Ecological Research (1993) 8, 247-267

REVIEW and in the of the boreal zone

P. G. KEVAN,1 E. A. TIKHMENEV2 AND M. Usux1 1 Department of Env, ronmental Biology, University of Guelph, Guelph, Ontario, N1G 2W1, Canada and 2 Institute for Biological Problems of the North, Academy of Sciences, K. Marx Pr. 24, Magadan, 685000 Russia

Pollination systems in the boreal zone range from generalist to specialist, both entomologically and botanically. The relative importance of wind pollination, pollination, sexual separation between and within plants, and between , hermaphroditism of flowers, and various breeding systems are related to growth form and habitat. The diversity and specializations of anthophilous insects parallel those in other bioge0graphic zones, but seem less developed. We suggest that this reflects the combined effects of evolutionary youth, severity of climate, restriction of symbiont ranges within those of their hosts, and the naturally frequent perturbations by fire or insect outbreaks in the zone, requiring faunal and floral vagility and constraining specialization in . Modern perturbations by logging and pesticides seem to be well buffered because of the relative openness of the ecosystem (compared to others), although damage has been documented. Insect pollination is as much a keystone process in the boreal forest as elsewhere, despite the immediate counter-impression given by the dominance ofwind-pollinated conifers. Nevertheless, there are few studies, botanical or entomological in situ. The boreal system offers important opportunities in general and applied research in pollination ecology and synecology generally.

Key words: anthecology; boreal; floral biology; ; taiga.

INTRODUCTION Baldwin (1991). Bonan and Shugart (1989) and Zoladeski and Maycock (1990) explain the dynam- The boreal zone is a circumpolar vegetational belt ics of the boreal ecosystem as regulated by soil (also called the taiga) that stretches from northwest- conditions, including permafrost, weather factors, ern Europe eastward through , the Russian fire and outbreaks of defoliating insects. Far East, and across North America from Pacific to Although the flora of the taiga is well known, its Atlantic Ocean shores. In places the taiga spans insect fauna is not. There is no compendium of more than 10 ~ of latitude. Although this huge area boreal , such as exists for the arctic is not homogeneous and contains various subdivi- (Danks 1981). It is difficult to typify boreal insects, sions and ecotones, as well as enclaves of treeless except by those that are monophagous on plants communities, its overall physiognomy is quite uni- typical of taiga. Danks (1979, 1981) and Danks form. The dominant plants are species of spruce and Foottit (1989) draw attention to a few examples (Picea), larch (Larix), fir (Abies), pine (Pinus), of insects that show geographical ranges which poplar (Populus) and birch (Betula), which together parallel the limits of the boreal forest in North with shrubs, herbs and bryophytes, comprise the America (e.g. Vespula albida Sladen, Xylotrechus characteristic plant communities of the taiga as undulatus Say). A that seems to parallel these described by Moir (1958), La Roi (1967), La Roi limits from Hokkaido Island to Sweden is Lasio- and Stringer (1976), Larsen (1980), Chertov glossum (Evylaeus) boreale Svensson (Svensson ( 1981), Elliott-Fisk (1988), Zoladeski (1989) and et al. 1977). More recently, Danks and Foottit (1989) have attempted to rationalize some aspects Accepted 1 June 1993. of boreal entomology. Nevertheless, too little is 248 P.G. Kevan et al. known to allow much synthesis of the proportions of prevent erosion in otherwise denuded landscapes. the fauna fitting various ecological roles, as has been Further, they provide cover for seedlings of sun- done for the arctic (Danks 1987). It is one of these intolerant trees (e.g. balsam fir, Abies balsamea [L.] roles, pollination, which we discuss here. Mill., and white spruce, Picea glauca [Moench] A. The coniferous (Di-Giovanni & Kevan 1990) and Voss). deciduous trees that dominate the taiga are anemo- The plant communities of early successional stages philous (wind pollinated; Regal 1982; Whitehead (in the first decade) are generally shortlived (Hein- 1983). However to appreciate the importance of selman 1981) but comprise the most active biotic pollination by insects to the boreal ecosystem, one communities of both flora and fauna. One facet of must examine the dynamics of succession leading to the reproductive biolgy of the plants that is vital to the establishment of the forest. the ecological processes of succession and trophic Most stands of boreal trees are young (< 100 relationships is pollination. If the plants are not years old). Spruce and pine stands of more than 250 pollinated then there are no fruits for wildlife years are rare and occur in areas protected from fire consumption nor seeds for dispersal. (Rowe & Scotter 1973). It is probable that before The aims of this review are fourfold. We examine, the coming of Europeans, lightning (and perhaps from a botanical perspective, the pollination and humans) set fires that periodically burned large breeding systems of the flora of the boreal zone and tracts of forest in North America and the Russian attempt to make some generalizations and explana- Far East. Dry conditions, accompanied by a high tions about the differences between trees~ shrubs and incidence of forest fires, occur at about 30 year herbs in different habitats within the boreal zone. intervals, as borne out by historical and palaeonto- We then review the boreal fauna ofanthophiles with logical records (Rowe & Scotter 1983). More re- a view to indicating the importance of their cently, logging by clear-cutting and prescribed relations for both plants and themselves. We also burning (McRae 1979) have increased the amount address the issue of pesticide use in boreal forests of temporarily deforested ground over large areas of as it affects both pollinators and pollinated plants. the boreal zone. Finally, we draw some overall conclusions about the The taiga trees are well adapted to rapid re- dynamic interactions of insects and flowers in the invasion of deforested areas because of their wind ecology, biogeography, management and conserva- dispersed seeds. Other plants have seed banks in the tion of the boreal forest. soil. The understorey plants of the mature boreal forest are mostly inconspicuous, even though they sometimes have showy flowers or fruits. However POLLINATION AND BREEDING the underground stems and roots of bear-berry SYSTEMS (Arctostaphylos uva-ursi (L.) Spreng.), cranberries and blueberries (Vaccinium spp.), labrador tea (Le- The boreal forest is home to many conspicuous dum spp.), dwarf birches (Betula spp.), alders insects which are known anthophiles and contains (Alnus spp.), willows (Salix spp.) and other fleshy- many plants with flowers that are typical of ento- fruited shrubs (e.g. Ribes, Rosaceae, , mophily. We shall explore the intricacies of the Cornaceae) often are not damaged by fire. They pollination relationships of boreal plants and insects regenerate rapidly after fire to produce a lush and to place their ecological importance into perspective. fruitful vegetation (see Johnson 1975; Flinn & In general, the Gymnospermae comprise only Wein 1977). Rowe (1983) provides a synthesis of about 2% of the flora of the taiga. the strategies plants use to recolonize burnt areas. From an examination of the literature we conclude Herbaceous vegetation may be dispersed into defor- that pollination information is available on only ested areas by wind (e.g. Epilobium spp., Gramin- 10% of the North American Angiospermae and eae, Cyperaceae, Asteraceae, ) or by vertebrates (e.g. that studies in situ make up only half of that Aralia spp., Liliaceae). The soil seed bank is also an proportion. important source of regeneration (Johnson 1975). There is little information on pollination biology The shrubs and herbs provide much of the food in the boreal zone. Silen (1905, 1906) recorded and cover for wildlife. They help retain moisture and many visitors to boreal flowers in from his Pollination ecology of the boreal zone 249 observations between 1895 and 1905 but did not canadensis [Theobald] and (e.g. Xanthorhoe comment on the plants' breeding systems. In the munitata [Hbn.]; Thien 1969; Thien & Utech USSR, Vereshchagina (1968), Ponomarev and 1970). obtusata (Banks ex Pursh) Lind- Vereshchagina (1973) and Kaigorodova (1976) ley is also pollinated by mosquitoes and moths appear to be the only scientists to have made (Gorham 1976; Voss & Riefner 1983). Listera systematic anthecological studies in the taiga, specif- cordata (L.) R. Br. is pollinated by fungus gnats ically in the Ural area. Vereshchagina (1968) and (Sdatidae and Mycetophilidae) in the western Ponomarev and Vereshchagina (1973) suggested coastal redwood forests of North America (Mesler et that most of the species typical of the taiga that they al. 1980). Coeloglossum viride (L.) Hartman is investigated are autogamous (some being cleistoga- visited by and small which pick up mously so). Thus, it might appear that pollinia on their heads (Silen 1905, 1906; Hagerup and obligate entomophily are not typical for the 1952; Catling 1983). boreal forest. Data from Helenurm and Barrett (1987), Barrett and Helenurm (1987) and those Ericales studies summarized below (from most to least specialized) indicate that this generalization should The Ericaceae are not quite as diverse as the orchids, be treated with scepticism and, although it may be but comprise much more biomass. Although self- thought that few specialized pollination relation- compatibility seems to be the rule, automatic self- ships occur in the taiga, a number do exist. pollination does not take place (Haslerud 1974; Reader 1977). Vaccinium spp. (including Oxycoc- cus) are pollinated by from the largest Bombus to the smallest Halictidae (see Mohr & Kevan 1987 The most specialized pollination mechanisms in the for north Ontario). In some populations of Vaccin- Angiospermae belong to the Orchidaceae. Auto- ium angustifolium male and female sterility has been matic self-pollination in orchids is rare, as is aga- indicated (Hall & Aalders 1961; Aalders & Hall mospermy (van der Pijl & Dodson 1966; but see 1963; Hall et al. 1966). At least some Rhododen- Catling 1990), so one might readily infer that most dron spp. are pollinated by bees, some Diptera and boreal orchids require the attentions of pollinating occasionally other insects (Tikhmenev 1979, insects for seed set. Boreal orchids are neither 1981), as is true with Kalmia spp. (Small 1976; numerous nor diverse. In North America, there are Reader 1977; Tikhmenev 1979; Real & Rathcke about 30 species, mostly widespread. Catling and 1988, 1991; Rathcke & Real 1993), Rhodora spp. Catling (1991) note that about 16% of orchids (Thorpe 1979), Ledum groenlandicum Oeder (Small growing in the boreal zone are auto-pollinating 1976; Reader 1977), Chamaedaphne calyculata (L.) (especially in the Epidendroideae) and that aga- Moench (Small 1976; Reader 1977). Arctostaphy- mospermy is restricted to the Spiranthoidea. The los uva-ursi, Andromeda glaucophylla Link (Small Cyripedoidea, Spiranthoidea and Epidendroidea are 1976) and Gaultheria procumbens L. (Reader mostly bee pollinated, but pollination by Lepi- 1977). doptera predominates in Orchidoidea. In the boreal Recent research on Pyrolaceae in Denmark and zone, long-tongued bees are the most important Sweden by Knudsen and Tollsten (1991) and pollinators (12 of 30 species) and autogamy the next Knudsen and Olesen (1993) indicates the special- most important means of seed set (9 species; Catling ized nature and importance of buzz-pollination 1984). Arethusa bulbosa L., Calypso bulbosa (L.) (Buchmann 1983) by and pointed Oakes, Calopogon tuberosus (L.) BSP, Pogonia ophio- out the importance of self- and cross-pollination in glossoides (k) Ker-Gawi., Goodyera repens (L.) R. Br. Moneses uniflora, Pyrola spp., Orthilia and Chi- and Cypripedium spp. are pollinated mostly by bees maphila. Orthilia secunda (L.) House is fruitful in (Mosquin 1970; Thien & Marcks !972; Plowright the absence of pollinators in New Brunswick, etal. 1980; Kallunki 1981; Boyden 1982; Catling Canada (Barrett & Helenurm 1987) but not in 1983; Barrett & Helenurm 1987). Habenaria obtu- Scandinavia (Knudsen & Olesen 1993). It is sara (Banks ex Pursh.) Lindl. is pollinated by assumed that the recorded hybrids in Pyrola spp. mosquitoes ( [DeGeer] and Aedes (Haber 1988) were mediated by insect pollination. 250 P.G. Kevan et al.

