honeybees in the australian environment

Honeybees in the Australian EnvironmentAuthor(s): David C. PatonSource: BioScience, Vol. 43, No. 2 (Feb., 1993), pp. 95-103Published by: University of California Press on behalf of the American Institute of Biological SciencesStable URL: http://www.jstor.org/stable/1311970 .

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Honeybees in the

Australian Environment

Does Apis mellifera disrupt or benefit the native biota

David C. Paton

A major perturbation to the Australian environment be- gan 200 years ago, when Eu-

ropeans settled on the continent. With that colonization, natural habitats were cleared and degraded, and a wide variety of domesticated animals and plants were introduced (Saunders et al. 1990). One of the animals introduced was the honeybee, Apis mellifera. This social bee arrived approximately 150 years ago (Doull 1973), and now feral colonies and colonies managed by beekeepers are spread over most of Australia.

Until recently, honeybees have been condoned in the Australian environment because they were assumed to benefit native plants by adding to the pollination services provided by native fauna. That view is changing as biologists study the intricate relationships between some of the native plants and their native pollinators (e.g., Ford 1986, Paton 1986, Pyke 1990). These studies show that honeybees may displace native pollinators from flowers (e.g., Pyke and Balzer 1985) and may not trigger the pollination mechanisms of the flowers they visit (e.g., Bell 1987, Taylor and Whelan 1988).

Similar concerns have been expressed for other regions where A. mellifera has been introduced, includ-

David C. Paton is an Australian Research Fellow in the Department of Zoology, University of Adelaide, Adelaide, SA 5001, Australia. He now studies interactions between honeybees and Australian biota. He has spent much of the last 15 years studying nectarivorous birds and the plants they pollinate. ? 1993 American Institute of Biological Sciences

There is much debate about honeybee management in

conservation reserves

ing North and South America and Japan. In the Americas, a range of native bees has been found to switch to less profitable resources when honeybees are abundant at the richest patches of flowers (e.g., Roubik 1978,1980,1982, Schaffer et al. 1979, 1983, Ginsberg 1983). In Japan, Sakagami (1959) reports aggressive interactions between introduced A. mellifera and native Apis cerana.

Pollen-harvesting honeybees may also reduce the quantities of pollen transferred by bumblebees (Bombus spp.) to stigmas of Impatiens capensis and so have an adverse effect on seed production for some North American plants (Wilson and Thomson 1991). Even in Europe, where A. mellifera is found naturally, there is concern that continued loss of natural habitats and changes in land use and management of apiaries may conflict with conservation of other pollinators and se- lected plants (e.g., Williams et al. 1991). Australian plants and their pollinators have evolved largely in the absence of social bees (Michener 1979), and they may be extremely susceptible to perturbations from introduced honeybees.

In this article, I provide an over- view of the interactions between hon-

eybees and the Australian biota by describing some of the research results. I also point out where further research is required and outline possible strategies for the management of honeybees in the Australian environment. Interactions between honeybees and the Australian biota are complex, varying both spatially and temporally, and involve many taxa. This variation and taxonomic diversity complicates the task of assessing potential impacts and developing simple management programs.

Which plants and animals interact with honeybees? Many Australian plants are used as sources of nectar and pollen by honeybees. For example, in sandplain heaths and woodlands between Jurien and Dongara in Western Australia, Wills has recorded honeybees visiting the flowers of 125 plant species from 61 genera in 29 families out of an available 413 plant species (Wills et al. 1990). In similar habitats near Adelaide in South Australia, honeybees visited the flowers of more than 180 of 360 species of native plants examined.1 These plants came from 80 genera and 32 plant families. The plants used include the wind-pollinated trees Allocasuarina (Casua- rinaceae), insect-pollinated herbs and shrubs (e.g., Hypoxis [Hypoxidaceae], Orthrosanthus [Iridaceae], Baeckea and Darwinia [Myrtaceae], Pultenaea and Daviesia [Leguminosae]), and

1D. C. Paton and L. Jansen, 1992, unpublished results.

February 1993 95



Table 1. Quantities of nectar and pollen removed by honeybees and native fauna visiting several Australian plants near Rocky River in Flinders Chase National Park, South Australia. Several sets of data are given for most species to illustrate temporal variation in resource use. Further details in Paton (1990). This table reproduced with permission of CSIRO.

Visits flower-1 * day-' Percent resource removed* Plant species Month Honeybee Bird Native bee Honeybee Bird Native bee Nectar

Eucalyptus cosmophylla August 87t 2.8 9.5 0.02 14.1 85.8 0.1 Eucalyptus cosmophylla August 87* 54.6 28.5 0.25 29.9 70.0 0.1 Eucalyptus remota January 89 3.7 7.1 0.03 16.1 83.7 0.2 Callistemon rugulosus November 88 5.4 9.0 40.9 59.1 Callistemon rugulosus December 88 13.1 0.8 92.1 7.9 Adenanthos terminalis August 87 4.7 100.0 Adenanthos terminalis January 89 3.6 0.1 97.2 2.8

Pollen Correa reflexa May 87 0.3 0.9 38.7 61.3 Correa reflexa July 87 7.0 2.4 75.9 24.1 Correa reflexa August 87 4.6 0.7 93.1 6.9 Eucalyptus remota January 89 5.5 7.1 <0.001 88.0 12.0 <0.001 Adenanthos terminalis August 87 4.7 100.0 Adenanthos terminalis January 89 1.5 0.1 99.0 1.0

*Percentage of nectar and pollen being produced that was taken by each taxa. tMid-August. ?Late August.

large shrubs and trees pollinated largely by birds (e.g., various Euca- lyptus and Callistemon [Myrtaceae], and Grevillea and Banksia [Pro- teaceae]).

