Nectar availability and flower choice by eastern spinebills foraging on mountain correa

Nectar availability and flower choice by eastern spinebills foraging on mountain correa

ANIMAL BEHAVIOUR, 2006, 72, 1387e1394 doi:10.1016/j.anbehav.2006.03.024 Nectar availability and flower choice by eastern spinebills foraging on mounta...

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ANIMAL BEHAVIOUR, 2006, 72, 1387e1394 doi:10.1016/j.anbehav.2006.03.024

Nectar availability and flower choice by eastern spinebills foraging on mountain correa JOLENE SCOBLE & M ICHA EL F. CLARKE

Department of Zoology, La Trobe University (Received 26 May 2005; initial acceptance 29 June 2005; final acceptance 25 March 2006; published online 18 October 2006; MS. number: 8567)

Nectarivorous birds are known to make choices at the landscape, plant species and individual plant levels when selecting foraging sites. However, little attention has been given to the fine-scale foraging choices that nectarivorous honeyeaters (Meliphagidae) make, such as those between individual flowers. We examined the variability in nectar availability between individual flowers of mountain correa, Correa lawrenciana, and used this information to predict the foraging behaviour of the eastern spinebill, Acanthorhynchus tenuirostris, a small (10e15 g) member of the Meliphagidae. Eastern spinebills preferentially foraged upon mountain correa flowers that were at the developmental stage offering the greatest volume of nectar. They did not discriminate between the flowers on the basis of corolla length (size), but this was not unexpected as nectar production was not correlated with flower size. Eastern spinebills were significantly less likely to forage at flowers with visual evidence of having been robbed of nectar by vertebrate and invertebrate competitors. They did not discriminate against flowers containing the flower mite, Hattena floricola, even though the flowers produced significantly less nectar when mites were present. This is the first study to show that a member of the Meliphagidae is capable of discriminating between individual flowers, favouring those most likely to contain most nectar. Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Nectar available to nectarivorous birds varies in time, space and quality. Nectar volume (Ford & Paton 1982; McFarland 1986a), sugar concentration (Hainsworth & Wolf 1976), sugar composition (Stiles 1976) and energetic content (Ford 1979; Ford & Paton 1982; McFarland 1986a, b) may vary considerably between species of plants. Furthermore, weather conditions have the potential to influence nectar production and availability (Ford & Paton 1982; Ford 1991). The ability of nectarivores to assess flowering intensity and/or production of nectar and use this information in foraging choices at landscape (Keast 1968), plant species (Ford & Paton 1982) and individual plant levels (Brody & Mitchell 1997) is well documented. However, variability in nectar production also exists among flowers within a plant (e.g. Pleasants 1983). Nectar production may vary with flower age (Gass & Montgomerie 1981; Morris 1996), stage of development (Delvin & Stephenson 1985) and flower size (Cruden & Herman 1983; Opler 1983). Correlations between nectar production and floral development or size have rarely been investigated in Australian zoophilous plant species.

Correspondence: M. F. Clarke, Department of Zoology, La Trobe University, Bundoora, 3086, Australia (email: [email protected]). 0003e 3472/06/$30.00/0

It would seem beneficial for avian nectarivores to be able to make foraging choices at finer levels, especially since information available at a plant/clump scale is likely to be less exact than information available from individual flowers (Wolf & Hainsworth 1991). Investigations into foraging choices made by hummingbirds suggest that they are able to discriminate between flowers on the basis of differences in nectar availability (Barrows 1976; Gass & Montgomerie 1981; Morris 1996). No such study has been carried out within one of the world’s largest group of nectarivores, the honeyeaters (Meliphagidae). Investigations into the foraging choices made by Australian honeyeaters have largely focused on decisions made at a coarse-grained (large) scale (Lamm & Wilson 1966; Keast 1968; Ford & Paton 1977, 1982; Paton & Ford 1977; Ford 1979; Pyke 1983; Vaughton 1990). The eastern spinebill, Acanthorhynchus tenuirostris, feeding on mountain correa, Correa lawrenciana, provides an ideal system in which to examine questions relating to choices between flowers by a meliphagid. Ford (1979) found irregularity in flowering and nectar production by Correa schlechtendalii. This ‘irregularity’ may reflect differences in nectar production by flowers of different ages or stages of development, or by flowers of different size, and may also be present in other Correa spp. such as C. lawrenciana.