Monotropa hypopitys L. is obligately autogamous house (1987) discuss Hedysarum boreale L. and its but retains features of entomophily (Hagerup pollinators from the Great Basin area of the USA, 1954; Vereshchagina 1970) and sets fruit without Seppar (1972) makes remarks on pollinators of external influence on transfer (Knudsen & Hedysarum cretaceum from the USSR, and D'AI- Olesen 1993). bore (1983) on pollinators of Trifolium pratense, Vicia cracca L., Hedysarum coronarium, Astragalus Zygomorphs glycyphyllos L. and Lupinus albus L. in Italy. The Lamiaceae are not well represented in the Many of the Scrophulariaceae are pollinated by bees. boreal zone and we are unable to find relevant The pollination ecology of Pedicularis spp. has been information. well studied (Macior 1975, 1982), but it is known that some species are automatically self-pollinated Hidden in the arctic (Williams & Batzli 1982; Meier & Kevan unpubl, data). The situation in the boreal Somewhat less specialized from the viewpoint of zone has not been examined. Castilleja spp. are also pollination are Boraginaceae (Mertensia spp.). Al- well adapted for pollination. In Kamchatka, though members of the genera of these families that Castilleja pallida (L.) Spreng., which grows in grow in alpine and temperate environments are meadows within the Larix/Betula lanata L. com- dependent on insects for pollination (Geber 1982), munity, showed about 50% seed set in flowers open we can find no information pertinent to this review. to pollination by insects but only 7% seed set in Impatiens capensis Meerb. (Balsaminaceae) is par- exclosures (Tikhmenev unpubl, data). Aga- tially dependent on Bombus and other insects for mospermy is known for Castilleja sulfurea Rydb. in pollination in the boreal forest (Rust 1977; the sub-alpine forest of Colorado, but outcrossing Mitchell-Olds & Waller 1985). The flowers when by bumblebees is obligate in Castilleja occidentalis in the male phase are more rewarding for longer and Torr. of the alpine tundra (Baldursson 1983). We attract more insects than when in the female phase have no data for the other showy or small flowered (Bell et al. 1984). The Campanulaceae and Lobeli- members of the family. aceae of the boreal forest are visited by Bombus and The Leguminosae is a family of similar diversity. other bees, but their breeding systems are not The flowers of plants of this family are adapted to known. Some genera of Primulaceae and Oxali- sternotribic pollination by bees. Some species that daceae are specialized for pollination by heterostyly occur in the boreal zone have been studied in other (Ganders 1979; Richards 1986) but again data are habitats which we will mention here. Astragalus missing for most boreal representatives. Vereshcha- alpinus L. is an obligate entomophile wherever it has gina (1965) indicates that Oxalis acetosella L. is been studied (Shamurin 1966; Shamurin & autogamous in the north Urals. Tikhmenev 1974; Kevan unpubl, data, from Colo- Many boreal Caryophyllaceae are likely to be rado alpine), as seems to be the case for most self-pollinating or agamosperms although the flow- Astragalus spp. (e.g. Karron 1987, 1989), but ers of most are attractive to insects. In the genera many species are self-compatible (Liston 1990). It Silene and Lychnis, dioecy and heterostyly are seems that studies on Oxytropis spp. are lacking, known but the boreal species have not been investi- although the flowers are known to be well visited by gated, except for Silene dioica (L.) Clairv. (Elmqvist bumblebees (Macior 1974; Bauer 1983; Kevan 1987). Most of the Ranunculaceae are probably unpubl, data). Swales (1979) suggests that some similar. Aquilegia spp. are adapted to pollination by arctic species are self-pollinating. Trifolium pratense long-tongued anthophiles such as moths and bees, L. is generally considered to be dependent on which are probably important in cross-pollination, bumblebees for pollination, but some self- although the flowers may readily self-pollinate pollinating races are known from northern Europe automatically (see Miller 1978). (Akerberg 1974). The requirements of other Trifo- The Onagraceae include several inconspicuously lium spp. vary. For others (Hedysarum spp., flowering Epilobium spp. as well as the showy Lathyrus spp., Vicia spp.) we can find no informa- Epilobium angustifolmm L. The latter is a well- tion pertinent to this review. Tepedino and Stack- known entomophilous nectar-rich plant that is espe- Pollination ecology of the boreal zone 251

