Biological Conservation 99 (2001) 17±28 www.elsevier.com/locate/biocon

The ecological consequences of social wasps (Vespula spp.) invading an ecosystem that has an abundant carbohydrate resource

J. Beggs * Landcare Research, Private Bag 6, Nelson, New Zealand

Abstract Introduced Vespula wasps have successfully invaded beech (Nothofagus) forests in New Zealand. By collecting honeydew, an abundant carbohydrate resource, wasps can reach high numbers. Honeydew is produced by an endemic scale insect which infests about 1 million hectares of land, 15% of New Zealand's remaining native forest. At the peak of the wasp season, honeydew beech forests had an average biomass of about 3.8 kg of introduced wasps haÀ1 (10,000 workers haÀ1). These abundant invaders reduce the standing crop of honeydew by more than 90% for 5 months of the year and so compete with native species (such as birds and invertebrates) that also consume honeydew. The behaviour of three species of native bird is a€ected by this reduction in honeydew, but it is unknown if this a€ects the survival or reproductive success of these birds. Nevertheless, to avoid altering the birds' beha- viour, wasp density should not increase above a level where wasps revisit honeydew threads more than once every 180±400 min. Additionally, the predation rate of wasps on some invertebrate prey species is so high that the probability of an individual surviving through the wasp season is virtually nil. Hence wasps probably reduce or eradicate populations of some invertebrates. Wasp abundance needs to be reduced by 80±90% to conserve some native invertebrate species. Wasps could also a€ect nutrient cycling in the honeydew beech forest community by reducing the ¯ow of carbon to micro-organisms in the phyllosphere and the soil, which ultimately could a€ect soil solution chemistry. Current control tools are unable to reduce wasp populations over large tracts of forest. The challenge is to identify and develop new control techniques to achieve widespread control for conservation gains. The impact of introduced social wasps provides a warning of the damage exotic ants could cause if they were to invade honeydew beech forest. New Zealand needs to be vigilant to reduce the risk of an invasion by ants or other social wasps. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: Biological invasion; Competition; Predation; Ecosystem processes; Honeydew; Vespula

1. Introduction vascular plants (Ministry for the Environment, 1997). Some of these aliens have become threats to native spe- Invasion biology and biosecurity is of increasing cies and ecosystem functioning. importance internationally as people and their asso- Increasingly, land-managers have to decide which ciated pests encroach on virtually every habitat and species (or genetically modi®ed species) are safe to ecosystem. The ecological processes and biodiversity of import, and which species should take priority for con- many invaded habitats and ecosystems are under threat, trol e€orts. Such decisions are hampered by the lack of in part because of the invasion of exotic species (e.g. a robust theory of invasion biology (Townsend, 1991). Loope and Mueller-Dombois, 1989; Ramakrishnan and To build such a theory requires a greater knowledge not Vitousek, 1989). Throughout New Zealand, more than only of what makes a species invasive, but also how 4300 introduced species have become established in the introduced species a€ect native species (Simberlo€, 1990). wild, including 90 species of vertebrates, perhaps 2200 Certain classes of introduced species are prone to species of invertebrates, and more than 2000 species of have e€ects throughout the receiving community (Sim- berlo€, 1990). Many social insects are in this category because they are polyphagous, and their reproductive * Corresponding author and dispersal characteristics make them particularly E-mail address: [email protected] e€ective invaders (Moller, 1996). They can pose a threat