1387 Ó 2006 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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ANIMAL BEHAVIOUR, 72, 6

Sugar composition, as well as nectar volume, may affect choice of flowers. Optimization models emphasize that constituents of food items not affecting energetic profitability, such as essential nutrients, may also influence food choice (Krebs et al. 1983). Whether differences in nectar volume and composition are available to eastern spinebills foraging on mountain correa is unknown. Their flower choice may also be complicated by interspecific competition. The long tubular flowers of most Correa spp. are morphologically suited to feeding by birds (Faegri & van der Pijl 1971). However, in the long tubular flowers favoured by hummingbirds, which are similar in morphology to Correa spp. flowers, nectar robbing is perpetrated by avian visitors with bills too short to feed on the nectar legitimately, and by insects that have difficulty physically reaching the nectaries (Inouye 1983; Irwin 2000). Foraging hummingbirds are capable of discriminating against robbed flowers, which offer reduced nectar availability (Irwin 2000). Further competition may come from flower mites. Seeman (1996) showed that flower mites Hattena cometis Domrow and H. panopla Domrow consume nectar of the host plants in which they reside. Eastern spinebills have been reported to be phoretic hosts for H. cometis (Domrow 1979) and H. floricola Halliday flower mites (B. Halliday, personal communication). As a nectar resource favoured by eastern spinebills, C. lawrenciana therefore clearly has the capacity to be patchy in space and time, providing foraging birds with a multitude of important choices. The aim of our study was to examine whether eastern spinebills discriminate between flowers when foraging upon C. lawrenciana var. latrobeana and if so, upon what basis they do so. We examined the variability in nectar production of individual flowers within a plant caused by the floral variables of age/stage of development, flower size, evidence of robbing and presence or absence of flower mites. With this knowledge we were then able to make and test predictions about which flowers eastern spinebills should choose, assuming they were foraging to maximize energy intake (Krebs et al. 1983).

METHODS

Study Sites The study sites were at Mt Disappointment State Forest, 60 km northeast of Melbourne, Victoria (37 310 S, 145 70 E), and Toolangi State Forest in Victoria, 70 km northeast of Melbourne, Victoria (37 310 6000 S, 145 280 E), Australia. All experiments conducted on mountain correa, C. lawrenciana var. latrobeana, flowers were carried out on Mt Disappointment. Observations of flower choice by eastern spinebills were conducted at Mt Disappointment (N ¼ 23) and in Toolangi State Forest (N ¼ 8). Both study sites were 600e800 m above sea level. Average daily temperature range at both sites is similar (Mt Disappointment State Forest 7.9e16.4 C; Toolangi State Forest 7.6e 15.2 C). However, annual rainfall at Toolangi State Forest (1377.9 mm) is approximately double that at Mt Disappointment State Forest (672.2 mm).

The study sites in both State Forests comprised regenerating mountain ash, Eucalyptus regnans, forest (around 30e50 years postlogging), approximately 40e50 m tall. The forest was typically characterized by a middle storey of smaller trees (e.g. Acacia melanoxylon and Acacia dealbata) and tall shrubs (e.g. Bedfordia arborescens, Pomaderris aspera, Olearia argophylla). A lower storey consisted of ferns and smaller shrubs that grew in dense stands (e.g. Cassinia longifolia and Prostanthera lasianthos). Mountain correa also formed part of the lower storey, growing in thick stands and as individual shrubs at these sites.

Data Collection and Analysis Flower development Preliminary observations indicated that mountain correa flowers changed in structure and colour as they aged. To establish the timing and duration of these changes within the life span of flowers, we marked, with ties, 10 unopened buds that were close to opening at each of four sites (five trees per site, two flowers per tree). We visited flowers daily between 4 April and 23 May 2003. Total flower length (base to petal tip), corolla, filament and style length were measured (0.1 mm) with Bergeon callipers. Base, corolla, style, filaments and anthers were scored for colour, using the Naturalist’s Color Guide (Smithe 1975). We also noted developmental changes such as pollen dehiscence. We identified changes in colour of corolla, anthers, filaments and style as the most reliable indicators of changes in flower development, and thus used these to classify flowers into seven broad developmental classes, referred to as ‘flower stages’ (Table 1). Only five flower stages (1e5, Table 1) were considered legitimate feeding choices for nectarivorous birds (Inouye 1983). Developmental rate differed between flowers, so time frames are considered guides only. Photographic standards were taken to document these changes and assist in flower classification. Examination of flowers was carried out under a Department of Natural Resources and Environmental research permit.

