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Beech honeydew: Seasonal variationand use by wasps, honey bees, andother insectsH. Moller a & J.A.V. Tilley aa Ecology Division, Department of Scientific and IndustrialResearch , Private Bag, Nelson , New ZealandPublished online: 09 Feb 2012.

To cite this article: H. Moller & J.A.V. Tilley (1989) Beech honeydew: Seasonal variation anduse by wasps, honey bees, and other insects, New Zealand Journal of Zoology, 16:3, 289-302,DOI: 10.1080/03014223.1989.10422894

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New Zealand Journal of Zoology, 1989, Vol. 16: 289-302 0301-4223/89/1603-0289~2.s0/0 © Crown Copyright 1989

289

Beech honeydew: Seasonal variation and use by wasps, honey bees, and other insects

H.MOLLER I.A.V. TILLEY

Ecology Division Department of Scientific and Industrial Research Private Bag, Nelson, New Zealand

Abstract Variation in the production of beech honeydew by the scale insect (Ultracoelostoma assimile), and in the density and abundance of insects feeding on it, was studied in a mixed beech (Nothojagus) forest near Nelson, New Zealand.

Nearly all anal tubes were connected toa feeding instar of the scale insect and so were able to deliver drops of honeydew to feeding insects and birds. The number of anal tubes and drops was high in winter and spring and declined to a trough in late summer and autumn. Drop quality (size and sugarconcentra-tion) also reached a low in the late summer and autumn. It is suggested that consumption of drops by wasps (mainly common wasps, Vespulavulgaris, but also German wasps, V. germanica) caused the paucity of honeydew in late summer and autumn. Wasps probably also prevented feral honey bees (Apis mellijera) from gathering honeydew then.

Wasps were by far the most abundant insect feeding on honeydew, peaking at an average of S8 wasps per m2 of trunk of honeydew-infested tree in March. Wasp numbers declined markedly in April. Concern is expressed about the impact of introduced wasps on endemic insects, honeydew and insect-feeding birds inhabiting the honeydew beech forests.

Keywords Honeydew; Ultracoelostomaassimile; Nothojagus; Vespula; Apis melli/era,· Bombus; conservation; honey production

Received 19 December 1988; accepted 8 February 1989

INTRODUCTION This study investigated honeydew production by the beech scale insect (Ultracoelostomaassimile) (Hom-optera: Margarodidae) in a beech (Nothojagus) forest near Nelson, New Zealand, and the abundance and use of honeydew by wasps, bees, and other insects. Encapsulated second- and third-instar beech scale insects siphon sap from the phloem vessels of beech trees. Most of the sap is not absorbed by the scale insect but passes through it to form a drop on the end of a waxy anal tube extending out of the tree (Crozier 1981; Moller & Tilley 1986; Morales et al. 1988).

Honeydew is important in New Zealand's South Island beech forests as a major food source of many birds and insects (Gaze & Clout 1983; Oout & Gaze 1984; Boyd 1987; Beggs & Wilson 1987).

The drops are the main energy source for feral and managed honey bees (Apis melli/era) in beech forests (see Smith 1978 for a review; Anon. 1979). It is therefore economically important to determine how the honeydew varies in abundance and quality, and the consequences of this variation for the foraging efficiency of honey bees. Commercial stocking of honey bees may affect honeydew and thereby the other animals that feed on it

Other important insects using the honeydew are the introduced social wasps (German wasps, Vespula germanica, and common wasps, V. vulgaris), which are serious pests of the beekeeping industry (Walton & Reid 1976). Wasps also feed on native insects living in the forest, and this may in tum affect insectivorous birds.

Despite the economic importance of honeydew and its value in the conservation of native birds in South Island beech forests, there has been remarkably little study of the beech scale insect, the variation in production of honeydew drops, or the role of honey-dew in the ecology of the forests. Crozier (1981) and Gaze & Clout (1983) interpreted much of the huge variation in the amount of honeydew with place and time as seasonal, but each study followed changes through only a single year. A potentially crucial variable, the drop size, was not measured in their studies.

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FIg. 1 Location of the Trass study area. Unshaded areas denote pine forest; hatched areas denote fannland; shaded areas denote beech forest

This paper reports the first steps in a long-tenn study of variation in honeydew abundance and quality. We describe honeydew variation over the first 2 years of study and the flucbJations in the numbers of wasps, feral honey bees, bumble bees (Bombus spp.), and large flies feeding on honeydew during the day. Details of the feeding behaviour of insects are described.

STUDY AREA

The Trass study area (41°23'S, 172°55'E).located in Compartment 391 ofBaigentsForeston Spooners Range, is 35 km southwest of Nelson. It is a 7.2 ha

isolated patch of native beech forest in a pine (Pinus radiata) plantation. It is one of several such remnant "islands" of native forest scattered in BaigentsForest and the adjacent Golden Downs State Forest Patches of native forest nearby are: Pretty Bridge Scenic Reserve (340 ha, 1 km from the Trass study area); WinnsBush(23ha,2km);SpoonersScenicReserve (150 ha, 9.5 km) (Fig. 1). Gaze & Clout (1983) and Clout & Gaze (1984) studied honeydew and birds in Winns Bush and Spooners Reserve. Our study area is bounded by mature pines (planted about 20 years ago), young pines (7 years old) and by land recently cleared but not yet re-planted.

