New Zealand Journal of Botany

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Birds as pollinators of Australian plants

Hugh A. Ford , David C. Paton & Neville Forde

To cite this article: Hugh A. Ford , David C. Paton & Neville Forde (1979) Birds as
pollinators of Australian plants, New Zealand Journal of Botany, 17:4, 509-519, DOI:
10.1080/0028825X.1979.10432566

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 New Zealand Journal ofBotany, 1979, Vol. 17: 509-19 509

Birds as pollinators of Australian plants

HUGH A. FORD!, DAVID C. PATON l , and NEVILLE FORDEl

IDepartment of Zoology, University of New England, Armidale, N.S.W., 2351, Australia
2*Department of Zoology, Monash University, Clayton, Victoria, 3168, Australia
3School of Applied Science, Torrens College of Advanced Education, S.A., 5032, Australia

Abstract Over one hundred species of birds have been seen visiting the flowers of some
250 species of plants in Australia. Honeyeaters and lorikeets are the most persistent flower-
feeders and some species depend almost entirely on nectar as a source of energy. Silvereyes,
parrots, woodswallows, pardalotes, thornbills, and a few other species of passerines
occasionally visit flowers. The genera most frequently visited are Eucalyptus, Callistemon,
Banksia, Grevillea, Adenanthos, Dryandra, Epacris, Astroloma, Amyema, Correa,
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Xanthorrhoea, Anigozanthos, and Eremophila. Some flowers, e.g., those of Eucalyptus, are
very generalised in structure and are visited and pollinated by insects as well as birds. Other
plants have shown a range of adaptations to attract birds to their flowers or deter insects.
Birds require significant rewards so that flowers must produce copious nectar. Flowers are
often clumped into inflorescences (e.g., Banksia) or individual flowers become large and
tubular or gullet-shaped (Eremophila). Flowers visited by birds are often red, though yellow
(Adenanthos) and green (e.g., Amyema, Correa) are common. Hairs in tubular flowers, and
lack of attractive smell may deter insects without affecting birds (e.g., Astroloma). In
Australia the relationships between birds and plants are not as specific as those shown for
hummingbirds and some of their flowers in tropical America. Most species of birds visit a
wide range of plants, and most plants are visited by a wide range of birds.
Pollen is usually placed on the forehead, face, and chin feathers of the bird oron its beak.
Birds have been proved to be effective pollinators of many plants in temperate Australia.
Little work has so far been carried out in tropical Australia.
Bird-pollinated flowers have mostly originated from insect-pollinated flowers though it
is possible that some (e.g., Banksia) were, or still are, pollinated by mammals.
It is not clear why so many of the dominant plant genera in temperate Australia are
pollinated by birds. Birds may be more reliable pollinators than insects when the climate and
flowering season are unpredictable, or during winter when many of the specifically bird-
pollinated plants flower. Birds may also increase the chance of outcrossing as they fly further
between plants than insects. Nutrients are often limiting in Australian ecosystems, whereas
energy rarely is. Therefore, massive nectar production is unlikely to place a strain on plants,
unless water is scarce. Finally, it is possible that birds may provide a service in addition to
pollination, they may protect the plant from herbivorous insects.

INTRODUCTION
In this review we shall first present the evidence that
birds are important pollinators of plants of several
characteristic Australian families. Secondly, we
shall briefly examine the floral characteristics of
some of these plants in the light of typical bird-
pollinated flowers elsewhere (Faegri & van der Pijl
1966). Finally, we shall consider the evolution of
bird-pollinated flowers from flowers pollinated by
*Present address: Department of Ecology and Evolution-
ary Biology, University of California, Irvine, California
92717, U.S.A.
other vectors and speculate about the reasons for the
widespread occurrence of bird-pollination in tem-
perate Australia.
EVIDENCE FOR BIRD POLLINATION
The prevalence of nectar feeding in Australian birds
can be seen from Table 1 which summarises records
of birds visiting and pollinating flowers of some of
the more important plant genera. Full de~s are
given in Appendix 1. One hundred and eleven
species of birds have been seen visiting flowers and
about 250 species of plants have been visited by
 510 New Zealand Journal of Botany, 1979, Vol. 17

Table 1 Pollen of plant genera carried by birds. Also number of individual birds carrying more than 10 grains.
+ = at least one bird of that group carrying pollen. + + = major pollinator.
Plant genus Lorikeets Meliphaga MelilhreplUS Phylidonyris Acantho- Anthochaera Other Other Total no.
rhynchus honeyeaters passerines of birds b

Callistemon + + ++ + 28
Eucalyptus ++ ++ + ++ + ++ + 108
Adenanthos + ++ ++ + 218
Grevillea ++ + ++ + 30
Banksia + + ++ ++ ++ + + 480
Dryandra +
Loranthaceaea ++ ++ + + + 72
Correa ++ + ++ ++ + 145
Astroloma ++ + ++ + + 57
Brachyloma + + + + + 4
Epacris + + + 21
Eremophila + ++ + 16
Xanthorrhoea + +
Anigo-
zanthos + ++
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alncludes Amyema. Lysiana. and Muellerina.

bFrom Paton & Ford (1977). Ford (1976). Ford (unpublished data).

