Two cuckoo bumblebees, Bombus (=Psithyrus) flavidus Eversmann and Bombus (=Psithyrus) quadricolor (Lepeletier), and one bumblebee-like muscid, Mesembrina mystacea (Meigen), were included in the analysis. We only used specimens collected in the study area by ourselves. The color similarity analysis used was adopted and modified after Plowright and Owen (1980), who investigated the association between color pattern and geographic area in bumblebees. This method provides an objective means of comparing color pattern among species. In our study, the dorsal surface of each species analyzed was divided into 20 transverse bands. The color (white, yellow, red, and black) of each band was determined in a dorsomedial and a dorsolateral area, as shown in Table I. For each pair of species, a similarity coefficient was calculated by summing the scores over all 20 + 20 body areas (1 for the same color and 0 for different colors) and dividing by 40 [corresponding to the Russel and Rao coefficient (Romesburg, 1984, p. 147)]. The possible range of values is from 0 to 1, with 1 indicating perfect similarity. The matrix of similarity coefficients for all pairs of species was then the basis for a clustering procedure using the average linkage method (UPGMA) in SYSTAT (1992). The same matrix and program were also used to produce a Kruskal–Shepard–Torgerson–Young multidimensional scaling (MDS) plot. RESULTS The similarity analysis of the color patterns presented in Table I showed that each of the two oestrids closely resembled different bumblebees. The cluster diagram (Fig. 1) shows that H. tarandi was most similar to B. lapponicus with a similarity coefficient of 0.75. This oestrid was also similar to B. monticola and B. alpinus (similarity coefficients 0.63). These three Bombus species + H. tarandi formed a distinct similarity group, separated from all other species (Fig. 1). C. trompe was in a different group with B. pratorum, B. jonellus, and the muscid Mesembrina mystacea, but was also

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Table I. Dorsal Pubescence Colors of 20 Dorsolateral + 20 Dorsomedial Areas of Transverse Bands on Species Used in the Analysisa Body color Species Apidae Bombus alpinus (L.) Bombus balteatus Dahlbom Bombus hypnorum (L.) Bombus jonellus (Kirby) Bombus jonellus (Kirby) Bombus lapponicus (Fabricius) Bombus lapponicus (Fabricius) Bombus lapponicus (Fabricius) Bombus monticola (Smith) Bombus monticola (Smith) Bombus lucorum (L.) Bombus lucorum (L.) Bombus pascuorum (Scopoli) Bombus pascuorum (Scopoli) Bombus pratorum (L.) Bombus quadricolor (Lepeletier)b Bombus flavidus Eversmannb Oestridae Hypoderma tarandi (L.) Cephenemyia trompe (Modeer) Muscidae Mesembrina mystacea (Meigen) a n,

Sex

Head

Thorax

Abdomen

n

l: BBB m: BBB l: BBB m: BBB l: BBB m: BBB l: BBB m: BBB l: YBB m: YBY l: YBY m: YBY l: BBB m: BBB l: BBB m: BBB l: BBB m: YBY l: BBB m: BBB l: BBB m: BBB l: BBB m: BBB l: BBB m: WBB l: BBB m: BBR l: BBB m: BBB l: BBB m: BBY l: BBB m: BYB

BBBBBBB BBBBBBB YYBBBYY YYBBBBY RRRRRRR RRRRRRR YYBBBYY YYBBBBY YYBBBYY YYBBBYY YYBBBYY YYBBBBY YYBBBYY YYBBBBY YYBBBYY YYBBBBY YYBBBBB YYBBBBB YBBBBBB BBBBBBB YYYBBBB YYBBBBB YYBBBBB YYBBBBB RRRRRRR RRRRRRR RRRRRRR RRRRRRR YYYBBBB YYBBBBB YYYBBBB YYBBBBB YYYBBYY YYBBBBY