We chose to study honeydew and animal numbers in a forest patch amidst pines because:

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Moller & Tilley-seasonal use of honeydew by insects 291

Fig.2 The mean number of anal tubes pet fIXed quadrat in each month. The 95% confidence inter-val is shown by a bar. Solid points September 1985 to August 1986. Open points October 1986 to August 1987.

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(i) baseline information on honeydew and bird numbers was available (Gaze & Clout 1983; Clout & Gaze 1984);

(ii) replicated experiments and measurements af-fecting animalnumbersand the honeydew eaten could be carried out;

(iii) such patches are used extensively for beekeep-ing in the Canterbury area; and

(iv) they are considered to be important for the con-servation ofnectarivorous and frugivorous birds (Clout & Gaze 1984; Clout 1984).

The Trass study site was chosen because it has levels of honeydew typical of the Nelson region. The land is gently sloping to the northwest with two major ridges 200 m apart, at about 300 m a.s.1. The canopy vegetation is predominantly beech (Notlwjagus spp.). All four species are present: red (N.jusca), hard (N. truncata), silver (N. menziesil), and black (N. solandri var. solandrl), but black predominates. Hard beech grows mainly on the ridges, but the other species are distributed throughout the area. All except silver beech have honeydew. Kamahi (Weinmanniaracemosa) is another common component of the canopy, and there are also several emergent rimu (Dacrydium cupressinum) and occasional pokaka (Elaeocarpus Iwokerianus). Putaputaweta (Carpodetus serratus) makes up a significant proportion of the subcanopy, and lancewood (Pseudopanax crassifolius), kanoka (Kunzea ericoides), mahoe (Melicytus ramiflorus), and Coprosma grandi/olia are also present. Silver fern (Cyathea dealbata) is common in the gullies. An understorey of small shrubs includes Pseudopanax anomalus, Pseudowintera axillaris, Leucopogon spp., several small-leaved Coprosma spp., and seedlings ofbroadleaf (Griselinia littoralis) and miro (Prumnopitysjerruginea).

Two New Zealand native honeyeaters, the tui (Prosthemadera novaeseelandiae) and bellbird (Antlwrnis melanura), were present throughout the study. Their numbers varied greatly between seasons. Other native birds recorded frequently were the silvereye (Zosterops lateralis), grey warbler (Gerygone igata), yellow-breasted tit (Petroica macrocephala), and fantail (Rhipidurajuliginosa). Common introduced birds were the chaffmch (Fringilla coelebs), blackbird (Turdus merula), song thrush (Turdusphilomelos),hedgesparrow (Prunella modularis), and goldfinch (Carduelis carduelis). Managed hives of honey bees are not kept at the Trass study area but feral colonies occupy cavities in tree trunks in the area.

METHODS The study area was visited for a 5 day period each month from September 1985 to August 1987. From August 1986, honeydew was measured in alternate months only. Honeydew abundance and quality were measured on at least four of the days of each visit between 0900 and 1100 h. A 50 cm x 5 cm quadrat was permanently marked on the northern aspect of the trunk of each of 10 selected trees at a height of 1.5 m. In February 1986 an additional 10 trees were monitored to provide a larger sample and thus overcome variation. Trees were selected non-randomly to include a range of infestations from light to heavy. Eighteen were black beech and two were hard beech. Honeydew drops within the quadrat were counted each assessment day. On I day in each monthly visit we also counted the number of honey-dew anal tubes without drops in each fixed quadrat. Mean drop size was calculated for each tree on each day by collecting a known number of drops from outside the quadrat in a capillary tube with a 1 mm

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Fig. 3 The mean percentage of anal tubescarrying ahoneydew drop in each month. Solid points Septem-ber 1985 to August 1986. Open points October 1986 to August 1987 .

SEP , OCT ' NOV ' DEC JAN ' FEB MAR ' APR MAY , JUN JUL ' AUG

length equivalent to 1 J.Ll of solution. The sugar con-centration of the drops was indexed from the fluid's refractivity, which we measured in a hand-held refractometer. Drops were gathered from a different discrete area of trunk below 2 m in successive days for these measurements of drop size and refractivity.

From March 1986 we counted the number of wasps, honey bees,and bumblebees that were feeding on honeydew in the lower 2 m of each trunk on the face containing the honeydew quadrat of each monitored tree.

From August 1986largeflies were also counted. These counts were made at any time of the day when we first approached a sampling tree. From autumn 1986 onwards any known wasp or honey bee colonies in the study area were inspected in the middle of each month. A "traffic count" of the number of honey bees seen entering or leaving hives in 10 consecutive 1 min counts was recorded. The detailed feeding movements of wasps, honey bees, bumble bees, and flies were observed.

In August, October, and December 1986 and in April and June 1987 many anal tubes (on 5 to 15 different trees) which were not carrying a drop were nudged with a scalpel. If no drop appeared, the capsule itself was tapped with the scalpel. The proportion of tubes which instantly formed a drop was noted. We then cut into the capsule from which tubes emerged but which did not produce a drop after being nudged, and determined what was inside.

Temperatures were recorded on each day we were at the study area. We avoided sampling in heavy rain. Otherwise there was no attempt to make our measurements in or at a given time after particularly bad weather.

