1999 daniel mcalpine memorial lecture · ring pycniospores from the pycnia of infected plants to...

Australasian Plant Pathology (1999) 28: 269-282

1999 Daniel McAlpine Memorial Lecture

Bees and fungi, with special reference to certain plant pathogens

D.E. Shaw

Presented at the 12th Biennial Conference of the Australasian Plant Pathology Society, Canberra, Australian Capital Territory, 27-30 September 1999.

C/- Department of Primary Industries, Meiers Road, Indooroopilly, Queensland 4068 Australia

Daniel McAlpine

This lecture commemorates the life and work of Daniel McAlpine and his contribution to plant pathology. McAlpine, a Scotsman, matriculated at London University, studied botany and geology at the Royal School of Mines, South Kensington, as well as biology under Professor Thomas Huxley, and was later appointed Professor of Natural History in Edinburgh. He migrated to Australia in 1884 and after teaching at Ormond College was appointed Vegetable Pathologist with the Depart- ment of Agriculture in Victoria in 1890. He investigated the plant disease situation in Australia and extended this knowledge to scientists and primary producers in various publications on plant disease in many crops and other plants. His work during 26 years has rightly earned him the title of 'Father of Plant Pathology' in this country (Came 1927-28; Fish 1970; 1976; White 1981).

Introduction

It is estimated that the world population will be 10 billion in 2050 AD (Rothschild 1998). The world's population depends on (in the first or other degrees) the vegetation of the planet for food, fodder, fibres, fuel, timber, paper, pharmaceuticals, oxygen, water etc. Two of the many components contributing to the wellbeing of the earth's vegetation are (1) the work of the plant pathologists, and (2) successful pollination.

The biotic pollinators include bees, wasps, flies, butterflies, moths, beetles and other insects, birds, marsupials, monkeys, lizards etc, with bees,

especially honey bees, being predominant in many parts of the world (Proctor et al. 1996).

Early records of honey hunters, beekeeping, and biotic pollination

The earliest record ofman's involvement with bees is a pictorial one of honey hunters on the wall of a cave in Spain ca. 6000 BC, and the first record of beekeeping is also a pictorial one from Egypt ca. 2400 BC (Crane 1983).

Although a carving from the palace of an Assyrian king ca. 860 BC shows hand pollination of date palm (Buchrnann and Nabhan 1996), and although Aristotle noted floral constancy by bees in the 4th century BC (Proctor et al. 1996), there was no knowledge of the role of insects in pollination until a few hundred years ago. About that time in the UK, Miller (1691-1771) worked with tulips and bees, and Dobbs (about 1750) confirmed his work and noted floral constancy. In Germany, Kolreuter (1 733-1 806) carried out experiments on insect pollination, examined many nectars, and concluded that nectar was the source of honey (Proctor et al. 1996).

Main field activities of honey bees

The four main field activities of honey bees and their relatives are the collection of nectar, pollen, propolis and water. Instead of nectar, bees in some areas collect insect honeydew. Nectar (and insect honeydew) is high in sugars; pollen in protein, vitamins, lipids and minerals; propolis (used for

Australasian Plant Pathology Vol. 28 (4) 1999

in-hive repair) in resin, wax and essential oils. Water is needed for the dilution of larval food and for cool- ing and humidifying the interior hive environment. Nectar and water are transported to the hive inter- nally in the honey stomach, whereas pollen and propolis are carried externally in pollen baskets (corbiculae) on the outside of the back legs.

Bees and fungi

Fungi are associated with bees in various ways, including the following:

1 . As atmospheric mycospora which may be deposited on flowers and on bees.

2. In nectar and honey. In nectar yeasts predomi- nate; in honey most spores do not grow (due to the high osmotic pressure etc.) but, if there, they may persist when honey is diluted.

3. On and in pollen. For example, pollen of lucerne may carry the fungus Verticillium alboatrum when incidentally transported by the alfalfa leafcutting bee Megachile rotundta (see Table 1).

4. In the hive and on provisions. Many species of fungi have been recorded.

5. On and in bees, and as pathogens of bees. The fungus Ascosphaera apis (the cause of chalkbrood) and other species ofAscosphaera have been examined molecularly by Anderson et al. (1998). Four new species in this genus have also been described, and three other isolates including A. apis, not previously known in Australia (Anderson and Gibson 1998).

6. In substitution and supplementary food. Brew- ers yeast is one of the important constituents of these foods.

7. In incidental transport during normal foraging. 8. In the collection of fungal spores in lieu of

pollen. Only the two last items will be discussed in the

following sections.

pycnidial secretion as in some rust fbngi. Only those records involving bees and plant pathogens are listed in Table 1, together with references. Only two of the items are mentioned below.

Various studies in the United States of America (USA) and Canada have tested fungi, mainly Gliocladium roseum, as possible control agents of fungal pathogens by bees, including Sclerotinia sclerotiorum causing stem rot of canola (Brassica napus) by honey bees (Apis mellifera) (Table 1). Tests carried out in Canada against Botrytis cinerea causing grey mould of strawberry and raspberry flowers used both honey bees (A. mellifera) and bumble bees (Bombus impatiens). Bee-vectored inoculum effectively controlled B. cinerea in petals, stamens and flowers of strawberry and in flowers of raspberry. However, raspberry fruits were not ad- equately protected, presumably because B. cinerea is able to infect drupelets directly as well as by invasion of flowers (Table 1).

In the USA, when the fungus Puccinia monoica infects its aecial host (species of Brassicaceae, especially Arabis) it causes leaves to be yellow and clumped, visually similar to the flowers of the but- tercup (Ranunculus sp.), and hence called 'pseudoflowers'. The pseudoflowers exude a sweet solution which attracts hallictic and andrenid bees as well as other insects. The insects help in transfer- ring pycniospores from the pycnia of infected plants to other pycnia. The pseudoflowers also produce a distinctive floral fragrance composed primarily of aromatic alcohols, aldehydes and esters, whereas infected plants produce only green leaf volatiles, mainly terpinoides, ubiquitous from vegetative tis- sue. The yellow pseudopetals also reflect UV light, so that the pseudoflowers give gustatory, olfactory and visual cues to bees (Table I).

Canada thistle (Cirsium awense) plants infected with the systemic sexual state of Puccinia punctiformis also produce fragrant volatiles but although this is stated (Connick and French 199 1) to facilitate cross-fertilisation by attracting insects, these have not apparently included bees.

Incidental transport

Plant pathogenic propagules may be incidentally transported by bees of various genera and species during their normal foraging as well as by many other insects. The foraging may involve the collection of nectar, or insect honeydew (secreted especially by aphids and scale insects), or fungal honeydew as in species of Claviceps, and the sweet

The collection of spores in lieu of pollen

The collection of spores by honey bees was first recorded in 1875, and since then the records have all involved bees in the family Apidae, mainly the European honey bee (Apis mellifera). The fungi collected in lieu of pollen have included various


Table 1 Plant pathogens incidentally transported by bees (various genera and species) (and other insects) during normal foraging

Pathogen Host Location Reference

Botrytis anthophila

B. cinerea

B. cinerea (per biocontrol fungus Gliocladium roseum)

B. cinerea (per biocontrol fungus G. roseum)

Claviceps fusifbrmis

Claviceps purpurea

Colletotrichum gloeosporioides

G. musae

Fusarium moniliforme (Gibberella fujikuroi) var. subglutinans

Microbotryum violaceum

Monilinia vaccinii corymbosi

Ovulina azaleae

Puccinia monoica & P thalspeos

Sclerotinia sclerotiorum

Sclerotinia sclerotiorum per biocontrol fungus Gliocladium sp.

