CSIRO PUBLISHING
www.publish.csiro.au/journals/ajb
Australian Journal of Botany, 2004, 52, 371–379
The swift parrot, Lathamus discolor (Psittacidae),
social bees (Apidae) and native insects as pollinators of
Eucalyptus globulus ssp. globulus (Myrtaceae)
A. B. HingstonA,C, B. M. PottsB and P. B. McQuillanA
A
School of Geography and Environmental Studies, University of Tasmania, Private Bag 78,
Hobart, Tas. 7001, Australia.
B
School of Plant Science and Cooperative Research Centre for Sustainable Production Forestry,
University of Tasmania, Private Bag 55, Hobart, Tas. 7001, Australia.
C
Corresponding author; email: [email protected]
Abstract. It has been argued that the production of sufficient nectar to attract bird pollinators would evolve if the
fitness benefits accruing from pollination services by birds, compared with insects, outweighed the cost of
increased allocation of photosynthate to nectar. This hypothesis implies that the pollination services provided by
birds must be considerably better than those provided by insects with which the plant has evolved. Consistent with
this, we found that the endangered native swift parrot Lathamus discolor (Shaw) was a very effective pollinator of
the native tree Eucalyptus globulus Labill. in Tasmania, facilitating an average of 76% of the maximum possible
seed set for open-pollinated flowers in just one visit to a flower, whereas single flower visits by native insects did
not facilitate any seed production. Flowers visited once by either species of introduced social bees, the honeybee
Apis mellifera L. or the bumblebee Bombus terrestris (L.), produced less than 7% of the maximum possible seed set
for open-pollinated flowers. Hence, easily managed social bees appear to be poor substitutes for bird pollinators in
commercial seed orchards of this tree. We propose three possible reasons why this largely bird-pollinated tree has
not evolved characters that deter insects from removing nectar.
BT03018
ABeta.irlBd.sHaindgbesotsnaspolinatorsofE. golbuls
Introduction
It has been predicted that birds are often better than insects
as pollinators of plant species with flowers from which they
both collect nectar (Stiles 1978; Bertin 1982a, 1982b; Paton
1986b). It is generally believed that bird-pollinated flowers
mostly evolved from insect-pollinated flowers (Faegri and
van der Pijl 1979; Ford et al. 1979; Hopper and Burbidge
1986; Paton 1986b). This involved increased allocation of
sugars to nectar production to meet the energy requirements
of birds (Stiles 1978; Faegri and van der Pijl 1979; Ford et al.
1979; Bertin 1982b; Paton 1986b). For such a change to be
favoured by natural selection, the fitness gains to the plant
from bird pollination must be great enough to offset the
increased costs associated with greater allocation of
photosynthate to nectar production (Stiles 1978; Bertin
1982a, 1982b; Paton 1986b). This implies that the
pollination services provided by birds must be considerably
better than those by insects with which the plant has evolved
(Stiles 1978; Bertin 1982a, 1982b; Paton 1986b). Better
pollination services from birds could result if they are more
likely to effect outcross pollination, or because they are more
© CSIRO 2004
reliable flower visitors in variable weather conditions, than
are insects (Paton 1986b).
Many plants that evolved sufficient nectar production to
attract birds also evolved floral characters that maximise the
proportion of their nectar available to highly effective bird
pollinators by discouraging less effective insects from
removing nectar (Faegri and van der Pijl 1979; Paton 1986b).
The absence of such characters in some plants that have
evolved sufficient nectar production to attract birds suggests
that there may sometimes be a selective advantage in
remaining attractive to insects. This implies that insects are
still able to provide useful pollination services at times and
places when birds are scarce (Ford et al. 1979).
An example of a plant species with flowers that are visited
by both birds and insects is the south-eastern Australian
forest tree Eucalyptus globulus Labill. ssp. globulus
(Myrtaceae) (hereafter E. globulus) (Hingston and Potts
1998; Hingston et al. 2004b). If the absence of
insect-deterring floral characters in E. globulus is the result
of insects being able to provide valuable pollination services
in the absence of birds, social bees may provide a simple
10.1071/BT03018
0067-1924/04/030371
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Australian Journal of Botany
means of ensuring high yields of good-quality seeds from
seed orchards of this tree. Seed orchards of E. globulus are
often planted in areas where its coevolved bird pollinators do
not occur, because this tree is grown extensively in
commercial forestry plantations in many temperate regions
of the world (Eldridge et al. 1993; Tibbits et al. 1997). In
these situations, populations of social bees, such as the
honeybee Apis mellifera L. and the large earth bumblebee
Bombus terrestris (L.), can be increased readily by importing
hives at the time of flowering. Even within the natural
distribution of E. globulus on the island of Tasmania, the
exotic A. mellifera is now the most frequent visitor to its
flowers (Hingston and Potts 1998; Hingston et al. 2004b).
B. terrestris also forages regularly on E. globulus in
Tasmania (Hingston and McQuillan 1998; Hingston 2002),
having spread rapidly across the island following its
discovery in 1992 (Hingston et al. 2002).
Because these introduced colonial bees are larger and
more energy-demanding than most native Tasmanian insects,
they may be more effective pollinators of E. globulus than
are insects with which it has evolved. It has been proposed
that insects may be poor pollinators of E. globulus because
they seldom contact the stigma of this large dish-shaped
flower (Hingston and Potts 1998). However, the large bodies
of both of these introduced bees, particularly B. terrestris,
could facilitate more frequent stigmatic contact than do visits
by most native insects. It has also been suggested that insects
may be poor pollinators of E. globulus because they
appeared to move infrequently among trees (Hingston and
Potts 1998). Such behaviour is likely because the production
of sufficient nectar to attract large endothermic animals,
such as birds, may satiate small ectothermic insects, thereby
reducing their need to move frequently among flowers (Paton
1986a). The flowers of E. globulus produce ~100 times more
nectar per day than produced by the closely related E. nitens
(Hingston 2002), which is exclusively insect-pollinated
(Hingston 2004a). Con- sequently, insects would not move as
widely as birds, thereby promoting selfing rather than
outcrossing (Ford et al. 1979; Eldridge et al. 1993; Paton
1993). Self-pollination in E. globulus results in the
production of fewer seeds, lower seed viability, slower
growth rates and higher mortality rates in offspring, than
occur after outcrossing (Hardner and Potts 1995; Hardner
et al. 1998; Pound et al. 2002a, 2002b). However, individual
A. mellifera collect ~100 times more nectar than they need
for their own use (Faegri and van der Pijl 1979), suggesting
that they might move more frequently among flowers and
plants than do native insects, thereby enhancing their value
as pollinators.