dally attractive to bumblebees foraging for nectar Lepidoptera, beetles, , , and short-tongued (Swales 1979) and pollen or both (Galen & Plow- as visitors. right 1985; Galen et al. 1985). A variety of other Among the Droseraceae, Drosera rotundifolia L. is insects including Lepidoptera, Cerambycidae, Syr- known to set seed when insects are excluded from phidae, Tabanidae and even Simuliidae (Henderson the flowers (Kevan & Blades unpubl, data). et al. 1979) also visit the flowers. Although the The Araliaceae, represented by Aralia hispida protandrous floral development on individual ram- Vent. and Aralia nudicaulis L., produce umbels of ets or spikes favours pollen transfer by insects small flowers, which a wide variety of insects visit (Benham 1969) between the self-compatible (Mos- (Barrett & Thomson 1982; Thomson et al. 1982). quin 1966) plants, the highly clonal growth (Myers- Aralia hispida is andromonoedous, with a complex cough 1980; Broderick 1990) might reduce true blooming sequence alternating between male and outcrossing, However the effects of self-pollination female phases, and is pollinated especially well by on embryonic abortion and genetic load (Wiens et bumblebees, which systematically forage over a al. 1987) may compensate for potentially lost trapline of individual plants (Thomson et al. 1982, heterozygosity in offspring. 1989). Aralia nudicaulis L. is dioecious. The polli- Among the boreal Liliaceae are some obligate nation biology of this plant, mostly concerning the entomophiles such as Clintonia borealis (Ait.) Raf. role of bumblebees, indicates complex ecological (Thaler & Howright 1980; Galen et al. 1985; interactions between the sexes for services Somer 1985; but see Barrett & Helenurm 1987) through inflorescence sizes, blooming times and and Maianthemum canadense Desf. (Plowright & rewards (Barrett & Helenurm 1981; Bawa et al. Thaler 1979; Thaler & Plowright 1980; Somer 1982; Flanagan & Moser 1985; Flanagan & Bain 1985; Thomson et al. 1985; Barrett & Helenurm 1988). Moose (Alces alces L.) may graze this plant 1987) although some are self-compatible (e.g. heavily (Edwards 1985). Clintonia borealis; Galen & Weger 1986; Barrett & Helenurm 1987). Nectar secretion in C borealis is Hidden and exposed nectar positively correlated with the size of the flower and the amount of sugar present increases with the age of Comus spp. (Cornaceae) are at least partially depen- the flowers if insects are excluded (Plowright 1981). dent on insects for pollination (Plowright & Thaler Little is known about Smilacina, Tofiddia, Lilium 1979; Thaler & Plowright 1980; Somer 1985; or Allium. The pollination systems of boreal Iri- Thomson et al. 1985; Barrett & Helenurm 1987) daceae are unknown. and Comus canadensis L. has a special explosive mechanism for pollen release (Mosquin 1985, as Chamaepericlymenum canadense (L.) Aschers and Exposed nectar Graebn.). The Caprifoliaceae contain typically entomophil- Most Cruciferae, Saxifragaceae, Apiaceae, Rosaceae ous species. Viburnum spp. are at least partially and Hypericaceae are composed mainly of autoga- dependent on insect pollination (MiIiczky & Os- mous and agamospermous species but most are good 1979; Plowright & Thaler 1979; Thaler & attractive to insects. However among the Rosaceae Howright 1980). Lonicera dioica L. is not dioecious are some obligate outcrossers, which depend on and (as the name implies) and may be competent at are highly attractive to insects (e.g. Rubus arcticus L. self-pollination, as are other members of the genus, [Kangasjarvi & Oksanen 1989], Rubus idaeus L. even in the boreal forest (K. Barber pers. comm.). [see Hansen & Osgood 1983], Rubus chamaemorus Lonicera canadensis Bartr. has a low degree of L. [which is dioecious; Hippa et al. 1978, 1981; self-compatibility but cannot self-pollinate without Agren et al. 1986; ~igren 1988a,b]). Hypericum an animal to vector its pollen (K. Barber pers. perforatum L. (Hypericaceae) is a facultative comm.). Linnaea borealis L. appears to be self- apomict (Crompton et al. 1988). pollinating (Barrett & Helenurm 1987; Tikhmenev The significance of the minute but fragrant unpubl, data). Diervilla lonicera Mill. is well visited flowers of Galium spp. (Rubiaceae) in pollination and cross-pollinated by Bombus spp. in New Bruns- has been noted by Batra (1984) who includes wick (Howright & Thomson 1980) but, early in its 252 P.G. Kevan et al.