RESULTS Additions of new monitoring trees The confidence intervals around the mean number of anal tubes per qUadrat were so high in the frrst months of study (Fig: 2) that 10 new trees were marked and monitored from February 1986 onwards. One of the new trees died in late April 1986 and has therefore been excluded from all the results except where indicated. We compared the honeydew measurements on the 10 original trees with the 9 surviving new trees from February 1986 onwards using Kruskal Wallis tests. There were no significant differences (P >0.05) between groups for number of anal tubes,numberofdrops, the percentage of tubes carrying drops, or the size of the drops. The drops from the 10 original ttees had a significantly (P = 0.004) lower refractivity (x = 28.9%) than drops from the 9 surviving new ttees (x = 31.0%), but this Table 1 Average honeydew measurements and density of insects for all samples and trees.

Measurement Mean n SE Anal tubes! 2225 305 88 m1 of trunk

Honeydew drops! m1 of trunk

823 1225 30

Size of drops 0.43 1109 0.0089 ijl.1)

Refractivity 30.6 1086 0.44 (%)

Tubes carrying 27.7 305 1.14 drops (%)

Wasps! m10ftrunk

10.8 1427 0.67

Honeybees! 0.15 1384 0.025 m1 of trunk

Bumble bees! 0.022 1385 0.0062 m10ftrunk

Flies! 0.011 968 0.0042 m2 of trunk

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Moller & Tilley-seasonal use of honeydew by insects 293

Fig. 4 The mean number of honeydew drops per fIxed quadrat ineachmonth. Solid points Septem-ber 1985 to August 1986. Open points October 1986 to August 1987. >-

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difference is slight. Accordingly, values for honey-dew on all 19 trees are pooled for each month after January 1986 in Fig. 2-6 and Table 1.

Anal tubes The avemge number of anal tubes (with and without drops) was high in the winter and early spring and declined to a trough in late summer in both years (Fig. 2). This trough was lower in 1987 than in 1986. Peak numbers of tubes were lower in 1986 than in 1985 and 1987.

Overall, 68% of dropless tubes formed a drop when we gently nudged the tube or capsule. The proportion delivering a drop after being stimulated varied seasonally (r = 8.89, d.f. = 3, P <0.05; Table 2). Even those that failed to produce a drop when tapped were usually (89% of 228) connected to a

second- or third-instar insect (Table 2). This means that overall 96% of anal tubes were connected to a second or third feeding instar and could therefore potentially form a honeydew drop. The few capsules not containing a feeding instar contained a non-feeding adult and/or her eggs, dead instars, or appeared to be empty.

Although the majority of tubes were connected to a feeding instar in most months, fewer than half the anal tubes carried a drop (Fig. 3). The proportion carrying a drop varied erratically, with no seasonal consistency (Fig. 3).

Honeydew drops The number of drops present (Fig. 4) depends on the number of anal tubes (Fig. 2) and the proportion which carry a drop (Fig. 3). There were sporadic

Table 2 The number of anal tubes producing drops when nudged, and the contents of capsules where the tube did not produce a drop after being stimulated.

Contents of capsules where no drop formed Total % where 2{3 Dead

Month tubes drop formed instar instar Adult Eggs Empty Unknown

Aug 1986 260 65 80 0 1 1 6 3 Oct 1986 • • 47 0 2 0 2 0 Dec 1986 65 58 25 0 0 0 2 0 Apr 1987 50 82 8 0 1 0 0 0 Jun 1987 172 71 42 8 0 0 0 0 All months 547# 68# 202 8 4 1 10 3

• not measured # excludes Oct 1986

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FIg.S Themeandropsizeineach month. Solid points September 1985 to August 1986. Open points October 1986 to August 1987.

Fig. 6 The mean refractivity of honeydew drops in each month. Key as for Fig. 2. Insufficient honeydew could be gathered to measure refractivity in February 1987.

FIg. 7 The average number of wasps per mZ of trunk in each month. Solid points for 1986, open points for 1987.

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Moller & Tilley-seasonal use of honeydew by insects 295

Fig.S Themeannwnber(±9S% confidence interval) offeral honey bees leaving or entering four bee-hives in each month (upper) and the ambient air temperature at the time of the counts (lower).

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periods from May to October when the number of drops was bigh, and some intervening periods when numbers were low (Fig. 4). There were consistently few in spring and early summer but least of all in the late summer and autumn (February-April) in both years (Fig. 4). The February, March, and April numbers were about one tenth of the bighestrecorded in winter and spring.

The average drop size was large throughout the spring but declined rapidly in January to reach the smallest size between February and April of both years (Fig. 5). Drops were smaller in 1987 than in 1986 in this late summer and autumn period. The average drop during the autumn low point was about one eighth of the largest drop recorded.

The average refractivity of drops was generally low in summer, autumn, and early winter (Fig. 6).

The values were generally above 40% in winter and spring, with lower values presumably because of variations in the weather just before sampling.

Insect numbers By far the most abundant insects feeding on the honeydew were wasps, followed by feral honey bees, bumble bees, and flies, respectively (Table 1). The number of wasps rose dramatically in January and February and pealcedinMarch, when the highest density recorded was 283/m" in 1987 (Fig. 7; Appendix 1). There were nearly twice as many wasps in March and April of 1987 as in the same months of 1986. Virtually no wasps were seen on the trees after June in both years (Appendix 1).

Of 282 wasps swatted or collected in wasp traps (described by Sandlant & Moller 1989) in 1986,

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FIg.9 Scattergramofhoneydew drop size versus number of wasps per drop on 20 different trees in April 1986. The tree which died later that month is shown with an open dot.