This paper compares the effectiveness of A. mellifera and
B. terrestris as pollinators of E. globulus with those of a
native bird and native insects within the tree’s natural
distribution in south-eastern Tasmania. It also examines
whether differences among anthophile species in pollinator
A. B. Hingston et al.
effectiveness can be attributed to the frequency with which
various taxa contact stigmas, as previously suggested by
Hingston and Potts (1998).
Materials and methods
Study species
The flowers of E. globulus exhibit an allophilic syndrome (sensu Faegri
and van der Pijl 1979), with nectar and pollen exposed to all flower
visitors. They are actinomorphic and dish-shaped, with a single robust
style emerging from a broad nectar-secreting hypanthium that is
surrounded by a dense, showy annulus of long white stamens (Curtis
and Morris 1975). The floral bud measures 15–30 mm in length and
15–20 mm in diameter (Curtis and Morris 1975).
The flowers of Eucalyptus are protandrous (Pryor 1976). Floral
development involves initial shedding of the woody operculum, to
expose the anthers and non-receptive stigma (Boland et al. 1984). In
E. globulus, peak stigmatic receptivity occurs ~1 week after operculum
shedding (Hardner and Potts 1995) and flowers usually senesce when
~15 days old (Brown 1989).
Field procedures
The effectiveness of flower visitors as pollinators of E. globulus was
investigated by comparing the numbers of capsules and seeds produced
following single visits to flowers with receptive virgin stigmas on four
trees scattered along a 40-km section of the Derwent River near Hobart.
Single visits to flowers were made on trees designated numbers 353,
1085 and 1086 between December 1999 and January 2000, and on tree
number 6151 in December 2000. Ample opportunities for outcrossing
were present in the form of numerous conspecifics flowering near all
experimental trees.
To ensure that animals foraged normally at flowers with receptive
stigmas, a technique was devised that allowed pollen and nectar to be
removed from flowers during the week prior to peak stigmatic
receptivity without stigmas being contacted. Opercula were removed
from flowers as they were beginning to separate from the receptacles.
The newly exposed styles were immediately covered with a section of
tightly fitting plastic tube (AWG 10-12 std, UNASCO Pty Ltd,
Giraween, NSW) that had previously had the distal end sealed by heat,
thus isolating the style (Harbard et al. 1999; Williams et al. 1999).
Tubes were removed from flowers during fine, mild to hot weather
between 0900 hours and 1800 hours 5–8 days later, to expose the
receptive virgin stigmas. Each of these female-phase flowers was
watched from a distance of less than 1 m until a single naturally
foraging insect contacted the gynoecium, androecium or hypanthium.
Other flowers with virgin stigmas were exposed to single visits by
one of two captive swift parrots, Lathamus discolor (Shaw), between
1000 hours and 1600 hours. The parrots were taken in a small cage to
the experimental trees, and the branches carrying the flowers with
virgin stigmas were presented to them through the door of the cage. The
caged birds were provided with a few male-phase flowers from other
trees as a source of outcross pollen (Paton 1991), and also had access to
male-phase flowers on the same branch as the flowers with virgin
stigmas, as a source of self-pollen. L. discolor actively consumes
eucalypt pollen (Gartrell et al. 2000; Gartrell and Jones 2001) and,
therefore, has the potential to rapidly acquire large loads of pollen on
the bill and head. During experiments in December 1999 and January
2000, the birds also had outcross pollen brushed onto their heads with
a cotton bud prior to the first branch being put through the door of the
cage. The outcross pollen used was a mix collected from approximately
10 trees on 14 September 1999 and had subsequently been stored in
gelatin capsules in glass vials with silica gel in a freezer. Pollen was
applied at least once every 10 flowers visited. However, the paucity of
E. globulus flowers during spring 2000 precluded the collection of
Birds and bees as pollinators of E. globulus
Australian Journal of Botany
373
Table 1. Numbers of flowers subjected to permanent stigma coverage, supplementary outcross pollination or single visits
by various animals, on four trees of Eucalyptus globulus, and the proportions of visits that resulted in stigmatic contact
In cases where not all flowers were probed for nectar, the number not probed for nectar is shown in parentheses, together with the
activity of the flower visitor: p = attempting to collect pollen; w = walking over the flower without attempting to feed
Family
Psittacidae
Apidae
Colletidae
Halictidae
Scoliidae
Sphecidae
Vespidae
Formicidae
Calliphoridae
Syrphidae
Cantharidae
Cerambycidae
A
Pollination treatment or visitor
Permanent stigma coverage
Cross supplement
Lathamus discolorA
Apis mellifera
Bombus terrestris
Leioproctus spp.
Hylaeus (Prosopisteron) spp.
Homalictus spp.
sp.
sp. 3
Vespula sp.
Small ant
Calliphora spp.
sp. 1
Chauliognathus spp.
spp.
353
1085
7
23
3/1.00
6/0.50
2/1.00
38
20
29/1.00
57(1p)/0.39
7/1.00
2/0.00
Tree code
1086
38
27
28/0.89
71/0.41
21/0.71
1/0.00
6151
32
30
32/1.00
50/0.79
1/1.00
8/0.38
32/0.10
2/0.50
1/0.00
1/1.00
1/1.00
2(1p)/0.50
2(1p)/1.00
1/1.00
16/0.27
3(2p)/0.00
127(17w)/0.80
All Lathamus discolor visits were by captive birds.
enough pollen to apply pollen to the birds manually during the second
season, and pollen loading had to be limited to provision of male-phase
flowers.