birds. Myrtaceae, Proteaceae, Epacridaceae,
Loranthaceae, Rutaceae, Myoporaceae, Xanthorr-
hoeaceae, Haemodoraceae, and Fabaceae contain
most of the species visited frequently by birds.
Eucalyptus, with 74 species visited by 83 species of
birds is by far the most important genus. South
Australia has been better covered than the other
states with regard to observations of birds feeding on
flowers. Of 52 species of Eucalyptus there, birds
have been seen visiting 27, and are probably
important pollinators of at least 23 species. Maybe
about half or 200 species of Eucalyptus in total are
pollinated by birds. Banksia, Grevillea. Adenan-
thos. Eremophila. Dryandra. Amyema. Astroloma,
and Callistemon are other major genera. Possibly
about 1000 species of plants in Australia have birds
as major pollinators, a very large total in a predomi-
nantly temperate area. Possible reasons for this are
discussed later.
The honeyeaters (Meliphagidae) are the most
diverse family of passerine birds in Australia, with 70
species. Probably all visit flowers to a greater or
lesser extent. Whereas some take nectar only casu-
ally (Myzantha) others are highly dependent on
nectar (Phylidonyris) (Recher 1971, 1977; Keast
1976; Ford & Paton 1976a,b, 1977). They range in
size from the tiny myzomelas, weighing c. 6 g, to the
aggressive wattlebirds (Anthochaera) and friarbirds
(Philemon), weighing over 100 g. Their beaks range
from short in Meliphaga (Lichenostomus) to long
and decurved in the spinebills (Acanthorhynchus).
Generally, honeyeaters are less morphologically
diverse (e.g., in their beaks and wings) than the New
World hummingbirds (Trochilidae).
Many other groups of birds also visit flowers,
although honeyeaters are the main nectar feeders
and pollinators in Australia. The lorikeets (Loriinae)
and a few other parrots are frequent blossom
feeders, taking pollen as well as nectar (Churchill &
Christensen 1970). Amongst the passerines, silver-
eyes (Zosterops), woodswallows (Artamus), chats
(Ephthianura), and the single Australian species of
sunbird (Nectarinia) frequently take nectar. Parda-
lotes (Pardalotus), trillers (Lalage), orioles (Orio-
Ius), thornbills (Acanthiza), shrike-thrushes (Col-
luricincla), treecreepers (Climacteris), sittellas
(Daphaenositta), bower-birds (Ptilorhynchus), and
butcherbirds (Cracticus) have also been seen at
flowers.
It has previously been assumed that birds were
the pollinators of the plants they visited (see, e.g.,
Brewster 1915) and some observers (e.g., Sargent
1928) even noted pollen on the feathers of birds. The
beautiful photographs of Morcombe (1968) illustrate
the suitability of birds as pollinators. However, it
was not until the 1970s that pollen was collected from
Australian birds and identified. Many birds, mostly
honeyeaters, have been found to carry pollen of
Eucalyptus. Callistemon. Grevillea. Adenanthos.
Banksia. Amyema. Correa. Epacris. Astroloma.
Brachyloma. and Eremophila (Table 1, also see
Paton & Ford 1977 and Ford 1976). Pollen was
brushed from the head feathers and from the beak.
Sometimes only a few pollen grains were collected,
but often hundreds and occasionally thousands of
grains were found. Pollen placement of the different
flowers on the birds is discussed later. Individual
birds often carry pollen of several species of plants,
though usually one type predominates.
The fact that birds carry pollen is not proof that
they are pollinators. Pollen needs to be placed on a
receptive stigma of the same species. This is almost
impossible to observe in nature, so a stuffed honey-
eater was probed into flowers of representatives of
 Ford et al. - Birds as pollinators
Table 2 Deposition of pollen on stigmas of several plant
species after probing flowers with a stuffed New Holland
honeyeater.
No. flowers % with pollen
probed after probing
Adenanthos terminalis 34 97
Grevillea ilicifolia 20 95
Grevillea lavandulacea 25 100
Banksia marginata 46 85
Banksia ornata 51 100
Lysiana exocarpi 39 81
Correa schlechtendalii 6 100
Astroloma conostephioides 36 100
Epacris impressa 30 100
most of the major genera (Paton & Ford 1977). All
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flowers probed in this way had no pollen previously
on their stigmas, but almost all had after probing
(Table 2). This rather crude approximation of what
happens naturally was almost totally successful at
pollination except in Lysiana and Banksia where
about one-fifth of the flowers were not pollinated.
Most flowers had c. 20-40 grains on their stigmas.
Further evidence of bird-pollination was obtained
from examining flowers visited by honeyeaters in the
wild. In Astroloma and Epacris from 65 to 90% of
visited flowers carried pollen on their stigmata,
against ~90% for flowers not seen to have been
visited. The latter high figure was obtained in late
afternoon when probably all flowers had been visited
(Paton & Ford 1977). Hopper & Burbridge (1978)
provided good evidence that wattlebirds pollinated
two species of kangaroo paw (Anigozanthos). They
related the behaviour of the birds which occasionally
visited both species on one feeding bout to the few
hybrid plants.
Thus, a wide range of bird species visit a wide
range of plant species in Australia for their nectar
and presumably frequently pollinate them. Definite
proof of pollination by birds is available for some of
the most important genera in southern Australia.
Some species of hummingbirds show a specific
relationship with one or a few species of plants
(Snow & Snow 1972, Wolfetal. 1976). This degree of
specialisation is not shown by birds and plants in
Australia. Most of the regular nectar feeders (Phyli-
donyris, Anthochaera, Acanthorhynchus) visit a
very wide range of flowers, and these plants are
themselves visited by many species of birds. The few
plants which have only been seen to have been
visited by one species of bird are either uncommon,
not typically bird-pollinated (e.g., Boronia, Glycine,
Myoporum) , or occur in habitats which have not
been studied extensively (e.g., Streptothamnus in
cool, temperate rain forest). Almost all of the work
on bird-pollination in Australia has been carried out
in heath or sclerophyll forest. There is very little
information for any kind of rain forest. A few plants
511
(e.g., Epacris) may be visited predominantly by the
smaller honeyeaters and possibly there are more
specific relationships here. These plants tend to
produce small quantities of nectar and so may be
uneconomical for larger birds. Honeyeaters are
generalists and opportunists, as evidenced by their
willingness to visit exotic plants (unpublished data,
and McCulloch 1977).
FLORAL CHARACTERISTICS OF
BIRD-POLLINATED PLANTS IN AUSTRALIA
Faegri & van der Pijl (1966) have summarised the
syndrome of the typical bird-pollinated flower.
Characteristics include: bright colour, usually red;
tubular, gullet, or bell-shaped flower; strong corolla
with no landing stage; lack of smell; abundant
nectar; and anthers and stigma distant from nectary.
Other features which may be shown by bird-pollin-
ated flowers are clumping of flowers and brush type
of flower or inflorescence. These characteristics,
and those of the bird-pollinated members of some
genera of Australian plants, are summarised in Table
3. Although Australia has many flowers which may
be regarded as typical of bird-pollinated ones else-
where (e.g., Anigozanthos, Lysiana, Eremophila,
Astroloma), there are many which differ from the
typical bird-pollinated flower, in one or more of their
characteristics.
Colour
Grant & Grant (1968) showed that hummingbirds do
not show a strong preference for red even though
many of their flowers are red. Raven (1972)
suggested that most insects have a poor sensitivity to
red and so nectar is less likely to be stolen from red
flowers. Thus flowers morphologically adapted for
bird-pollination are usually red. Butterfly-pollinated
flowers are also often red. Although red, pink, and
orange are common colours in Australian bird-
flowers, other colours such as white (Eucalyptus),
yellow (some Adenanthos, Lysiana, and Eremo-
phi/a), and green (some Amyema and Correa) are
also common. Some flowers are black (some
Macropidia, Grevillea, Kennedya nigricans) or grey
(Amyema). The flowers are inconspicuous in some
bird-pollinated flowers (e.g., Phebalium, J.
Armstrong, pers. comm.; and Adenanthos
terminalis).
Shape
The epacrids and Correa have tubular flowers,
whereas Lysiana, Eremophila, and Grevillea have
gullet-shaped flowers. Some flowers visited by birds
are very open, especially Eucalyptus but also
Amyema and Xanthorrhoea. Most of these flowers
have large or many stamens. Flowers are clumped in
many Eucalyptus, Amyema, and Grevillea and
packed into tight inflorescences in Banksia and
Xanthorrhoea. There are no landing-stages on the:
 512 New Zealand Journal of Botany, 1979, Vol. 17