Honeybees must also interact with the thousands of species of Australian animals that harvest nectar and pollen from these plants, including flies, beetles, wasps, bees, ants, birds, and small mammals (Armstrong 1979,

60 -

a) 40-

0

0

10 20 30 40 50

Honeybee visits per flower per day

Pyke 1990). These animals differ markedly in size, morphology, and behavior from honeybees, and such differences are likely to result in honeybees providing pollinator services that are somewhat different from the services provided by native fauna. For example, most Australian native bees are much smaller than honeybees and are solitary, and small solitary bees tend to have different activity pat-

o ', a) 0 E

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Figure 1. Models of the quantities of nectar and pollen removed by honeybees from (a) Eucalyptus cosmophylla and (b) Correa reflexa as a function of the numbers of honeybees and honeyeaters visiting flowers. In both models, the amounts of resource consumed by honeybees are plotted for three levels of bird visitation (5, 10, and 30 visits per flower per day for E. cosmophylla and 0.5, 1.5, and 2.5 visits per flower per day for C. reflexa). In these models, the proportions of floral resources not taken by honeybees were taken by birds. The models are based on observed patterns of visitation and measured efficiencies of nectar or pollen removal from flowers for honeybees and birds; they take into account any diurnal patterns for nectar secretion or anther dehiscence. Details of these measurements and assumptions used for these models are given in Paton (1990). Figure reproduced with permission of CSIRO.

terns than social bees (e.g., Schaffer et al. 1983). Nectar-feeding birds are also prominent pollinators of a wide variety of Australian plants (e.g., Ford et al. 1979). These birds are much larger than honeybees and forage over a wider range of environmental conditions than insects. Unfortunately, the ecology of many of these native animals is poorly known, hampering attempts to select appropriate species for studying interactions between them and honeybees.

In selecting appropriate species for study, a possible criterion is the proportion of floral resources (nectar and pollen) consumed by honeybees. If honeybees consume only a small proportion of the floral resources produced by a plant, then they are unlikely to be having a significant impact on either those plants or their native pollinators. If they consume a large proportion of these resources, there may be significant detrimental interactions. Do honeybees consume a large quantity of the floral resources produced by Australian plants?

Consumption of floral resources by honeybees Estimating the quantities of nectar and pollen being consumed by different fauna involves determining when and how frequently different fauna

BioScience Vol. 43 No. 2 96



visit flowers and measuring the nectar and pollen produced by flowers, as well as that present at samples of flowers before and after visits by different taxa. Methods are described in Paton (1982a,b, 1985, 1990) and Paton and Turner (1985).

Calculations for a range of plants that are largely bird-pollinated show that a large proportion of the nectar and/or pollen produced is often har- vested by honeybees (Paton 1985, 1990; Table 1). On some occasions, honeybees removed more than 90% of the floral resources produced by some plants. Clearly, interactions between honeybees and at least some of the Australian biota are not trivial and warrant further study.

In general, the amounts of nectar and pollen removed by honeybees from bird-pollinated plants increases with increases in honeybee visitation (Table 1, Figure 1), but there is a limit to the amount that honeybees can take. In these examples, nectar secretion and anthesis occur overnight as well as during the day. Because few animals visit these flowers at night, nectar and pollen accumulate by dawn. The birds are active at dawn, so they have almost exclusive use of these resources until honeybees become active later in the morning. By midmorning, honeybees can swamp the flowers, and nectar and pollen availability can be maintained at negligible levels for the rest of the day (Paton 1982a, 1985).2

Such conditions suggest that there is little surplus food and that floral resources are potentially limiting for honeybees and native fauna (Ford 1979). However, provided honeyeaters can harvest much of their daily food requirements during the first few hours of the day and store this food for later use, they should never be totally excluded by honeybees. Initial research shows that honeyeaters may have limited capacity to rapidly store energy, prefering to steadily accumulate food reserves throughout the day (e.g., Collins and Clow 1978, Collins and Morellini 1979, Collins et al. 1980).

The models of resource use in Fig- ure 1 show that when honeybee numbers and visitation rates to bird-pollinated flowers are low, small increases in honeybee numbers lead to substan-

2D. C. Paton, 1992, unpublished results.

Table 2. Changes in the frequency with which New Holland honeyeaters visited the flowers of Callistemon rugulosus and changes in territory sizes for these birds with changes in the numbers of honeybees working flowers near Goolwa, South Australia, in spring 1983. Honeybee activity was scored by counting honeybees at 50-200 inflorescences at regular intervals through the day. Daily visitation by birds was determined by counting the number of visits made by birds to samples of flowers during five 1-hour periods spread evenly over a 14-hour day. Data are expressed as mean ?SE (n), where n for honeyeater visits is the number of independent determinations made during that level of honeybee activity and n for flowers is the number of territories measured. Visitation rates by birds to flowers were significantly lower (analysis of variance, F = 12.7, df = 3,32, p < 0.001), and territory sizes significantly larger (analysis of variance, F = 21.3, df = 3,106, p < 0.001) when honeybee numbers were higher. Maximal number of Number of flowers honeybees seen per Honeyeater visits in honeyeater 1000 flowers per flower per day territories

0.0-5.0 9.6 ? 0.8 (9) 4343 ? 185 (16) 5.1-10.0 5.5 - 1.0 (9) 5387 + 219 (38)

10.1-15.0 5.0 ? 0.8 (9) 6112 ? 306 (28) > 15.0 3.0 ? 0.3 (9) 7606 + 304 (28)

tial increases in the amounts of floral resources they consume. Similar increases do not occur when high popu- lations increase. The responses of native biota may vary depending on the extent to which floral resources can be further depressed.