49% were common wasps. In 1987, 97% of 422 collected were common wasps. The species of wasp to which each nest belonged was not determined in 1986, but 19 of the 20 nests in 1987 were found to be of common wasps.

The number of feral honey bees found on the monitored trees varied erratically (Appendix 1). They were absent from the honeydew trees during the period of high wasp numbers in January to April each year, despite the warm temperatures, but they appeared on even quite cold days in winter, spring, and early summer (Appendix 1). Counts of honey bees entering and leaving four nests in hollow beech trees were comparatively low in the wasp season (January to April) despite the warm temperatures (Fig. 8). The number of honey bees counted on honeydew trees correlated with the "traffic counts" of numbers leaving or entering nests in most months (Appendix 1 cfFig. 8). Moderate numbers of honey bees entered or left nests in August 1986andFebruary 1987 but did not appear on the honeydew trees then, presumably becausethebees foragedon floral nectar. Wasps were seen entering and leaving one of the feral nests in March 1987,presumably to steal honey.

New Zealand Journal of Zoology, 1989, Vol. 16

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FIg. 10 Scattergram of honeydew refractivity versus nwnber of wasps per drop in 20 different trees in April 1986. The tree which died later that month is shown with an open dot.

In 1986 three of six feral honey bee colonies died or moved over the wasp season; however, only one of the four colonies we counted in 1987 disappeared during or just after the period of wasp abundance.

Bumble bees fed on the honeydew trees during the period when there were most wasps, but flies were recorded only before and after the influx of wasps (Appendix 1). The counts for flies and bumble bees are too variable for us to discern whether there was any seasonal pattern (Appendix 1).

Ants were abundant on some honeydew trees. In most months they feed on drops spilled onto the bark. When the wasps were numerous we occasionally saw ants taking drops from the ends of anal tubes, perhaps because the tubes were then much shorter.

Insect behaviour Wasps and honey bees feed on honeydew in a variety of complex and fascinating ways. Sometimes they hover to take a drop from the end of an anal tube. They then fly between tubes in a direct manner. On other occasions they land on the tree surface to consume a drop encountered the instant before. The insects may then search by crawling or take wing again in search of another drop. At other times the

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Moller & Tilley-seasonal use of honeydew by insects 297

wasp or bee spends virtually all its time crawling over the trunk "lapping" the substrate, particularly in crevices. It is probably imbibing sugar from spilled honeydew drops. Drops are sometimes encountered and taken during this lapping mode of feeding, but often the animal passes within a millimetre of an anal tube without taking the drop.

Honey bees, wasps, flies, and bumble bees sometimes accidentally brush drops off the anal tubes onto their bodies or knock the drops onto the ground or substrate. They then groom themselves to remove drops stuck to their bodies. Bumble bees use their long proboscis to feed mainly in crevices; there appear to be more bumble bees on trees with deep crevices in their bark.

In March, April, and May large numbers of wasps fall out of the honeydew trees. A shower of falling wasps can be triggered with a wave of the hand, because some wasps have difficulty flying. Similarly, the wasps that hit the ground often have difficulty taking off again, cmwling away while beating their wings.

Honeydew and wasp numbers on different trees The way that some indicators of honeydew abundance decline with the appearance of huge numbers of wasps, and then increase again when the wasps decline (Fig. 2,4, 5, cf. 7) suggests that drop feeding by wasps depresses honeydew levels. We investigated this correlation in time by looking for a similar correlation in space. Trees with more wasps per drop tended to have smaller drops (r = 0.46, d.f. = 18, P <0.05; Fig. 9) in April 1986. There was no relationship between the number of wasps per drop and the refractivity of the drops (r = 0.01, dJ. = 18, P >0.10; Fig. 10).

DISCUSSION Anal tubes Since most anal tubes were connected to a second-or third-instar scale insect (Table 2), relict tubes must drop off soon after the moulting of the third instar into a non-feeding adult female or a male cmwler. This means that nearly all the tubes on the trees can potentially form a drop, which is then available for a variety of consumers. Counts of anal tubes are therefore a robust index of the theoretical maximum standing crop of drops for a given place and time. There was a decline from late spring to summer in both years at Trass (Fig. 2) and in Crozier's (1978) study at Mt Oxford in Canterbury; it may

represent a predictable seasonal event However, Crozier (1978) found a marked resurgence in tube numbers in autumn to peak in April/May and then a decline throughout the subsequent winter. There is no sign of such an autumn peak in numbers at Trass. Morales etal. (1988) found no significant differences in the proportions of the different female life stages in different months. However, of necessity, only a small number of quadmts were sampled in their study and they were not chosen randomly. More detailed in situ measurements are needed before we can assess the importance and predictability of pop-ulation fluctuations of the scale insects in determining the seasonal variation in honeydew resource levels.