blooming, may be incompletely serviced (Thomson show staminate bias (Lloyd 1974; Ganeshaiah & 1985). We are unaware of any information on Shaankar 1991). Symphoricarpos spp. The boreal Gentianaceae are fruitful in the ab- Sarracenia purpurea sence of pollinators (as they are in the alpine of Sarracenia purpurea L. (Sarraceniaceae), a plant Colorado; Kevan unpubl, data), but little is known. almost emblematic of the boreal zone in North The flowers are not highly attractive to insects in the America, is an obligate entomophile that relies on boreal forest. Bombus and possibly Blaesoxipha fletcheri (Ald.) The pollination system of Plantago spp. (Planta- (Sarcophagidae) for pollination (Thomas 1986; ginaceae), some of which are found in the boreal Kevan unpubl, data). forest, has been described by Ponomarev and Kolesnik (1974) who say that species fall into two Bryophyta groups, completely anemophilous and those retain- ing entomophilous features. Stelleman (1984) Entomophily in mosses is not generally appreciated working in the Netherlands, describes Plantago but Koponen (1990) has reviewed the system, major L. as ambophil0us (i.e. with wind and insects involving chemical mimicry and dung-attracted as the pollen vectors). Diptera (Scathophagidae, Muscidae and Antho- myiidae), in the dung-inhabiting Splachnaceae. The Asteraceae flies appear to benefit by greater copulatory success, and the moss' spores are dispersed to dung where The Asteraceae are mostly pollinated by a wide they germinate. variety of insects. The family contains a range from obligate outcrossers to agamosperms, but little is known of the boreal species. Gross and Wemer THE FAUNA OF ANTHOPHILES (1983) indicate that the Solidago spp. they studied (including S. juncea Ait., S. gra_minifolia (L.) Salisb. Collembola, Hemiptera, Thysanoptera and S. canadensis L., which occur in boreal forests) are self-incompatible obligate entomophiles. Most The diversity of anthophilous insects is great and Asteraceae are highly attractive to many species of includes hexapods from Collembola to Hy- anthophiles (exceptions Anaphalis, Artemisia) and menoptera (Kevan & Baker 1983, 1984). In the are excellent collection sites for bees, Syrphidae, boreal zone, Sminthuridae (Collembola) have been Tachinidae and other insects. Among Aster spp. collected from the blossoms of Calla palustris L. studied in Wisconsin, there appears to be partition- south of Algonquin Park (Kevan unpubl, data). ing by bees on the basis of the length of their Some Hemiptera are common on flowers, particu- proboscides (Graenicher 1909). larly Miridae, Anthocoridae, Nabidae, Lygaeidae, Coreidae, Pentatomidae and Phymatidae. The flo- Sa//x ral biology of these groups ranges from nectar- sucking and plant-feeding to predation and Salicaceae are dioecious and Salix spp. are highly ambush, but no synthetic review of the Hemiptera attractive to insects (Hocking 1953; Pellmyr & as anthophiles has been made. The Thysanoptera Karkkainen 1987; Elmqvist et al. 1988a,b). Even are well known anthophiles (Lewis 1973; Heming birds may use nectar from willow catkins (e.g. in Danks 1979: 349; Chiasson 1986) even on European blue tit Parus caerulus L. [Paridae]: Kay flowers in the boreal zone (Kevan unpubl, data; 1985). They are generally thought of as ento- Usui unpubl, data). mophilous but several species benefit from some wind pollination (Argus 1974; Vroege & Stelleman Coleoptera 1990). In Scandinavia, Salix spp. show a sex ratio strongly biased towards pistillate plants (Elmqvist et The Cleridae also commonly feed on pollen (Bright al. 1988a,b) as in other locations (Arctic: Crawford in Danks 1979: 377) and the Nitidulidae, Melan- & Balfour 1983) and in Salix cinerea (Kay in dryidae, Mordellidae and Meloidae are often found Richards 1986:327 whereas most dioecious plants on flowers (Campbell in Danks 1979: 381). In the Pollination ecology of the boreal zone 2 5 3

Meloidae, members of the genus Meloe lay eggs in than one species (2 individuals) from Linnaea soil, then larvae climb on to flowers and become borealis L., one species (1 individual) from Maian- phoretic on bees (MacSwain 1956). Less common themum canadense and more than three species (76 are the Rhipiphoridae, which lay eggs on flowers individuals) from Oxalis montana Raf. These where the larvae hatch, attach to bees and are taken records strongly suggest an anthophilous habit for to live parasitically in bee nests. Nevertheless, there this genus in a family of Coleoptera not renowned are few records of flower visiting (e.g. one record of for flower visiting (but see Petlmyr & Patt [1986] Cateretes pennatus [Pullion] Nitidulidae from Ara- for pollination ofLysichiton americanum Hult6n and lia nudicaulis in New Brunswick [Barrett & St John [Araceae] by Pelecomalius testaceum Mann. Helenurm 1987). in the Pacific northwest of North America). The Chrysomelidae and Cerambyddae contain anthophilous species and are well represented in the Diptera boreal zone. Barrett and Helenurm (1987) record representatives of both families from flowers: Tra- The Diptera contain notorious boreal insects and chysida aspera brevifrons (How&) (Cerambyddae) anthophiles. However the adult feeding habits of from A. nudicaulis, Pidonia ruficollis (Say) (Ceram- many taxa are not well known. Among the Culico- bycidae) from Clintonia borealis and the chry- morpha (see Hocking 1953), it is well known that somelid Orsodacne atra (Ahrens) from Comus the Culicidae, especially (but not exclusively) the canadensis. males, feed on floral nectar (Hocking 1953; Sand- Among the Coleoptera are a number of families holm & Price 1962; Schaefer & Miura 1972; well represented in the boreal zone and known to Grimstad & DeFoliart 1974, 1975; Magnarelli include anthophiles. Although fit 1978, 1979, 1983). Flower visiting has been re- that description, records of them from boreal corded in most families of Nematocera but not flowers are few (see Barrett & Helenurm 1987). necessarily from boreal Communities. Among the Usui (pers. obs.) collected assimilis Brachycera, northern Stratiomyidae, Tabanidae (see (Kby.) on flowers of Vaccinium spp. The Elat- Hocking 1953), Asiloidea (exc. Asilidae), Bombyli- eridae have been recorded as anthophiles with idae, Empididae and Dolichopodidae are all fre- Dalopius spp. from Comus canadensis, Agriotes quently found at flowers, no matter what other food stabilis LeC. from Maianthemum canadense in they consume as adults. However, the significance New Brunswick (Barrett & Helenurm 1987) and of this habit to the bionomics of these abundant Ctenicera morula (LeC.) for Vaccinium spp. flowers insects has not been well explored. at Chapleau, Ontario (Usui unpubl, data). Al- The most conspicuous of dipteran anthophiles are though these beetles are often found in flowers, in the Cydorrhapha, represented by the Syrphidae, little is known of the food habits of adults in which feed on both nectar and pollen. Barrett and general (Becker in Danks 1970: 374). Can- Helenurm (1987) list species of Syrphidae from tharidae are also common on flowers, but records most of the flowers they studied. Among the from boreal plants are few (Cantharis spp. on C. Acalyptratae commonly associated with flowers are canadensis by Barrett & Helenurm 1987). Barrett members of the Conopidae, Milichiidae, and Chlo- and Helenurm (1987) also recorded a few flower- ropidae. visiting representatives of Curculionidae (Anthono- The Calyptratae have representatives as common mus spp. and Tychius stephensi Schoenherr from C. anthophiles. The Tachinidae, Anthomyiidae, Mus- canadensis) and Buprestidae (Anthaxia ex pansea cidae and Sarcophagidae are often found feeding on LeC. from Trillium undulatum Willd.). nectar and some on pollen at flowers (see examples Particularly interesting is the frequency of Eus- in Barrett & Helenurm 1987). The relationship of phalerum spp. (Staphylinidae) at flowers recorded in B. fletcheri and Sarracenia purpurea has been noted Barrett and Helenurm (1987). Their collections previously, but the fascinating association of Chias- included more than three species (40 individuals) tocheta spp. (Anthomyiidae), a seed parasite, and its from Aralia nudicaulis, one species (1 individual) host, Trollius europaeus L. (Ranunculaceae), for from C. canadensis, more than one species (6 which it is the exclusive pollinator, is extraordinary individuals) from Cypripedium acaule Ait., more (Pellmyr 1989). 254 P.G. Kevanetal.