At the end of the first day when L. discolor were used in 1999,
pollen swabs were taken from the heads of both birds with four pieces
of transparent adhesive tape that were then placed onto microscope
slides. Pollen samples were taken from the upper, lower, left and right
sides of each bird’s head. The eucalypt pollen grains in the first 5.5 mm
from the bill tip, and between 5.5 mm and 11 mm from the bill tip (the
regions that contacted stigmas), were then counted (0–5.5 mm, mean =
1482, s.e. = 526; 5.5–11 mm, mean = 5306, s.e. = 1589) to verify that
these loads were similar to those carried by 20 mist-netted conspecifics
captured near flowering E. globulus (0–5.5 mm, mean = 4808, s.e. =
905; 5.5–11 mm, mean = 5748, s.e. = 1188; Hingston 2002).
Immediately after receiving a single visit from either an insect or
bird, styles were recovered with the tube. The flower was then tagged,
the identity of the visitor was recorded, along with whether the stigma
was contacted, and whether nectar or pollen was removed. Flowers were
subsequently checked to ensure the tubes remained in place until stigma
senescence.
Other flowers that did not have stigmatic tubes received
supplementary outcross pollen when receptive, to estimate the
maximum possible capsule and seed production per open-pollinated
flower on each tree. Pollen was applied to receptive stigmas late in the
day after insect activity had ceased, to reduce the chances of this
outcross pollen being secondarily transferred onto other flowers by
geitonogamous pollination (e.g. DeGrandi-Hoffman and Martin 1995;
DeGrandi-Hoffman and Watkins 2000). During the first season,
manually applied pollen was from the same outcross-pollen mix that
was used to load L. discolor. The pollen used in the second season was
collected from numerous trees on 7 September 2000 and also stored in
a freezer. Other flowers had their styles covered with tubes throughout
their lives, to ensure effective prevention of pollination.
Capsules were harvested ~1 year after flowering, and placed
individually in paper envelopes to dehisce so that the viable seeds could
be counted. For each pollination treatment on each tree, the mean number
of seeds produced per flower was calculated as the product of the mean
number of capsules per flower and the mean number of seeds per capsule.
Data analyses
The only taxa that visited flowers on all trees were the captive
L. discolor, and the freely foraging A. mellifera and B. terrestris. Hence,
the mean numbers of capsules and seeds produced per flower visited by
each of these taxa, and flowers subjected to supplementary
cross-pollination, were compared by using one-way ANOVA of the tree
mean values. This analysis was repeated by using only those flowers the
stigmas of which were definitely contacted by animals, to determine
whether differences among taxa in pollinator effectiveness were the
result of differences in the frequency of stigmatic contact. All datasets
were square-root transformed to meet the assumptions of normality and
homogeneous variances. Whenever statistically significant differences
were found among treatments, subsequent pairwise comparisons were
made by using Tukey’s tests. The mean numbers of capsules and seeds
produced per flower where the stigma was definitely contacted by
A. mellifera were also compared with the fecundity of flowers where
A. mellifera removed nectar without contacting stigmas on the four
trees, using paired t-tests.
Results
Female-phase flowers of E. globulus were visited by captive
L. discolor and 13 insect taxa (Table 1). These visits almost
always involved attempts to obtain nectar, although flowers
were occasionally visited in the search for pollen, or
contacted by insects walking over flowers (Table 1).
A. mellifera was the most common and widespread insect
visiting the flowers. B. terrestris also visited flowers on all
four trees. Soldier beetles Chauliognathus lugubris
(Fabricius) and Hylaeus (Prosopisteron) bees (Hylaeinae)
374
Australian Journal of Botany
A. B. Hingston et al.
Table 2.
Mean numbers of capsules and seeds produced per flower visit by various taxa and control treatments for four trees (353, 1085,
1086 and 6151) of Eucalyptus globulus
Different letters following values within total columns denote significant (P < 0.05) differences between treatments in fecundity, as determined by
Tukey’s tests, subsequent to 1-way ANOVA on square-root transformed data. Taxonomic affinities of visitors are given in Table 1
Pollination treatment or visitor
Stigma coverage
Cross supplement
Lathamus discolor
Apis mellifera
Bombus terrestris
353
1085
0
0.87
1.00
0.33
0
0
0.50
0.14
0.05
0.14
Capsules/flower
1086
6151
0
0.93
0.64
0.07
0.14
0
0.27
0.25
0
0
were common on tree number 6151, and native bees in the
genus Leioproctus (Colletinae) were recorded in low
numbers from three trees (Table 1).
Seeds were produced following supplementary outcross
pollination and single flower visits by L. discolor,
A. mellifera and B. terrestris (Table 2). However, single
flower visits by other insects failed to result in production of
seeds. The total absence of seed production from flowers
with stigmas exposed to insects other than social bees
indicates that the experimental removal and replacement of
the tube on the style did not result in any seed set. Any pollen
knocked onto the stigma while passing the flowers through
the door to the L. discolor would have been self-pollen and,
therefore, probably contributed little to seed production.
Therefore, it is reasonable to assume that seed production
following single visits by L. discolor, A. mellifera and
B. terrestris was the result of pollen deposition by those
animals and not by our actions.
Significant differences in capsule (F3,12 = 5.93, P = 0.010,
power of test = 0.70) and seed (F3,12 = 9.81, P = 0.0015, power
of test = 0.88) sets occurred among flowers visited once by
L. discolor, A. mellifera or B. terrestris, and open-pollinated
flowers receiving supplementary outcross pollen (Table 2).
Capsule and seed sets following supplementary outcross
pollination of open-pollinated flowers did not differ
significantly from those following single flower visits by
L. discolor, but were significantly greater than those
following single flower visits by either A. mellifera or
B. terrestris (Table 2). L. discolor facilitated the production
of significantly more seeds, but not capsules, than did either
A. mellifera or B. terrestris per visit. Across the four trees,
capsule and seed sets following single visits by L. discolor
averaged 80 and 76%, respectively, of the maximum possible
fecundity estimated by applying outcross pollen to receptive
stigmas that were permanently exposed to flower visitors. In
contrast, single flower visits by A. mellifera facilitated only
17 and 6.8% of the maximum possible capsule and seed sets
for open-pollinated flowers, and those by B. terrestris only 11
and 6.3%, respectively (Table 2).