Nectar production We investigated nectar production over 24 h at each of four sites. Only one site was visited per day for initial nectar extraction. We extracted nectar from sample flowers on 8, 10, 16, 18 and 23 July 2003. On each of six trees sampled per site, we chose one robbed and one unrobbed flower per age class whenever possible. To extract nectar we used 10-ml disposable glass Drummond micropipettes (microcapillaries), placing the tip of the micropipette inside the flower beside the nectaries. The length of each microcapillary occupied by nectar was measured (mm) with Bergeon callipers, and the nectar volume determined. Nectar samples were stored in individual 5-ml plastic epindorph tubes and frozen at 20 C. After nectar was extracted, Tac-gel (Rentokil Initial Pty Ltd, Chatsworth, Australia) was applied around the base of each flower, which was then individually bagged with

SCOBLE & CLARKE: EASTERN SPINEBILL FLOWER CHOICE

Table 1. Definitions of developmental stages in Correa lawrenciana flowers based upon colour and structural changes observed over the life span of sample flowers Floral stage Bud 1 (days 1e2) 2 (days 3e7) 3 (days 8e9) 4 (days 10e13) 5 (days 14þ) 6

Characteristics (in order of importance) Petals have not yet split from corolla, so legitimate feeding is not possible Anthers generally not protruding, but if they are, green membrane is unbroken and pollen dehiscence is not yet initiated. Corolla bright green (161/159 or 161/58). Style and filaments green Anthers dehiscing bright yellow pollen (55 or 157/55). Corolla green. Style and filaments green Anthers containing little, if any pollen (157 or 157/55). Corolla green. Style and filaments generally green, small amount of red may have begun to appear Style and filaments typically light red and green. Corolla green or light olive. Anthers contain no pollen and are light yellow (157) Filaments dark red, occasionally incorporating green. Older flowers have dark olive filaments. Style red, and may also incorporate green. Older flowers have dark red to olive styles. Corolla olive, older corollas tend to be darker olive. Anthers contain no pollen and are pale yellow (157) Petals have curled in, so legitimate feeding is not possible

Numbers in parentheses refer to colour classes from Smithe (1975).

green nylon mesh, to prevent nectar consumption by birds and insects (Colwell 1995). We visited all flowers 24 h later (9, 11, 17, 19 and 24 July 2003), in the same order and sampled the nectar to determine 24-h production. After the 24-h nectar sample was taken, all flowers were measured (total flower length), picked and stored in ethanol. Flower mites were extracted, and the dorsoventral shield of each individual was measured (0.1 mm) with a compound microscope fitted with an eyepiece micrometer. The sum of dorsoventral shield lengths of all mites in a flower was used as an estimate of mite biomass per flower.

of the assay was proportional to the amount of the appropriate sugar present in the original nectar sample. The sugar assay buffer contained 20 mM imidazole (5 mM K-phosphate, pH 7.0), 5 mM MgCl2, 0.5 mM NADþ, 0.5 mM ATP, 0.2 mg/ml BSA and 0.2 U/ml of the indicator enzyme G6PDH. Suitable aliquots of nectar samples were added to 3 ml of assay buffer and mixed well by repeated pipetting. To ensure that spectrophotometric readings were within a suitable range (A340 < 1.0), we generally diluted samples in distilled water by a factor of 1/10 to 1/15, and added 3-ml aliquots of diluted nectar to the assay. After zeroing the spectrophotometer (Pharmacia LKB Novaspec II) against a distilled water blank, we recorded the A340 of the buffer and nectar mixture.