Experiments to measure the responses of native biota to introductions of hives of honeybees should measure background levels of honeybees and consumption of resources

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before any introductions. For example, when floral resources are fully ex- ploited, increases in honeybees in areas where honeybee numbers are low are likely to reduce the share of floral resources taken by the birds and so provoke a behavioral or numerical response from them. Similar introductions in areas where honeybees are already taking a large share of the resources are less likely to do so. At high population densities, further in-

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Figure 2. Diurnal patterns of visitation to flowers by honeybees (dashed line) and native bees (solid line) at (a) Orthrosanthus multiflorus, (b) Swainsona lessertifolia, (c) Acacia paradoxa, and (d) Pimelea flava at Flinders Chase National Park, South Australia, during spring 1990. For Acacia, data are plotted as visits per flower head per hour. For the other species, data are plotted as visits per flower per hour. Data are based on 15-30 minute observations made at hourly intervals over 2 to 3 days on 165-311 flowers for Orthrosanthus, 726-1293 flowers for Swainsona, 8375-9235 flower heads for Acacia, and 9282-12,483 flowers for Pimelea.

February 1993

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97



Table 3. Spatial patterns in the use of Callistemon rugulosus flowers by nectar-collecting honeybees. Use of inflorescences on a plant was scored by counting the numbers of honeybees foraging at 250 inflorescences fully exposed on the exterior of the plant's canopy, 250 partially covered, and 250 fully covered by the plant's foliage. Use of flowers on an inflorescence was scored by dividing inflorescences into three equal parts (proximal, middle, and distal) and counting the number of honeybees foraging at flowers in each third. Honeybees used exposed inflorescences more extensively than those that were partially or fully covered (X2 = 26.4, df = 2, p < 0.001) and used flowers in the distal and proximal thirds of an inflorescence more than flowers centrally located within an inflorescence (X2 = 25.8, df = 2, p < 0.001). Position of Number of Position of Number of inflorescence honeybees flower on honeybees on plant counted inflorescence counted

Exposed 95 Proximal third 248 Partially covered 61 Middle third 191 Fully covered 37 Distal third 394

troductions of honeybees may fail to elicit a response from nectarivorous birds, and a lack of response does not indicate a lack of competition between honeybees and native fauna.

In many parts of Australia, experimental manipulations that involve the removal of honeybees from an area may be more appropriate. At high densities of honeybees, measuring increases in competitive interactions between hives of honeybees may be more appropriate than measuring responses of native fauna. The assumption is that if colonies of honeybees are competing, then competitive interactions are also likely between honeybees and native fauna using the same resources. The existence of competitive interactions between colonies of honeybees also has important implications for the efficient management of commercial apiaries.

Interactions between honeybees and native bees Australian insects now share most of their sources of nectar and pollen with honeybees. An important group of flower-visiting insects in Australia are native bees (Apoidea). Most of Aus- tralia's native bees are much smaller than the introduced honeybee and are not social (Michener 1970, 1979). Their activity at flowers is usually concentrated in the middle of the day, when ambient temperatures are high- est. Honeybees begin foraging at lower ambient temperatures and have first use of most flowers (e.g., Figure 2). This difference in foraging activity gives the introduced honeybee a distinct advantage in any competitive interaction, particularly if floral resources are present mainly in the morn-

ing, as they are in many of these plants. For some plants, including Orthrosanthus, honeybees can remove most of the pollen from flowers before native bees start foraging and will even tear open undehisced anthers to remove pollen.

How does one measure if this consumption of resources by honeybees is detrimental to native bees? Counts of native bees visiting flowers in areas before and after the introduction of hives of honeybees have been used in some preliminary studies to assess impacts of honeybees (e.g., Pyke and Balzer 1985). The usual assumption is that, as honeybee numbers increase, the numbers of native bees working the same flowers should decrease if competition exists (Pyke 1990). Such an assumption may not be correct.

Consider the following scenario. Female native bees collect nectar and pollen and package that food with an egg in a chamber or cell within a nesting burrow and then repeat this

procedure (Michener 1970). Assume that there are 100 female bees in an area and that the bees take 5 minutes to collect a load of nectar or pollen before returning to their burrows. Once in the burrow, they take 10 minutes to unload before going out to forage again. Now introduce honeybees that remove a large proportion of the nectar or pollen produced in the area. As a result, native bees find less food at each of the flowers they visit and consequently spend more time foraging to obtain a full load. To make the calculations simple, assume that under the new conditions with honeybees present a native bee takes twice as long (10 minutes) to collect a load before returning to her burrow. Because unloading still takes 10 minutes, the net effect of introducing honeybees might be to increase the numbers of native bees working flowers at one time.

In the example given here, the numbers of native bees foraging simulta- neously would have risen from 33 to 50, despite the actual numbers living in the area remaining at 100. So counts of native bees at flowers may not be easily interpreted, except that changing numbers indicate some interaction. The few Australian studies have all reported decreases in counts of native bees at flowers when honeybee numbers have increased (Pyke 1990), but shifts in resource use have not been studied. Native bees in other countries sometimes shift to poorer quality resources in response to increased numbers of honeybees (e.g., Ginsberg 1983, Roubik 1978, Schaffer

Figure 3. Diagram of an inflorescence of Callistemon rugulosus, showing easy access for honeybees to the nectaries of flowers at either end. Note that some of the flowers along the stem have been removed for illustrative purposes and that the density of filaments is much greater than shown.




et al. 1983). If the foraging efficiency of native

bees is reduced when honeybees are present, then there should be lower reproductive success of native bees. Each female would need to spend more time harvesting resources to pro- vision a developing larva and consequently should produce fewer larvae. So, the impact of honeybees on native bees might not be expressed until the next generation, when fewer native bees emerge.

Sugden and Pyke (1991) investi- gated the reproductive biology of the native bee Exoneura asimillima, com- paring the numbers of adults, larvae, and pupae in colonies of this bee in areas with and without added bee- hives. They found no convincing evidence of reduced reproductive activity in an area where hives of honeybees had been added compared with control areas with background feral popu- lations of honeybees. However, they did not determine if food resources were limiting and whether the addition of extra hives reduced those food levels further at the experimental site. One possibility is that food resources were not limiting. Exoneura was cho- sen for study because reproductive parameters could be measured and not because there was prior evidence to suggest that honeybees consumed a large proportion of their food supply.