The tubes can be broken off, probably by rain, but also by the consumers feeding on the drops. We have occasionally seen wasps break off an anal tube and carry it away. When harvesting drops the wasps appear to nibble at the tip of the anal tube, and we suppose that this gradually shortens the tubes so that they tend to be very short in the months when wasps are abundant Presumably this gradual shortening could remove the tube altogether, as could the occasional snapping off of a longer length of tube by the wasp. If so, the lower number of anal tubes in summer and autumn 1987 compared to 1986 may have resulted from higher densities of wasps in 1987 (Fig. 7; Appendix 1) and not entirely from the population dynamics of the scale insect itself. Until we have detailed measures of the mte of removal and regenemtion of anal tubes we will not know how important wasps and other predators are in reducing the numbers of anal tubes, and therefore of potential drops in summer and autumn. Number of drops Often, less than half the tubes were carrying a drop (Fig. 3), presumably because drops had been knocked off by rain and wind or removed by consumers. The rate of regenemtion of drops may also be partially determined by tree physiology and climate; evapo-transpiration and soil moisture may affect turgor pressures within the tree, which in turn may influence the speed with which drops reform after removal. The scale insect may passively siphon sap, but may also be partly able to control flow rate. The amount of fluid being siphoned by all the scale insects might itself affect tree physiology and subsequentrecharge mte. The proportion of tubes which instantly formed a drop when tapped (Table 2) varied significantly between months, which suggests that the rate of recharge varies seasonally. The influences of weather and varying recharge rates will have to be unravelled

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by future study. The proportion of tubes carrying drops has emerged as an important variable which fluctuates widely. Its determinants need to be under-stood before the variation in drop numbers can be modelled closely.

A decline in the number of honeydew drops in spring and early summer was recorded by Crozier (1978, 1981), Gaze & Clout (1983), and in this study. Otherwise, the seasonal patterns in all three studies of honeydew have been' quite different Crozier (1978) found a sharp increase in the number of honeydew drops (and tubes) in March and April in Canterbury, whereas this did not occur until Mayl June in our study. Clout & Gaze (1983) also had evidence of a minor resurgence in Marchi April but the peak number of drops was recorded in the pre-ceding spring. Since Gaze & Oout (1983) did not count the number of tubes we do not know if these differences reflect differences in the numbers of the scale insect in the second and third-instar, weather, orcroppingbyconsumers. More work will be needed to discern whether there is a predictable seasonal variation in honeydew, and to determine what causes the variation in seasonal patterns between areas. Quality of drops Drops in late summer and autumn were only an eighth the size of those in winter and spring (Fig. 5). Since some drops were so tiny as to be unmeasurable in February, March, and April the real difference was underestimated by these figures.

Refractivity is a reliable technique for measuring the sugar concentration of the drops (Beggs 1988). Honeydew tended to have a lower sugar concentration in summer, autumn, and early winter than in late winter and spring (Fig. 6). A similar pattern in refractivity was observed by Gaze & Oout (1983).

Drop size and refractivity can vary diurnally (Gaze & Clout 1983; Boyd 1987) and with height on the tree (Beggs 1988), so the measurements presented here from mid to late morning at 1.5 m height are only indices of changes in honeydew in the whole forest. Once the influence of weather on our measure-ments has beendetermined,aclearerseasonaI pattern in changing refractivity is likely to emerge. Wind and rain knock off drops, and moisture streaming down the tubes dilutes the honeydew in the drop. Undisturbed drops become stickier as water is evaporated in dry and windy conditions. Some of the drops resembled toffee after long stable periods in the winter. The time that a drop remains to undergo this process of concentration or dilution will be affected by consumer pressure. Therefore, the in-

New Zealand Journal of Zoology, 1989, Vol. 16

crease in consumer pressure (Fig. 7; Appendix 1) may have contributed to the generally lowerrefractiv-ity of the honeydew in the summer, autumn, and early winter months.

Whatever the cause of the observed changes, the smaller size of drops in summer and autumn, when combined with the low sugar concentration then, means that drops have considerably less than one tenth as much energy in summer and autumn than in winter and spring. Consumers harvesting the lower number of drops in late summer and autumn may not only find them harder to gather, but also far less energetically rewarding. Future work on foraging on honeydew will have to include consideration of drop quality and ease of consumption as well as abundance.

Insect behaviour Switches in feeding behaviour often result in differences in foraging efficiency, but we do not know whether the foraging decisions taken by honey bees and wasps maximise the rate of energy intake as proposed by optimal foraging theory (reviewed Krebs et al. 1983; Gray 1987). The most likely reason that so many wasps fall to the ground is exhaustion, although intoxication from fermenting honeydew splashed onto the tree trunk is also a possibility.

Close examination of wasps and honey bees while feeding shows that they knock the anal tube. They do this particularly when they crawl (rather than fly) between feeds and work their way along a tube to imbibe the drop from its tip. Sap flowed when we physically manipulated the anal tubes, and a similar mechanical stimulation of flow may result from the insects' feeding movements.

Wasp numbers Wasps are by far the most numerous foragers on honeydew between January and May, whereas feral honey bees are the predominant insect in spring and late autumn. Overall, there are very few insects eating the honeydew in winter.

The number of insects seen feeding on the honeydew trees may have varied because of changing meteorological conditions affecting the number of foragers outside nests, as well the number alive. Estimates of temperature thresholds for flight of common and German wasps have varied from 2°C to 15°C (Herold 1952; Taylor 1963; Potter 1965; Spradbery 1973), but Perrott (1975) noted some German wasp workers flying in temperatures as low

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Moller & Tilley-seasonal use of honeydew by insects 299

as 0.6°C near Nelson. Until detailed work is done in New Zealand we will not know whether there is a graded response of decreased flight activity with de-creasing temperature down to some (as yet unknown) temperature where flight ceases altogether.