Lepidoptera borers and the potential value of floral resources in the nutrition of the adults. In the Lepidoptera, it can be assumed that almost all Among the Parasitica, the value of nectar to adult (Rhopalocera) feed on floral nectar. Un- nutrition is well known in temperate (Syme 1975) fortunately, the adult feeding habits of most moths, to arctic (Kevan 19 73) regions. Their importance in even those of great economic importance in the pollination is probably small in boreal environ- boreal forest and elsewhere, are not understood. ments. In the Aculeata, the flower visiting habits of Many taxa of microlepidoptera probably do not feed Chrysididae, Formicidae and Sphecoidea are as adults. In most of the taxa of larger moths it is known, but the importance of that in the boreal has expected that the adults feed on floral nectar at not been investigated. Even the flower relations of night. Some Pyralidae are involved in the pollina- boreal Apoidea have scarcely been studied. tion of some orchids (see previous Orchidaceae Our recent studies (Usui & Kevan unpubl, data) section). Barrett and Helenurm (1987) list a few of the flower relations of boreal Apoidea have Noctuidae on the flowers they studied in New revealed 97 species of bees in six families. Table 1 Brunswick. However no systematic overview of the compares the relative proportions of taxa within nutrition of adult moths seems to have been made. Apoidea for North America north of Mexico and the This probably reflects the techniques used to collect boreal zone. The diversity of boreal bees is clearly these primarily nocturnal insects. Munroe (in Danks low, but within taxa, the proportionate diversity 1979: 434) points out that the lack of information indicates that, at the generic level, the Apoidea are on the pollinating activities of Canadian Lepi- diverse. The Anthophoridae are relatively poorly doptera needs consideration. represented. At the specific level, the diversity of bumblebees makes the relatively speciose in Hymenoptera the boreal zone, followed by the Colletidae, Halic- tidae and Megachilidae. The Hymenoptera contain the most important The biology of boreal bees is not well known. anthophiles, the Apoidea. Ne;eertheless, among the Aspects of the foraging behaviours of bumblebees Symphyta, flower visiting is well known, although have been researched by Heinrich (1976a,b, not well studied in the boreal zone or elsewhere. This 1979a,b) with respect to their ergonomics. Their is an important gap in knowledge considering the foraging behaviour with respect to specific plants importance of this group as defoliators and wood has been investigated by various researchers, noted

Table 1 Relativeproportions of Apoidea within North Americanorth of Mexico and the boreal zone (North Ontario). The numbers of genera and species in North America north of Mexico are from Hurd (1979)

Family Genera Species N. Ontario N. Americanorth Ratio N. Ontario N. Americanorth Ratio of Mexico of Mexico No. % of No. % of a : c b : d No. % of No. % of a : c b : d (a) fauna (c) fauna (a) fauna (c) fauna (b) (d) (b) (d) Andrenidae 3 14.3 I4 12.1 021 1.18 20 20.6 1 t99 33.9 0.02 0.61 Anthophoridae 4 19.0 44 37.9 0.09 0.50 7 + 7.2 989 27.9 0.01 0.26 Apidae 2 9.5 4 3.4 0.50 2.79 12 12.4 54 1.5 0.22 8.27 Colletidae 2 9.5 5 4.3 0.40 2.21 12 + 12.4 153 4.3 0.08 2.88 Halictidae 5 23.8 21 18.1 0.24 1.31 22 + 22.7 506 14.3 0.04 1.59 Megachilidae 5 23.8 23 19.8 0.22 1.20 24 24.7 607 17.1 0.04 1.44 Melittidae 0 0.0 3 2.6 0.00 0.00 0 0.0 30 0.8 0.00 0.00 Oxaeidae 0 0.0 2 1.7 0.00 0.00 0 0.0 4 0.0 0.00 0.00 Total 21 -- 116 -- 0.18 -- 97 -- 3542 -- 0.03 -- Pollination ecology of the boreal zone 2 5 5 previously. Boreal bees, like those in other biomes, in forestry on insect pollinators (Box I) and Table 3 forage extensively for floral nectar and pollen. We provides data on the deleterious effects of pesticides have little information on specialized floral relation- on plant reproduction in forests (Box IV). It should ships such as for Bombus consobrinus Dahlbom and be noted that the plants listed in Table 3 are septentrionale Koelle in Scandinavia (L~- common to the boreal zone. ken 1950, 1973; Mjelde 1983; Laverty & Plow- The effects of pesticide applications on natural right 1988) or special resource provisioning by frugivores are most evident when herbicides are plants (e.g. oil: Vogel 1974; Neff& Simpson 1981) used to control regenerating plants that compete or even of the use of unusual, but abundant with conifers in burns or cut-overs. There, the resources such as pine pollen (e.g. its use by Osmia reduction in blueberry productivity is almost total spp. in Nevada: Rust 1987). (Usui & Kevan unpubl, data from Chapleau, On- The nesting biology of some boreal bees has been tario) and this must affect the food resource of many investigated by Fye (1965) for Megachilidae (Os- . These include black bears for which blue- mia, Megachile, Hoplitis) and Colletidae (Hylaeus). berries and other fruits are an important part of the Plowright and Laverty (1984) remark on the gen- diet, influencing hibernation, health and birth, and eral biology of Bombus, including those associated early nutrition of cubs (Kolenosky 1989). The with boreal communities. effects on other wildlife have been discussed by Kevan and Collins (1974) who describe the eco- logical web of effects that influence positively the EFFECTS OF PESTICIDES ON 'health of frugivorous birds in a fruit-poor forest. POLLINATION The birds become pests on blueberry barrens, al- ready below production potential because of severe Chemical pesticides are known to perturb relation- reductions in populations of pollinators. ships in pollination ecology (National Research Council of Canada 1981) and have been shown to have adverse effects on pollinators and plant fecun- DISCUSSION dity in boreal and other forest communities. The problem of pesticides applied for forest General ecological and evolutionary protection has been reviewed recently by Kevan and constraints Plowright (1993) and particularly with regard to fenitrothion (Kevan & Howright 1989). From these For evolutionary ecologists the boreal zone has much reviews it is dear that pollinator populations in and to offer, from the viewpoint of basic science to around boreal forests of New Brunswick, Quebec applications for management and conservation. The and Ontario have suffered set-backs. Figure 1 mutualisms associated with pollination biology are presents the kinds of pollination processes that have barely understood, yet are components of a keystone been adversely affected by applications of pesticides process which links the plant and animal life of this in general and those for which there is evidence in the vast region. boreal zone. Although only a few studies stand out as boreal in The effect of pesticides on pollen development essence, many others are directly or indirectly rele- (Fig. 1, Box II) in boreal plants is probably insignif- vant. The boreal flora contains the gamut of exam- icantly small because of the amounts of pesticide ples of plants with highly specialized pollination used and the minute chance of pollen coming into systems involving wind and insects to those with contact with the material. Thus, the ensuing prob- generalized pollination biology, self-pollination and lems (Box III) are probably minimal for anemophil- agamospermy. ous plants, unless the gynoecial apparatus is The role of the boreal insect fauna in pollination is adversely affected (no firm evidence for forestry even less appreciated. However the diversity of pesticides [Box II]). The effects for entomophilous anthophilous insects spans the spectrum from pollination are documented in Tables 2 and 3 and, springtails to long-tongued bees and butterflies. The depending on the pesticide used, may be small or importance of floral resources to many boreal in- severe. Table 2 summarizes effects of pesticides used sects, even well known pest species, is unknown. 2 5 6 P.G. Kevan et al.