0006-3207/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(00)00185-3 18 J. Beggs / Biological Conservation 99 (2001) 17±28 to their host community, causing changes in community coated with a black sooty mould [probably Capnocybe composition (Howarth, 1985; Wojcik, 1994; Moller, novae-zealandiae (Hughes); Morales et al., 1988] which 1996), and this has the potential for ¯ow-on e€ects to is maintained by the honeydew. The mould provides ecological processes. food for many arthropods (Morales et al., 1988), which Two species of introduced Vespula wasp have estab- in turn are consumed by other animals. It is probable lished in New Zealand Ð German wasps [Vespula ger- that honeydew promotes the growth of a variety of manica (Fabr.), Hymenoptera: Vespidae] arrived in other micro-organisms. This has been well demon- 1945, but were displaced in some forests by common strated for micro-organisms in the phyllosphere and the wasps [V. vulgaris (L.)] which arrived in the late 1970s soil in northern hemisphere communities where honey- (Clapperton et al., 1989, 1994). Common wasps are now dew is present (Dighton, 1978; Dik et al., 1991; Stadler abundant in New Zealand beech (Nothofagus spp.) for- and MuÈ ller, 1996; Stadler et al., 1998). Micro-organisms ests infested by the honeydew-producing native scale a€ect several ecosystem processes in Europe, such as insects Ultracoelostoma assimile (Maskell) and U. brit- throughfall of dissolved organic carbon, and nitrogen tani (Morales; Margarodidae: Homoptera; Thomas et ¯uxes (Stadler and Michalzik, 1998; Stadler et al., 1998; al., 1990). The term `honeydew beech forest' refers to Michalzik et al.,1999). It is possible that honeydew beech forest infested with the scale insects. Honeydew, plays a similar key role in nutrient cycling in New also an important food resource of many native verte- Zealand honeydew beech forests. brate species (Gaze and Clout, 1983; Clout and Gaze, Honeydew is by far the most abundant nectar-like 1984; Beggs and Wilson, 1987; Moller and Tilley, 1989), resource in beech forest and is consumed by a range of provides an abundant food resource that allows social birds, lizards and invertebrates (Fig. 1; Gaze and Clout, wasps to reach very high numbers and have a major 1983; Clout and Gaze, 1984; Beggs and Wilson, 1987; predation impact on some native invertebrate species Moller and Tilley, 1989). For instance, kaka (Nestor (Harris, 1991; Toft and Rees, 1998; Beggs and Rees, meridionalis meridionalis), a native parrot, can obtain 1999). Therefore, wasps may also have a competitive their daily energy requirement by feeding on honeydew e€ect on native species, especially birds. for about 3 h (Beggs and Wilson, 1991). In the northern Common wasps in honeydew beech forest have been hemisphere more than 250 invertebrate species are the focus of more than a decade of research to docu- known to consume honeydew (Zoebelein, 1956), but ment their spread, population dynamics and impact, there are relatively few published accounts of native and to develop tools to reduce their abundance. While invertebrates feeding on New Zealand honeydew. In the initial impetus for the work was fuelled because of many parts of the world ants form the dominant group their direct e€ect on humans, there is now increasing in the guild of invertebrate honeydew consumers (HoÈ ll- concern over their impact on natural habitats. The dobler and Wilson, 1990). In New Zealand ants do feed principal cause of this impact in honeydew beech forest on honeydew, but they are not numerous (personal is the plundering of a key resource Ð honeydew. The observation), nor has their relationship with honeydew aim of this review is to summarise what is known about the impact of wasps in beech forests, to identify critical gaps in our knowledge, and to identify important les- sons from the wasp invasion of New Zealand, particu- larly with respect to potential future invaders.