Thecaphora deformans

Unidentified Ustilago violacea

see Microbotrym violaceum

Verticillium alboatrum

Red clover

Strawberry flowers

Strawberry &/or Strawberry flowers

Strawberries

Pearl millet

Honey from rye

Limes

Musa balbisiana

Pineapple

UK

Denmark

Canada

USA

India

Austria

USA

Colombia

Brazil

Possibly Silene acaulis Russia Possibly Stellaria longipes Canada Viscaria vulgaris Sweden T/i vulgaris & Melampyrum pratense Sweden

Blueberries & USA huckleberries

Azalea spp. USA

Arabis drummondii USA & other genera of Brassicaceae

Rapeseed Canada

Canola Canada

Dwarf gorse UK

Aubergines UK

Lucerne Canada

Silow 1933

Kovacs 1968

Peng et al. 199 1 ; 1992 Sutton & Peng 1993 Yu & Sutton 1994; Sutton et al. 1997

Hood & Miller 1997

Sharma et al. 1983; Verma & Pathak 1984

Anon. 1953

Pefia & Duncan 1989

Cardeiiosa-Barriga 1963

Costa & Lordello 1998

Hereg 1924 Kevan & Parmelee 1972 Jennersten 1983a; 19836; 1985; 1988 Jennersten & Kwak 199 1

Batra, L.R. 1983 Batra & Batra 1985 Batra, S.W.T. 1987

Smith & Weiss 1942 Weiss & Smith 1940

Raguso & Roy 1998 Roy 1993; 1994a, 19946 Roy & Raguso 1997

Stelfox et al. 1978

Israel & Boland 1992

Brett 1966

Griffiths & Roberts 1966

Huang & Richards 1983 Huang & Kokko 1985 Huang et al. 1985; 1986


plant pathogens causing rust and powdery mildew diseases, and species of Neurospora (non-pathogenic to man, other animals and plants), as well as a few other fungi. The Neurospora has been mainly recorded on filter mud, the precipitated impurities obtained during cane sugar extraction. The records, although infinitesimal in number compared with pollen collection , have now occurred on all conti- nents (except Antarctica) and in the East and West Indies. The records are not expanded here but are listed with references in Table 2, with common names as in the original papers. Some aspects ofthe collections are briefly discussed in the following sections.

Duration of collecting Data on this aspect are not available for some records, but have been recorded for others including the following. Bees collected spores of powdery mildew (Oidium farinosum) from apple trees during 14 days in Germany (Kraus 1920). In Israel, large numbers ofbees gathered the spores of poplar rust (Melampsora larici-populina) in October-November 1940. In 194 1 the rust appeared in the latter half ofAugust and spores were collected until the beginning September, when the bees disappeared. At the beginning of October the bees reappeared at the start of a second rust attack (Minz 1942).

In January and February 1954, 1955, 1957 and 1958, microscopic examination of corbicular loads in the Mahebleshwar area of India showed that they consisted uniformly of spores of Zaghouania oleae which infects Olea dioica. None of the loads collected in January-February 1956 showed the spores, perhaps due to the flowering of Nil- girianthus heyeanus v. neesii, which blooms only once in three years (Deodikar et al. 1958).

In the Netherlands, bees collected spores of Melampsora larici-populina in August-October 1986 (Moraal 1988), while in Mexico spores of Cronartium conigenum were collected fi-om rusted pine cones in June-July (Trujillo Flores and Pefia Garcia 1989). Corbicular loads sampled on 24,28 and 29 September 1992 in the United Kingdom contained spores of poplar rust (M. larici-populina) (Kirk 1994; 1996, personal communication).

Conidia of Neurospora were present and being collected by bees during a visit by Drs G.R. and A.M. Stirling to a heap of filter mud ca. 110 km north of Brisbane (Table 2). During the first visit they estimated that there were 20 bees per mZ. The bees were still foraging on the same heap during a

second visit 10 days later (although there was reduced coverage of fungus due to rain) when they estimated 40 bees per m2. Colonies of Neurospora occurring at sites in a coastal strip over 1000 krn long in eastern Australia (Shaw 1990a) have been checked only intermittently during the last two dec- ades, but bees foraging on this resource (Neu- rospora) have been recorded 25 times during a period of 22 years (Shaw and Robertson 1980; Shaw 1990b; 1993; 1998 and herein).

The continuous spore collection at some of the sites listed in Table 2 indicates the apparent accept- ance by the housekeeping bees of the propagules and the continued recruitment of foragers to these resources.

Reasons for the 'in lieu' collecting Some authors attributed the collection of fungal spores to a dearth of pollen at the time. In New Zealand, Bennie (1 942) stated that the reason bees collected spores of Puccinia graminis (avenae) from a chaff cutter which had cut rusted oat straw the previous day was because the severe winter had killed all the gorse and broom blossom with a resultant shortage of pollen in early spring. In India, aeciospores of Zaghouania oleae were collected in those years when a local tree (Nilgirianthus heyneanus var. neesii) was not flowering, as it blooms only once in three years (Deodikar et al. 1958). During 1963 in Jamaica, honey bees were seen to visit allspice (Pimenta dioica) at a time when trees bore no flowers but which were infected with Puccinia psidii. Loads in the corbiculae consisted of pure samples of urediniospores (Chapman 1964). In Florida, bees were recorded collecting spores of Puccinia oxalidis on Oxalis spp. at a time when frost had killed perhaps 95% of the local blossoms (Wolfenbarger 1997). In South Afi-ica, Melampsora spores growing on the weed Euphorbia geniculata were collected during periods of general pollen scarcity (Johannsmeier 198 1). Collections of spores of Cronartium conigenum from Pinus spp. in Mexico were particularly abundant from mid-June to mid-July, a period of few flowers, but diminished later with the occurrence of a greater variety and quantity of pollen (Trujillo Flores and Pefia Garcia 1989). In New South Wales, honey bees collected conidia of Oidium sp. on rose leaves in a garden during a two years' drought (Ray 198 1 personal communication).

On the other hand, various authors recorded the collection of fungal spores in lieu ofpollen at times


when flowers were present in the vicinity. For example, bees collected spores of Caeoma nitens rust of wild dewberry in Texas because it h i s h e d an easy and abundant supply, although some plants of various species were flowering in the vicinity (Lang 1901). In Germany, bees were noted at the time of apple blossoming collecting either the conidia of powdery mildew (caused by Oidium farinosum) or apple pollen (Kraus 1920). In Sarawak, the Giant Asian honey bee (Apis dorsata) twice collected urediniospores of tropical maize rust (caused by Pucciniapolysora) although ample pollen was available on the same plants, and which pollen, in fact, was being collected by the stingless bees (Trigona spp.) (Turner 1974). Spores of Melampsora larici-populina on poplars were collected by honey bees in Western Australia, although urediniospores of plum rust (caused by Tranzschelia pruni-spinosa) were also present but were ignored (Dell 1977). Bees collected spores of willow rust (caused by Melampsora sp.) in the USA and although some bees were visiting sage (Salvia sp.) in the same area, they were very few compared with the activity in the willows, i.e., the bees clearly pre- ferred foraging the willow rust to nearby sage which provides both pollen and nectar (Williams and Tomlinson 1985). Bees in South Africa collected spores of Melampsora ricini on the castor oil plant, ignoring flowers in the vicinity (Wingfield et al. 1989).