There was amidsummer upswing to alate summer and autumn peak in the number of German wasps caught by Thomas (1960) at Hamilton and by Perrott (1975) at Tennyson Inlet in the Marlborough Sounds. The variety of baits and trapping techniques used precludes meaningful close comparison between these studies, but together they confIrm a huge seasonal pulse in numbers ofvespulid wasps,peaking in midsrimmerandearly autumn. In our study, wasps were not seen in midwinter and we found no evidence of perennial nests (Sandlant& Moller 1989), whereas Thomas (1960) and Perrott (1975) both reported over-wintering.

The extremely high densities of wasps may be a feature of the Nelson honeydew forests or of common wasps in general, or it may reflect particularly suitable weather conditions in the years of this study. The densities of common wasps may also be higher than normal because of their recent arrival. They were fustrecorded in Nelson in 1984 (Donovan 1984) and so may have only recently spread to our study area. However, the markings of common and German wasps are so similar that it is possible that common wasps predominated in the Nelson area long before they were fIrst recognised. Even if the common wasp has only justreached our study area, competition between the two species may mean that its appearance has been partly offset by a decline in the number of German wasps.

Wasps are notorious for their wide fluctuations in numbers from year to year (Akre & Reed 1981; Archer 1985). We have also noted a huge variation in wasp numbers between patches of honeydew-infested forest at anyone time within 20 kIn of our Trass site. The results of our honeydew study cannot be assumed to apply elsewhere until this variation in wasp numbers in time and space hasbeen investigated and can be predicted. Intensive study of vespine wasps in New Zealand is urgenL

Competition between wasps and feral honey bees The flight activity of honey bees increases with tem-perature, but is also affected by light intensity and perhaps relative humidity, rain, wind speed, and feeding conditions (Lundie 1925; Gary 1967; Wratt 1968; Nunez 1977; Szabo 1980; Burrill & Dietz 1981). The counts of honey bee numbers entering and leaving nests will have been a function of the

number of bees in the COlony as well as these clima-tological and food constraints on flight activity. We found feral bees flying in comparatively large numbers at ambient air temperatures as low as 5.9°C in winter (Fig. 8), whereas Burrill & Dietz (1981) record an absolute lower threshold for flight at 9 .OOC. Perhaps colonies acclimatise their flight activ-ity to local weather, or perhaps they are forced to forage in marginal weather conditions if foodreserves are low.

Counts of honey bees on tree trunks correlate with the honey bee "traffIc" in and out of nests (Fig. 8; cf Appendix 1). The correlation also suggests that honeydew is the major food of feral honey bees living in theforesL WecanthereforeplaceconfIdence on the seasonal patterns of counts on trees (Appendix I), despite their variability.

The comparative lack of foraging by the honey bees in late summer and early autumn was not because of temperature, since the days were warm then (Fig. 8; Appendix 1). Boyd (1987) noted the same decrease of honey bees when the number of wasps increased markedly in January and February 1986 at Trass. Honey bee activity increased in late autumn of 1987, after the wasps disappeared and the honeydew had again increased.

These correlations indicate a strong competitive interaction between honey bees and wasps. Beekeep-ers believe that honey bees stay in their hives to protect their honey store when many wasps are about. Such guarding may contribute to the low numberofbeesoutforaging, but the lack of honeydew at this time may make foraging impossible or un-rewarding. This switch from food gathering to staying in the nest is likely to have caused most of the sea-sonal fluctuation in the numbers of foragers (Fig. 8; Appendix 1) rather than simply reflecting fluctuations in the number of honey bees in the colony. The latter probably also occurs, in part because workers are preyed on by wasps when away from the hive (pers. obs.). The feral honey bee colonies are somewhat buffered from the effects of wasps on honeydew so long as their store of pollen and honey is suffIcient to continue rearing broods and to keep the nest-bound adults alive. High numbers of wasps may have triggered the demise of three of the six honey bee colonies we observed in the 1986 autumn. but we have no data on the longevity or performance of feral honey bee colonies in New Zealand with which to compare our fmdings.

The economic impact of wasps on beekeeping is usually considered to be because of the loss of hives which are robbed of honey already gathered (Walton

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& Reid 1976). Our study suggests that a loss of prod-uction caused by wasp competition is also a potential-ly serious problem for the honeydew honey industry. Impact of wasps The seasonal variation in the size of honeydew drops correlates closely with the abundance of wasps. A tree with more wasps per drop will have its drops visited more often by wasps; its drops will not last as long, and will therefore have less time to grow large. The significant negative correlation between drop size and wasps per drop at one time (Fig. 9) therefore suggests that the seasonal changes in drop size are driven by wasps (Fig. 5). Drops in April were also smaller in 1987 than in 1986, which may have been because there were more wasps in 1987 (Fig. 7). Correlations between wasp numbers and the numbers of anal tubes, the proportion of tubes carrying drops, and refractivity are less strong. Stronger correlations may yet emerge once we can account for the effects of weather and season, but wasps may haverelatively little influence on these honeydew parameters. The total lack of acorrelation in space between refractivity and wasps per drop (Fig. 10) may indicate that consumption by wasps has relatively little impact on this parameter of honeydew quality, in particular. Alternatively, wasps may depress refractivity but any effect of differential predation by wasps may be swamped by a greater variation in honeydew refrac-tivity between trees as a result of tree physiology or site factors. Wasps may be attracted more to trees with sap of higher sugar concentration, even when the effect of many con specifics feeding there is to depress the sugar concentration of the sap that would otherwise have been obtained. Exclosureexperiments are now in progress to test these possibilities, and to prove whether the correlations we observed in time and space with the other honeydew parameters and wasp numbers are causally linked. In the meantime the correlations provide circumstantial evidence that the huge wasp numbers observed had a strong damp-ening influence on the amount and quality of honey-dew available between February and May.