The effectiveness of L. discolor as a pollinator of
E. globulus can be attributed, at least partly, to the fact that
Grand mean
0
0.64a
0.51ab
0.11b
0.07b
353
1085
0
10.70
04.00
01.67
0
0
5.25
1.59
0.11
1.86
Seeds/flower
1086
6151
0
11.70
15.05
00.45
00.21
0
5.10
4.31
0
0
Grand mean
0
8.19a
6.24a
0.56b
0.52b
they almost always contacted stigmas while feeding from
female-phase flowers (Table 1). This usually involved
contact with the bill and tongue as they licked nectar from
the hypanthium. In contrast, smaller insects, such as
A. mellifera, were able to access nectar without contacting
stigmas (Table 1) because of the large gap between the
stamens and style. Smaller insects only contacted stigmas if
they clambered over the style as they moved between the
hypanthial pits where nectar pooled, or if they used the
stigma as a landing or take-off platform on the flower. As a
result, insect contact with stigmas usually involved their legs,
mesosoma or metasoma.
The relative ineffectiveness of insects as pollinators of
E. globulus cannot be attributed entirely to their ability to
remove nectar without contacting stigmas. Because of their
large size, B. terrestris contacted stigmas almost as
frequently as did L. discolor (Table 1). However, they
facilitated significantly lower seed set per visit than did
L. discolor (Table 2). Moreover, when single visits to flowers
that did not result in stigmatic contact were excluded from
the analysis, significant differences among L. discolor,
A. mellifera and B. terrestris in capsule (F2,9 = 4.32,
P = 0.048, power of test = 0.55) and seed (F2,9 = 7.07,
P = 0.014, power of test = 0.69) production following single
visits were still apparent. As for analysis of single visits that
included those that did not involve stigmatic contact,
L. discolor facilitated the production of significantly more
seeds, but not capsules, than did either A. mellifera or
B. terrestris per flower visit that involved stigmatic contact
(Table 3). Indeed, fecundity from flowers whose stigmas
were contacted by A. mellifera was not significantly greater,
for capsule (t3 = 0.95, P = 0.41) or seed set (t3 = 0.71,
P = 0.53), than that where A. mellifera had removed nectar
without contacting stigmas (Tables 2 and 3).
Discussion
Management implications
The finding that single visits to flowers of E. globulus by
L. discolor resulted in 76% as many seeds as from
supplementary outcross pollination of open-pollinated
Birds and bees as pollinators of E. globulus
Australian Journal of Botany
375
Table 3.
Mean numbers of capsules and seeds produced per flower visit involving stigmatic contact for four trees (353,
1085, 1086 and 6151) of Eucalyptus globulus
Different letters following values within total columns denote significant (P < 0.05) differences between treatments in fecundity,
as determined by Tukey’s tests, subsequent to 1-way ANOVA on square-root transformed data. Taxonomic affinities of visitors are
given in Table 1
Flower visitor
Lathamus discolor
Apis mellifera
Bombus terrestris
353
1085
1.00
0.33
0
0.14
0.09
0.14
Capsules/flower
1086
6151
0.65
0.07
0.13
0.26
0
0
flowers suggests that these birds may be able to provide good
pollination services in seed orchards of this tree. This is
remarkably high, considering that the numbers of seeds
produced from flowers of plants with full or partial
self-incompatibility, following manual outcross pollination,
may be unattainable following visits by animal pollinators
that usually carry a mixture of self- and outcross pollen
(Thomson 2001). Although these birds were loaded with
outcross pollen prior to feeding on female-phase flowers,
they also consumed pollen from male-phase flowers on the
same branch as the experimental female-phase flowers, when
the branch was introduced to their cage, and therefore would
have also accumulated self-pollen. For this reason, the
proportional composition of self- and outcross pollen carried
by L. discolor used in this experiment may have
approximated that carried by freely foraging conspecifics
that fly regularly between trees (Hingston et al in press).
Freely foraging L. discolor carry large numbers of eucalypt
pollen grains on their bills (Hingston et al., in press), and
scanning electron microscopy clearly showed many eucalypt
pollen grains on the tongues of two L. discolor that died as a
result of collisions with windows (Hingston et al., in press).
Pollen carryover on L. discolor could therefore be long,
resulting in deposition of outcross pollen on many flowers
within a foraging bout in a single tree (Paton 1982).
It is possible that fecundity following single flower visits
by wild L. discolor was underestimated in this experiment
because, after pollen was brushed onto the heads of the
captive birds used in this experiment, the captive birds
carried an average of less than one-third of the pollen grains
of their freely foraging conspecifics on the distal 5.5 mm of
the bill. Because pollen was applied in this way when the
captive birds foraged on only three of the four trees studied,
pollen loads were probably even smaller than this when they
foraged at flowers of Tree 6151.
Unfortunately, the capacity for L. discolor to provide
pollination services to seed orchards is limited by its
distribution in south-eastern Australia and by its declining
population (Brown 1989; Swift Parrot Recovery Team
2001). The most recent estimate of its global wild population
is less than 2500 adults (Swift Parrot Recovery Team 2001).
In spite of this, L. discolor still occurs in large numbers on
Grand mean
353
1085
0.51a
0.12a
0.07a
4.00
0.67
0
1.59
0.14
1.86
Seeds/flower
1086
6151
16.02
0.69
0.30
4.45
0
0
Grand mean
6.51a
0.37b
0.54b
flowering E. globulus at some times and places in Tasmania
(Brown 1989; Hingston and Potts 1998; Hingston 2002;
Hingston et al. 2004b). Therefore, this bird is likely to be
responsible for the production of large quantities of seeds in
some stands of E. globulus, and efforts aimed at the recovery
of L. discolor (Swift Parrot Recovery Team 2001) are likely
to benefit seed production of E. globulus in Tasmania.
Many other bird species are also attracted to the flowers
of E. globulus in Tasmania, particularly other parrots and
honeyeaters (Meliphagidae) (Brown 1989; Hingston and
Potts 1998; Hingston 2002; Hingston et al. 2004b, in press).