Perhaps the first stage in collecting appropriate data is to determine if the rates at which native bees can harvest resources change with changes in resource levels at flowers. Many native bees, because they are much smaller than honeybees, might not experience any difficulty in harvesting adequate food for maximal performance even when honeybees have cropped the resources extensively.

Interactions between honeybees and birds In Australia, more than 100 species of birds have been seen harvesting nectar from flowers (Ford et al. 1979). Most of these species are honeyeaters (Meliphagidae), some of which de- pend on nectar or a similar carbohy- drate for energy (e.g., the New Hol- land honeyeater Phylidonyris novaehollandiae; Paton 1982a, 1988). Numbers of honeyeaters living in areas of southern Australia are often

correlated with the quantity of nectar being produced, and breeding usually coincides with periods of abundant nectar (Ford 1979, Ford and Paton 1985, Paton 1985, Pyke 1983, 1988, Pyke and Recher 1986). In some cases, the birds defend clearly defined feeding territories in which dominant individuals aggressively exclude intrud- ers to gain more or less exclusive use of nectar in their territories (Ford 1981, McFarland 1986, Paton 1986). Given the importance of nectar to these birds, losses to honeybees of 50% or more of the nectar produced by some bird-pollinated plants (e.g., Table 1) are likely to affect bird numbers and their behavior.

In southeastern Australia, the scarlet bottlebrush Callistemon rugulosus is a plant favored by honeyeaters. Individual plants can reach 4 m in height and 12 m in diameter. Typi- cally, this Callistemon occurs in patches in low-lying areas or along creeks that flow in winter. Patches can consist of just a few plants to several hundred individuals clumped together. Individual plants can bear up to several hundred scarlet inflorescences, mostly around the periphery of the plant's canopy, where they are obvious to flower visitors. Each inflorescence consists of 20-70 tightly packed flowers that bloom synchro- nously in spring. Both honeyeaters and honeybees frequently visit these flowers. Honeybees harvest both nec-

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Figure 4. Pollen removal from Correa reflexa by honeybees. The figure plots the mean percentage of pollen remaining after intact and previously unvisited flowers were visited one or more times by a pollen-collecting honeybee. Intact flowers of C. reflexa produce 70,600 + 2200 pollen grains (SE, 90 determinations), so this number is used for 100%. Consult Paton (1990, 1991) for details of methods.

tar and pollen from the flowers, whereas the birds take only nectar.

If there is no interaction between honeybees and honeyeaters, then there should be no change in the behavior of the birds when the number of honeybees working the flowers of C. rugulosus changes. However, this was not the case in areas near Goolwa in South Australia. In this area, the numbers of honeybees working Callist-

Table 4. Spatial patterns in the use of Callistemon rugulosus flowers by New Holland honeyeaters in the presence and absence of honeybees. Use of inflorescences was scored during one-hour observations. Exposed inflorescences were more numerous than partially covered and fully covered inflorescences, so data are expressed as visits per inflorescence per hour. The number of inflorescence hours is given in parentheses. Use of flowers within an inflorescence was scored by recording the numbers of probes made by New Holland honeyeaters at flowers in the proximal, middle, and distal thirds of inflorescences. A total of 550 probes was scored at times when honeybees were not foraging, and 1346 probes were scored when honeybees were foraging. New Holland honeyeaters used all inflorescences and all flowers equally when honeybees were absent (X2 = 2.59 and 3.00 respectively, df = 2, p > 0.05) but favored exposed inflorescences and centrally located flowers within an inflorescence when honeybees were present (X2 = 727 and 133 respectively, df = 2, p < 0.001).

Position of flower Frequency of use by New Holland honeyeaters or inflorescence Honeybees absent Honeybees present

Inflorescences Visits * inflorescence-1 * h-1

Exposed 3.44 (133) 1.26 (848) Partially covered 3.68 (57) 2.62 (424) Fully covered 3.00 (29) 4.06 (193)

Flowers Percentage of probes Proximal third 34.2 28.2 Middle third 35.8 47.9 Distal third 30.0 23.9

February 1993 99



Table 5. Fruit production by flowers of Callistemon rugulosus placed inside and outside wire mesh cages at three levels of honeybee activity: low (ca. S bees/1000 flowers daily maxima), medium (ca. 10 bees/1000 flowers), and high (ca. 15 bees/1000 flowers). The wire mesh cages excluded birds but did not alter visitation rates by honeybees. Data were collected from 12 plants, each having a caged and uncaged treatment. Total number of flowers in each treatment is given in

parentheses. Although there was significant heterogeneity between replicates, that heterogeneity results in analyses of pooled data being, if anything, conservative. Analyses of pooled data show that fruit production increased significantly for caged flowers as honeybee activity increased (X2 = 45.1, df = 2, p < 0.001); fruit production at caged flowers was significantly lower than that at

uncaged flowers (X2 = 181.6, 121.6, and 12.8 for low, medium, and high densities of honeybees, respectively, df = 1, p < 0.001); and fruit production at uncaged flowers exposed to birds and bees declined significantly with increases in honeybee activity (X2 = 38.0, df = 2, p < 0.001).

Level of Percent flowers setting fruit Percent flowers setting fruit honeybee inside wire cages outside wire cages activity (honeybees only) (honeybees and birds)

Low Medium

High

6.7 (735) 15.3 (2584) 17.1 (1317)

emon flowers increased with proxim- ity to a large commercial apiary, sea- sonally as honeybees switched to Callistemon as other resources declined, and after the introduction of additional hives to experimental plots. When few honeybees worked the flowers, honeyeaters visited individual flowers on average 9.6 times per day, but when honeybee activity was high this visitation was reduced significantly to only 3.0 visits per flower per day (Table 2). In addition, the birds adjusted their foraging by avoiding the flowers that were used most extensively by honeybees.