Table 3 Characteristics ofa typical bird-pollinated flower, and those of the main Australian genera pollinated by birds.
Genus ColoUl'" Flower/ Smell Nectarb Anther/ Source
inflorescence (cal/fl. nectary
shape orinflor.) distance
(mm)
"typical Red Tubular, bell, None Plentiful Distant Faegri & van der Pijl
s~ndrome" Cgullet/brush (1966)
Ca listemon Red, green, yellow Open/brush None 5-20/fl. 20 Paton & Ford (1977)
Calothamnus Red Semi-tubular/ None 10/fl. 25 Collins (unpublished
brush data)
Eucalyptus White, red, yellow Open/brush None 1~5/fl. 5-15 Paton & Ford (1977)
Darwinia Red, yellow Small tubelbell None ? 5-15 Keighery (1975)
Adenanthos Red, pink, orange, Gullet None 2-5/fl. 20 Paton & Ford (1977)
yellow
Grevillea Red, yellow, orange, Gullet None 5-10/fl. 25-30 Paton & Ford (1977)
green, pink, black
Banksia Yellow, orange, red, Gullet/brush Strong 100-2000/ 20-50 Paton & Ford (1977)
cream, greenish, brown musky inflor.
Dryandra Yellow Gullet Heavy, 50-100/ 20-30 Robinson (1947)
nauseous inflor. Collins
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(unpublished data)
Amyema Red, green, orange, grey Open/brush None 2-10/fl. 20-30 Paton & Ford (1977)
Correa Green, red, white Tube Slight 5-20/fl. 20-30 Paton & Ford (1977)
fruity
Brachyloma Pink Small tube None 5/fl. 3-5 Paton & Ford (1977)
Epacris Red, white, pink Tube None 0.5-2/fl. 10-20 Paton & Ford (1977)
Astroloma Red, white Tube None 7-12/fl. 15-20 Paton & Ford (1977)
Eremophila Red, yellow Gullet None 50/fl. 30-50 Paton & Ford (1977)
Xanthorrhoea White Open/brush Musky 20/fl. 10-20 Ford (unpublished data)
Anigozanthos Red, yellow, green Gullet None 50/fl. 30-80 Mees(1967)
"Commonest colour first, bird-pollinated species only.
bDaily production, nectar production varies greatly between species, individual plants, and days.
CA gullet-shaped flower has a zygomorphic tube, usually with one or more slits.