These probably also make major contributions to pollination
of E. globulus, because large differences in efficiency among
bird species as pollinators of individual species of Australian
plants have not been found previously (Paton 1991). Because
anthophilous parrots and honeyeaters are common and
widespread across Australia (Ford et al. 1979), effective bird
pollinators of E. globulus should occur wherever this tree is
cultivated in Australia. Birds are also likely to pollinate seed
orchards of E. globulus outside Australia because specialised
nectarivorous birds inhabit most temperate regions of the
world. Sunbirds (Nectariniidae) occur in South Africa, the
Middle East and eastern Asia, and hummingbirds
(Trochilidae) and sugar-birds (Coerebidae) in the Americas
(Faegri and van der Pijl 1979; Ford 1985). Even in Europe,
which has no specialised nectarivorous birds, omnivorous
birds consume nectar, including that of Eucalyptus (Ford
1985). However, as a consequence of actively consuming
pollen, L. discolor carries significantly more eucalypt-pollen
grains on its bill and head than do honeyeaters (Hingston
et al., in press). In addition, the long thin bills of honeyeaters
allow them to collect nectar from the cup-shaped flowers of
eucalypts without always contacting the stigma, whereas
parrots inevitably contact the stigma because of their short
broad bills (Paton and Ford 1977). For these reasons,
honeyeaters and some other nectarivorous birds may not be
as effective as L. discolor at pollination of E. globulus
(Hingston and Potts 1998; Hingston et al. in press).
Because both A. mellifera and B. terrestris were far less
effective as pollinators than was L. discolor, increasing their
abundances could possibly reduce seed set in E. globulus.
The introduction of large numbers of ineffective bees could
376
Australian Journal of Botany
reduce the total levels of pollination by decreasing the
quantity of pollen available for transfer by more effective
pollinators (Pyke 1990; Wilson and Thomson 1991; Paton
1993). Moreover, plant fecundity can be adversely affected
by the presence of ineffective pollinators when they reduce
the frequency with which effective pollinators visit flowers
because of resource competition (Paton 1993; Roubik 1996;
Irwin and Brody 1998).
Although A. mellifera and B. terrestris were not as
effective at pollination as L. discolor per visit, the capacity of
these bees to facilitate some seed set suggests that at high
densities, and in the absence of bird pollinators, they could
make useful contributions to seed production. However, the
number of seeds produced following multiple visits by
A. mellifera appears not to be a linear function of the number
of visits and the number of seeds produced following one
visit. Although single visits by A. mellifera facilitated the
production of 6.8% as many seeds as did supplementary
outcross pollinations in this experiment, flowers exposed to
hundreds of visits by A. mellifera (and other insects, but not
birds) produced only 33.4% as many seeds as did
supplementary outcross pollinations in another experiment
(Hingston 2002). Because flowers receiving a single visit by
L. discolor in this experiment produced 76.2% as many seeds
as were produced from flowers receiving supplementary
outcross pollinations, A. mellifera appears to be a poor
substitute for bird pollinators.
A previous study found greater numbers of seeds per
capsule in a Tasmanian seed orchard of E. globulus
following a flowering season when hives of A. mellifera
were present, than in the previous year when hives were not
deployed (Moncur et al. 1993). However, the results of that
study must be interpreted with caution because it did not
account for the proportions of flowers that produced
capsules and was confounded by the treatments occurring
in different years (Paton 1996). Seed production is
influenced by many other factors that differ among years,
such as flowering intensity (Carpenter 1976; Andersson
1988), weather conditions, and activity levels of seed
predators and other pollinators (Eldridge et al. 1993).
Therefore, the results of Moncur et al. (1993) should only
be regarded as correlations based on two data points. Even
if it was valid to draw conclusions of cause and effect from
correlations based on two data points, such conclusions
could not be drawn because no evidence of increases in
numbers of A. mellifera on the flowers after introduction of
hives was obtained (Moncur et al. 1993). It cannot be
assumed that the introduction of hives by Moncur et al.
(1993) increased the numbers of A. mellifera visiting the
flowers (Paton 1996), because feral populations of
A. mellifera are widespread in Australia (Oldroyd et al.
1995; Oldroyd 1998) and the number of feral A. mellifera
has been found to increase rapidly following removal of
hives (Schaffer et al. 1983).
A. B. Hingston et al.
Why are insects poor pollinators?
Insects appear to be poor pollinators of E. globulus, as
previously suggested (Hingston and Potts 1998). However,
infrequent stigmatic contacts by insects, one of the reasons
why Hingston and Potts (1998) suggested insects may be less
effective pollinators of E. globulus than are birds, was
discounted as a major causal mechanism in this study.
Although most insect species did not contact stigmas as
frequently as did birds, which is the case in many other
Australian native plants adapted to vertebrate pollination
(Collins et al. 1984; Paton and Turner 1985; Taylor and
Whelan 1988; Vaughton 1992, 1996; Paton 1993;
Richardson et al. 2000; Kalinganire et al. 2001), single visits
by insects that did result in stigmatic contact still produced
few seeds. Indeed, the only insect that consistently contacted
stigmas as frequently as did L. discolor, the large introduced
bee B. terrestris, was a significantly poorer pollinator than
was L. discolor.
It is more likely that the other reason suggested by
Hingston and Potts (1998) why insects may be less effective
than birds as pollinators of E. globulus, namely higher
proportions of self-pollination because of infrequent
interplant movements by insects, was the major causal
mechanism. Because fewer seeds were produced following
stigmatic contact by insects than by L. discolor, and because
E. globulus is largely self-incompatible (Hardner and Potts
1995; Hardner et al. 1998; Pound et al. 2002a, 2002b),
insects almost certainly deposited less outcross pollen per
stigmatic contact than did L. discolor. Although L. discolor
might deposit more pollen per stigmatic contact than do
insects, the numbers of pollen grains deposited by
B. terrestris and A. mellifera sometimes exceed the
maximum possible seed production per open-pollinated
flower (Hingston 2002), suggesting that most pollen
deposited by these insects could be self-pollen or inviable.
Further evidence of this comes from the small numbers of
seeds developing after A. mellifera visited flowers without
contacting stigmas, which suggests that their movements
may have caused pollen to fall from the anthers onto the
stigma of the same flower. Because stigmatic contact did not
enhance seed set above this level, most pollen deposited on
stigmas as a result of contact by A. mellifera was also
probably self-pollen.