Nectar analysis We analysed nectar samples from three sites to quantify the relative amounts, concentrations and total quantities of the sugars glucose, fructose and sucrose present in each sample. All three sugars in each nectar sample were measured sequentially in a single tube by enzymatic analysis. (1) Each sugar was sequentially converted to glucose 6-phosphate, by using sugar-specific enzymes. First, hexokinase (HK) was used to phosphorylate glucose to glucose 6-phosphate. This enzyme also phosphorylated fructose to fructose 6-phosphate. Second, phosphoglucose isomerase (PGI) was added to convert the fructose 6-phosphate (derived from fructose in the previous step) to glucose 6-phosphate. Third, invertase (INV) was added to hydrolyse the disaccharide sucrose to its monosaccharide components, glucose and fructose, both of which were then converted to glucose 6-phosphate by the HK and PGI already present in the mixture. (2) The glucose 6-phosphate resulting from each of the three sugars in turn was then acted on by the indicator enzyme, glucose 6-phosphate dehydrogenase (G6PDH) to form 6-phosphogluconolactone. As part of this reaction, the cofactor NADþ was reduced to NADH. Since the reduced form of the cofactor absorbs strongly at 340 nm but the oxidized form does not, this reaction could be monitored spectrophotometrically at 340 nm. The increase in the absorbance at 340 nm (A340) after each stage

Movements of eastern spinebills To avoid resampling individual birds during observations of flower choice, we observed local movements of seven individually colour-banded eastern spinebills in Mt Disappointment State Forest to establish maximum distances that birds would travel during foraging and other activities. Birds were captured in mist nets and banded with a unique combination of three coloured Darvic bands and a single numbered alloy band issued by the Australian Bird and Bat Banding Scheme. Capture, banding and observational procedures were in accordance with the conditions approved under a La Trobe University Animal Ethics Permit and a Victorian Department of Natural Resources and Environment Research Permit. Observations of banded birds were made with binoculars on 11 separate days between 10 June and 6 September 2003 during a total of 35 h of observation time. Mapping of movements by eastern spinebills showed a high degree of site fidelity, and virtually no overlap in areas used by marked individuals. No colour-banded individuals were observed at two locations more than 70 m apart. Consequently, when making observations of flower choice by eastern spinebills, we used only observations of birds at least 80 m apart in the analysis, to reduce the likelihood of resampling any given bird.

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Flower choice by eastern spinebills We made single observations of 31 eastern spinebills feeding on nectar of mountain correa flowers to investigate the hypothesis that eastern spinebills visit all open flowers in proportion to their abundance. This relates to the proportion of floral stages, flower length, mite presence, and evidence of flowers having been robbed. The first flower an individual bird was observed to visit (the ‘chosen flower’) was marked with a bag tie. Using a measuring tape and bag ties, we created a 1-m3 ‘box’ around the chosen flower, which was the centre point. All open flowers (the ‘other flowers’) within this area were assigned a developmental class (stages 1e5) and their total length (mm) measured with Burgeon callipers. We also recorded the abundance of mites and evidence of robbing for each flower.

Statistical Analysis For all statistical analyses we used SPSS version 10.0 (SPSS Inc., Chicago, IL, U.S.A.). Owing to the small sample size and presence of many data points with a zero value, assumptions of normality and homogeneity were rarely met. Hence all analyses were completed with nonparametric tests. Two-tailed tests and a significance of 0.05 were used in all analyses.

RESULTS

Variation in Nectar Production The volume of nectar produced over 24 h varied significantly across different developmental classes (Kruskale Wallis test: c22 ¼ 146:7, P < 0.001; Fig. 1), peaking in stage 2. Stage 2 flowers produced significantly more nectar than stage 1 flowers (ManneWhitney U test: Z ¼ 2.2, N1 ¼ 73, N2 ¼ 29, P ¼ 0.025) and stage 3 flowers (Z ¼ 5.2, N1 ¼ 73, N2 ¼ 54, P < 0.001). As floral stages 4 and 5 generally produced no nectar over 24 h, or only negligible volumes, no statistical comparisons were carried out with these two floral stages within this or subsequent analyses. Since the concentrations of glucose, fructose and sucrose did not vary significantly across stages 1e3 (Fig. 2), nectar volume was a good indicator of the total amount of sugar available to nectarivores at the different stages of flower development. No significant relation was found between flower length and the volume of nectar produced over a 24-h period (Spearman rank correlation: rS ¼ 0.039, N ¼ 156, P ¼ 0.627).