2. The honeydew resource

Honeydew is the sugary exudate produced by scale insects that infest black beech (Nothofagus solandri var. solandri), mountain beech (N. solandri var. cli€ortioides), red beech (N. fusca), and hard beech (N. truncata), but rarely silver beech (N. menziesii). Encapsulated second and third larval instars insert their stylet into the phloem vessels of the host tree, and excrete excess carbohydrate via a waxy anal ®lament protruding from the tree (Mor- ales et al., 1988; Morales, 1991). This honeydew is rich in carbon (mostly fructose, sucrose, glucose and oligo- Fig. 1. Overview of the major interactions in¯uenced by introduced Ves- saccharides) but low in protein (Grant and Beggs, 1989). pula wasps in beech forest infested with honeydew producing scale insects. Honeydew provides a major energy source at several Many of the interactions involve predation and competition. Dotted lines trophic levels (Fig. 1). Honeydew trees are typically indicate interactions that have received little or no scienti®c study. J. Beggs / Biological Conservation 99 (2001) 17±28 19 been studied. Furthermore, there are only a few species (6 300 000 ha; Newsome, 1987). Increasing the rainfall of native ant in New Zealand (Valentine and Walker, limit by 500 mm per annum only slightly increased the 1991). In many New Zealand honeydew beech forests, area estimate (by 2%), but decreasing rainfall by 500 the most dominant honeydew feeders are now intro- mm decreased the area estimate by 18%. This lower duced social wasps (Moller and Tilley, 1989). Other limit excluded most of the West Coast (where honeydew exotic insects feeding on honeydew can also become is present, e.g. Kelly, 1990), so a 3000 mm rainfall limit numerous, e.g. feral honeybees (Apis mellifera (L.), gives a distribution closer to the observed one. I have Hymenoptera: Apidae) up to 21.7 mÀ2 tree trunk and observed the scale insects at higher altitudes than the bumble bees (Bombus spp., Hymenoptera: Apidae) up criterion used here (800 m a.s.l.), so the estimate may be to 4.2 mÀ2 (Moller and Tilley, 1989). However, during conservative in this respect. However, the scale insects the wasp season (January±April) the density of social may not occur in some of the forests indicated, or only wasps is usually two to three orders of magnitude higher occur at low densities, so this means I may have over- than these species (Moller and Tilley, 1989). estimated the resource. On the other hand, light infes- tations of honeydew are found in other parts of the 2.1. Distribution country, including the North Island (Wardle, 1984). Data on its distribution, or the species producing it in The scale insects are most common in the northern these areas are limited. Survey work is required to South Island, on the eastern side from Mount Somers determine the real extent of this resource. northwards, and on the western side from Greymouth northwards (Crozier, 1981; Wardle, 1984). However, the 2.2. Abundance insect's distribution is very patchy (Kelly, 1990), and it is absent from entire catchments [such as the Wilber- Scale insect densities vary between sites. Estimates force and Harper-Avoca (Crozier, 1981)]. It becomes range from about 1Â105 haÀ1 in Westland (Kelly, 1990) uncommon above approximately 800 m a.s.l (Belton to about 2Â107 scale insects haÀ1 in Canterbury (Cro- and Crozier, 1979; Crozier, 1981; Beggs, 1991). Popula- zier, 1978) and up to between 3Â105 haÀ1 (Beggs, tion densities tend to be highest in areas of low to moderate rainfall (Belton, 1978; Crozier, 1978). A geographic information system (GIS) was used to model the distribution of the scale insect using these published criteria. Areas of forest containing beech, beech-scrub mixtures, and beech-grassland mixtures as portrayed in the Vegetative Cover Map of New Zealand (Newsome, 1987) were ®ltered in a sequence of overlays to exclude those areas outside the geographic or ecolo- gical range of the insects. The southern geographic limit was approximated by a sequence of roads, railways and ridgelines extending from Greymouth on the west coast to a point on the east coast about 150 km south of Greymouth (Fig. 2). The catchments known not to support scale insect populations were excluded using digital catchment boundaries originally delineated from 1:63 360 scale topographic maps (Water and Soil Direc- torate of the former Ministry of Works and Develop- ment). The altitudinal criterion was addressed using the 1:250 000 scale Digital Topographic Database devel- oped by Land Information New Zealand. The refer- ences to low-moderate rainfall (Belton, 1978; Crozier, 1978) were not quanti®ed, but, based on ®eld observa- tions, the annual rainfall limit was set at 3000 mm. Areas with rainfall greater than this were excluded using the surfaces of Giltrap (1993). This method provided a crude estimation of the land area where honeydew is available as a resource, com- prising some 1 000 000 ha (Fig. 2). Therefore, honeydew Fig. 2. Shaded areas estimate the distribution of honeydew-producing scale insects, Ultracoelostoma assimile and U. brittani. See text for beech forest represents about 15% of the approximate details of criteria and boundaries used to model their distribution extent of indigenous forest cover in New Zealand using a geographic information system. 20 J. Beggs / Biological Conservation 99 (2001) 17±28 unpublished data) and 2Â106 haÀ1 (Moller et al., 1996b) crop renewal rate is a good ®t except for very short (<1 in Nelson. The density of the scale insects per tree is also h) cropping times as it predicts complete elimination of highly variable, with tree species, tree size, altitude, the honeydew if threads are cropped more frequently aspect, and proximity to forest edge all playing a role than once every 38 min. This is not what has been (e.g. Crozier, 1978; Wardle, 1984; Kelly, 1990). Thus, observed to happen, hence the function is inferred to there are reports ranging from 5 insects mÀ2 tree trunk ¯atten out sometime between 0±1 h cropping time to more than 2000 mÀ2 (Moller and Tilley, 1989; Kelly, (Moller et al., 1996a; Fig. 3). 1990). This leads to a variation in the number of drops Belton (1978) estimated daily production to be ®ve mÀ2 tree trunk, which accounts for most of the varia- times the standing crop and estimated that 20±40% of tion in the standing crop of honeydew (Moller et al., all carbon ®xed by the beech trees may be lost through 1996b). Additional survey work is required to quantify honeydew. However, Kelly et al. (1992) calculated that the abundance of scale insects in honeydew beech forest. during daylight hours, honeydew production was 11.5 At the moment, honeydew beech forest includes forests times the mean standing crop, and that beech trees may with only trace amounts of honeydew, and forests where lose more than 80% of their carbon via honeydew. We honeydew is very abundant. need better data on seasonal production (including Honeydew production varies seasonally (Moller and sugar concentration) of honeydew to obtain a reliable Tilley, 1989), temporally (Gaze and Clout, 1983; Kelly ®gure on this. et al., 1992) and with prevailing weather (Moller and Tilley, 1989). Honeydew production per insect and insect density are positively correlated, with a mean volume of honeydew produced per insect over 24 h of 0.17 ml (95% C.I. 0.15±0.18; Kelly et al., 1992). Total annual production for Ultracoelostoma spp. is not known because the only measurements made (Kelly et al., 1992) did not include sugar concentration or annual variation. However, assuming honeydew production is the same throughout the year (based on a 24 h mea- surement at one site in August), and given the range of insect densities recorded, then about 6±1200 litres of honeydew are produced haÀ1 yearÀ1. In northern hemisphere forests, honeydew production has been found to be dependent on aphid age, plant developmental stage, and temperature. On Norway spruce [Picea abies (L.) Karst.], the average amount of honeydew produced by Cinara spp. was 0.165 mg aphidÀ1 dayÀ1 (dry mass; Stadler et al., 1998). The total honeydew production for 70±80 year old trees is esti- mated to be 400±700 kg fresh mass haÀ1 yearÀ1 (ZwoÈ l- fer, 1952; Zoebelein, 1954; Ecklo€, 1972 quoted in Stadler et al., 1998). The New Zealand honeydew resource may be greater haÀ1 yearÀ1 than in the north- ern hemisphere since the scale insect produces honey- dew year-round, whereas the aphids are seasonal. There are measures of standing crop, and these com- monly include drop volume and sugar concentration (e.g. Gaze and Clout, 1983; Moller and Tilley, 1989; Beggs and Wilson, 1991). Both variables decrease sig- ni®cantly during summer/autumn when wasps are pre- sent, but have a value of around 60 ml dropÀ1 and 40% refractivity outside the wasp season (Moller and Tilley, 1989). Exclosures have been used to measure the rate of renewal of the standing crop (Moller et al., 1996a). Full drop size was reached after 24 h, but after 3 days the Fig. 3. Logarithmic (a) and semi-log (b) plots to predict honeydew standing crop was only 74% of its 10-day value (Fig. 3) standing crop at successively longer periods after cropping (r2=0.932). because the number of drops and sugar concentration The error bars are 95% con®dence intervals from 6 beech trees. increased more slowly. The logarithmic shape to standing Figure from Moller et al. (1996a). J. Beggs / Biological Conservation 99 (2001) 17±28 21