Anon. (1952) drew attention to the possibility of German wasps competing with birds, particularly tui and bellbirds,fornectar andfruil Ourresults, and those of Beggs (1988) and Beggs & Wilson (1987), provide quantitative evidence for a large impact of common and German wasps on honeydew abundance in Nelson's Nothofagus forests. Donovan (1978) and Thomas (1987) draw attention to the possibility that predation on insects by vespine wasps may significantly depress the numbers of insects in New

New Zealand Journal of Zoology, 1989, Vol. 16

Zealand's forests. The huge densities of common and German wasps, indicated by this study, make such an impact likely. This raises concern for the conservation of native insects. The insects and both nectarivorous and insectivorous birds may also be drastically affected by predation and competition for food with the two species of introduced vespine wasps. The effect of this latest addition of a hugely successful introduced animal should be seen as add-ing to the ravages of introduced mammals (reviewed by Gibb & Flux 1973) and habitat despoilation that have been imposed on endemic forest communities since humans colonised New Zealand's shores.

ACKNOWLEDGMENTS Peter Gaze and Bruce Thomas helped set up the Trass study area. They and ShaarinaBoyd contributed to observa-tions and discussions on honeydew and its use at Trass. DavidGlennie describedthevegetationin the area. Baigents Forest Industries own the study area and have fully co-operated throughout. The Canterbury Beekeepers Associa-tion lent us a refractometer for the study. Jacqueline Beggs, Lisa Crozier, John Flux, Peter Gaze, and Tony Pritchard commented on an earlierdraftofthis manuscript. The Department of Conservation partly funded the work in 1987.

REFERENCES Akre, R. D.; Reed, H. C. 1981: Population cycles of

yellow jackets (Hymenoptera: Vespidae) in the Pacific northwest. Environmental entomology 10: 267-274.

Anon. 1952: European wasp. Notornis 4: 23. ---1979: Beech honeydew honey - a vast

potential. New Zealand beekeeper 40: 6-9. Archer, M. E. 1985: Population dynamics of the social

wasps Vespula vulgaris and Vespula getmanica in England. JOUTruzl of animal ecology 54: 473-485.

Beggs, 1. R. 1988: Energetics ofkaka in a South Island beech forest. UnpublishedMSc thesis, University of Auckland, Auckland, New Zealand.

Beggs, J. R.; Wilson, P. R. 1987: Energetics of South Island kaka (Nestor meridioruzlis meridioruzlis) feeding on the larvae of kanuka longhorn beetles (Oc/vocydus huttoni). New Zealand journal of ecology 10: 143-147.

Boyd, S. A. 1987: Patterns of use of beech honeydew by birds and insects. UnpUblished MSc thesis, University of Auckland, Auckland, New Zealand

Burrill, M.; Dietz, A. 1981: The response of honey bees to variations in solar radiation and temperature. Apidologie 12: 319-328.

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Clout, M. N. 1984: Improving exotic forests for native birds. New Zealand journal of forestry 29: 193-200.

Clout, M. N.; Gaze. P.D. 1984: Effects of plantation forestry on birds in New Zealand. Journal of applied ecology 21: 795-815.

Crozier, L. 1978: A study of beech honeydew in Oxford State Forest. Unpublished BForSc thesis, University -of Canterbury, Christchurch, New Zealand.

Crozier, L. R. 1981: Beech honeydew: forest produce. New Zealandjournal offorestry 26: 200-200.

Donovan, B. 1. 1978: The German wasp, Vespula germanica (F.) (Hymenoptera: V espidae) in New Zealand. In: Smith, J. (Compiler). Papers presented at honeydew seminar, Christchurch, August 1978. Christchurch, New Zealand, Ministry of Agriculture and Fisheries. pp.49-63.

---1984: Occurrenceofthecommonwasp, Vespula vulgaris (L.) (Hymenoptera: Vespidae) in New Zealand. New Zealand journal of zoology 11: 417~27.

Gary, N. E. 1967: Diurnal variations in the intensity of flight activity from honeybee colonies. Journal of apicultural research 6: 65-68.

Gaze, P. D.; Clout, M. N. 1983: Honeydew and its importance to birds in beech forests of South Island, New Zealand New Zealand journal of ecology 6: 33-37.

Gibb, J. A; Flux, J. E. C. 1973: Mammals. In: Williams, G.R. ed., The natural history of New Zealand. Wellington, Reed. pp. 334-371.

Gray, R. D. 1987: Faith and foraging: A critique of the 'Paradigm argument from design'. In: Kamil, A.C.; Krebs, J.R.; Pulliam, H.R. ed., Foraging behaviour. New York. Plenum Press. pp. 69-140.

Herold, W. 1952: Beobachtungen uber die Arbeitstung einiger Arbeiter von Vespa germanica F. -Dolichovespula germanica (F.). Biologisches zentralblatt71: 461~69.

Krebs, J. R.; Stephens, D. W.; Sutherland, W. J. 1983: Perspectives in optimal foraging. In: Brush, A. H.; Clark. G. A. Jr. ed., Perspectives in ornithology. Cambridge University Press. pp. 165-216.