30 25 Nectar volume (µl)

1390

20 15 10 5 0 N =

29 1

73 2

54 54 3 4 Flower stage

54 5

Figure 1. Nectar production (ml) of flower stages 1e5 over 24 h. Data presented represent both flowers that had been robbed and those that had not been robbed, prior to bagging. Boxes indicate the interquartile range. Horizontal lines within boxes indicate medians. Whiskers extend to the highest or lowest value within 1.5 times the interquartile range. Data points with values 1.5e3 times, above or below, the interquartile range are outliers (B). Those with values more than 3 times, above or below, the interquartile range are extreme points (*). As data outliers and extreme points did not alter the significance level, they were included in the analysis. N: number of flowers sampled at each stage.

through stands of mountain correa, making large splits down the side of corollas to reach the nectar. Splits of this nature were by far the most common type of damage observed in mountain correa flowers (J. Scoble, personal observation). Small holes were apparent in a few flowers throughout the study period, especially during winter months (JuneeAugust). Unrobbed stage 2 flowers tended to produce more nectar over a 24-h period (median 4.1 ml, range 0e11.6 ml, N ¼ 39 flowers) than robbed flowers (median 2.1 ml, range 0e 29.2 ml, N ¼ 34 flowers), although the difference was not statistically significant (ManneWhitney U test: Z ¼ 1.9, P ¼ 0.062). No differences were detected at stages 1 (Z ¼ 0.3, Nunrobbed ¼ 21, Nrobbed ¼ 8, P ¼ 0.750) and 3 (Z ¼ 0.1, Nunrobbed ¼ 24, Nrobbed ¼ 30, P ¼ 0.848). Concentrations of glucose, fructose and sucrose did not differ significantly between robbed and unrobbed flowers (floral stages 1e3 were analysed together, N ¼ 34 robbed, 18 unrobbed flowers; glucose: ManneWhitney U test: Z ¼ 0.2, P ¼ 0.832; fructose: Z ¼ 0.3, P ¼ 0.758; sucrose: Z ¼ 0.9, P ¼ 0.376).

Flower mites Impact of Illegitimate Consumers Nectar robbers Robbing was rare in stage 1 flowers but reached a peak in stage 3 flowers (Table 2). During observations of eastern spinebills, we often saw silvereyes, Zosterops lateralis, in flocks of approximately 10e30 individuals. No aggressive interactions were observed between silvereyes and eastern spinebills. Flocks of silvereyes would move quickly

Hattena floricola mites were present in approximately half (N ¼ 29) of stage 1 flowers (56%), two-thirds of stage 2 flowers (68%, N ¼ 73) and three-quarters of stage 3 flowers (78%, N ¼ 54). The percentage of flowers containing mites peaked in stage 4 flowers (85%, N ¼ 54) and less than two-thirds (61%) of stage 5 flowers had mites (N ¼ 54). The volume of nectar present after 24 h in flowers with and without mites (Fig. 3) did not differ significantly for

SCOBLE & CLARKE: EASTERN SPINEBILL FLOWER CHOICE

Table 2. Number and percentage (in parentheses) of robbed and unrobbed flowers in Correa lawrenciana stages 1e5

700 600

(a)

Floral stage

Unrobbed

Robbed

Glucose (mM)

500 1 2 3 4 5

400 300 200

142 162 111 113 156

(91.03) (57.45) (53.88) (60.75) (58.21)

14 120 95 73 112

(8.97) (42.55) (46.12) (39.25) (41.79)

100 0 N =

8 1

34 2

10 3

700 600

(b)

stage 2 flowers there was also a strong negative correlation between the mite biomass per flower and the volume of nectar present in that flower after 24 h (Spearman rank correlation: rS ¼ 0.43, N ¼ 73, P < 0.001). No such relation was found in floral stages 1 (rS ¼ 0.13, N ¼ 29, P ¼ 0.514) or 3 (rS ¼ 0.14, N ¼ 54, P ¼ 0.309).