Honeybees show distinct preferences for certain flowers when harvesting nectar from C. rugulosus. For example, they visit flowers at the two ends of an inflorescence more frequently than those in the center (Fig- ure 3, Table 3). They also favor inflorescences exposed on the ends of branches at the periphery of the plant's canopy over those that are completely or partially hidden by foliage within the plant (Table 3).

These patterns can probably be explained by the ease with which different flowers can be visited by honeybees. First, the basal nectaries are more easily accessed from the side of flowers at the ends of inflorescences (Figure 3). To visit flowers in the center of the inflorescence, the bees must force their way through a mat of filaments to reach nectar at the base of the flower. This difficulty is reflected in transit times between flowers. Hon- eybees travel between two flowers in the middle of an inflorescence in, on average, 6.98 seconds (SE = 0.47, n =

35.1 (770) 27.9 (2662) 22.6 (1330)

59), but the average time to travel between two flowers at the same end of an inflorescence was significantly shorter-only 2.26 seconds (SE = 0.17, n = 38, t = 7.78, p < 0.001). Second, inflorescences that are hidden deep within the canopy of a plant may provide difficult access for bees and may not be as conspicuous to them as those on the exterior of the plant.

In the absence of honeybees, honeyeaters with their long and stout bills show no spatial patterns to floral visitation, visiting all flowers equally (Table 4). However, when honeybees are working the flowers, the birds show a strong bias to inflorescences that are borne deep within the canopy of the plant and also a strong bias to visit the central flowers within an inflorescence (Table 4). Clearly, honeybees alter the foraging patterns of the birds, with the birds concentrating their foraging activity at the flowers used least by honeybees. This response suggests that honeybees competitively exclude native birds from some of the flowers produced by C. rugulosus.

Further support for a competitive interaction can be generated by inves- tigating changes in the numbers of birds using patches of Callistemon. In areas near Goolwa in South Australia, color-banded New Holland honeyeaters often defend individual feeding territories that include the flowers produced by several Callistemon plants. The sizes of these territories are easily determined by watching the birds, marking the boundaries of their territories, and then counting the flowers enclosed. If honeybees have no influence on the ability of the birds to

harvest nectar, then changes in the numbers of honeybees working flowers should not alter the sizes of the birds' territories. However, the numbers of Callistemon flowers defended by territorial New Holland honeyeaters increased significantly when the numbers of honeybees working the flowers increased (Table 2). At high population densities of honeybees, the birds usually defended more than 7000 flowers, almost double the number defended when there were few honeybees working the flowers.

When the number of honeybees working flowers was increased ex- perimentally by placing ten hives next to a patch of Callistemon, the dominant birds (adult males) in that patch expanded their territories by displac- ing subordinates (juveniles and females) from adjacent territories and adding all or parts of these territories to their own. In the experimental patch, the territories of five dominant New Holland honeyeaters increased significantly from 4744 (SE = 216) to 7523 (SE = 290) flowers after the introduction of the bee hives (analysis of variance, F = 59.12, df = 1,8, p < 0.001). In control areas where honeybee numbers were not manipulated, territories of five individual birds did not increase significantly.

Although the manipulation of honeybee numbers and response of honeyeaters needs to be replicated, the results from this trial are consistent with observations shown in Tables 2 and 4. They suggest that the number of territories and hence birds living in a patch is reduced when honeybees consume some of the nectar. Such a result is consistent with honeybees competitively excluding some birds from flowers. Complete exclusion is unlikely because the bees are unable to remove all the nectar from all of the flowers and thus there is always some nectar available for the birds. The birds also have first use in the early morning of nectar produced overnight, and so some individuals should suc- ceed in securing sufficient nectar for their daily needs even when honeybee numbers are high.

The next stage in these assessments is to determine if being displaced from Callistemon flowers threatens the honeyeaters' long-term survival. Pre- sumably, there has been competitive interaction between the birds and bees




for approximately 100 years. Because the birds have survived, they appear not to be threatened. Factors at other times of the year, rather than competition with honeybees for Callistemon nectar in spring, may well limit the population sizes of these birds. The impact of the competitive interactions, however, may be more complex than just simple exclusion of part of the honeyeater population. Females appear to be displaced more frequently than males, and this disproportionate loss of females may affect honeyeater population dynamics more than if both sexes were displaced equally.

Interactions between honeybees and plants Changes in the numbers and behavior of native pollinators also have the potential to disrupt the pollination of plants, reduce seed production, and potentially threaten the long-term survival of the plants. Do honeybees provide pollination services that are com- parable to those provided by the native fauna that they have displaced? If not, do the plants experience reduced levels of seed production?

Interactions between honeybees and honeyeaters working the flowers of C. rugulosus near Goolwa provide a good example of possible impacts on plants. This Callistemon is largely self-incompatible and needs cross-pollination to set significant amounts of fruit. When 685 bagged flowers were cross-pollinated by hand, 45.4% set fruit, but only 11.0% of bagged flowers set fruit after self-pollination. Thus, to be effective, pollinators should regularly contact the reproductive parts of the flowers and move frequently between plants.

Honeybees harvesting nectar from Callistemon, however, only struck the stigma on 4.4% of visits (based on more than 8000 observations; see Fig- ure 3). Pollen-harvesting honeybees struck the stigma more frequently, but still on only 16.7% of 1649 visits. The larger honeyeaters, on the other hand, frequently contacted the stigma of the flower being probed (more than 50% of occasions) as well as those of adjacent flowers (determined from photography).