flower but insects experience little difficulty in
obtaining access to nectar of all except the tubular
flowers. Birds have little difficulty perching on
twigs, stems (Anigozanthos) , or even the inflor-
escences (Banksia) to obtain nectar.
SmeU
Most bird-pollinated flowers in Australia have little
smell other than that of the plant as a whole. Some
Eucalyptus flowers have a strong, honey smell.
Some Banksia and Xanthorrhoea have a strong,
musky, somewhat unpleasant smell. Correa also has
a slight smell.
Nectar
Some flowers (Epacris, a few small-flowered Euca-
lyptus) produce only c. 1 cal (4 J) of nectar per day,
whereas the most prolific (Eucalyptus cosmophylla,
Anigozanthos, Eremophila) produce 50-100 cal.
Most average 5-20 cal although there is great
variation between individual plants and the same
plant under different 'weather conditions. Banksia
inflorescences may produce up to 4000 cal from c.
200 newly opened flowers. These rates of production
compare with those of hummingbird flowers (Wolf et
al. 1976). Nectar is produced in Banksia, Eucalyp-
tus, Grevillea. and Correa and other genera over-
night as well as during the day, and Carpenter (1978)
has shown that Banksia ericifolia produces most of
its nectar at night or early morning. Pollen is most
conspicuous in bird-pollinated flowers in the early
morning. Birds require about 10-50 kcal per day and
visit several hundred to many thousand flowers per
day. Often individual flowers are visited five or more
times each day by birds.
PoUen placement
In most of the tubular or gullet-shaped flowers the
anthers and stigma extend beyond the tube. In the
epacrids. however, the anthers are within the corolla
tube and pollen is sticky and adheres to the birds'
beaks. In Grevillea. Adenanthos. and Banksia pollen
is presented on the end of the style around the stigma
which later becomes receptive to pollen from
another plant. Placement of the pollen of these three
genera is localised on the honeyeater's head. The
sympatric Anigozanthos manglesii and A. humilis
place pollen on the nape and forehead, respectively.
of wattlebirds and so achieve some, but not
complete, reproductive isolation (Hopper & Bur-
bridge 1978). The anthers of A. manglesii are 80 mm
from the nectary and pollen is dusted on the backs of
small honeyeaters (Acanthorhynchus) (Mees 1967).
In Eucalyptus. Callistemon. Amyema, and
 Ford et al. - Birds as pollinators
Xanthorrhoea pollen placement is not very localised
and pollen may be dusted all over the face, and even
on the undersurface of the body. Lorikeets harvest
the pollen of some species of Eucalyptus and may
pollinate the flowers with their tongues.
Thus bird-pollinated flowers in Australia are
highly diverse. The most obvious departures from
the typical bird-flower syndrome are in the shape -
simple, cup-shaped flowers are common (e.g.,
Eucalyptus); colour - white, yellow, and green are
common, grey and black flowers occur; and smell -
Banksia and Xanthorrhoea have a strong smell.
EVOLUTION OF BIRD-POLLINATED
PLANTS IN AUSTRALIA
Honeyeaters and other Australian nectar-feeding
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birds have brush-tongues. It has been suggested
(Keast 1976) that these have evolved along with
nectar feeding. Could brush-tongues have evolved
before nectar-feeding, possibly as an adaptation to
lick up droplets of dew in the arid parts of Australia
or to lick up sugary secretions from damaged plant
material or honeydew? The tongue would then be
preadapted to nectar feeding. Birds may also or
alternatively have been attracted to insects feeding
on flowers, and casually started to take nectar. One
difficulty with this explanation is that nectar-
rewards would initially have been very small,
although nectar-production within a species is even
now very variable, so sufficient could have been
produced on occasions.
Australian flowers visited and po1Iinated by
birds are clearly very diverse. Plants which are
morphologically highly specialised for bird-pollin-
ation (Anigozanthos. Banksia. Correa. Astroloma.
and some species of Eremophila. Grevillea) occur
alongside much more generalised types (Eucalyptus.
Amyema). The latter appear as important, if not
more important as nectar-sources for the birds (Ford
& Paton 1977. Ford 1979. Keast 1976). Many of the
plants po1Iinated by birds (chiefly the brush types)
are also visited and probably pollinated by other
animals. We suggest ways in which bird-pollination
evolved in the major bird-po1Iinated groups of plants
in Australia and finally speculate about how, when,
and why pollination by birds originated.
Most species of Eucalyptus attract large
numbers of insects to their flowers, and some are
visited by mammals (Morcombe 1968). It has even
been suggested that the insects are the main attrac-
tant for birds and mammals. It is difficult to judge the
relative importance of these visitors to the plant.
Insect hairs, bird feathers, and mammal fur are all
good surfaces for the attachment of pollen. The
stamens of Eucalyptus are so numerous and
spreading that few visitors would avoid a dusting of
pollen. Present eucalypts show a range from small-
flowered, predominantly insect-pollinated forms
513
(e.g., E. foecunda) to much larger, predominantly
bird-pollinated forms (e.g., E. cosmophylla. E.
macrocarpa). Early eucalypts were presumably
insect-pollinated. Birds would have found it easy to
gain access to the flowers and nectar production may
have been sufficient as it is today in some small-
flowered forms (e.g., E. fasciculosa). Increased
nectar production would have been favoured in
some species. The amount of nectar produced by the
present larger-flowered species (E. leucoxylon, E.
cosmophylla, and E. incrassata) would be excessive
as an insect-attractant. Most insects would be able to
obtain most of their requirements from a single
flower and thus would be ineffective cross-pollin-
ators (Heinrich & Raven 1972). In addition, the
larger-flowered forms show a tendency to have
evolved red stamens (e.g., E. leucoxylon rosea, E.
sideroxylon. E. macrocarpa), possibly to escape the
attention of insects. A parallel change may have
taken place in Callistemon where the red-flowered
species are most favoured by birds.
Bond & Brown (in press) studied honeybees
(Apis mellifera) and honeyeaters feeding on the
flowers of Eucalyptus incrassata. They found that
honeyeaters took most of the nectar in the early
morning, with the bees mopping up what was left.
Ford (1979) inferred that the same was happening in
other eucalypts and it is also true of Callistemon
(Paton, unpublished data). Presumably native bees
fed in a similar way before the honeybee was intro-
duced. Under this system the plant could well
achieve greater efficiency from all of its pollinators.
Eucalyptus can thus be seen as a genus with morpho-
logically un specialised flowers pollinated by a wide
range of vectors. Rather than being seen as a primi-
tive condition this may be a highly advantageous
strategy in recent Australian forests where the
climate is erratic and flowering not very predictable.