While there are now records of bees collecting Neurospora conidia, these have been from large blooms of the fungus which have provided ample spores. For example, in Bolivia, the bees gathered a load of spores possibly in a third or less of the time commonly utilised when collecting pollen from flowers, as in an area of a few cm2 they encountered sufficient quantities to complete their load (Kempff Mercado 1955). This was also the experience in eastern Australia, where bees collected from large areas of Neurospora, but not from small colonies, or those with limited sporulation under drought conditions, where the relatively few spores available were apparently not a sufficient reward for the energy that would be expended in foraging (Shaw 1998).

Therefore, fungal spores have been collected at times of pollen dearth, but also at other times when presumably the reward (in spores) has been sufficient to repay the energy expended in the collection.

Fungal spores are, of course, available through- out the entire period of a bee's daytime foraging, whereas pollen of some flowers is only available at

certain times of the day. One further point should be mentioned, viz., that if bees collect fungal spores in lieu of pollen they will not be fulfilling their role as pollinators. However, as some records occurred in times of pollen dearth there may in fact have been reduced pollination, even if the bees had not been collecting fungal spores at the time.

Size of pollen and fungal spores collected by bees Although pollen grains measure from 5 to over 200 pm in diameter (Faegris and Iversen 1989), and even >300 pm (Roubik 1989), the size of grains usually collected by bees is in the smaller range of up to 100 pm with mean 34 pm (Roberts and Vallespir 1978) with grain contents lipid-rich rather than starchy (Baker and Baker 1983). The size of the fungal spores collected by bees (rust urediniospores ca. 2 0 4 0 x 10-25 pm; powdery mildew conidia ca. 20-30 x 10-20 pm, and Neurospora conidia ca. 5-1 5 pm) falls within the range of grains usually collected by honey bees.

Type of bee All the records in Table 2 refer to the European honey bee (Apis mellifera) except for two records of the Giant Asian honey bee (A, dorsata) (both Turner 1974) and two records of Trigona spp. (Trigona cf. branneri) (Burr et al . 1996) and 7: amalthea (Roubik 1989). The preponderance of records involving A. mellifera may merely reflect the attention given to this species in beekeeping milieus around the world.

Spore forms collected Most of the rust hngi collected were urediniospores, with only a few records of aeciospores or aeciospore-like propagules (Zabriskie 1875; Deodikar et al. 1958); ustilospores of Ustilago (Betts 19 12) and of Ustilaginales (Maurizio 1975); and conidia of Oidium spp. and Neurospora. All these spores are dry deciduous spores with ease of detachment and are normally wind-blown (anemophilous). However, there are now two records of species of stingless bees (Trigona) foraging on the fruiting bodies of a stinkhorn (Staheliomyces cinctus, Phallaceae) and the gleba of an unidentified fungus in Ecuador and Panama, respectively, when the bees removed parts of the thalli before packing the pieces into their corbiculae.

Colour Honey bee are usually highly sensitive to long-wave ultra violet (LW UV) and insensitive to red, with a visible spectrum of 300-ca. 650 nm,


Table 2 Records of fungal spores collected in lieu of pollen by honey bees (Apis mellijera), two records by A. dorsata and two records by species of Trigona

Pathogen Host or substrate Location Reference

Rust fungi

Caeoma luminatumA

C. nitensA

Wild blackberry Wild dewberry (Rubus

trivialis)

n i B

USA (NY State) USA (2 sites)

Cooke 1885 Lang 1901

Coleosporium senecionis

Cronartium conigenum Cytopsora oleae see

Zaghouania oleae Gliocladium see

fungal hosts Melampsora euphorbiae

M. (larici-) populina M. larici-populina

USA (?) Jaycox 1989, pers. comm. to following authors

Trujillo Flores & Pefia Garcia 1989

Pinus douglasiana & I! oocarpa

Mexico

Euphorbia heliscopia

Populus spp. Populus spp.

Pakistan Israel (1 940; 1941 twice) Australia (NSW)

Ahmad & Ahmad 1986 Minz 1942 Walker et al. 1974

Walker 1975a Dell 1977 Moraal 1988

M, larici-populina

M. larici-populina Populus nigra var. italica

Populus x euramericana 'Zeeland'

Populus spp.

n.LB, presumably Populus spp.

Populus spp.

Australia (W. Aust.) Netherlands

M. larici-populina

M. larici-populina

Chile UK

Savile 1980, pers. comm. Kirk 1994, 1996 pers. comm.

M. medusae Australia

(NSW) USA

Walker et al. 1974 Walker 19756

Todd & Bretherick 1942 M. occidentalis (?) Native cottonwoods USA (1 sample & 1 site) McGregor 1978, pers. comm.

USA Bessey 190 1 M. 'populina' (possibly M. larici-populina)

M. ricini

Melanzpsora sp.

Cottonwoods

Ricinus communis

Euphorbia geniculata

Sth Africa Wingfield et al. 1988 Sth Africa Johannsmeier 198 1 USA Williams & Tomlinson 1985 Melampsora sp. (probably Salix sp. (probably S.

M. bigelowii)

Melan2psora sp./spp laevigata)

Populus spp. Australia (Qld, 2 records)

Goebel 1982, pers. comm. Weatherhead 1982, pers.

comm. Armstrong 1981, pers. comm. Melanzpsora sphpp . Populus deltoides Australia

(NSW, 2 sites) Australia (NSW) USA (2 sites) Italy New Zealand

Melanzpsora sp. (Melanzpsora ?) rust Phragmiditrm voilaceum

Puccinia graminis (avenae)

P oxalidis

l? oxalidisC

Populus sp. Salix spp. Blackberry Chaff-cutting machine of

oats

Bielefel 199 1, pers. comm. McGregor 1978, pers. comm. Persano Oddo & Intoppa 198 1 Bennie 1942

Oxalis tuberosa & Oxalis sp.USA Wolfenbarger 1977

Oxalzs sp. Australia (Qld) Kleinschmidt 1983, pers. ( 0 . corymbosa) comm.

P polysoraD Zea mays Sarawak Turner 1974

2 74 Australasian Plant Pathology Vol. 28 (4) 1999

Table 2 continued

Pathogen Host o r substrate Location Reference

P psidii Allspice, Pimenta dioica "Uredineae sp." n.LB Uredo l ~ m i n a t a ~ - ~ Raspberry and wild

blackcap ' Uromyces euphorbiae?'

see U. proeminens

U proeminens n.i.B (as U. euphorbiae?)

Zaghouania oleae Brood comb (as Cytopsora oleae)

Z. oleae (as C. oleae) Olea dioica

'A rust'

Powdery mildew fungi

Oidium farinosum

Oidium sp.

Oidium so.

Neurospora s pp.