BBBRRRRRRR BBBBBRRRRR YYYYBBWWWW YYYBBBWWWW BBBBBBBWWW BBBBBBBWWW YBBBBBWWWW BBBBBBBWWB YYBBBBBWWW YBBBBBBWWW YYRRRRYYYR BBRRRRRRRR YYRRRRRYYY BBRRRRRRYR BYRRRRRYYY BBRRRRRYYY BBRRRRRRRR BBBRRRRRRR BBRRRRRRRR BBBRRRRRRR BBYYYBBWWW BBYYBBBWWW BBYYBBBWWW BBYYBBBWWW RRRRRRRRRR RRRRRRRRRR BBRRRRRRRR BBRRRRRRRR BBBBBBBBYY BBBBBBBYYY BBWBBWWWRR BBBBBBWBBB YBBBBBYYBR YBBBBBYYBR

1

l: BBB m: BBB l: BBY m: BBY

YYYBBYY YYYBBBY YYYBBBY YYYBBBY

YYYRRRRRRR YYYRRRRRRR YBBBBBYYYY BBBBBBBYYY

5

l: RRR m: BBB

YYYYYBB YYYYYBB

BBBBBBYYYY BBBBBBYYYY

5

1 1 9 3 36 35 4 6 10 1 2 1 1 1 1 4

5

Number of investigated specimens (equals number of specimens collected in the study area except for the oestrids). l, dorsolateral; m, dorsomedial. W, white; Y, yellow; R, red; B, black. , queens; , workers; , males (drones). b Cuckoo bumblebees, also known under the genus name Psithyrus (Williams, 1994).

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Fig. 1. Cluster diagram based on the similarity analysis of dorsal color pattern (see text) of the reindeer oestrids Hypoderma tarandi and Cephenemyia trompe and bumblebees species found in the same habitats. The muscid Mesembrina mystacea is also included.

close to B. jonellus, B. balteatus, and the cuckoo bumblebees Bombus flavidus and B. quadricolor; the latter is a cuckoo parasite of B. pascuorum (Løken, 1984). C. trompe was closer (similarity coefficient 0.80) to B. pratorum than H. tarandi was to B. lapponicus, but both resemblances were remarkably high. The two closest species in the cluster diagram, B. monticola and B. alpinus, had a similarity score of 0.93. B. lapponicus and B. monticola, so taxonomically close that they only recently have been recognized as two separate species (Svensson, 1979; Pamilo et al., 1987), had a similarity score of 0.63. The MDS plot (Fig. 2) shows the oestrid and bumblebee species included in two closely similar groups, in which H. tarandi closely resembled B. lapponicus, B. monticola, and B. alpinus, and C. trompe closely resembled B. pratorum, B. quadricolor, B. lucorum, B. flavidus, and B. jonellus. Both B. pascuorum and B. hypnorum were comparatively distant from the other species, as was the case in the cluster diagram. The diagrams (Figs. 1 and 2) reveal that B. jonellus and its parasite B. flavidus (Løken, 1984) were very similar in color, but this was not the case for host–parasite association of B. pascuorum and B. quadricolor. The muscid Mesembrina mystacea appeared to mimic the same bumblebee species (Fig. 2) as did C. trompe. The oestrid species were similar in size to the bumblebees, even if the bumblebees were more variable. The queens were normally a little bigger, and the workers sometimes smaller, than the oestrids.

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Fig. 2. Multidimensional scaling (MDS) plot based on the similarity analysis of dorsal color pattern of the reindeer oestrids Hypoderma tarandi and Cephenemyia trompe and the investigated bumblebee species. The muscid M. mystacea is also included. Species close to each other in the plot have similar color pattern.

Bombus lapponicus, B. jonellus, and B. monticola were the most abundant bumblebee species captured in the habitats where the oestrids were observed and captured (eclosion, mating, or host-seeking sites). For the other bumblebee species listed in Table I the numbers n provide a rough quantification of their relative abundance. The oestrids analyzed (average values of five individuals of each species) were typical of the hundreds caught in CO2 -baited traps (Anderson and Nilssen, 1996a). All bumblebees analyzed (Table I) were collected between 4 July and 29 August. Other bumblebees were seen at various field sites both before and after these dates, but not captured. Bumblebees were first observed at a field site (Vaddas) on 19 June 1984, and last observed (Suolovuopmi) on 30 August 1985 (we conducted no studies before and after these dates). Løken (1973) studied museum specimens of Bombus spp. collected in other studies and found the first and last dates of collection (Table II). Many species first appear in April or May and most species are active to the end of September. Thus, the Bombus spp. appear well before and after the flight activity of the reindeer oestrids. These oestrids appear mostly in July and August (Anderson and Nilssen, 1996a).