PLANT toxicologylecotoxicology1

II

~ Pollinator nutrition ~ Pollendeveiopment LLINATOR 1 Hstil development eclt%;~176 y Pollen release/exposure Pistil maturation Pollinator bionomics Pollen transport receptivity P oUinatorpop,_, !a_r Pollinator behaviourl effwiency 1 J ~PoIlengermination ~ 2 Pollen tube growth Pollen cell division HI Fertilization of ovule Embryo development Seedand fruit production Crop yields

(~,,a * <2 12> * Agr/cu/um// ugivores, etc. Humaneconomy/ ~ affairs 1 Fig. 1. Components of pollination directly affected by pesticides (bold, italic type); indirectly affected (italic); and presumably affected (bold); together with processes known to be directly affected (arrows) (redrawn from Kevan & Plowright 1989). *Supportive data from boreal forest; *relevant data in Sutherland et aL (1984) for Pseudotsuga menziesii (Mirb.) Franco and Picea glauca (Moench) Voss.

Table 2 Reductions in pollinator populations attributed to insecticide usage in forestry (Kevan & Plowright 1993)

Insecticide Pollinators Effect Location Fenitrothion Wild pollinators of blueberries Negative New Brunswick Bumblebees Negative New Brunswick Solitary bees Negative New Brunswick diversity Changed Quebec Aminocarb Pollinators including Diptera Negative New Brunswick Bumblebees No effect recorded New Brunswick Solitary bees Negative New Brunswick Bumbie bee diversity Changed Quebec Carbaryl Wild bees No effect recorded Montana Negative Maine Carbaryl + acephate Wild bees Negative Pacific NW. USA Diflubenzuron Wild bees No effect recorded Pacific NW. USA Pollination ecology of the boreal zone 257

Table 3 The effects of insecticides applied in forests on the fruit set ofentomophilous plants (summary of data from Kevan & Plowright 1992)

Plant species Insecticides Location Fenitrothion Aminocarb Carbaryl Vaccinium angustifolium & Negative effect* -- -- New Brunswick I1". myrtilloides Rhodora canadensis Negative effect* Negative effect* -- New Brunswick Kalmia angustifolia Negative effect* No significant effect -- New Brunswick Maianthemum canadense Negative effect* No significant effect -- Quebec Negative effect* Negative effect* -- New Brunswick Comus canadensis Negative effect* No significant effect -- Quebec Negative effect* No significant effect -- New Brunswick Comus stolonifera Negative effect* Negative effect (ns) -- New Brunswick Comus alternifolia Negative effect* -- -- New Brunswick Aralia nudicaulis Negative effect* Negative effect* -- Quebec Negative effect* -- -- New Brunswick Clintonia borealis No significant effect No significant effect -- Qubec Negative effect* No significant effect -- New Brunswick Trifoliumpratense Negative effect* -- -- New Brunswick Viburnum cassinoides -- -- Negative effect* Maine Viburnum trilobum Negative effect* -- -- New Brunswick Cypripedium acaule Negative effect* -- -- New Brunswick Prunus pensylvanicat No significant effect No significant effect No significant effect Ontario Ranunculus* No significant effect -- -- Newfoundland *Significant effect; ns: effect noted as a trend, but not statistically significant; *species inappropriate for testing.

Unfortunately little can be gleaned of the habits of the community is short. The most conspicuous is the same species, even in other environments, be- that in which Vaccinium spp. assume dominance cause studies have not been done. after fires or cut-overs. Then, it takes only about a One feature of the boreal flora and fauna is the decade for the entomophilous plants to be over- paucity of endemic taxa. This may be explained in topped by trees and shaded so that flowering is two ways. First, the relatively young geological age inhibited or the plants die out (Hall & Shay 1981). of the zone has not provided time for endemics to The Vaccinium-dominated sere exemplifies the evolve and, second, the zone is chronically disturbed generalist pollination systems which operate. Vac- by fire and outbreaks of pest insects. Both features of cinium angustifolium itself has a wide array of the zone's ecosystem would tend to encourage vagile pollinators (Finnamore & Neary 1978; Mohr & organisms capable of rapid colonization of newly Kevan 1987) and represents one of the more opened and successional habitats. That, coupled specialized pollination systems in terms of floral with the absence of any major biogeographic barriers complexity and pollinator manipulation of the in most of continental America, Europe and Asia flowers to bring about pollination. within the boreal zone or with zones to the south or north, would work against endemism being com- Pollination, breeding systems and growth mon (see also Kevan & Danks 1986). form With both the flora and fauna adapted to distur- bance and being vagile, constraints on the adaptive- Nevertheless it is worthwhile to compare pollination ness of specialized mutualisms would be strong. For in the boreal zone with that in other zones. Using the a specialized mutualism to persist, both partners lists of Moir (1958), Zoladeski (1989) and Larsen would have to colonize their appropriate sere simul- (1980) we find that 34% of the flora is anemophil- taneously if either were to survive. The duration of ous and 65% zoophilous (1% unknown). Dioecism seres in which insect pollination is a major process of is represented in the flora at slightly over 6% and 258 P.G. Kevan et al.