Honeybees also rarely moved between plants. For example, in areas where individual plants were widely

spaced (more than 3 m apart) individual honeybees were tracked for a total of 9.9 hours and were observed probing more than 4600 flowers. Not once during these observations was a honeybee observed to fly to an adjacent plant. In these areas, territorial New Holland honeyeaters moved between plants 7.3 times per hour (10 h of observation), equivalent to one in- terplant move every 400 probes. Thus, when honeybees displace honeyeaters from patches of Callistemon, the quality of the pollination service is expected to decline. If seed production is limited by pollinators, then such displacement would lead to reduced seed production.

Rates of fruit production for C. rugulosus varied with the numbers of bees and birds working the flowers. First, the numbers of flowers that set fruit inside wire mesh cages, where birds were excluded, increased as the numbers of bees increased (Table 5). This observation indicates that honeybees can pollinate Callistemon flowers. However, the rates at which caged flowers set fruit (7-17%; Table 5) were similar to rates achieved after self-pollination of flowers by hand and well below those achieved after cross-pollination. The low fruit production at caged flowers is therefore consistent with honeybees effecting little cross-pollination for this population of Callistemon.

Fruit production at flowers exposed to both birds and bees, however, was significantly higher than that for caged flowers (Table 5), indicating that birds provided important pollination services to the plant. Furthermore, this fruit production declined significantly from 35.1 to 22.6 per 100 flowers as the numbers of honeybees using the flowers increased (Table 5). Thus, displacement of pollinating birds by less effective honeybees leads to a reduction in fruit production for this population of Callistemon.

Honeybees can also alter pollination rates by removing pollen from flowers and affecting the amounts subsequently transferred by native pollinators. Correa reflexa sets more fruit and more pods if cross-pollinated (Table 6). In the wild, honeyeaters pollinate the flowers when they drink nectar, as do honeybees when they harvest pollen. However, fruit and pod production are significantly

Table 6. Fruit and pod production by Correa reflexa after different experimental treatments. The autogamous treatment involved only bag- ging flowers before anthesis. Selfed and crossed treatments involved pollinating bagged flowers by hand with self pollen or cross pollen, respectively. The bees-only treatment excluded birds from flowers by using 1-centimeter plastic mesh. Note that the maximal number of pods that a flower can set is four. Data were accu- mulated from 21-25 plants for each treatment at Flinders Chase National Park between 1986 and 1988. The number of flowers in each treatment is given in parentheses. Differences between the bees-only and the birds-and-bees treatment in percent flowers setting fruits and in pods set per fruit were both significant (X2 = 54.3, df = 1, p < 0.001, and t = 5.1, df = 273, p < 0.001 respectively).

Percent flowers Pods/fruit Treatment setting fruit (mean ? SE)

Autogamy 3.5 (487) 1.4 + 0.1 Selfed 9.4 (233) 2.0 + 0.2 Crossed 18.9 (375) 3.0 + 0.1

Bees only 10.7 (704) 2.2 + 0.1 Birds and bees 26.1 (754) 3.0 + 0.1

reduced when birds but not bees are excluded from flowers (Table 6). This observation implies that honeybees are less effective pollinators than are birds.

Two factors contribute to the difference in efficiency. First, the flowers of C. reflexa are protandrous, with the eight anthers dehiscing synchro- nously early in the flower's life. Hon- eybees generally visit recently opened flowers that are in male phase, because such flowers are rich in pollen. They rarely visit older flowers that are in female phase, and so honeybees are less effective pollinators than the birds that visit all floral stages. Second, honeybees forage over a more re- stricted area than the birds and so transport pollen over shorter distances and more often within a plant than between plants.

Visits to flowers by honeybees often outnumber those by birds (e.g., Table 1), and honeybees are often the first to visit recently opened flowers. On that first visit, a honeybee can remove or dislodge 87% of the pollen (Figure 4). A bird dislodges 34-53% of the pollen on the first visit to an intact flower (Paton 1991). Often flowers receive several visits by honeybees before a bird probes the flower. By this time, little pollen remains.

Does this loss of pollen to honey-

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Table 7. Influence of pollen availability at source flowers on subsequent dispersal of pollen to sink flowers by captive eastern spinebills visiting Correa reflexa flowers. Differences in the number of sink flowers receiving pollen and in the total number of grains deposited were significant (analysis of variance, F = 7.9, df = 2.37, p < 0.001 in both cases).

Number Total number of intact Number of of grains anthers on Number Number of probes sink flowers deposited on source of trials into sink flowers receiving pollen ten sink flowers

8 15 7.3 + 1.0 6.2 ? 0.7 89.6 ? 14.0 4 12 7.9 ? 1.0 5.4 ? 0.7 51.8 ? 19.1 1 13 6.9 ? 0.7 2.5 ? 0.7 14.6 ? 4.5

bees reduce the amount of pollen that is transferred to flowers by birds? Simple trials using captive honeyeaters have been used to measure the impact of pollen removal by honeybees on subsequent rates of bird-pollination for C. reflexa. In these trials, captive birds (eastern spinebills Acantho- rhynchus tenuirostris) were presented with eleven Correa flowers: a source flower that supplied pollen and ten sink flowers that received pollen. Sink flowers had been emasculated before the anthers dehisced, and so they con- tained no pollen. Thus, any pollen that these flowers received during a trial must have come from the source flower. The ratio of source flowers to sink flowers in these trials approxi- mates the natural ratio. C. reflexa blooms for 3-4 months and maintains a more or less constant number of flowers in bloom during this period. Individual flowers live for approximately nine days. Consequently, one flower in nine would be expected to have recently (i.e., in the past 24 h) released pollen.