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Nilssen, Anderson, and Bergersen Table II. First and Last Dates of Collection of Queens and Workers of Bombus spp. According to the Investigation of Museum Specimens by Løken (1973)a Species B. alpinus B. balteatus B. hypnorum B. jonellus B. lapponicus/B. monticola B. lucorum B. pascuorum B. pratorum a These

First collected

Last collected

08 May 19 June 16 May 15 June 25 March 22 April 19 April 04 May 06 May 03 June 18 March 14 April 16 April 02 May 29 March 25 April

28 August 28 August 27 August 28 August 24 Sept 10 Sept 28 Sept 25 Sept 24 August 02 Sept 06 Oct 29 Sept 14 Oct 11 Oct 05 Sept 25 Sept

data reflect the seasonal appearances of these species in Scandinavia.

Throughout our studies we observed and caught various bumblebees on days when climatic conditions were not favorable for oestrid activity (i.e., no oestrids seen at mating places or caught in baited traps). Bumblebees also were active at and around oestrid mating places before and after the daily appearance of the oestrids (Anderson and Nilssen, 1996a). Thus, all data we obtained established that the various bumblebees in Table I occurred in the same habitats previous to, simultaneously with, and after the daily and seasonal occurrence of the oestrids. Like the oestrids, bumblebees were seen and captured in habitats above and below the tree limit. At hilltop mating places of C. trompe, bumblebees always were distributed over a much wider area (i.e., both the sides and tops) than the C. trompe males. On five favorable days for oestrid activity when bumblebee and male C. trompe numbers were recorded only on hilltops, bumblebee numbers equalled or slightly exceeded the 5–10 males present. On other climatically marginal days when only 1–2 C. trompe were present at mating places, or on days when none were seen (unpublished data), we usually saw several foraging bumblebees. Bumblebees were not seen at rocky, streamside H. tarandi mating places (Anderson et al., 1994), but along the stream and on the surrounding hillsides we saw more bumblebees than H. tarandi males seen at mating places. (At most H. tarandi mating places we saw only 1–5 males present at any one time; the maximum number seen on one day varied from 10 to 12). Trap catches could not be used for relative abundance comparisons because the host-seeking oestrid females were attracted by CO2 and bumblebees were not.

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The predominant insectivorous birds observed at different study areas were Tree Pipit (Anthus trivialis), Golden Plover (Pluvialis apricarius), Redwing (Turdus iliacus), and Arctic Tern (Sterna paradisaea). In some years Long-tailed Skua (Stercorarius longicaudus) also was comparatively common. None of these birds were seen feeding on oestrids. On 31 July 1986 we observed two terns (Sterna paradisaea), and on 3 and 9 August 1987 we observed four terns hovering, swooping down, and picking up prey from exposed rock surfaces as they flew back and forth adjacent to and over an area that included an identified H. tarandi mating place. As only 1–2 H. tarandi males were seen at the mating place at any one time on these dates, and no terns were attracted to either of two H. tarandi females glued to rocks on 9 August, we surmised that the terns were feeding on crane flies, blow flies, or anthomyiids that were seen on rock surfaces during periodic surveys for H. tarandi.