Eucalypts appear to keep all their options open, they
can be po1Iinated first by birds, later in the day by
insects such as bees, flies, and beetles, and at night
by mammals and possibly moths. Birds may be more
important in cold weather, insects in warm weather.
Lorikeets consume Eucalyptus pollen in large
quantities (Churchill & Christensen 1970), however,
even this may be advantageous to the plants as the
flowers are rarely damaged and the lorikeefs tongue
may effect pollination (Hopper & Burbidge 1979).
The evolution of bird-pollination in the Epa-
cridaceae may be traced through a series of condi-
tions. Insect-pollinated genera like Leucopogon
have small tubular flowers. Probably bees, long-
tongued flies, and Lepidoptera are their main pollin-
ators. Brachyloma has larger flowers, produces
moderate amounts of nectar, and is visited by both
insects and birds. Astroloma and perhaps Styphelia
may be exclusively bird-pollinated. They have long
narrow corollas with hairs near the lips (as do
Leucopogon) maybe to exclude short-tongued
 514
insects from their copious nectar or to keep water
away from the anthers.
Mistletoes of the genus Amyema produce
moderate quantities of nectar and are important
sources of nectar for birds in summer in southern
Australia. An Amyema flower is initially tubular, the
perianth splitting first medially. At this stage birds
can obtain access and force the flower open to take
the nectar. The petals later fold back to allow easier
access to a wide range of insects. Amyema flowers
are red, red and green, or occasionally entirely green
or grey and are often hard to see amongst the reddish
foliage. Possibly these colours deter insects. No less
than 28 species of birds have been recorded visiting
Amyema, along with a range of bees, wasps, flies,
and butterflies. Amyema thus retains the options of
bird and insect vectors. Lysiana, Muellerina.
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Nuytsia, and Amylotheca are more exclusively bird-
pollinated.
The Proteaceae include many important genera
for birds. Australia had few species of large bees
equivalent to the bumble bees ofthe Northern Hemi-
sphere until the introduction of Apis mellifera
(Michener 1970), so how can one explain the evolu-
tion of a long and often curved style as shown in
Grevillea. Adenanthos. and Hakea? Probably large
Diptera, butterflies, and moths were important in the
evolution of the bird-pollinated members of these
genera. They still pollinate some species today.
Species of Banksia, with their dense inflorescences
of thousands of flowers and massive nectar produc-
tion, are obviously highly specialised for a verte-
brate pollinator. Birds are frequent visitors to and
important pollinators of many species of Banksia.
Mammals too may be important pollinators of
some genera pollinated by birds. Morcombe (1967)
found that the very rare marsupial dibbler (Ante-
chinus apicalis) in Western Australia fed on Banksia
nectar. He also noted native rats (Rattus fuscipes)
were caught in traps near Banksia inflorescences.
Rourke & Wiens (1977) suggested that a group of
Western Australian Banksia were chiefly or entirely
mammal-pollinated. Holm (1978) suggested that the
honey-possum (Tarsipes spenserae) feeds entirely
on nectar and pollen and independently stated that
some Banksia species could be exclusively mammal-
pollinated. Carpenter (1978) was unable to find much
Banksia ericifolia pollen on honeyeaters in New
South Wales but found three native rats (Rattus
fuscipes) carrying heavy loads of pollen. Character-
istics which could specifically favour mammals are
massive nectar-production, strong smell. hooked
styles, and inflorescences close to the ground (geo-
florous) and hidden in dense foliage. However,
Banksia collina in New South Wales. which shows
all of these characteristics (Ford, unpublished data),
is visited by many species of birds which carry large
amounts of pollen. Hopper (1980) found that honey-
eaters carried pollen of straight-styled B. baxter; and
New Zealand Journal of Botany, 1979, Vol. 17
hooked-styled B. occidentalis in Western Australia.
Honey-possums carried very little Banksia pollen,
though a few animals carried a little Beaufortia or
Calothamnus pollen (Myrtaceae).
Rats are recent arrivals in Australia (Watts
1974) and are probably only opportunistic feeders on
nectar. At least since European settlement the more
specialised nectar-feeding marsupials (Tarsipes,
Antechinus apicalis. and pygmy-possums (Cercar-
tetus) have been relatively uncommon, but more
generalised marsupials (e.g., Antechinus stuartil)
which also take nectar and carry pollen (Recher
1979) are often numerous. The importance of
mammals as pollinators of Banksia should be studied
further. The possible evolution of bird- and mammal-
pollination will be discussed later.
Eremophila is a large, important genus for birds
though about half the species are insect-pollinated
(e.g., E. scoparia Chinnock, pers. comm.). It
probably diversified in the drier inland parts of
Australia relatively recently (Barlow 1971). The
changes from insect- to bird-pollination are rela-
tively small, involving only an increased size of the
corolla, greater nectar production and a tendency
towards the possession of red flowers.
We have suggested ways in which bird-pollin-
ation could have evolved in the more important
groups of plants in which it is prevalent today.
However, when did bird-pollination originate and in
relation to which plants? Table 4 presents the
possible origin of various plant, bird, and mammal
groups in Australia. There seems little doubt that the
Myrtaceae, Proteaceae, Epacridaceae, and Loran-
thaceae (Raven & Axelrod 1972, Johnson & Briggs
1975) were present by the early Tertiary and with
them the marsupials (Sharman 1974) and probably
the parrots (Cracraft 1976). At about this time
Australia was starting to move apart from Antarctica
and enter a period of isolation from the other conti-
nents. Some passerine birds may have been present
then but practically all the families now in Australia
would have arrived or evolved much later. Birds are
notoriously infrequent in the fossil record and no
passerines are known before the Pleistocene. The
current hypothesis is that there were a few invasions
from the north when Australia was well isolated and
that some of these underwent a massive adaptive
radiation to give many of Australia's characteristic
birds, including the honeyeaters (Sibley 1976). Other
species, e.g., the sunbird and silvereye, are much
more recent arrivals.
Keast (1976) considers that the honeyeaters co-
evolved with Eucalyptus and probably other
Australian plants. Eucalyptus has probably under-
gone its adaptive radiation relatively recently Oast 30
million years or less). Many species are adapted to
semi-arid environments (prevalent in the late
Tertiary) and most species hybridise freely. Euca-
lyptus-type pollen has been found in Eocene
 Ford et al. - Birds as pollinators 515
Table 4 Suggested origin of various plant. bird. and mammal groups in Australia.