N. sitophila

N. sitophila N. intermedia

Apple Rosa sp. Cucurbita pep0 Pumpkin & rock melon Zucchini

Burnt tree trunks Steamed Pinus logs Filter mud

Neurospora sp. Filter mud

Neurospora sp. Filter mud

Other records

Ustilaginales Ustilago sp. 'A fungus growth' Hyparrhenia Jilipendula

var. pilosa (Poaceae) Stahellornyces cinctusF 'A gleba'

Jamaica Chapman 1964 Switzerland Maurizio 1950 USA Zabriskie 1875

USA Schmidt & Johnson 1984 Schmidt et al. 1987

India Deodikar et al. 1958 (Padgaon)

India (Mahabraleshwar Deodikar et al. 1958 4 records)

USA Schmidt et al. 1989

Germany Kraus 1920

Australia (NSW) Ray 198 1, pers, comm. Australia (Qld) Hardy 1989, pers. comm. Australia (Qld) Herrington 199 1, pers. comm Australia (Qld) Moffat 1994, pers. comm.

Bolivia Kempff Mercado 1955 Australia (Qld) Shaw 1993 Australia (Qld & NSW) Shaw & Robertson 1980

(10 records) Shaw 1990b Australia (Qld) Shaw 1990b, 1998

(12 records) Australia (Qld) Stirling 1998, pers. comm.

(2 records, not previously listed)

Switzerland Maurizio 1975

UK Betts 1912 Sth Africa Lundie 1938

(E. Transvaal) Ecuador Burr et al. 1996 Panama Roubik 1989

*Refer Shaw (1 990b) for discussion on nomenclature. Bn.i. = no information. CIdentity of rust fungus not determined, but as only one species is recorded on Oxalis in Queensland, it is listed as Puccinia oxalidis. DApis dorsata (2 records). EBees were not observed collecting rust spores, but corbicular contents were microscopically similar to the rust in the vicinity. FTrigona cf. branneri. "Trigona arnalthea.

Australasian Plant Pathology Vol. 28 (4) 1999 275

against the human range of 400-800 nm (von Frisch 19.50; Seeley 1995). Massed Neurospora conidia (which microscopically appear individually colour- less) reflect LW UV (Shaw and Robertson 1980), as do powdery mildew conidia (Shaw 1990b). Rust fungi, however, whose urediniospores and aeciospores are individually pigmented either in the cell wall andlor in the cytoplasm, probably have non- reflectance (absorbance) as uredinia on leaves and massed detached urediniospores of Melampsora larici-populina, Puccinia maydis, F oxalidis and P paullula did not reflect LW UV (Shaw 19906). The nearer the colour of the massed rust spores to yellow, however, the more likely they are to fall within the range of the bees' visible spectrum.

Fungal constancy Microscopical checks of corbicular samples of many pathogens and Neu- rospora spp. listed in Table 2 showed nearly 100% homogeneity of contents, i.e., there was collecting constancy for fungal spores, just as there is floral constancy for pollen collection from profitable sources. Exceptions were those reported by Kraus (1920) where in a few cases bees collected apple pollen and then changed to mildew spores.

Destination of fungal loads Corbicular loads of pollen are stored in hive cells around the brood. Fungal spores collected by bees have also been recorded in a few cases in hive cells. These records include those of Zaghouania oleae whose spores were detected in broodcomb in India (Deodikar et a / . 1958). In another case in Jamaica (Chapman 1964) the comb contained a high proportion of urediniospores of Puccinla psidii collected from allspice. In Western Australia, spores of Melampsora larici-populina were located in pollen stores in a hive (Dell 1977) and spores of M. euphorbiae were found stored in considerable quantity in comb in Pakistan (Ahmad and Ahmad 1986). Spores of Cronartium conigenum collected from Pinus were found in the hive cells in Mexico (Trujillo Flores and Pefia Garcia 1989). Of course, fungal loads recovered in pollen traps at hive entrances are not available in samples from hive storage cells.

Nutritive requirements of honey bees This aspect was summarised in Shaw (1990b) as follows. Pollens with less than 20% crude protein cannot satisfy colony requirements for optimum production (Kleinschmidt and Kondos 1976), whereas bees consuming more than 23% protein were able to

successfully rear brood (Herbert and Shimanuki 1978). Fungal yeasts, of course, have been used in pollen substitute and supplementary diets for many years. Ten amino acids (arginine, histidine, leucine, isoleucine, lysine, methionine, phenyalalanine, threonine, tryptophan and valine) are considered essential for growth of bees and three others (gly- cine, proline and serine) which are not essential for growth exert a stimulating effect on suboptimal growth levels (De Groot 1953).

Chemical composition of fungal spores The general composition of fungal cells was comprehen- sively reviewed by Birkenshaw (1 965), Lilly (1965) and Wolf (1 982). As this was summarised by Shaw (1990b) it is not repeated here. However, protein records for sporzs of Melampsora occidentalis were 9.1% (McGregor 1978 personal communication), 25.9% for Puccinia graminis tritici (Shu et al. 1954) and 25.8% for Neurospora sitophila (Owens et al. 1958). One major and two minor carotenes have been reported for I! gr, tritici (Irvine et al. 1954) and eight for N. crassa (Goldie and Subden 1973).

The effect on the brood Very little information is available on the effect of ingestion of fungal spores on the brood. No deleterious effects were noticed after collection of the rust spores Caeoma nitens (Zabriskie 1875) in the USA. In Switzerland, the eating of rust spores (given as 'Uredineae sp.') collected by honey bees, increased the length of life of the bees to some extent, and had only a slight effect on the hypopharyngeal glands and fat body (Maurizio 1950). There were no adverse effects on the bees as a result of collecting rust spores of Zaghouania oleae during pollen dearths in India (Deodikar et al. 1958). On the other hand, the stor- ing of spores of Melampsora euphorbiae in the comb in considerable quantity at three sites in Pakistan resulted in fairly high mortality of brood and bees (Ahmad and Ahmad 1986), although no details were given. In a survival study ofhoney bees using various pollens in the USA, Schmidt et al. (1987) included a collection of rust spores ascribed to 'Uromyces euphorbiae?' (a synonym of U. proeminens) of unknown plant source, which (with three pollens among several) induced decreased life span of bees. In later tests (Schmidt et al. 1989) honey bees did not avoid 'a rust' (unidentified) and some pollens, but did avoid pollen from three other plants.


In the pollen storage cells ofthe hive, pollen (and fungal spores if any) would be mixed, so brood would receive a varied diet. Further experiments are required on the effect of feeding identified fungal spores to bees as a sole diet and in mixtures with identified pollens.

Plant pathological risk Several workers considered that rust spores collected in lieu of pollen might cause dissemination of the pathogen. Lang (190 l), for example, thought this might be the case for the rust (caused by Caeoma nitens) of wild dewberry in the USA, and Turner (1974) wondered whether the Giant Asian honey bee (Apis dorsata) could assist in the spread of tropical maize rust (caused by Pucciniapolysora). Other workers, however, considered this unlikely. Kraus (1 920) was convinced that bees gathering conidia of the apple mildew fungus (Oidium farinosum) never visited healthy leaves, so that there was little if any chance of infection. Moraal(1988) also considered it unlikely that the collection of poplar rust spores in the Neth- erlands had much effect on the development and propagation of the disease.