In each trial, captive honeyeaters were allowed to visit each of the flowers between five and ten times (Table 7), similar to the frequency with which birds visit Correa flowers in the field (e.g., Table 1). All flowers were then retrieved. We counted, using a micro- scope, the pollen deposited on the stigma of each flower. To vary the amount of pollen at source flowers and mimic the results of bee visits, some anthers were removed. When pollen was removed from source flowers, significantly fewer sink flowers received pollen and the total number of pollen grains landing on their stigmas was also significantly reduced (Table 7). Appropriate field work is now required to determine if these impacts occur in the wild and lead to reduced production of seeds for this plant in areas stocked with honeybees.

Management of honeybees in the environment

There is much debate in Australia about the management of honeybees in reserves set aside for conservation. The sorts of interactions I have described in this article are often cited as evidence of honeybees having a negative influence on Australian flora and fauna, and they are considered ample reason for excluding honeybees from such areas.

The exclusion of honeybees from reserves, however, is easier said than done. Park managers may be able to remove feral colonies and prevent beekeepers from placing their hives in reserves, but they are unlikely to prevent honeybees intruding from adjacent areas. For example, beekeepers excluded from a reserve could place their hives on adjacent land, and from there they could exploit the floral resources of a reserve. Complete exclusion from reserves, therefore, would require honeybee-excluded buffer zones of several kilometers in width around a reserve. Legislation would be required before buffer zones could be enforced.

Exclusion of honeybees from reserves, however, may be premature. So far, I have highlighted the potential damage that honeybees might cause to some plants and animals, but these dangers need to be balanced against possible beneficial interactions. For example, some native plants may have lost their endemic pollinators, perhaps because of extensive land clearance, fires, chance, or even past competition with honeybees. Honeybees, in visiting the flowers of these plants, may provide pollinator service and enable those plants to set seed.

For example, the flowers of Orth- rosanthus multiflorus bloom for only one day, during which native bees often fail to visit all the flowers and

may not visit any flowers on some days (Figure 2).3 On the other hand, the flowers of this plant are visited as often as 50 times by honeybees, so honeybees undoubtly provide significant pollination services for this plant. Whether the presence of many honeybees causes the lack of visits by native bees is not known, but the low visitation rates of native bees may be independent of honeybee activity. A variety of other Australian plants are also known to be inadequately serviced by their natural pollinators (e.g., Paton 1988), and these plants too may benefit from honeybee activity at their flowers. Thus, park managers may wish to place hives on some reserves to help secure seed production for particular plants.

Sensible management plans for A. mellifera in Australia ideally would balance the negative interactions against positive interactions and consider the value of the honeybee indus- try to horticulture. Only then could they recommend the exclusion or in- clusion of honeybees for a reserve.

The major factor limiting the de- velopment of these management plans is the dearth of information on the requirements of native plants and their pollinators and the impact of honeybees and other perturbations (e.g., land clearance and grazing by stock) on these endemic systems. Future research should select an appropriate range of flora and fauna for study and manipulate the numbers of honeybees working the flowers of target plants. Based on material provided in Figure 1, the most useful manipulations of honeybee numbers may be those per- formed when honeybee numbers are low. With more knowledge, appropriate management might involve re- habilitating areas (e.g., increasing breeding habitat) to suit certain endemic pollinators rather than manag- ing honeybees.

In the interim, thought should be given to adjusting the sizes and loca- tions of apiaries that are currently placed in reserves. In large apiaries, there is a high possibility that individual hives compete for the same resources. Limiting the size of apiaries might lead to more efficient use of floral resources, giving beekeepers a better return per hive, and guarantee

3See footnote 2.




that a certain level of resources remains for use by native biota. Even- tual management of honeybees in reserves, then, may involve regularly adjusting the sizes of apiaries to available resource levels.

Acknowledgments Research reported in this paper was funded by the Australian Research Council, by grants from the South Australian Department of Environ- ment and Planning, and by Earthwatch and its research corps. I thank A. Boulton, L. Jansen, P. Kevan, J. Miller, G. Pyke, K. Stove, J. Thomson, and two anonymous reviewers for providing constructive comments on drafts of this paper.

References cited

Armstrong, J. A. 1979. Biotic pollination mechanisms in the Australian flora: a review. NZ J. Bot. 17: 467-508.

Bell, D. T. 1987. Honeybees and native flora in Western Australia. Pages 48-58 in J. D. Blyth, ed. Beekeeping and Management. West Australia Department of Conserva- tion and Land Management, Como, Austra- lia.

Collins, B. G., G. Cary, and G. Packard. 1980. Energy assimilation, expenditure and stor- age by the brown honeyeater, Lichmera indistincta. J. Comp Physiol. B 137: 157-163.

Collins, B. G., and H. Clow. 1978. Feeding behaviour and energetics of the western spinebill, Acanthorhynchus superciliosis (Aves: Meliphagidae). Aust. J. Zool. 26: 269-277.

Collins, B. G., and P. C. Morellini. 1979. The influence of nectar concentration and time of day upon the energy intake and expenditure by the singing honeyeater, Meliphaga virescens. Physiol. Zool. 52: 165-175.

Doull, K. 1973. Bees and their role in pollination. Aust. Plants 7: 223, 230-231, 234-236.

Ford, H. A. 1979. Interspecific competition in Australian honeyeaters: depletion of common resources. Aust. J. Ecol. 4: 145-164.

.1981. Territorial behaviour in an Aus- tralian nectar-feeding bird. Aust. J. Ecol. 6: 131-134.

.1986. Concluding remarks: germina- tion of new ideas or flights of fancy? Pages 155-158 in H. A. Ford and D. C. Paton, eds. The Dynamic Partnership: Birds and Plants in Southern Australia. South Australia Gov- ernment Printer, Adelaide, Australia.

Ford, H. A., and D. C. Paton. 1985. Habitat

selection in Australian honeyeaters, with special reference to nectar productivity. Pages 367-388 in M. L. Cody, ed. Habitat Selection in Birds. Academic Press, San Di- ego, CA.