Ended
million years ago
Pleistocene Rattus
Sunbird
Silvereye
Pliocene Eremophila
Bird-pollinated epacrids
Miocene II Eucalyptus Rodents
Honeyeaters
Oligocene 25
Eocene 40 Banksia
Pre-Eucalyptus
Palaeocene 55 Early mistletoe on Nothofagus
Cretaceous 70 Epacridaceae Parrots
Loranthaceae Marsupials
Myrtaceae
Proteaceae
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deposits and more probably Eucalyptus dates from Rodents more recently started taking nectar in South
the Pliocene (Martin 1973). However, many myrta- America, Australia, and Hawaii. Rodents reached
ceous pollens are very similar. Early honeyeaters Australia 15-20 million years ago (Miocene), but
and Eucalyptus may have been contemporary, Rattus arrived less than I million years ago (Watts
though it is surprising that the Eucalyptus flower has 1974). It is possible that Banksia and some of the
undergone so little diversification for its bird, insect, Myrtaceae coevolved with marsupial pollinators and
and possibly mammal pollinators. It seems probable honeyeaters arrived much later on the scene. Birds
that the relationship between honeyeaters and Euca- like thornbills and shrike-thrushes, which are
lyptus is more recent than the origin of bird-pollin- un specialised for nectar-feeding, can visit Banksia
ation in Australia. Possibly the diversification of the and Eucalyptus today, so it is possible that early
honeyeater genus Meliphaga and Eucalyptus have honeyeaters or their ancestors first started feeding
coincided. Alternatively the bird-pollinated euca- on Banksia or early Myrtaceae before visiting other
lypts could have coevolved with lorikeets and the flowers. Nectar often drips from Banksia inflores-
honeyeaters more recently started to exploit them. cences and so would attract unspecialised visitors.
In the Epacridaceae the major diversification of Carpenter (1978) suggests that 13 of the 52 modem
species, presumably including the bird-pollinated species of Banksia could be mammal-pollinated as
ones, was post-Miocene (last 10 million years), they have hooked styles. She and Rourke & Wiens
although some of the genera are as old as Eocene (1977) suggest that mammal-pollinated banksias
(Leucopogon, Smith-White 1955). Coevolution have evolved from bird-pollinated ones. We are here
between honeyeaters and the long-tubular epacrids suggesting the reverse. It would be valuable to find
thus may have been relatively recent, though the out which species of Banksia are pollinated by
flowers are certainly more specialised for birds than mammals or birds and which are the more primitive
are those of Eucalyptus. members of the genus. The more generalised flowers
Pollen of Banksia or Dryandra dates from the of bird (and mammal) pollinated Myrtaceae, today,
Eocene and these genera appear to have evolved provide fewer clues on their original pollinators.
from the primitive rain-forest genus Musgravea Finally, the Loranthaceae were present by the
(Johnson & Briggs 1975). Banksia fruiting cones late Cretaceous, well before the honeyeaters.
have been found in brown coal deposits in Victoria Several genera, including the bird-pollinated Muel-
which are probably at least as early as Miocene. This lerina and Nuytsia, are believed to be very old
was most likely before the origin of honey eaters and (Barlow & Wiens 1971). That Muellerina occurs on
it seems appropriate at this stage to consider Notho/agus also suggests this. Mistletoes are
mammal-pollination as a prelude to bird-pollination. dispersed by birds in Australia now, but what did the
Sussman & Raven (1978) suggest that mammals dispersing in the late Cretaceous? Was there a
were important pollinators of Myrtaceae and Prote- primitive passerine in Australia, or a specialised
aceae. Marsupials in the Upper Cretaceous were parrot, or were marsupials the dispersers? If there
probably replaced by primates in the Palaeocene, was a primitive passerine could it also have been a
and these were replaced by bats and birds in the pollinator?· There is thus the possibility that bird-
Eocene and Miocene. Australia retains a few pollin- pollination existed by the beginning of the Tertiary in
ating marsupials and Madagascar has nectar-feeding Australia, maybe involving a very specific relation-
lemurs in the absence of more modem primates. ship. Honeyeaters are a very successful and aggres-
 516
sive group (Keast 1976) and could easily have
displaced other pollinating birds, just as the mistle-
toebird (Dicaeum hirundinaceum) may be displacing
the painted honeyeater (Grantiella picta) which is a
specialist feeder on mistletoe berries. Thus, bird-
pollination could have originated very early in
Australia, and may pre-date pollination by
marsupials.
REASONS FOR THE PREVALENCE OF
BIRD-POLLINATION IN TEMPERATE
AUSTRALIA
Most of the evidence for bird-pollination described
above comes from studies carried out near Adelaide,
Melbourne, Perth, and Sydney, at 34-4O"S. Nectar is
a major source of food for some 20 species of birds
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and a minor source for over 20 others. Birds are
major pollinators of some 30 genera of plants and
many of these (Eucalyptus and Banksia) are highly
diverse and abundant genera.
There are no nectar-feeding birds between 34°
and 40"N in southern Europe and north Africa and
only two species of sunbirds (Nectariniidae) in Asia.
North America has a total of eight species of
hummingbirds north of 34°N (peterson 1961). The
southern continents have more nectar-feeding bird
species. There are four species of sunbirds and two
sugarbirds (Promerops) in southern Africa (only a
small portion of which is further south than 34°S)
(Roberts 1940) and about five species of humming-
birds at equivalent latitudes in South America (de
Schauensee 1970). New Zealand which has few land
birds nevertheless has seven nectar-feeding species.