As was pointed out previously (Shaw 1990b) and is reiterated here, spores packed into the corbiculae in lieu of pollen are moistened with liquid from the honey stomach, and this, and the physical compaction in the corbiculae and later in the hive cells, may exclude them from dissemination. Spores may also adhere loosely to the bee's body parts and hairs (as do pollen grains (Free and Williams 1972) and as illustrated by Leach (1940)), and as found with tropical maize rust spores (Turner 1974) and conidia of Neurospora sitophila (Shaw (1 993), although auto-grooming of such grains is part ofthe pollen-collecting process in honey bees. There is therefore the possibility that there may be in-hive transfer of any spores remaining on the body after auto- or during allo-grooming, or in-hive contact. No efficient transfer of avocado pollen, however, occurred within the hive in tests carried out recently (Ish-Am and Eisikowitch 1998). Also, even if spores were transferred during in-hive contact, or if launched into air currents if blown from the bee's body, they would still need to be viable at the time, and land on a susceptible host and find suitable conditions for germination.

Also, the bees will probably return again and again to a profitable source, viz., the pathogen on already infected hosts. This is a different state of affairs from the incidental transport of pathogenic

propagules during normal foraging, when bees (and other insects) visit uninfected as well as infected plants. Therefore, while this aspect - the plant pathological risk involved in the collection of spores in lieu of pollen - should not be overlooked, there would seem little chance of transmission, even given optimum conditions for infection.

Future records More observers are required to determine whether bees are making further collections, and if so, what fungi from what hosts or sub- strates are involved. It would seem desirable for any future records to include information on pathological, mycoiogical, apicultural and environmental aspects, such as listed previously (Shaw 1990b). The amount of fungal spores collected is infinitesimal when compared with the amount of pollen collected, but it has occurred, and no doubt will continue to occur, in some cases at least in crisis situations during periods of pollen dearth (Shaw 1990b).

The chemical composition of the spores, especially the protein levels of at least some of them, would seem to remove these fungi from the category of worthless substances, as in Faegri and Pijl (1979), and place them rather in the category of nutrients. Neurospora, for example, is non- pathogenic to man, other animals and plants, and is already used as a human food in Indonesia and Sarawak.

Recent work on ancient bees

Bees and wasps have long been thought to have evolved in the early Cretaceous (146 to 65 mya or Ma) with flowering plants. The origin of flowering plants was itself regarded by Darwin as an 'abomi- nable mystery'. And what is the position 150 years later regarding the origin of flowering plants? The most recent ordinal classification (APG 1998) stated (in modern terms) that the position of the root of the flowering plant phylogeny remains elusive. The work published less than a year ago on what is claimed to be the earl iest flowering plant, Archaefructus liaoningensis, gives its date at 140 mya or earlier (Sun et al. 1998).

Nests and groups of cocoons (ichnofossils) attributed to ancient bees have now been found in strata dated at 220 mya in the Petrified Forest National Park, USA. This work extends the range of bees and their nesting behaviour (reflecting social


interaction) by 140-155 million years to 220 mya, and indicates that bees and wasps almost certainly predate flowering plants by at least 100 million years (Bown et al. 1997); Hasiotis 1997; 1998 (1999); Hasiotis et al. 1995; 19960; 19966). The ichnofossil cell linings provide biochemical evidence of a phylogenetic link to modem bees in the Colletidae and Anthophoridae (Kay et al. 1997). This work also raises the question as to the nutrients of the ancient bees (ifthey predated flowering plants) and Hasiotis et al. (1999b) suggested that they probably foraged on carrion, gymnosperm and cycad pollen, resins, plant juices and fungi.

It is not known whether fungi were present at the time, as their fossil record does not extend back that far. Rust fungi in Hyalopsora, Milesina, and Urediniopsis are considered by some rust special- ists to be the most primitive of the rusts - (although Hart (1988), after a phylogenetic study, placed the suprastomatal tropical rusts as the most primitive) - and these three genera are heteroecious rusts, i.e., they have host alternation between ferns and firs. It is known that present day bees will collect rust spores from present day gymnosperms, such as honey bees have done in Mexico with spores of Cronartium conigenum on pine (Table 2), but whether the ancient bees did so, and whether there was host alternation at that time, is not known. Although of quite a different magnitude to the origin ofthe flowering plants, I think that the origin of host alternation in the rust fungi is another 'abomi- nable mystery'. This origin may have happened millions of years ago, but the fact of alternation of hosts is with us today, and I suggest that this should now be investigated with molecular tools. The study should not only include the disparity of the host pairs on the telial and aecial plants, but the inter- woven aspects as to why haploid basidiospores borne on the telial host cannot infect that host, and why the binucleate aeciospores borne on the aecial host cannot infect that host, but can infect the telial host.

The body fossil insect records include a Meliponine bee in New Jersey amber dated at 8 0 mya and a stingless bee with resin in the corbiculae at 20 mya (Roubik 1989; Poinar 1993; Ross 1998). What would be highly desirable would be the finding in authentic amber of an ancient bee with fungal spores in the corbiculae. If ever such is found, it would give important data on the age of the fungus and on bee behaviour.

Acknowledgements

Slide illustrations shown during the lecture were those of the author (some previously published in the Transactions of the British Mycological Society and The Mycologist) or reproduced from publications ofthe following: The Archaeology ofBeekeep- ing, and The Pollen Loads of the Honey Bee: Inter- national Bee Research Association, Cardiff, CF 10 3DT, UK; The Hive and the Honey Bee: Dadant & Sons, Hamilton, Ill., USA; Guide to Bees a n d Honey: Cassell, Wellington House, Strand, London, UK; Nature's Use of Colour in Plants and Flowers: Eurobook, Wallingford, Oxon OX10 OXU, UK; Amber: The Natural Time Capsule: The Natural History Museum, London, UK. The original slide of powdery mildew on pumpkin is held by the Department of Primary Industries, Indooroopilly, and that of Neurospora sp. on a heap of filter mud by Drs G.R. and A.M. Stirling. The use of facilities at Indooroopilly is gratefully acknowledged.

References

Ahmad, R. and Ahmad, M. (1986) -Introduction to Apis mellfera (L.) and factors affecting its establishment in Pakistan. Apiacta 21: 9-14.

Anderson, D.L., Gibbs, A.J., Gibson, N.L. (1998) -1den- tification and phylogeny of spore-cyst fungi (Ascosphaera spp.) using ribosomal DNA sequences. Mycological Research 102: 54 1-547.

Anderson, D.L. and Gibson, N.L. (1998) -New species and isolates of spore-cyst fungi (Plectomycetes: Ascosphaerales) from Australia. Australian Systemic Botany 11: 53-72.

Anon. (1 953) - (Unusual honey in Carinthia.) Karnten Biene 22(11/12):207. In German (Not seen. Abstract in Apicultural Abstracts 6 : 108, 1995).

APG (Angiosperm Phylogeny Group) (1998) -An ordinal classification for the families of flowering plants. Annals of the Missouri Botanical Garden 85: 53 1 - 553.

Baker, H.G. and Baker, I. (1983) - Same evolutionary and taxonomic implications of variation in the chemical reserves of pollen. In Pollen: Biology and Impli- cations for Plant Breeding (Eds D.L. Mulcahy and E. Ottaviano) pp. 43-52. Elsevier, New York.

Batra, L.R. (1983) - Monilinia vaccinii-corymbosi (Sclerotiniaceae), its biology on blueberry and com- parison with related species. Mycologia 75: 13 1-152.