DISCUSSION The color similarity analysis of the two reindeer oestrids and the various bumblebees found simultaneously in the same habitats was in good agreement with what the human eye perceives: H. tarandi most strongly resembles B. lapponicus, whereas C. trompe looks remarkably like B. pratorum. However, we conclude that B. lapponicus, B. monticola, and B. alpinus comprise a Mullerian ¨ guild whose members serve as Batesian models for H. tarandi (Figs. 1 and 2). Although B. pratorum is most similar to C. trompe (Figs. 1 and 2), it may not be the best functional model because of its perceived scarcity in the study area (Table I). Thus, although not as close to C. trompe (Figs. 1 and 2), B. jonellus and B. lucorum may be functioning as more effective models within a different Mullerian ¨ guild (if future bumblebee-specific surveys confirm our limited relative abundance data). The muscid Mesembrina mystacea possibly also mimics the same species as does C. trompe. The color similarity between host–parasite pairs (true bumblebees and cuckoo bees) is well recognized and is best explained by Mullerian ¨ mimicry (Plowright and Owen, 1980). The present study revealed that the cuckoo bee B. flavidus resembled its host B. jonellus, but the host–parasite association of B. quadricolor and B. pascuorum was not characterized by closeness in color similarity (Fig. 2). Mullerian ¨ mimicry also resulted in the same color patterns having evolved among different assemblages of bumblebees (Plowright and Owen, 1980). When this phenomenon occurs, an aposematic species benefits from having the same warning colors as other aposematic species in the assemblage because predators only have to learn one color pattern; another benefit is that only small numbers of prey are killed as predators learn to avoid the

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harmful or distasteful species. Both direct and circumstantial evidence suggests that bumblebees are avoided by avian predators. As Mullerian ¨ mimicry is operating among bumblebees, and the oestrids are Batesian mimics of different bumblebees; this increases the probability that predators would be deceived into avoiding the oestrid mimics. Given the holarctic distribution of the reindeer oestrids, they probably coexist with many more species or subspecies of bumblebees than found in this study. As dark colors are common to many arctic insects (Downes, 1962, 1965; Kevan and Shorthouse, 1970) the color pattern of both bumblebees and the oestrids may serve both an aposematic and thermoregulatory function. Dark insects are known to absorb radiant heat even at low intensities (Digby, 1955; Hamilton, 1973; Schultz and Hadley, 1987; Anderson et al., 1994). Both oestrid species are conspicuous in the field, especially H. tarandi because of its red-orange abdomen. The concentrations of large numbers of males at small, unique mating places (Anderson et al., 1994; Nilssen and Anderson, 1995) and their intense intermittent flight activity make them even more conspicuous. Because we focused mostly on oestrids during our studies (Anderson et al., 1994, Anderson and Nilssen, 1996a, b; Nilssen and Anderson, 1995), we usually only noted the presence or absence of bumblebees at oestrid mating places; on sporadic occasions when bumblebee and male oestrid numbers were compared the bees were more abundant. The color pattern is identical for C. trompe males and females and very similar in both sexes of H. tarandi. However, H. tarandi females more closely resemble the bumblebee models than do males. In Batesian mimicry, the ratio of models to mimics may be important in deterring predation, but to be effective it is not necessary that models outnumber the mimics (Brower, 1960; Nonacs, 1985). However, whenever we compared the densities of bumblebees with H. tarandi and C. trompe males, bumblebees always were more abundant (the sex ratio of both oestrids is 1 : 1). While the oestrid females were engaged in host-seeking they were widely scattered above and below the tree line (Anderson and Nilssen, 1996a, b); except when attracted to host-mimicking traps, they were not often encountered. Bumblebees, on the other hand, were seen everywhere on flowering plants. Adult oestrids are characterized as having low population densities (e.g., Breev, 1973; Anderson, 1975; Minar, ´ 1984; Scholl, 1993; Nilssen and Haugerud, 1995), whereas bumblebees (both workers and males) may become very numerous throughout the summer (Løken, 1973). Also, foraging bumblebees were widely distributed throughout all habitats having flowering plants, whereas the aggregations of male oestrids were confined to small specific mating places. These phenomena may have been important in the evolution of the bumblebee–oestrid mimicry complex. In spite of low