3. Wasps Assuming 1 million ha of forest are infested with honeydew-producing scale insects (Fig. 2), then this also 3.1. Wasp distribution and abundance approximates the extent of forest infested with high numbers of wasps. Wasps have been recorded in den- Common and German (V. germanica) wasps are now sities up to 370 wasps mÀ2 of tree trunk in such forest distributed throughout New Zealand in a wide range of (Moller et al., 1991a). Average nest density was habitats (Clapperton et al., 1989, 1994), and over a wide 11.2Æ0.3 (standard error) haÀ1 in seven honeydew range of altitudes (Beggs, 1991; Fordham, 1991). How- beech forest sites measured for 10 years (Beggs, unpub- ever, common wasps have displaced German wasps lished data). However, there is enormous spatial and from honeydew beech forest (Harris et al., 1991). This temporal variation in abundance. Nest densities for 19 may be because common wasps are more ecient at honeydew beech forest sites measured in 1989 ranged harvesting honeydew (Harris et al., 1994). Common from 1 to 33 nests haÀ1 (Thomas et al., 1990). Wasp wasps collect honeydew at a faster rate than German nest density also varies from year to year, ranging wasps, and spend less time lapping honeydew (which between 8 and 34 wasp nests haÀ1 in 4 years at one site has often fermented) from the trunk when the standing (Beggs et al., 1998). crop of honeydew is low, so that fewer of them become lethargic and less e€ective feeders. This may have a 3.2. Wasp impact on honeydew ¯ow-on e€ect to queen production and ultimately result in a greater proportion of common wasps in honeydew Between 50 and 65% of foraging wasps collect hon- beech forests (Harris et al., 1994). However, species eydew, and they are able to carry loads of about 15 mlof speci®c usurpation of spring nests has not been investi- honeydew at a time (Harris, 1991). Thus, the estimated gated and may provide an additional, or alternative, intake of honeydew was between 80 and 340 l haÀ1 mechanism for species replacement (Harris et al., 1994). yearÀ1 at two sites, depending on the density of wasps Wasps are more prevalent where there is honeydew. (Harris, 1991). This may be about 70% of the annual Wasp numbers were indexed using 20 traps baited with honeydew production (Table 1). sardine catfood at 25 sites in the northern South Island. The number, size and sugar concentration of honey- Traps were hung at chest height at 10 m intervals for 24 dew drops varies seasonally, reaching a low in late hours once a week during the summer/autumn of 1990 summer and autumn, which coincides with peak wasp (Beggs et al., 1990). Traps in honeydew beech forest abundance (Moller and Tilley, 1989; Moller et al., caught many more wasps than traps in sites without 1996b). Exclosure experiments have demonstrated that honeydew (Fig. 4; Mann±Whitney U-test P<0.05). wasps are responsible for this reduction in the amount Wasp abundance was also indexed along a 2-km altitu- of honeydew available (Beggs and Wilson, 1991; Moller dinal transect at one site, and was found to be higher et al., 1991a). Wasps reduced the standing crop of hon- where honeydew was more abundant (Beggs, 1991). eydew by more than 99% for about 4 months, and 90% for a further 2 months (Moller et al., 1991a). Standing crop is continually renewed, but wasp density is often too high for it to recover to anywhere near its 10-day value (Moller et al., 1996a). Sometimes the scale insect produces another drop of honeydew if it is gently tapped (Moller and Tilley, 1989), suggesting that physical factors such as capillary