Fructose (mM)

500

Flower Choice by Eastern Spinebills

400 300 200 100 0 N =

8 1

34 2

10 3

30 (c)

Sucrose (mM)

20

10

Stage 2 flowers were the most commonly chosen (N ¼ 23), stages 1 (N ¼ 5) and 3 (N ¼ 3) were foraged at less frequently, and eastern spinebills were never observed visiting stage 4 or 5 flowers. Therefore, we used only data from flower stages 1e3 to generate expected frequencies. Eastern spinebills foraged at stage 2 flowers significantly more often than would be expected, given the frequency of floral stages available on the plant (Fig. 4). Stage 2 flowers were 27e39 mm long. Flowers from 27 to 33 mm were classified as ‘small’ and those 34e39 mm as ‘large’. Eastern spinebills did not show a preference for large over small stage 2 flowers, foraging on both sizes in proportion to their abundance on the plant (chi-square test: c21 ¼ 0:1, P ¼ 0.7). Of the 23 foraging observations at stage 2 flowers, eastern spinebills did not forage in proportion to the abundance of robbed and unrobbed flowers (Table 2), but significantly preferred unrobbed (N ¼ 19) to robbed flowers (N ¼ 4; c21 ¼ 5:9, P ¼ 0.02). Although 68% of

0 30

8 1

34 2 Flower stage

10 3

Figure 2. (a) Concentration of glucose (mM) in floral stages 1e3 (KruskaleWallis test: c22 ¼ 2:0, P ¼ 0.366). (b) Concentration of fructose (mM) in floral stages 1e3 (c22 ¼ 1:9, P ¼ 0.394). (c) Concentration of sucrose (mM) in floral stages 1e3 (c22 ¼ 1:6, P ¼ 0.449). Note different scale on Y axis, owing to much lower concentrations of sucrose than glucose or fructose. See legend to Fig. 1 for explanation of box plots.

Nectar volume (µl)

25 N =

20 15 10 5 0 N = 13

16 1

stage 1 (ManneWhitney U test: Z ¼ 1.3, N1 ¼ 16, N2 ¼ 13, P ¼ 0.187) or stage 3: (Z ¼ 1.7, N1 ¼ 42, N2 ¼ 12, P ¼ 0.093) flowers. However, in stage 2 flowers, those with mites had significantly less nectar present than those without mites (Z ¼ 2.4, N1 ¼ 50, N2 ¼ 23, P ¼ 0.015). In

23

50 2 Flower stage

12

42 3

Figure 3. Influence of Hattena floricola flower mite absence/presence on 24-h nectar availability in flowers at stages 1e3. ,: flowers lacking mites; F: flowers containing mites. See legend to Fig. 1 for explanation of box plots.

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100 90 Percentage of total flowers

1392

80 70 60 50 40 30 20 10 0

1

2

3

4

5

Flower stage Figure 4. Abundance of floral stages available (,, N ¼ 1075) and choice by eastern spinebills foraging at Correa lawrenciana (-, N ¼ 31) presented as percentages (chi-square test: c22 ¼ 33:8, P < 0.001).

flowers contained mites, eastern spinebills did not discriminate against flowers with mites, choosing four stage 2 flowers without mites and 19 with mites (c21 ¼ 0:8, P ¼ 0.75).

DISCUSSION

Flower Choice by Eastern Spinebills Since the amount of each type of sugar was directly proportional to nectar volume in C. lawrenciana, stage 2 flowers offered the greatest energetic reward. We observed that eastern spinebills foraged preferentially upon mountain correa flowers at this stage of development. This is consistent with the hypothesis that birds are attempting to maximize net energy intake when choosing between individual mountain correa flowers within their immediate foraging location. Eastern spinebills are able to assess and respond to differences in available nectar resources between areas (Lamm & Wilson 1966; Ford & Paton 1982), plant species (Wilson 1964) and density of inflorescences within individual plant species (McFarland 1986a, b). Fine-scale discrimination has been reported for nectarivores belonging to other families (e.g. Delvin & Stephenson 1985; Maloof & Inouye 2000) and in captive regent honeyeaters, Xanthomyza phrygia (Burke & Fulham 2003). However, ours is the first study to show that a meliphagid, the eastern spinebill, can make foraging decisions at such a fine scale in a natural environment. Nectar production rates can sometimes be related to flower size (Cruden & Herman 1983; Opler 1983). However, no significant relation was found between flower size (as indicated by corolla length) and 24-h nectar production in C. lawrenciana flowers. Consequently, it was not surprising that eastern spinebills did not forage preferentially on larger stage 2 flowers, given that no energetic gains are likely.