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population densities, large numbers of C. trompe males sometimes can be aggregated at certain mating places. On one occasion we saw approximately 60 males at one mating place, but at most of the 23 mating places we found, there were only 5–15 males per mating place on favorable days (Nilssen and Anderson, 1995; and unpublished data). Therefore, except at the very best mating places (Nilssen and Anderson, 1995), our estimates of bumblebee numbers revealed that they always were more numerous than C. trompe males. For H. tarandi, we usually saw fewer than 5 males per mating place, and the maximum numbers were only 10–12 (Anderson et al., 1994). We always saw more bumblebees than this adjacent to the streamside mating places and on the surrounding hillsides. Because males may remain at such sites for several hours per day, whereas females visit such places for just a few minutes (only long enough to mate), males are more exposed to predators than females. On warm, sunny days when maximum numbers of males are present, and as they periodically launch into flight from their perch sites, the frequent male–male pursuit flights make males especially conspicuous, an attribute that would tend to attract predators. However, in different years unfavorable weather prevented oestrid activity on 56–68% of the days (Anderson and Nilssen, 1996a), and males usually are only active at mating places for 2–5 hr of each favorable day (Anderson et al., 1994; and unpublished data). Their activity always started after bumblebees became active and stopped before bumblebee activity subsided. Bumblebees were numerous at all study sites where we trapped and netted oestrids, and they occurred with oestrids in the same microhabitats and at the same time. They also were present prior to and after the seasonal occurrence of both oestrids, and on many days when climatic conditions inhibited oestrid activity. On days when both oestrid and bumblebees were active, bumblebees also were active earlier in the day than oestrids, indicating a lower temperature threshold for activity. Bumblebees are known to have sophisticated preflight warmup mechanisms, enabling them to be active at low temperatures, sometimes even to near 0◦ C (Heinrich, 1993). Oestrids apparently lack such ability of endothermic thermogenesis (unpublished data), but rely instead on sunshine (basking) and ambient temperature only. There is little evidence that mimics are protected from natural enemies in nature, and realistic estimates of the antipredation value seem to be scarce (Waldbauer, 1988). Likewise, the degree of protection H. tarandi and C. trompe obtain by being bumblebee mimics is open to question, but we never saw birds attempt to feed on either species, although we spent hundreds of hours observing flies at mating sites (Anderson et al., 1994; Nilssen and Anderson, 1995). Both oestrid species are conspicuous flies, and the frequent male–male chases at mating places makes them even more noticeable (Anderson et al.,

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1994; Nilssen and Anderson, 1995). Being quite large and containing a large amount of fat [60 and 35 mg in newly eclosed H. tarandi and C. trompe, respectively (Nilssen, 1997)], these two oestrids could be tempting prey for smaller birds. However, there appear to be no records of this occurring. Sdobnikov (1935) reported that Motacilla alba, M. citreola, M. borealis, and Emberiza pusilla often remained near reindeer herds over which various flies were hovering, including tabanids and oestrids. Although he did not report birds feeding on flies, such birds may have been feeding on nonaposematically colored tabanids and other Diptera. In the absence of models, or in the presence of inexperienced predators, Batesian mimics may be extremely vulnerable (Malcolm, 1990). Consequently, if oestrids are present in a location that lacks bumblebees, they may be more heavily predated than in a region where bumblebees are abundant. Bumblebees may therefore influence the population dynamics of reindeer oestrids. However, if responses to aposematic warning signals are inherited (instinctive) rather than learnt (Waldbauer, 1988; Guilford, 1990; Alatalo and Mappes, 1996), oestrids may still be protected. Besides, birds are highly mobile and may learn the harmfulness of bumblebees elsewhere. In either case, oestrids would benefit by resembling bumblebees. As reindeer oestrids have a holarctic distribution, it would be interesting to investigate the arctic-alpine bumblebee fauna in North America and northern Russia to see if they have the same models in these geographic areas. No one can distinguish palaearctic reindeer oestrids from nearctic ones (Wood, 1987). Consequently, if the mimicry hypothesis is correct, there should be bumblebee models in North America that either are the same species as in Eurasia, or are very similar in outer appearance. According to Pamilo et al. (1987), there are about 294 species in the genus Bombus, including 44 in the (previous) genus Psithyrus (=Bombus sensu Williams, 1994) in the Holarctic. Among these, it is likely that several subarctic or arctic species that occur within the distribution of reindeer may serve as models. B. lapponicus, the hypothesized main model for H. tarandi, has a holarctic distribution (Svensson, 1979, and references therein). Hence, the distribution of B. lapponicus may cover most of the distribution of H. tarandi.

ACKNOWLEDGMENTS We thank Utviklingsfondet for Reindrift, Alta, Norway, for partial financial support. We thank Prof. H. V. Daly, University of California, Berkeley, and Prof. R. W. Thorp, University of California, Davis, for reviewing the manuscript.

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