278 Australasian Plant Pathology Vol. 28 (4) 1999

Batra, L.R. and Batra, S.W.T. (1985) - Floral mimicry induced by mummy-berry fungus exploits host's pollinators as vectors. Science 228 (4702): 1011- 1013.

Batra, S. W.T. (1987) -Deceit and corruption in the blueberry patch. Natural History 96: (56 (plate))-57-59.

Bennie, R.B. (1942) -Pollen substitute for bees. New Zealand BeeKeeper 4: 17- 18.

Bessey, C.E. (1901) -More about fungus spores as bee bread. Plant World 4: 96.

Betts, A.D. (1 912) -The fungi of the bee-hive. Journal of Economic Biology 7: 129- 162.

Birkenshaw, J.H. (1965) - Chemical constituents of the fungal cell. In The Fungi: an Advanced Treatise, Vol. I (Eds G.C. Ainsworth and A.S. Sussman) pp. 179- 228. Academic Press, London, UK.

Bown, T.M., Hasiotis, S.T., Genise, J.F., Maldonado, F. and Brouwers, E.M. (1997) - Trace fossils of Hy- menoptera and other insects, and paleoenvironments of the Claron Formation (Paleocene and Eocene), southwestern Utah. United States Geological Survey Bulletin 2153: 41-58.

Brett, M. (1966) - Thecaphora deformans on Ulex mi- nor. Transactions ofthe British Mycological Society 49: 529-543.

Buchmann, S.O. and Nabhan, G.P. (1996) - The Forgot- ten Pollinators. Island Press, Washington, DC.

Burr, B., Barthlott, W. and Westerkamp, C. (1996) - Staheliomyces (Phallales) visisted by Trigona (Apidae): melittophily in spore dispersal of an Amazonia stinkhorn? Journal of Tropical Ecology 12: 41 1-445.

Cardeflosa-Barriga, R. (1963) - La antracnosis del P1atana"Cachaco" en el Tolema. Turrialba 13: 88-95.

Carne, W.M. (1927-1928) -An outline of the history of Phytopathology with special reference to its development in Australia. Journal o f the Royal Society of Western Australia 14: 24-36.

Chapman, P.G. (1964) - Urediospore collections by honey bees from Pucciniapsidii. Annals ofthe Ento- mological Society ofAmerica 57: 264.

Connick, W.J. Jr and French, R.C. (1991) - Volatiles emitted during the sexual stage of the Canada Thistle rust fungus and by thistle flowers. Journal ofAgricul- tural and Food Chemistry 39: 185- 188.

Cook, A.J. (1 885) -Fungus spores for bee-bread. Glean- ings in Bee Culture 12: 455-456.

Costa, J.L. da S. and Lordello, S. (1988) - (Role of insects in the dissemination of Fusarium disease of


pineapple). Fitopatologia Brasileira 13: 63-65. (Not seen. Abstract in Review ofplant Pathology 69 Item 3160 1990).

Crane, E. (1983) - The Archaeology ofBeekeeping Gerald Duckworth & Co. Ltd, London, UK.

De Groot, A.P. (1953) -Protein and amino acid requirements of the honeybee (Apis mellzjka L.). Physzologia comparata et oecologia 3, Fasc. 2 and 3 (Not seen. Cited by Dietz 1975).

Dell, B. (1977) -The collection of poplar rust spores by honey bees. Western Australian Naturalist 13: 199- 201.

Deodikar, G.P., Thakar: C.V., Shah, P.N., Salvia, S.R. and Chitale, P.S. (1958) -Foraging of honeybees on fungal rust spores (Cytopsora oleae) on Olea dioica. Bee World 39: 120-121.

Dietz, A. (1975) -Nutrition of the adult honey bee. In The Hive and the Honey Bee. Dadant & Sons, Ham- ilton, 111. USA.

Faegri, K. and Iversen, J. (1989) - Textbook ofpollen Analysis. 4th edition. John Wiley & Sons, Chichester, New York.

Faegri, K. and Pijl, L. van der (1979) - The Principles ofPollination Ecology. Pergamon Press, Oxford, UK.

Fish, S. (1970) -The history of plant pathology in Aus- tralia. Review of Phytopathology 8: 13-3 1.

Fish, S. (1 976) - Daniel McAlpine: A pioneer plant pathologist of Australia. Australian Plant Pathology Society Newsletter 5: 1 1 - 13.

Free, J.B. and Williams, I.H. (1972) -The transport of pollen on the body hairs of honeybees (Apis mellifera L.) and bumblebees (Bombus spp. L.). Journal of Applied Ecology 9: 609-61 5.

Frisch, K. von. (1950) -Bees: their Vision, Chemical Senses, and Language. Johnathan Cape, London, UK.

Gold~e, A H and Subden, R E (1 973) - Separation of the neutral carotenoids In Neurospora crassa usmg con- cave gradient elutlon chromatography Journal of Chromatography 84 192- 194

Griffiths, D. and Roberts, E.J. (1996) -Bumble Bees as pollinators of glasshouse crops. In Bumble Bees for Pleasure and Profit (Ed A. Matheson.), pp. 33-39. International Bee Research Association, Cardiff, UK.

Hart, J. (1988) -Rust fungi and host plant coevolution: Do primitive hosts harbor primitive parasites? Cladistics 4: 339-366.

Has~o t~s , S T (1 997) - A buzz before flowers Plateau Journal, Museum ofNorthern Arlzona 1 20-27 (Not seen C~ted by H a s ~ o t ~ s et a1 19996)

279

Hasiotis, S.T. (1 998)-No bones about it ... its continental ichnology: Palaios 13.1 4 pp. http:llwww.ngdc.noaa. govlmgg/sepm/palaois19802lhasiotis.htm (1999).

Hasiotis, S.T., Dubiel, R.F. and Demko, T.M. (1995) - Triassic hymenopterous nests: Insect eusociality pre- dates Angiosperm plants. Rocky Mountain Section, Geological Society ofAmerica Regional Meeting 27 ( 4 ) : 13.

Hasiotis, S.T.. Dubiel, R.F. and Demko, T.M. (1 999a) - A holistic approach to reconstructing triassic paleo- ecosystems: using ichnofossils and paleosols as a basic framework. http://ww.quu.nps.gov/grd/geology/ paleo/drd3_3/pef02, htm

Hasiotis. S.T.. Dubiel, R.F., Kay, P.T., Demko, T.M., Kowalska, K. and McDaniel, D. (19996) - Research update on hymenopteran nests and cocoons. Upper Triassic Chinle Formation, Petrified Forest National Park, Arizona. http://www/agd.nps.gov/drd/geologyi paleolgrd3-3lpefol.htm

Herbert, E.W. and Shimanuki, H. (1978) - Effects of thiamine or riboflavin-deficient diet fed to new emerged honey bees, Apis mellifera L. Apidologie 9: 34 1-348.

H ~ e g , O.A. (1 924) -Pollen on bumblebees from Novaya Zemlya. Report of the scientific results of the Norwe- gian Expedition to Novaya Zemlya 1921. No. 27: 4- 18. (Ed 0. Holtedahl.) (Not seen. Cited by Kevan and Parmelee 1972).

Hood, W.M. and Miller, W. (1997) - Biocontrol of botrytis fruit rot on strawberries using honey bees to vector an agent. American Bee Journal 137: 224-225.