Many of the bird-pollinated plants in the southern
continents are Myrtaceae and Proteaceae.
It seems hard to believe that birds have
occupied a role which was vacant due to the absence
of appropriate insects. Just among the bees Australia
has maybe 3000 species, though few are large. Most
are associated with the Myrtaceae, the family with
the most bird-pollinated species (Michener 1970).
Another possibility is that birds have taken over
from mammals as pollinators. This may be true of
o;ome Proteaceae but probably not of other families.
What are the costs and advantages to the plants
of having birds as pollinators? Many genera, such as
Eucalyptus, Banksia, Grevillea, Amyema, are very
successful, especially in areas with poor soil. The
costs to the plant would be increased nectar pro-
duction, stronger, larger flowers, and altered colour-
ation. Energy in the form of sunlight is rarely limiting
in Australia, so sugars are inexpensive to produce,
though water is sometimes limiting. The costs of
larger, stronger flowers could be offset by the pro-
duction offewer flowers. This is evident in Eucalyp-
tus (compare the big flowers of E. cosmophylla, with
c. 1000 per plant, and the tiny flowers of E.foecunda
with tens of thousands per plant). Alternatively,
New Zealand Journal of Botany, 1979, Vol. 17
flowers could be packed tightly together (e.g.,
Banksia).
There are several possible advantages in birds
as pollinators. Firstly, they may increase the chance
of outcrossing. Birds require much more energy than
insects and, although this is partly offset by greater
production of nectar, they probably visit flowers
much more quickly than insects do. There are few
data supporting this, though Ford (1979) found birds
visited 23-75 Eucalyptus per min. whereas honey-
bees visited only 6 E. incrassata flowers per min
(Bond & Brown, in press) Hopper (pers. comm.)
found that honeyeaters visited 5~70 Syzygium
flowers per min, against 4-60 per min for a range
of insects.
Birds thus visit more flowers and probably fly
further during a feeding bout. Visits between neigh-
bouring plants are thus more likely with birds. As
discussed earlier, birds carry appreciable quantities
of pollen and can effect pollination in most flowers
they visit. The relative efficiency of birds and insects
needs to be measured experimentally by removing
one or both vectors from flowers and looking at
seed-set.
The effectiveness of birds as cross-pollinators
depends on their behaviour, which depends on the
richness and predictability of the nectar source. As
a nectar source becomes richer it is more likely to
attract birds and so be pollinated. However, as it
becomes richer the birds will travel less further and
may eventually become territorial around a few
plants or even a single plant. Thus. cross-pollination
will decrease. Carpenter (1976) found this to be true
with Hawaiian honeycreepers and Metrosideros.
Honeyeaters often hold territories in the non-breed-
ing and breeding season (Ford & Paton. unpublished
data). In plants which are defended cross-pollination
will mostly be achieved by intruding birds which
may visit only a few flowers from each plant before
being chased a considerable distance. Territorial
birds often visit plants outside their territories
(Paton, unpublished data). The optimum strategy a
plant could adopt to maximise cross-pollination
would be to have sufficient nectar to attract birds yet
insufficient to satisfy all of one bird's requirements.
Table 5 shows that many individual plants produce
nectar at about this level, although there are excep-
tions, e.g., Eucalyptus cosmophylla. The prevalence
of bird-pollination in temperate Australia compared
with other continents cannot be accounted for solely
by these suggested, but as yet unproved, advantages
of birds as cross-pollinators.
On average the climate in coastal southern
Australia is equable (e.g., Adelaide. July mean 12°c,
January mean 22°c; Sydney, July mean nOe,
January mean 22°c). However. day-to-day fluctu-
ations are often large and unpredictable. It may be
hard for insects to evolve as reliable pollinators
under these conditions especially for winter-flower-
 Ford et al. - Birds as pollinators 517
Table 5 Approximate daily requirements of nectar- Iyptus). Possibly both of these strategies have
feeding birds and daily nectar production of some evolved to reduce insect predation on flowers. fruits,
Australian plants, in full flower (Ford & Paton,
unpublished data). and seeds. Herbivorous insects are often very
abundant and may destroy most of the foliage, and
Birds IO-SO kcal/day probably seeds and fruit of Eucalyptus (Morrow
Eucalyptus cosmophylla 100 kcal/plant/day 1977).
Callistemon macropunctatus 20
Small Eucalyptus 20 A further possibility is that birds may also
Banksia 1-20 behave as protectors. Honeyeaters take a wide range
Xanthorrhoea 2.S of insects and may be very abundant when some
Grevillea 2-6 plants flower. They could significantly reduce the
Astroloma 2
Adenanthos 1.5 numbers of some herbivorous insects. Parallels
Amyema 1-2 could be drawn with the acacia-ants of central
Correa I America (Janzen 1966). The sclerophyll forests and
Epacris O.I...{).S heaths of southern Australia where bird-pollination
is most important are characterised by a deficiency
in nutrients, especially phosphorus. Thus, although
ing plants. Birds on the other hand are buffered sugars can be produced cheaply, proteins and other
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against changes in weather to a much greater extent essentials are produced at considerable cost. So the
and could be more reliable pollinators. Many of the prolific production of nectar may be a small price to
bird-pollinated plants flower in winter, others are pay for even slight protection of foliage, flowers,
unpredictable in their flowering (e.g., some Euca- pollen, and fruit.