Some researchers have shown that floral nectar resources are associated with colour cues present in flowers (Gass & Montgomerie 1981; Morris 1996). Colour markers (Miller et al. 1985) and variation in colour and pattern (Healy & Hurly 1998) have been positively associated with speed of learning the location of rewarding flowers in hummingbirds, Selasphorus rufus and Archilochus colubris. We found that flowers with particular characteristics produce higher volumes of nectar (e.g. stage 2 flowers had dehiscing anthers with bright yellow pollen that at later stages was largely removed, exposing the light yellow anthers), and eastern spinebills preferentially visited these flowers. However, we have not shown which cues eastern spinebills use to identify flowers more likely to contain nectar. While it seems likely that eastern spinebills are capable of associating visual cues, and possibly others (Ford et al. 1979; Irwin 2000), with higher nectar levels to forage efficiently at mountain correa flowers, further study is required to clarify this aspect of their foraging ecology.

Nectar Robbing Flower choice by eastern spinebills and other nectarivorous birds is further complicated by the presence of competitors for the nectar. Nectar robbing was widespread in mountain correa, peaking at 46% of all flowers at some sites. Levels of nectar robbing appear to depend greatly on the system in question, with a wide range of values reported for zoophilous plants (Irwin 2001). Splits in the flower were the most common evidence of nectar robbing, and were predominately made by silvereyes. These birds have also been recorded pecking flowers to obtain nectar (Paton & Ford 1977). It is unlikely that eastern spinebills were responsible for damage incurred by flowers; honeyeaters rarely damage flowers when foraging, and those that do usually have short bills (Paton & Ford 1977), unlike the long-billed eastern spinebill (Higgins et al. 2001). Nectar robbing experienced by mountain correa decreased 24-h nectar production in affected stage 2 flowers at a level approaching significance. A decrease in nectar production by robbed flowers may be caused by damage to nectaries incurred by the physical process of robbing (McDade & Kinsman 1980), as no changes in nectar sugar concentration were evident. Given the potential decrease in energetic rewards in robbed stage 2 flowers, one might expect a preference for unrobbed flowers by eastern spinebills foraging within this floral stage of development. Eastern spinebills strongly preferred unrobbed flowers within floral stage 2, indicating that they share the ability of hummingbirds to avoid robbed flowers offering reduced energetic rewards (Irwin & Brody 1998; Irwin 2000; Temeles & Pan 2002). It is unlikely that eastern spinebills avoided robbed flowers because of aggression by silvereyes as no aggression between these species was observed. Maloof & Inouye (2000) suggested that if avian nectarivores expect a lower reward at robbed flowers, they may use the visual cue of a hole or split to avoid such flowers. The split made by silvereyes is typically at least a third of the corolla length (J. Scoble, personal observation) and

SCOBLE & CLARKE: EASTERN SPINEBILL FLOWER CHOICE

appears to be an easily detectable visual cue. However, broad-tailed, Selasphorus platycercus, and rufous hummingbirds, S. rufus foraging upon scarlet gilia, Ipomopsis aggregata, plants avoided robbed flowers without using visual or spatial cues (Irwin & Brody 1998; Irwin 2000). Irwin (2000) suggested that probing empty flowers may act as a cue to leave an unrewarding plant. The use of cues may be complemented by a spatial memory of flowers in territorial nectarivores (Healy & Hurly 1998). Regent honeyeaters appear to be capable of predicting replenishment rates of their natural food plants and visit flowers accordingly (Burke & Fulham 2003). The use of spatial memory when foraging has also been demonstrated in hummingbirds (Brown & Gass 1993; Sutherland & Gass 1995). Further study is required to elucidate the role of territoriality and spatial memory in the foraging behaviour of eastern spinebills.