Huang, H.C. and Kokko, E.G. (1985) - Infection of alfalfa pollen by Verticillium albo-atrum. Phyto- pathology 75: 859-865.

Huang. H.C. and Richards, K.W. (1983) - Vertrcillium alboatrunz contamination of leaf pieces forming cells for the alfalfa leafcutter bee. Canadian Jouiwal of Plant Pathology 5: 248-250.

Huang, H.C., Hanna, M.R. and Kokko, E.G. (1985) - Mechanisms of seed contamination by Verticilliunz albo-atrunz in alfalfa. Phytopathology 75: 482-488.

Huang, H.C.; Richards, K.W. and Kokk, E.G. (1986) - Role of the leafcutter bee in dissemination of Verticil- lizm albo-atrum in alfalfa Phytopathology 76: 75-79.

Irvine, G.N., Golbchuk, M, and Anderson, J.A. (1954) -The carotenoid pigments of the uredospores of rust fungi. Canadian Journal ofplant Pathology 5: 248- 250.

Ish-Am. G. and Eisikowtch, D. (1998) - Mobility of honey bees (Apidae, Apis nzellifera L.) during foraging in avocado orchards Apidologie 29: 209-2 19

Israel, M.S. and Boland, G.J. (1992) -Influence of for- mulation on efficacy of honey bees to transmit biological controls for management of sclerotinia stem rot of canola. Canadian Journal ofPlant Pathology 14: 244 (Abstract).

Jennersten, 0. ( 1 9 8 3 ~ ) -Butterfly visitors as vectors of Ustilago violacea spores between caryophyllaceous plants. Oikos 40: 125-130.

Jennersten, 0. (I 983 b ) - Local plant population as eco- logical island: the infection of Kscaria vulgaris by the fungus Ustilago violacea. Oikos 41: 391-395.

Jennersten, 0 (1985) - Pollination and fungal disease transmission: interaction between Viscaria vulgaris, Ustilago and insects. Doctoral Dissertation, Uppsala University, Sweden 165 pp. (Not seen. Abstract in Apicultural Abstracts 40: 1082, 1989).

Jennersten, 0 (1988) -Insect dispersal of fungal disease: effects of Ustilago infections on pollinator attraction in Viscaria vulgaris. Oikos 51: 163-170.

Jennersten, 0 and Kwak, M.M. (1 991) -Competition for bumblebee visitation between Melampyrumpratense and Viscaria vulgaris with healthy and Ustilago-infected flowers. Oecologia 86: 88-89.

Johannsmeier, M.F. (1981) - Corbicular loads of the African honeybee. South Afvican Bee Journal 53: 3-6.

Kay, P.T., King, J.D. and Hasiotis, S.T. (1997)-Petrified Forest National Park Upper Triassic trace fossils yield biochemical evidence of phylogenetic link to modern bees (Hymenoptera, Apodea). Geological Society of America National Meeting, Salt Lake City, UT, 29 (6): 102.

Kempff Mercado, N. (1955) - Un hongo substituto de polen. Gaceta del Colmenar, Buenos Aires pp. 3-4.

Kevan, P.G. and Parmelee, J.A. (1972) - Insect-flower- fungus relationships for the transmission of the smut Ustilago violacea by flower-visiting insects in the high Arctic. Greenhouse-Garden-Grass 11 : 6-1 3

Kirk, W.D. ( 1 994) - A Colour Guide to Pollen Loads of the Honey Bee. International Bee Research Associa- tion, Cardiff, U.K.

Kleinschmidt, G.J. and Kondos, A.C. (1976) -The influence of crude protein levels of colony production. '4 ustralasian Beekeeper 78: 36-39.

Kovacs, G. (1 968) -(Study on the infection of strawberry by Botrytis cinerea Pers. and on methods of control.) Kongelige Veterinaer - og Landbohojskole Arsskriji 89: 84-99 (Not seen. Abstract in Review ofApplied Mycology 48: 1245, 1969).

Kraus, P.X. (1920)- (White apple mildew as bee bread.) Der deutsche Imker aus Bohmen 33: 120-1 22.


Lang, W.H. Jr. (1901)-Fungus spores as bee bread. Plant Proctor, M., Yeo, P. and Lack, A. (1996) - The Natural World 4: 49-5 1. History of Pollination, HarperCollinsPublishers,

Leach, J.G. (1940) -Insect Transmission of Plant Dis- eases. McGraw-Hill Book Co. Inc., New York.

Lilly, V.G. (1965) -Chemical constituents of the fungal cell. In The Fungi: an advanced Treatise. Vol. I. (Eds G.C. Ainsworth and A.S. Sussman), pp. 163-177. Academic Press, London, UK.

Lundie, A.E. (1938) -Honeybees working on a fungus growth. (Hyparrheniafilipendula var. pilosa). South African Bee Journal 13: 19.

Maurizio, A. (1950) - The influence of pollen feeding and brood rearing on length of life and physiological conditions of the honeybee: Preliminary report. Bee World 31: 9-12.

Maurizio: A. (1975) - (Der Honeg). (Second edition) Verlag Eugen Umer, Stuttgart, Germany. (Not seen. Cited by Trujillo Flores and PeAa Garcia 1989).

London; UK

Raguso, R.A. and Roy, B.A. (1998) - 'Floral' scent production by Puccinia rust fungi that mimic flowers. Molecular Ecology 7: 1127-1 136.

Roberts, R.B, and Vallespir, S.R. (1978) -Specialization of hairs bearing pollen and oil on the legs of bees (Apoidea: Hymenoptera). Annals of the Entomologi- cal Society ofAmerica 71: 619-627.

Ross, A. (1 998) -Amber: The Natural Time Capsule. The Natural History Museum, London, UK.

Rothschild, G.H.L. (1998) -Applied entomology, pros- pects and challenges for the next millennium. In Pest Management - Future Challenges. Sixth Australasian Applied Entomology Research Conference, The Uni- versity of Queensland, Brisbane, Australia, 29 Sep- tember - 2 October, 1998. (Eds M.P. Zalucki, R.A.I. Drew and G.G. White). 1: 1-10.

Minn, G. -Bees gather rust 'pores ofMelam~sora Roubik, D,W, (1989) -Ecology and&-atLLra[ History of populina Kleb. Hassadeh 22: 173 (Not seen. Abstract Bees, Cambridge University Press, Cam- in Review ofApplied Mycology 23: 366, 1994). bridge, UK.

Moraal, L'G' - (The poplar rust as a food source Roy, B, (1 993) - Floral mimicry by a plant pathogen, for a gall midge and the honeybee.) Entomologische n,ature 362: 56- j8, Berichten 48: 148-186 (Not seen. Abstract in Apicultural Abstracts 42: 565, 1991). Roy, B.A. ( 1 9 9 4 ~ ) - The effects of pathogen-induced

pseudoflowers and buttercups on each others' insect Owens, R.G., Novotny, H.M., and Michels, M. (1958)- visitation, Ecology 75: 352-3 58,

Composition of Neurospora sitophila. Contributions fvom Boyce ~ h o m ~ s o n hstitute for plant ~esearch 19: Roy, B.A. (1 994b) - The use and abuse of pollinators by 353-374. fungi. Trends in Ecology and Evolution 9: 335-339.