Ford, H. A., D. C. Paton, and N. Forde. 1979. Birds as pollinators of Australian plants. NZJ. Bot. 17: 509-519.

Ginsberg, H. S. 1983. Foraging ecology of bees in an old field. Ecology 64: 165-175.

McFarland, D. C. 1986. Determinants of territory size in New Holland honeyeaters Phylidonyris novaehollandiae. Emu 86: 180-185.

Michener, C.D. 1970. Superfamily Apoidea. Pages 943-951 in Insects of Australia. Melbourne University Press, Melbourne, Australia.

. 1979. Biogeography of the bees. Ann. Mo. Bot. Gard. 66: 277-347.

Paton, D. C. 1982a. The diet of the New Hol- land honeyeater Phylidonyris novaehollandiae. Aust. J. Ecol. 7: 279-298.

. 1982b. The influence of honeyeaters on flowering strategies of Australian plants. Pages 95-108 in J. A. Armstrong, J. M. Powell, and A. J. Richards, eds. Pollination and Evolution. Royal Botanic Gardens, Sydney, Australia.

. 1985. Food supply, population struc- ture, and behaviour of New Holland honeyeaters Phylidonyris novaehollandiae in woodland near Horsham, Victoria. Pages 219-230 in A. Keast, H. F. Recher, H. Ford, and D. A. Saunders, eds. Birds of Eucalypt Forests and Woodlands: Ecology, Conservation, Management. Royal Australasian Ornithological Union and Sur- rey Beatty & Sons, Sydney, Australia.

. 1986. Honeyeaters and their plants in south-eastern Australia. Pages 9-19 in H. A. Ford and D. C. Paton, eds. The Dynamic Partnership: Birds and Plants in Southern Australia. South Australia Government Printer, Adelaide, Australia.

.1988. Interdependence of Australian honeyeaters (Meliphaghidae) and nectar- producing plants. Pages 549-559 in Acta XIX Congressus Internationalis Orn- ithologicii. XIX Congressus Internationalis Ornithologicus, Ottawa, ON, Canada.

. 1990. Budgets for the use of floral resources in mallee-heath. Pages 189-193 in J. C. Noble, P. J. Joss, and G. K. Jones, eds. The Mallee Lands: A Conservation Perspective. CSIRO, Melbourne, Australia.

. 1991. Variation in meliphagid morphology and its influence on pollen dispersal in Australian plants. Pages 1611-1616 in Acta XX Congressus Internationalis Ornithologicii. New Zealand Ornithologi- cal Congress Trust Board, Wellington, New Zealand.

Paton, D. C., and V. Turner. 1985. Pollination of Banksia ericifolia Smith: birds, mammals and insects as pollen vectors. Aust. J. Bot. 33:271-286.

Pyke, G. H. 1983. Relationships between honeyeater numbers and nectar production

in heathlands near Sydney. Aust. J. Ecol. 5: 343-370.

. 1988. Yearly variation in seasonal patterns of honeyeater abundance, flower density and nectar production in heathland near Sydney. Aust. J. Ecol. 13:1-10.

. 1990. Apiarists versus scientists: a bittersweet case. Aust. Nat. Hist. 23: 386-392.

Pyke, G. H., and L. Balzer. 1985. The effect of the introduced honey-bee on Australian native bees. Occasional paper no. 7, New South Wales National Parks and Wildlife Service, Sydney, Australia.

Pyke, G. H., and H. F. Recher. 1986. Relation- ship between nectar production and seasonal patterns of density and nesting of resident honeyeaters in heathland near Sydney. Aust. J. Ecol. 11: 195-200.

Roubik, D. W. 1978. Competitive interactions between neotropical pollinators and Africanized honey bees. Science 201: 1030-1032.

. 1980. Foraging behavior of competing Africanized honeybees and stingless bees. Ecology 61: 836-845.

.1982. Ecological impact of Africanized honeybees on native neotropical pollinators. Pages 233-247 in P. Jaisson, ed. Social Insects in the Tropics. Pressus de l'Universite Paris XIII, Paris, France.

Sakagami, S. F. 1959. Some interspecific rela- tions between Japanese and European honeybees. J. Anim. Ecol. 28: 51-68.

Saunders, D. A., A. J. M. Hopkins, and R. A. How, eds. 1990. Australian ecosystems: 200 years of utilization, degradation and reconstruction. Proc. Ecol. Soc. Aust. 16.

Schaffer, W. M., D. B. Jensen, D. E. Hobbs, J. Gurevitch, J. R. Todd, and M. V. Schaffer. 1979. Competition, foraging energetics, and the cost of sociality in three species of bees. Ecology 60: 976-987.

Schaffer, W. M., D. W. Zeh, S. L.Buchmann, S. Kleinhans, M. V. Schaffer and J. Antrim. 1983. Competition for nectar between introduced honey bees and native North American bees and ants. Ecology 64: 564-577.

Sugden, E. A., and G. H. Pyke. 1991. Effects of honeybees on colonies of Exoneura asimillima, an Australian native bee. Aust. J. Ecol. 16: 171-181.

Taylor, G., and R. J. Whelan. 1988. Can honey bees pollinate Grevillea? Aust. Zool. 24: 193-196.

Williams, I. H., S. A. Corbett, and J. L. Osborne. 1991. Beekeeping, wild bees and pollination in the European community. Bee World 72: 170-180.

Wills, R. T., M. N. Lyons, and D. T. Bell. 1990. The European honey bee in Western Austra- lian kwongan: foraging preferences and some implications for management. Proc. Ecol. Soc. Aust. 16: 167-176.

Wilson, P., and J. D. Thomson. 1991. Hetero- geneity among floral visitors leads to dis- cordance between removal and deposition of pollen. Ecology 72: 1503-1507.

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