It is not possible to follow the movements of insects in
large trees such as E. globulus to verify our contention that
they deposit mostly self-pollen. However, this is supported
by observations of little change in the composition of
flower-visiting insect communities on individual trees of
E. globulus between consecutive days (Hingston and Potts
1998), and by studies of other plant species that found that
flower-visiting insects frequently remain on one plant for
long periods (Hodgson 1976; Beardsell et al. 1993; Paton
1993). For example, Paton (1993) never saw A. mellifera fly
Birds and bees as pollinators of E. globulus
between Callistemon rugulosus (Myrtaceae) plants
separated by as little as 3 m while they visited a total of 4600
flowers during 9.9 h, whereas New Holland honeyeaters,
Phylidonyris novaehollandiae, averaged 7.3 interplant
movements per hour and one every 400 flowers visited
(Paton 1993).
Evolutionary implications
Eucalyptus globulus may be rather specialised towards
ornithophily, in spite of displaying an apparently allophilic
syndrome and being visited by numerous insects, supporting
the hypothesis of Stiles (1978), Bertin (1982a, 1982b) and
Paton (1986b) that birds are often more efficient than insects
as pollinators of plant species with flowers from which they
both collect nectar. This finding cautions against predicting
a plant’s pollinators from either floral form or visitor profile,
indicating that many more studies such as this are needed to
determine the extent to which the frequent observations of
flowers being visited by a wide variety of potential
pollinators (e.g. Herrera 1988, 1996; Waser et al. 1996;
Bosch et al. 1997; Hingston and McQuillan 2000) reflect the
frequency of generalisation by plants in their pollinator
requirements.
The absence of seed set following single flower visits by
native insects raises the question of why E. globulus has not
evolved means of deterring insects from taking nectar. Many
other bird-pollinated flowers have evolved characters to
maximise the proportion of their nectar available to birds by
discouraging insects from removing nectar (Faegri and van
der Pijl 1979; Paton 1986b). Such characters include tubular
corollas and long hairs that physically block insect access to
nectar (Ford et al. 1979; Paton 1986b), sticky corolla
surfaces that capture insects (Rebelo et al. 1985), and red
coloration to make the flowers less obvious to insects (Faegri
and van der Pijl 1979; Ford et al. 1979; Paton 1986b). In
some bird-pollinated species of Eucalyptus the stamens are
red (Ford et al. 1979), or incurved over the nectaries to block
access by insects (Bond and Brown 1979; Hopper and Moran
1981; Hopper and Burbidge 1986).
It may be that native-insect visitors consumed so little
nectar that there was little selective advantage in excluding
them. This explanation would be valid if native-insect
visitation rates were not higher in the past than they are
currently, where introduced bees are the most abundant
flower visitors to E. globulus (see also Hingston and Potts
1998; Hingston et al. 2004b) and appear to be responsible for
most nectar consumption (Hingston 2002; Hingston et al.
2004b). Alternatively, there may be a selective advantage in
having some insect visitors in situations where bird
pollinators are scarce. Although single flower visits by native
insects did not facilitate any seed set in this experiment, this
may have been the result of them depositing insufficient
outcross pollen in one visit to initiate fruit set (Olsen 1997),
and multiple insect visits might result in seed set. If so, there
Australian Journal of Botany
377
may be a selective advantage in having insects visit flowers
low in the canopy, because pollination services to the lower
parts of E. globulus canopies are inferior to those in the
upper parts (Patterson et al. 2001) and birds seldom visit
flowers in the lower parts of canopies (Hingston 2002;
Hingston et al. 2004b). This may result in contrasting
selective forces acting in different parts of the canopy, i.e.
selection for exclusion of insects in the upper canopy, and
attracting insects in the lower canopy.
Incurved stamens that prevent insects from taking nectar,
as occurs in E. stoatei (Hopper and Moran 1981; Hopper and
Burbidge 1986) and to a lesser extent in E. incrassata (Bond
and Brown 1979), may not have evolved in E. globulus if
L. discolor or other short-billed birds have historically
played a very important role in its pollination. Incurved
stamens would prevent short-billed birds from taking nectar,
limiting the suite of potential bird pollinators to long-billed
honeyeaters (Hopper and Moran 1981). Hence, the loss of
some nectar to insects may be an unavoidable cost associated
with making nectar available to effective short-billed bird
pollinators such as L. discolor.
Acknowledgments
We are extremely grateful to Brett Gartrell of the School of
Zoology, University of Tasmania, for the use of his captive
swift parrots held under Tasmanian Parks and Wildlife
Service permit Numbers 1263/98, 1263/01, FA 98122, FA
98107, FA 98108, FA 99109 and FA 00041. Thanks also go
to Pakinee Hingston for assistance with fieldwork and
counting seeds, Liz McGown and the Southern Tree
Breeding Association for access to their trees, David
Ratkowsky for statistical advice, and Stephen Mallick, Peter
Kevan, Margaret Sedgley, Glenn Iason, David Paton and an
anonymous referee for their helpful comments. This research
was supported by Australian Postgraduate Award and
Cooperative Research Centre for Sustainable Production
Forestry scholarships to A. B. H., and carried out under
University of Tasmania Ethics Committee approval Number
98068.
References
Andersson S (1988) Size-dependent pollination efficiency in Anchusa
officinalis (Boraginaceae): causes and consequences. Oecologia 76,
125–130.
Beardsell DV, Knox RB, Williams EG (1993) Breeding system and
reproductive success of Thryptomene calycina (Myrtaceae).
Australian Journal of Botany 41, 333–353.
Bertin RI (1982a) Floral biology, hummingbird pollination and fruit
production of trumpet creeper (Campsis radicans, Bignoniaceae).
American Journal of Botany 69, 122–134.
Bertin RI (1982b) The ruby-throated hummingbird and its major food
plants: ranges, flowering phenology, and migration. Canadian
Journal of Zoology 60, 210–219.
Boland DJ, Brooker MIH, Chippendale GM, Hall N, Hyland BPM,
Johnston RD, Kleinig DA, Turner JD (1984) ‘Forest trees of
Australia.’ (Thomas Nelson Australia and CSIRO: Melbourne)
378
Australian Journal of Botany
Bond HW, Brown WL (1979) The exploitation of floral nectar in
Eucalyptus incrassata by honeyeaters and honeybees. Oecologia
44, 105–111.
Bosch J, Retana J, Cerdá X (1997) Flowering phenology, floral traits
and pollinator composition in a herbaceous Mediterranean plant
community. Oecologia 109, 583–591. doi:10.1007/S004420050120
Brown PB (1989) ‘The swift parrot Lathamus discolor (White). A
report on its ecology, distribution and status, including management
considerations.’ (Department of Lands Parks and Wildlife: Hobart)
Carpenter FL (1976) Plant–pollinator interactions in Hawaii:
pollination energetics of Metrosideros collina (Myrtaceae). Ecology
57, 1125–1144.