non-dioecious breeding systems at 75%. We know loo ~ -lilT: 90 " "v"'+'/;> ' i i ...... too little of the remaining 19% to comment. Among 80 ~ '- ....

the anemophilous plants, at least 4% are dioecious 70 ~ ...r : ~ ......

and 51% not, but for 45% of the anemophilous "E 60 ",\ ...... i : .... flora we feel too little is known. We understand the SO ~ ---'~'~---~ : : ...... zoophilous flora better and 7% is known to be o.. 40 ..... dioecious, 90% not so and 3% are unknown. ao ~ ...... The non-dioecious plants include the gamut of 20 ~ ...... lo ~ ...... systems from cleistogamous sellers to obligate self- 0 incompatible outcrossers with heterostyly. The flora 1 2 3 1 2 3 1 2 3 Trees Shrubs Herbs needs examination species by species, in situ to determine the breeding systems represented. Only Fig. 2. The sexual expression and pollination system of in the Orchidaceae has a survey been made (Catling trees, shrubs and herbs of the boreal zone; based on floral & Catling 1991) in which the increase in autopolli- lists of Moir (1958), Larsen (1980) and Zoladeski (1989). nation with latitude is suggested to reflect the 1: [] Bisexual, [] unisexual flowers; 2: unisexual, [] hermaphroditic plants; 3: [] zoophilous, [] anemophilous. paucity of pollinators (Catling 1990; Catling & Catling 1991). Nevertheless, autopollination, at 16% in the boreal zone, is not that pronounced. 1986; but see Charlesworth 1993). The correlation Some breeding systems that function for one species of and shrubbiness may be explained by in one part of its range may be subtly or clearly the lesser effectiveness of wind as a pollen vector different in other parts (Barrett 1988). The different close to the ground and the adaptive significance of races of Trifolium repens L. in Europe (Akerberg outcrossing in these plants. Some are highly donal 1974), Kalmia latifolia in the eastern USA (Rathcke (e.g. Rubus, Vaccinium, Salix), which obligates & Real 1993), perhaps Pyrola uniflora in eastern them to relatively long-distance dispersal of pollen Canada (Barrett & Helenurm_!987) versus in Den- compared to non-clonal plants of similar height. mark and Sweden (Knudsen & Olesen 1993) Other habitat constraints may pertain to the above, and some Orchidaceae (Catling 1983) serve as ex- but not as obviously as in the herbaceous flora in amples. Differences in other breeding systems, such which Gramineae, Cyperaceae and Juncaceae con- as dioecy and heterostyly, are known to occur be- stitute most of the anemophiles. These are plants of tween populations of various species of plants (Rich- open habitats. Many herbaceous anemophiles have ards 1986), but whether or not the boreal flora offers breeding systems that circumvent dependence on other examples remains to be investigated. cross-pollination (e.g. autogamy and agamo- We noted the same trend in sexuality versus spermy). The herbaceous anemophiles have specific growth form of boreal plants as that noted by minimally overlapping periods of pollen liberation Darwin (1877) and Bawa (1980). Most trees have and stigmatic receptivity both seasonally and diur- unisexual flowers and many are unisexual as plants. nally (Ponomarev 1966; Ponomarev & Podosen- Among the shrubs about one-third have unisexual ova 1974; Ponomarev 1978; Levkovskii & flowers, the remainder have bisexual flowers and the Tikhmenev 1982; Tikhmenev & Kevan unpubl. incidence of dioecy is, at most, about 30%. As data). For the herbaceous flora with zoophilous Thomson and Brunet (1990) point out, the various flowers, the proportion of obligate out-crossers is hypotheses for the of dioecy are still being probably low (see also Vereshchagina 1968; Pono- debated and none can be rejected. Almost all the marev & Vereshchagina 1973). Baker's law (Steb- herbs are hermaphroditic with bisexual flowers bins 1957) might be invoked for some because of (Fig. 2). The trees are anemophilous, whereas most their quick colonization, for a short duration, of of the shrubs are zoophilous and the herbs show a open areas in the forest (revegetation by woody mixture of anemophilous and zoophilous plants plants being rapid after fire or cut-over). Such (Fig. 2). The correlation of the preponderance of plants, sometimes called weeds, are typically autog- and sexual separation of flowers in trees amous or agamospermous. Obligately out-crossing can be seen to have adaptive significance for promot- herbaceous plants might be expected to occur in the ing cross-pollination (Whitehead 1983; Richards more stable habitats such as in the established forest Pollination ecology of the boreal zone 259