Lundie. A E. 1925: The flight activities of the honeybee. Bulletin of the United States Department of Agriculture no. 1328.

Moller, H.; Tilley, J. A. V. 1986: Honeydew. a South Island beech forest resource. New Zealand DSIR Alpha no. 58.

Morales, C. F.; Hill, M. G.; Walker. A K. 1988: Life history of the sooty beech scale (Ultracoelostoma assimile) (Maskell), (Hemiptera: Margarodidae) in New Zea1andNothofagus forests. New Zealand entomologist 11: 24-37.

Nunez, J. 1977: Circadian variation of flight activity in colonies of Apis mellifera ligustica. Journal of insect physiology 23: 387-392.

Perrott, D. C. F. 1975: Factors affecting use of Mirex-poisoned protein baits for control of European wasp (Paravespula germanica) in New Zealand. New Zealandjournal of zoology 2: 491-508.

Potter, N. B. 1965: Some aspects of the biology of Vespula vulgaris L. UnpUblished PhD thesis. University of Bristol, Bristol, United Kingdom.

Sandlant, G. R.; Moller, H.1989: Abundance of common and German wasps (Hymenoptera: Vespidae) in the honeydew beech forests of New Zealand in 1987.NewZealandjournalofzoology 16: 333-343.

Smith, J. (compiler) 1978: Papers presented at honeydew seminar, Christchurch, August 1978. Christchurch, New Zealand, Ministry of Agriculture and Fisheries.

Spradbery, J. P.1973: Wasps, an account of the biology and natural history of solitary and social wasps. Seattle, University of Washington Press.

Szabo, T.!. 1980: Effect of weather factors on honeybee flight activity and colony weight gain. Journal of apicultural research 19(3): 164-171.

Taylor, L. R. 1963: Analysis of the effects of temperature on insects in flight. Journal of animal ecology 32: 99-117.

Thomas, B. W. 1987: Some observations on predation and scavenging by the introduced wasps Vespula germanica and V. vulgaris. The weta 10: 59-61.

Thomas. C. R. 1960: The European wasp (Vespula germanica F AB) in New Zealand. New Zealand DSIR information series no. 27.

Walton, G.M.;Reid, G.M.1976:The 1975 New Zealand European wasp survey. New Zealand beekeeper 38: 26-30.

Wratt, E. C. 1968: The pollinating activities of bumble bees and honey bees in relation to temperature, competing forage plants, and competition from other foragers. Journal of apicultural research 7(2): 61-66.

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302 New Zealand Journal of Zoology, 1989, Vol. 16

APPENDIX! Appendix 1 CoWllS of wasps, honey bees, bumble bees andflies/m2 of tree trunk in each month and the ambient air lemperablre during the COWllS.

Feral Air honey Bumble lemperature

Year Month Statistic Wasps bees bees Flies (0C)

1986 Mar i 30.80 n 42 SE 3.26 range 0-117.0

Apr I 18.02 0 0 11.6 n 76 76 76 SE 1.41 0 0 range 1.3-50.0 0 0 10.5-12.4

May i 2.44 0.10 0 8.8 n 76 76 76 SE 0.25 0.048 0 range 0-10.1 0-2.9 0 7.6-10.3

Jun i 1.21 0 0 5.5 n 56 56 56 SE 0.18 0 0 range 0-4.3 0 0 3.8-7.3

Jul i 0 0.44 0 5.7 n 76 76 76 SE 0 0.30 0 range 0 0-21.7 0 4.1-10.0

Aug I 0 0 0 6.0 n 76 76 76 SE 0 0 0 range 0 0 0 5.3-6.8 I 0.060 0.018 0.012 0.014 13.1 n 152 152 152 95 SE 0.023 0.012 0.012 0.014 range 0-1.8 0-1.3 0-1.8 0-1.3 11.3-17.2 I 0.076 0.61 0 0.048 18.7 n 152 152 152 152 SE 0.029 0.095 0 0.021 range 0-2.7 0-6.8 0 0-1.8 13.8-24.7

1981 Jan i 15.64 0 0.054 0 14.0 n 57 57 57 57 SE 2.05 0 0.038 0 range 0-84.9 0 0-1.8 0 11.7-15.7

Feb I 27.95 0 0.22 0 21.0 n 113 113 113 113 SE 2.22 0 0.068 0 range 0-118.4 0 0-4.2 0 15.0-24.6

Mar I 57.75 0 0 0 18.5 n 95 95 95 95 SE 5.86 0 0 0 range 1.3-282.9 0 0 0 15.7-22.3

Apr i 35.33 0 0 0 14.6 n 76 76 76 76 SE 3.38 0 0 0 range 2.6-143.7 0 0 0 8.5-17.9

May i 2.46 0.044 0 0 9.4 n 76 76 76 76 SE 0.36 0.025 0 0 range 0-13.2 0-1.4 0 0 6.8-12.3

Jun i 0.74 0.036 0 0 6.2 n 133 133 133 133 SE 0.14 0.021 0 0 range 0-10.1 0-2.1 0 0 2.1-11.1

Jul 1 0.028 0 0 0 6.4 n 76 76 76 76 SE 0.028 0 0 0 range 0-2.1 0 0 0 5.8-7.6

Aug i 0 0.60 0.012 0.020 10.1 n 95 95 95 95 SE 0 0.20 0.012 0.020 range 0 0-13.7 0-1.14 0-1.89 8.0-13.1

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