Collins BG, Newland C, Briffa P (1984) Nectar utilization and
pollination by Australian honeyeaters and insects visiting
Calothamnus quadrifidus (Myrtaceae). Australian Journal of
Ecology 9, 353–365.
Curtis WM, Morris DI (1975) ‘The student’s flora of Tasmania. Part 1.’
(University of Tasmania: Hobart)
DeGrandi-Hoffman G, Martin JH (1995) Does a honey bee (Apis
mellifera) colony’s foraging population on male-fertile sunflowers
(Helianthus annuus) affect the amount of pollen on nestmates
foraging on male steriles? Journal of Apicultural Research 34,
109–114.
DeGrandi-Hoffman G, Watkins JC (2000) The foraging activity of
honey bees Apis mellifera and non-Apis bees on hybrid sunflowers
(Helianthus annuus) and its influence on cross-pollination and seed
set. Journal of Apicultural Research 39, 37–45.
Eldridge K, Davidson J, Harwood C, van Wyk G (1993) ‘Eucalypt
domestication and breeding.’ (Clarendon Press: Oxford)
Faegri K, van der Pijl L (1979) ‘The principles of pollination ecology.’
(Pergamon Press: Oxford)
Ford HA (1985) Nectarivory and pollination by birds in southern
Australia and Europe. Oikos 44, 127–131.
Ford HA, Paton DC, Forde N (1979) Birds as pollinators of Australian
plants. New Zealand Journal of Botany 17, 509–519.
Gartrell BD, Jones SM (2001) Eucalyptus pollen grain emptying by two
Australian nectarivorous psittacines. Journal of Avian Biology 32,
224–230. doi:10.1111/J.0908-8857.2001.320304.X
Gartrell BD, Jones SM, Brereton RN, Astheimer LB (2000)
Morphological adaptations to nectarivory of the alimentary tract of
the swift parrot Lathamus discolor. Emu 100, 274–279.
Harbard JL, Griffin AR, Espejo J (1999) Mass controlled pollination of
Eucalyptus globulus: a practical reality. Canadian Journal of Forest
Research 29, 1457–1463. doi:10.1139/CJFR-29-10-1457
Hardner CM, Potts BM (1995) Inbreeding depression and changes in
variation after selfing in Eucalyptus globulus ssp. globulus. Silvae
Genetica 44, 46–54.
Hardner CM, Potts BM, Gore PL (1998) The relationship between cross
success and spatial proximity of Eucalyptus globulus ssp. globulus.
Evolution 52, 614–618.
Herrera CM (1996) Floral traits and adaptation to insect pollinators: a
devil’s advocate approach. In ‘Floral biology’. (Eds DG Lloyd,
SCH Barrett) pp. 65–87. (Chapman and Hall: New York)
Herrera J (1988) Pollination relationships in southeastern Spanish
Mediterranean shrublands. Journal of Ecology 76, 274–287.
Hingston AB (2002) Pollination ecology of Eucalyptus globulus subsp.
globulus and Eucalyptus nitens (Myrtaceae). PhD Thesis,
University of Tasmania, Hobart.
Hingston AB, McQuillan PB (1998) Does the recently introduced
bumblebee Bombus terrestris (Apidae) threaten Australian
ecosystems? Australian Journal of Ecology 23, 539–549.
Hingston AB, McQuillan PB (2000) Are pollination syndromes useful
predictors of floral visitors in Tasmania? Austral Ecology 25,
600–609. doi:10.1046/J.1442-9993.2000.01059.X
A. B. Hingston et al.
Hingston AB, Potts BM (1998) Floral visitors of Eucalyptus globulus
ssp. globulus in eastern Tasmania. Tasforests 10, 125–137.
Hingston AB, Marsden-Smedley J, Driscoll DA, Corbett S, Fenton J,
et al. (2002) Extent of invasion of Tasmanian native vegetation by
the exotic bumblebee Bombus terrestris (Apoidea: Apidae). Austral
Ecology 27, 162–172. doi:10.1046/J.1442-9993.2002.01179.X
Hingston AB, McQuillan PB, Potts BM (2004a) Pollinators in seed
orchards of Eucalyptus nitens (Myrtaceae). Australian Journal of
Botany 52, 209–222. doi:101071/BT03015
Hingston AB, Potts BM, McQuillan PB (2004b) Pollination services
provided by various size classes of flower visitors to Eucalyptus
globulus ssp. globulus (Myrtaceae). Australian Journal of Botany
52, 353–369. Doi:10.1071/BT03002
Hingston AB, Gartrell BD, Pinchback G (in press) How specialized is
the plant–pollinator association between Eucalyptus globulus ssp.
globulus and the swift parrot Lathamus discolor. Austral Ecology
(in press).
Hodgson LM (1976) Some aspects of flowering and reproductive
behavior in Eucalyptus grandis (Hill) Maiden at J.D.M. Keet Forest
Research Station (formerly Zomerkomst Forest Research Station).
1. Flowering, controlled pollination methods, pollination and
receptivity. South African Forestry Journal 97, 18–28.
Hopper SD, Burbidge AA (1986) Speciation of bird-pollinated plants in
south-western Australia. In ‘The dynamic partnership: birds and
plants in southern Australia’. (Eds HA Ford, DC Paton) pp. 20–31.
(The Flora and Fauna of South Australia Handbooks Committee:
Adelaide)
Hopper SD, Moran GF (1981) Bird pollination and the mating system
of E. stoatei. Australian Journal of Botany 29, 625–638.
Irwin RE, Brody AK (1998) Nectar robbing in Ipomopsis aggregata:
effects on pollinator behavior and plant fitness. Oecologia 116,
519–527. doi:10.1007/S004420050617
Kalinganire A, Harwood CE, Slee MU, Simons AJ (2001) Pollination
and fruit-set of Grevillea robusta in western Kenya. Austral Ecology
26, 637–648. doi:10.1046/J.1442-9993.2001.01139.X
Moncur MW, Charles R, Kleinschmidt GJ (1993) Can honeybees
increase seed production in blue gum, Eucalyptus globulus? The
Australasian Beekeeper December, 248–253.