(as examples in Barrett & Helenurm [1987] sug- associations, even though the importance of these to gest), in marshes and bogs (as in Sarraceniapurpurea the bionomics of the insect (even for pest species) or and various showy orchids) and perhaps in rocky, plant is unknown. Nevertheless, there are some treeless outcrops. peculiarities. Staphylinidae are not well known as Studies by Proctor (1978) are worth mention in anthophiles, yet Omalium and Anthobium are found that he examined anthecological adaptive types in in many flowers eating pollen and nectar, often 18 plant communities in Ireland. He categorized the being numerous (Proctor & Yeo 1973) and sta- plants as anemophilous, generalist entomophilous phyl'_-'~ '..ave been invoked as pollinators of Uvu- and specialist entomophilous. In general, he found laria perfoliata L. in North America (Whigham no association of the ratio of anemophily to general- 1974). The role of Eusphalerum in boreal anthecol- ist entomophily with the phytosociological progres- ogy (Barrett & Helenurm 1987) would be especially sion of increasing species richness and stability. interesting. However he did find a significantly positive relation Among the families of bees, the relative species of the ratio ofentomophily as a whole to anemophily dominance of the Apidae and the paucity of Antho- with phytosociological progression. In the most phoridae are striking. In the Apidae, Bombus and stable and species-rich communities, which in- Psithyrus, with 13 species total (Laverty & Harder cluded heaths, bogs and woods, the relationship was 1988), are the only genera, the latter parasitic on the highly positive for the ratios of both entomophily as former. These bees are excellent at overwintering, a whole and specialist entomophily to anemophily. are vagile, capable of generalist anthophily and are The trend in the boreal forest appears to be similar in social; features which allow them to exploit the some respects, but the pollination mechanisms of whole flowering season, resist short periods of the plants in the phytosociological progression must inclement weather in summer and offer mutual be related to their requirements, breeding system protection of workers, drones and queens. Further- and place in the strata. more the often large numbers of rodent burrows, Although the importance of zoophily and self- fallen trees and well-drained mossy substrates in pollination can be understood in terms of the size, summer provide appropriate nesting sites (Heinrich life-span and habitats of herbs and small shrubs (as 1979b). The Anthophoridae represent the other in other environments to the south or the north: e.g. extreme. Many genera (e.g. Peponapis, Xenoglossa, Kevan [ 1972 ], Tikhmenev [ 1984]) the importance Cemolobus, Melitoma, Ptilothrix, Ancyloscelis, Dia- of anemophily in trees is probably well explained by dasia) have special relations with particular taxa of Whitehead's (1983) and Regal's (1982) reasoning plants, which do not occur in the boreal zone. of the interaction of biotic and abiotic factors. Nomada, the most speciose genus (more than 500 Conspecific individuals grow close together in an species in Nomadinae) of Anthophoridae, is para- environment of sharp seasonality and have early, sitic. We have collected only about seven species in highly synchronized flowering. Further, closed can- the boreal zone. We suggest that these bees are opy boreal forests are generally unsuitable for reli- unable to effectively track their vagile potential ably large populations of pollinators. hosts in the rapidly changing seres of the boreal zone The unsuitablility mentioned previously stems which support high populations of bees such as from seasonality, severe winter cold, generally high Colletidae, Halictidae and Andrenidae. Popov moisture content of the soil and the nature of the (1958) draws attention to the concentric biogeo- trees (small leaves or deciduous and with resinous graphic ranges of Lysimachia (Primulaceae) (larg- wood), which together limit the overwintering, est), its pollinators, Macropis spp. (Melittidae), and oviposition and nesting sites available to specialized its parasites, Epedoides spp. (Anthophoridae) anthophiles. These issues are discussed in the follow- (smallest). Although none are boreal, the iesson of ing section with particular reference to bees. the more restrictive ranges of symbiotic dependents versus those of their hosts seems to apply. The Andrenidae of the boreal zone are relatively Faunal features depauperate (Knerer & At-wood 1964; Table 1) and The fauna of anthophiles in the boreal zone contains this may reflect the specialist relationships of some numerous taxa that are well known for the flora] taxa (e.g. Perdita with more than 500 species; 260 P.G. Kevan et al.

Linsley 1958; Stephen et al. 1969) which do not the ecosystem; (ii) the frequent perturbation of the reach the boreal zone. The specialist relationships do forest as part of its natural history; (iii) the require- extend into the boreal zone with blueberry bees such ment for organisms in such an environment to be as Andrena bradleyi Viereck, Andrena longifacies vagile, which in turn restricts opportunity for tightly LaBerge, and Andrena regulans Malloch (Mitchell evolved mutualisms to evolve; and (iv) the severity 1960; Bouseman & LaBerge 1979; LaBerge 1980). and duration of winter cold in limiting the flora and The boreal Megachilidae are represented mostly by fauna to taxa with strong adaptations to overwinter- Megachile and Osmia. The Halictidae are repre- ing and the short summer season. sented mostly by Dialictus, Lassioglossum, Evylaeus The pollination systems in the boreal forest seem (see Knerer & Atwood 1962). Halictus and the to be rather open by comparison with some others parasitic Sphecodes. The Colletidae are represented (possibly in deserts and tropical rain forest) making by Colletes and Hylaeus. them relatively well buffered against perturbations, Another constraint to living in the boreal zone is including fire, logging and the impact of pesticides. the winter cold (Fye 1972). Among solitary bees The extent to which the buffering capacity can there is little information on their abilities to over- absorb the frequency, extent and type of perturba- winter. Krunic and Salt (1971) found that neither tions is a matter of concern to sustainable forestry Megachile rotundata (Fabricius) nor Megachile rela- and environmental conservation, and a matter of tiva Cresson are frost-tolerant, but the latter can great debate. withstand freezing temperatures whereas the former cannot. In general, the ability to supercool and resist freezing is an adaptation that insects have to their ACKNOWLEDGEMENTS environment (Somme 1982) and one might expect evolutionary or phylogenetic constraints to apply to This work was funded in part by NSERC Grant No. the northern extent of insects' ranges (see Danks A-8098 to PGK. We wish to thank Kevin Barber, 1978) even though variability is known (Somme Vince Nealis and anonymous reviewers for critical 1982). The availability and siaitability of overwin- review of the manuscript. Colleagues, including A. tering sites for bees in the boreal zone is not known. Gordon and M. Offer at University of Guelph, M. Bumblebees, if like most in England, require Obbard and G. B. Kolenosky at Ontario Ministry of shaded, well-drained sites into which the insemi- Natural Resources, and C. D. Michener, F. Silviera nated queens can burrow (see Alford 1969; Fussell and M. Lane at University of Kansas have been & Corbet 1992). Solitary bees may overwinter as helpful in discussing various aspects of this paper. prepupae or as adults (Halictidae) in their nests. The Great help in the of boreal insects col- ground-nesting species (e.g. Colletes, most Halic- lected in Chapleau Crown Game Preserve was tidae, Andrena) would seem less exposed to extreme provided by the following: T. Laverty (Apidae: cold than the twig-nesting bees (e.g. Hylaeus; Saka- Bombus and Psithyrus) at the University of Western gami & Toda 1986). Those nesting in wood, such as Ontario, L. Packer (Halictidae) at York University, some Megachilidae (e.g.M. frigida Smith) and G. Knerer (Halictidae) at University of Toronto, G. Anthophoridae (e.g. Anthophora [Clisodon] termi- Eickwort (Halictidae: Dialictus) at Cornell Univer- halls Cresson), may withstand intermediately severe sity, W. LaBerge (Andrenidae) at Illinois Natural cold. Museum, C. D. Michener (Megachilidae and Col- letidae), R. Brooks (Anthophoridae: Anthophora), B. Alexander (Anthophoridae: Nomada) and A. SUMMARY Roig (Anthophoridae: Epeolus) at University of Kansas, and E. C. Becker, J. McNamara, E. Rickey In summary, we suggest that the diversity of (Coleoptera), R. Skidmore (Orthoptera), K. B. pollination systems from both botanical and ento- Bolte (Lepidoptera), H. B. Bisdee, J. Denis, H. mological perspectives is great, ranging from spe- Goulet and L, Masner (Hymenoptera) at Biosys- cialist to generalist. Constraints on the extent and tematics Research Centre, Ottawa. We are also most potential for high degrees of specialization stem grateful to J. ,Lupson for her assistance in the from a suite of factors: (i) the relatively young age of preparation of the manuscript. Pollination ecology of the boreal zone 261

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