PeAa, J.E. and Duncan, R. (1989) - Role of arthropods Roy, B.A. and Raguso, R.A. (1997) - Olfactory versus in the transmission of postbloom fruitdrop. Proceed- visual cues in afloral mimicry system. Oecologia 109: ings ofthe Florida State Horticultural Society 102: 414-426 249-25 I .

Schmidt. J.O.. Buchmann, S.L. and Glaiim, M. ( 1989) - Peng, G., Sutton, J.C, and Kevan, P.G. (1991) - Evalu- The nutritional value of Typha latifolia pollen for

ation of honey bees for applying Gliocladium roseunz bees. Journal ofApicultura1 Research 28: 155-165. to strawberry flowers to control gray mold caused by Botrytis cinerea. Canadian Journal ofplant Pathol-

Schmidt, J.O. and Johnson, B.E. (1984) - Pollen feeding preferences of Apis melltfera (Hymenoptera:

ogy 12: 283 (Abstract). Apidae), apolylectic bee. Southwestern Entomologist Peng, G., Sutton, J.C. and Kevan, P.G. (1992) - Effec- 9: 41-47

tiveness of honey bees for applying the biocontrol Schmidt, J.O., Thoenes, S.C. and Levin, M.D. (1987) - agent Gliocladium roseum to strawberry flowers to Survival of honey bees: Apis mellifera (Hymenoptera: suppress Botytis cinerea. Canadian Journal ofplant Apidae) fed various pollen sources. Annals of the Pathology 14: 1 17-1 29. Entomological Society ofAnzerica 80: 176-1 83. -

Odd', L' and Intoppa, F' (1981)-(Foraging On Seeley, T,D, (1996) - The M/isdonz of the Hive, Harvard fungal spores by honeybees.) Apicoltore Moderno 72: University Press, Cambridge, Mass., USA. 185-188. (Not seen. Abstract in ApiculturalAbstr~acts 34: 169L, 1983). Sharma, Y.P., Singh, R.S. and Tripath, R.K. (1983)-Role

of insects in secondary spread of the ergot disease of Poinar, (3.0. Jr. (1993) -Insects in amber. Annual Review

pearl millet (Pennisetum americanum). Indian Phy- of Entomology 46: 145-159.

topathology 36: 131-133.

Australasian Plant Pathology Vol. 28 (4) 1999 28 1

Shaw, D.E. ( 1 9 9 0 ~ ) - Blooms of Neurospora in Aus- tralia. The Mycologist 4: 6- 13.

Shaw, D.E. (1990b) -The incidental collection of fungal spores by bees and the collection of spores in lieu of pollen. Bee World 71: 158-176.

Shaw, D.E. (1993) - Honeybees collecting Neurospora spores from steamed Pinus logs in Queensland. My- cologist 7: 182-185.

Shaw, D.E. (1998) - Species of Neurospora recorded in Australia and the continued collection ofNeurospora conidia by honey bees (Apis mellifera) in lieu of pollen. Mycologist 12: 154-158.

Shaw, D.E. and Robertson, D.F. (1980) - Collection of Neurospora by honeybees. Transactions of the Brit- ish Mycological Society 74: 459-464.

Shu, P., Tanner, K.G. and Ledingham, G.A. (1954) - Studies on the respiration of resting and germinating uredospores of wheat stem rust. Canadian Journal of Botany 32: 16-23,

Silow, R.A. (1933) - A systemic disease of red clover caused by Botrytis anthophila Bond. Transactions of the British Mycological Society 18: 239-248.

Smith, F.F. and Weiss; F. (1942) -Relationship of insects to the spread of azalea flower spot. U.S. Department of Agriculture, Technical Bulletin No. 798.

Stelfox, D., Williams, J.R., Soehngen, U, and Topping, R.C. (1978) - Transport of Sclerotinia sclerotiorum ascospores by rapeseed pollen in Alberta. Plant Dis- ease Reporter 62: 576-579.

Sun, G., Dilcher, D.L., Zheng, S. and Zhou, Z. (1998) - In search of the first flower: a Jurassic angiosperm, Archaefructus, from Northeast China. Science 282: 1692-1695.

Sutton, J.C., De-Wei, L., Yu, H., Pringgao, Z. and Valdebenito-Sanhueza, R.M. (1997) - Gliocladium roseum: a versatile adversary of Botrytis cinerea in crops. Plant Disease 81: 3 16-328.

S~itton, J.C. and Peng, G. (1993) - Manipulation and vectoring of biocontrol organisms to manage foliage and fruit diseases in cropping systems. Annual Review of Phytopathology 31: 473-493.

Todd, F.E. and Bretherick, 0. (1 942) -The composition of pollens. Journal ofEconomic Entomology 35: 3 12- 317.

'Irujillo Flores, F.J. and Pefia Garcia, L.E. (1989)- (Col- lection and storage of spores of Cronartium conigenum Hedc. et Hunt, by Apis mell2fera L.) Apicultura Moderna 1 : 15-1 6.

Turner, G.J. (1974) -Possible transmission of Puccinia polysora by bees. Transaction of the British Myco- logical Society 62: 205-206.

Verma, O.P. and Pathak, V.N. (1 984) -Role of insects in secondary spread of pearl millet ergot. Phytophylactica 15: 257-258.

Walker, J. (1 975a) - Melampsora larici-popzilina. Com- monwealth Mycological Institute Descriptions of Pathogenic Fungi and Bacteria: No. 479.

Walker, J. (1 9756) - Melampsora medusae. Common- wealth Mycological Institute Descriptions of Patho- genic Fungi and Bacteria: No. 480.

Walker, J., Hartman, D. and Bertus, A.L. (1 974) - Pop- lar rusts in Australia with comments on potential coni- fer rusts. European Journal of Forest Pathology 5: 100-118.

Weiss, F. and Smith, F.F. (1940) -A flower-spot disease of cultivated azaleas. U.S. Department of Agriculture Circular: No. 556.

White, N.H. (1981) -The history of plant pathology in Australia. In Plants and Man in Australia (Eds D.J. and S.G.M. Carr), pp. 42-95. Academic Press, New York.

Williams, S.C. and Tomlinson, J.T. (1985) - Gathering of aecial spores of willow rust by the honey bee, Apis mellfera (Hymenoptera: Apinae). Pan-PaciJic Ento- mologist 61: 345.

Wingfield, M.J., van Wyk, P.S. and Viviers, M. (1 989) - Rust-spores, bees and pollen. The Mycologist 3: 31- 32.

Wolf, G. (1982) -Physiology and biochemistry of spore germination. In The Rust Fungi (Eds K.J. Scott and A.K. Chakravorty), pp. 152-178. Academic Press, London, UK.

Wolfenbarger, D.O. (1977) - Honey bees forage rust spores of Oxalis sp. leaves. American Bee Journal 117: 441.

Yu, H. and Sutton, J.C. (1 994) -Vectoring of the biocontrol agent Gliocladium roseum to raspbeny flowers by bumblebees and honeybees. Phytopathology 84: 549 (Abstract).

Yu, H. and Sutton, J.C. (1997) -Effectiveness of bumblebees and honeybees for delivering inoculum of Gliocladium roseum to raspberry flowers to control Botrytis cinerea. Biological Control 10: 113-122.

Zabriskie, J.L. (1875) - Remarkable forage for bees. Beekeepers Magazine 3: 186-187.


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