Oldroyd BP (1998) Controlling feral honey bee, Apis mellifera L.
(Hymenoptera: Apidae), populations in Australia: Methodologies
and costs. Australian Journal of Entomology 37, 97–100.
Oldroyd BP, Cornuet J-M, Rowe D, Rinderer TE, Crozier RH (1995)
Racial admixture of Apis mellifera in Tasmania, Australia:
similarities and differences with natural hybrid zones in Europe.
Heredity 74, 315–325.
Olsen KM (1997) Pollination effectiveness and pollinator importance
in a population of Heterotheca subaxillaris (Asteraceae). Oecologia
109, 114–121. doi:10.1007/S004420050065
Paton DC (1982) The influence of honeyeaters on flowering strategies
of Australian plants. In ‘Pollination and evolution’. (Eds
JA Armstrong, JM Powell, JA Richards) pp. 95–108. (Royal
Botanic Gardens: Sydney)
Paton DC (1986a) Honeyeaters and their plants in south-eastern
Australia. In ‘The dynamic partnership: birds and plants in southern
Australia’. (Eds HA Ford, DC Paton) pp. 9–19. (The Flora and
Fauna of South Australia Handbooks Committee: Adelaide)
Paton DC (1986b) Evolution of bird pollination in Australia. In ‘The
dynamic partnership: birds and plants in southern Australia’. (Eds
HA Ford, DC Paton) pp. 32–41. (The Flora and Fauna of South
Australia Handbooks Committee: Adelaide)
Paton DC (1991) Variation in meliphagid morphology and its influence
on pollen dispersal in Australian plants. In ‘Acta XX congressus
internationalis ornithologici’. pp. 1611–1616. (New Zealand
Ornithological Congress Trust Board: Wellington)
Birds and bees as pollinators of E. globulus
Australian Journal of Botany
Paton DC (1993) Honeybees in the Australian environment. Does Apis
mellifera disrupt or benefit the native biota? Bioscience 43, 95–103.
Paton DC (1996) ‘Overview of feral and managed honeybees in
Australia: distribution, abundance, extent of interactions with native
biota, evidence of impacts and future research.’ (Australian Nature
Conservation Agency: Canberra)
Paton DC, Ford HA (1977) Pollination by birds of native plants in South
Australia. Emu 77, 73–85.
Paton DC, Turner V (1985) Pollination of Banksia ericifolia Smith:
birds, mammals and insects as pollen vectors. Australian Journal of
Botany 33, 271–286.
Patterson B, Vaillancourt RE, Potts BM (2001) Eucalypt seed
collectors: beware of sampling seed lots from low in the canopy!
Australian Forestry 64, 139–142.
Pound LM, Wallwork MAB, Potts BM, Sedgley M (2002a)
Self-incompatibility in Eucalyptus globulus ssp. globulus
(Myrtaceae). Australian Journal of Botany 50, 365–372.
doi:10.1071/BT01076
Pound LM, Wallwork MAB, Potts BM, Sedgley M (2002b) Early ovule
development following self- and cross-pollinations in Eucalyptus
globulus Labill. ssp. globulus. Annals of Botany 89, 613–620.
doi:10.1093/AOB/MCF089
Pryor LD (1976) ‘The biology of eucalypts.’ (Edward Arnold
Publishers Ltd: London)
Pyke GH (1990) Apiarists versus scientists: a bittersweet case.
Australian Natural History 23, 386–392.
Rebelo AG, Siegfried WR, Oliver EGH (1985) Pollination syndromes
of Erica species in the south-western Cape. South African Journal
of Botany 51, 270–280.
Richardson MBG, Ayre DJ, Whelan RJ (2000) Pollinator behaviour,
mate choice and the realised mating systems of Grevillea
mucronulata and Grevillea sphacelata. Australian Journal of
Botany 48, 357–366. doi:10.1071/BT98078
Roubik DW (1996) African honey bees as exotic pollinators in French
Guiana. In ‘The conservation of bees’. (Eds A Matheson,
SL Buchmann, C O’Toole) pp. 173–182. (Linnean Society of
London and the International Bee Research Association: London)
Schaffer WM, Zeh DW, Buchmann SL, Kleinhans S, Schaffer MV,
Antrim J (1983) Competition for nectar between introduced honey
bees and native North American bees and ants. Ecology 64,
564–577.
379
Stiles FG (1978) Ecological and evolutionary implications of bird
pollination. American Zoologist 18, 715–727.
Swift Parrot Recovery Team (2001) ‘Swift parrot recovery plan.’
(Department of Primary Industries, Water and Environment:
Hobart)
Taylor G, Whelan RJ (1988) Can honeybees pollinate Grevillea?
Australian Zoologist 24, 193–196.
Thomson JD (2001) Using pollination deficits to infer pollinator
declines: can theory guide us? Conservation Ecology 5, 6 [online]
URL: http://www.consecol.org/vol5/iss1/art6
Tibbits WN, Boomsma DB, Jarvis S (1997) Distribution, biology,
genetics, and improvement programs for Eucalyptus globulus and
E. nitens around the world. In ‘24th southern forest tree
improvement conference, June 9–12’. (Eds T White, D Huber,
G Powell) pp. 1–15. (Southern Tree Improvement Committee:
Orlando, FL)
Vaughton G (1992) Effectiveness of nectarivorous birds and honeybees
as pollinators of Banksia spinulosa (Proteaceae). Australian Journal
of Ecology 17, 43–50.
Vaughton G (1996) Pollination disruption by European honeybees in
the Australian bird-pollinated shrub Grevillea barklyana
(Proteaceae). Plant Systematics and Evolution 200, 89–100.
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996)
Generalization in pollination systems, and why it matters. Ecology
77, 1043–1060.
Williams DR, Potts BM, Black PG (1999) Testing single visit
pollination procedures for Eucalyptus globulus and E. nitens.
Australian Forestry 62, 346–352.
Wilson P, Thomson JD (1991) Heterogeneity among floral visitors
leads to discordance between removal and deposition of pollen.
Ecology 72, 1503–1507.
Manuscript received 4 February 2003, accepted 30 January 2004
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