Nectar Consumption by Flower Mites The presence of H. floricola flower mites was associated with a significantly reduced volume of available nectar in stage 2 flowers after 24 h. Furthermore, a significant negative correlation was found between increasing mite biomass and nectar volume. This suggests that H. floricola flower mites consume nectar or retard nectar production in mountain correa. Until relatively recently, the effect of nectar consumption by flower mites on availability of nectar to other consumers has been assumed to be insignificant (Colwell 1995). However, the few studies on hummingbird-pollinated plants and flower mites have shown that the potential for nectar consumption by mites is considerable (Colwell 1995; Lara & Ornelas 2001). Colwell (1995) predicted that such findings may prove characteristic of other flower miteehost plant systems. While possible interactions between flower mites and honeyeater-pollinated host plants have been given little attention, it appears that Colwell’s (1995) prediction may be correct for nectar consumption by H. floricola mites living in mountain correa flowers. Further investigation to quantify the proportion of available nectar consumed by H. floricola mites is required to confirm this. Despite a significant negative correlation between the presence and biomass of mites and nectar availability, we did not detect eastern spinebills avoiding stage 2 flowers with mites. There may be a number of reasons for this. Eastern spinebill foraging patterns in response to flower mites may not operate at a presence/absence level. Intraspecific competition for nectar resources, or even just normal energetic requirements may force eastern spinebills to visit some flowers with mites to meet their energetic needs, while avoiding flowers with large numbers of mites. Furthermore, low mite loadings may not reduce nectar availability to a level that renders visiting a flower energetically costly. If foraging nectarivores use nectar as a proximal foraging cue as suggested by Irwin (2000), nectar depletion by flower mites might cause birds to leave flowers early, but not avoid them.

Eastern spinebills appear to be foraging in accordance with the assumptions of optimal foraging models, by preferentially visiting individual mountain correa flowers of the developmental class offering the greatest energetic reward, and avoiding robbed flowers, which produce less nectar. Our study demonstrates yet another level at which honeyeaters are making choices when foraging, that of the individual flower. Together with earlier studies at the landscape (Keast 1968), plant species (Ford & Paton 1982) and individual plant levels (Brody & Mitchell 1997), our study highlights the complex foraging choices made by avian nectarivores as they cope with tremendous temporal and spatial variability in their food supply.

Acknowledgments We are grateful to Dr Bruce Halliday for identifying the flower mites and to Mr Ted Wearn for giving us access to the Mt Disappointment study site. We are also grateful to staff in the Department of Biochemistry, La Trobe University for providing assistance and facilities to J.S. for the analysis of nectar. References Barrows, E. M. 1976. Nectar robbing and pollination of Lantana camara (Verbenaceae). Biotropica, 8, 132e135. Brody, A. K. & Mitchell, R. J. 1997. Effects of experimental manipulation of inflorescence size on pollination and pre-dispersal of seed predation in the hummingbird-pollinated plant, Ipomopsis aggregata. Oecologia, 110, 86e93. Brown, G. S. & Gass, C. L. 1993. Spatial association learning by hummingbirds. Animal Behaviour, 46, 487e497. Burke, D. & Fulham, B. J. 2003. An evolved spatial memory bias in a nectar-feeding bird? Animal Behaviour, 66, 695e701. Colwell, R. K. 1995. Effects of nectar consumption by the hummingbird flower mite Proctolaelaps kirmsei on nectar availability in Hamelia patens. Biotropica, 27, 206e217. Cruden, R. W. & Herman, S. M. 1983. Studying nectar? Some observations on the art. In: The Biology of Nectaries (Ed. by B. Bentley & T. Elias), pp. 223e241. New York: Columbia University Press. Delvin, B. & Stephenson, A. G. 1985. Sex differential floral longevity, nectar secretion and pollinator foraging in a protandrous species. American Journal of Botany, 72, 303e310. Domrow, R. 1979. Ascid and ameroseiid mites phoretic on Australian mammals and birds. Records of the Western Australian Museum, 8, 97e116. Faegri, K. & van der Pijl, L. 1971. The Principles of Pollination Ecology. Rushcutters Bay, Australia: Pergamon Press. Ford, H. A. 1979. Interspecific competition in Australian honeyeaters: depletion of common resources. Australian Journal of Ecology, 4, 145e164. Ford, H. A. 1991. Coping with an erratic nectar source: eastern spinebills Acanthorhynchus tenuirostris at New England National Park. Emu, 91, 53e56. Ford, H. A. & Paton, D. C. 1977. The comparative ecology of ten species of honeyeaters in South Australia. Australian Journal of Ecology, 3, 399e407. Ford, H. A. & Paton, D. C. 1982. Partitioning of nectar resources in an Australian honeyeater community. Australian Journal of Ecology, 7, 149e159.

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