~ppendix 1 List of families and main genera which Nuytsia 2 o

Include species visited and ~llinated by birds; with Loranthus.
number of species of plants which have been seen to have Mistletoes
been visited by birds, number of species of birds seen unspecified 11
visiting plants of that genus/family, and carrying pollen,
and an estimate of number of species predominantly Rutaceae
pollinated by birds. (Full details of species of plant and Correa 6 13 9 10
bird, and source of information retained by H.A.F.) Diplolaena 2 4 o 2
Euodia 1 3 o
Plant No. plant No. bird No. bird Estimated Chorilaena 1 1 o
genus species s~c.ies species species Phebalium 1 2 o
visited vlsltmg pollinating bird- Boronia 1 I o
by birds genus genus pollinated Citrus
(introduced) 8 o
Myrtaceae
Eucalyptus 74 83 18 200 Myoporaceae
Callistemon 6 28 4 10 Eremophila i2 16 7 40
Melaleuca 4 13 0 SO Myoporum 1 1 o
Darwinia 4 6 0 20 Xanthorrhoeceae
Calothamnus 3 7 0 24 Xanthorrhoea 6 24 3
Leptospermum 3 8 0 Haemodoraceae
Beaufortia I 2 0 10 Anigozanthos 4 6 2 8
Angophora I 7 0 Macropidia 1 I o 1
Syzygium 3 6 0
Regelia I I 0 S Mimosaceae
Acacia 3 7 4
Proteaceae
Grevillea 19 3S 11 ISO Less important ramilies
Banksia 16 31 16 60 Fabaceae II SO
Adenanthos 7 12 8 23 Pittosporaceae 3
Dryandra 8 10 0 SO Lauraceae 2
Hakea 4 13 0 20 Pandanaceae 1
Lambertia 3 4 0 Malvaceae 2
Darlingia 1 1 0 Lythraceae 1
Amaryllidaceae I
Epacridaceae Thbmeleaceae I
Astroloma S 19 8 20 La iatae 2
Brachyloma 1 12 7 S Rosaceae 1
Epacris 2 11 4 S Santalaceae I
Styphelia 1 2 0 7 Flacourtiaceae 1
Melichrus 1 1 0 1 Agavaceae 1
Loranthaceae Verbenaceae 1
Amyema 4 29 10 IS Eleaocarpaceae I
Lysiana 1 8 6 6 Araliaceae 1
Muellerina 2 3 3 4 Naturalised
Amylotheca 1 3 0 2 exotics 6+ 2
 518
ACKNOWLEDGMENTS
Jim Armstrong and John Williams made many useful
comments on the manuscript. We are grateful to many
people including Brian Collins, Bob Chinnock, Steven
Hopper, Alan Burbidge, Noel Beadle, and Graham Pyke
whose opinions during discussion have greatly improved
the paper.
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