Table 1 Production of honeydew by Ultracoelostoma spp. and consumption of resources by introduced Vespula wasps in honeydew beech forest (see text for how variables were estimated)

Honeydew production (l haÀ1 yearÀ1) 6±1200

Wasp consumption Honeydew (l haÀ1 yearÀ1) 80±340 Invertebrates (kg haÀ1 yearÀ1) 1.4±8.1

Density Scale insects (haÀ1)1Â105±2Â107 Fig. 4. Number of wasps caught at honeydew and non-honeydew sites Wasp nests (haÀ1) 1±34 in the northern South Island in 1990. 22 J. Beggs / Biological Conservation 99 (2001) 17±28 action and turgor pressure may a€ect ¯ow rates. In While it is likely that wasps limit the abundance of certain circumstances the honeydew becomes so viscous some invertebrate prey species, it is not known the that it resembles to€ee (Moller and Tilley, 1989; Kelly et degree to which they reduce prey density. Wasp density al., 1992) and the anal ®lament becomes plugged. Clip- probably does not change as density of a particular ping the ®lament causes the exudation of fresh honey- species declines because there are plenty of alternative dew (Moller et al., unpublished observation). Rain has a prey species. However, the functional response of wasps similar e€ect (Moller et al., 1996a). During the wasp to prey density is unknown. The composition of prey season, wasps revisit the threads so frequently that the orders in the diet of wasps varied between some seasons honeydew does not concentrate as it would do nor- and some years (Harris, 1991), suggesting that the mally, and thus the scale insect probably produces more availability of di€erent prey species a€ected the diet of honeydew than it would without wasps. wasps. It is possible that wasps switch to other prey species when the abundance of a prey species becomes 3.3. E€ect of wasps on invertebrates low. This means some prey species may be kept at low density by wasps, but not eradicated. The abundance of carbohydrate food in honeydew There is anecdotal evidence that wasps have greatly beech forests supports high numbers of wasps, and reduced the abundance of some invertebrate species. A hence consumption of large quantities of protein food New Zealand Forest Service survey sampled Lepi- (Beggs and Rees, 1999). Honeydew provides a nonliv- doptera in Golden Downs forest for 5 years (1958± ing, alternative food supply that may allow wasps to 1962), before the arrival of common wasps. One abun- reduce or exclude populations of native insects, in much dant species, Pseudocoremia suavis (Butler) (Lepi- the same way as ants feeding on extra-¯oral nectaries doptera: Geometridae), peaked in late summer. After can restructure communities (Heads and Lawton, 1984; the arrival of common wasps only a few individuals of Lawton and Heads, 1984). this species were found in a similar forest about 40 km Wasp foragers prey on and scavenge a wide variety of away, despite 6 years of sampling (1991±1996; unpub- protein sources to feed their developing larvae (Spradb- lished data). To con®rm this, resampling should be done ery, 1973). In honeydew beech forest, of the identi®able using the same method in the same forest as the original prey items, about 30% were spiders, 20% caterpillars, survey. 20% ants and bees, 15% ¯ies and 15% other (Harris, 1991). Wasps consume between about 1.4 and 8.1 kg of 3.4. E€ect of wasps on birds invertebrates haÀ1 seasonÀ1 in the western and northern South Island respectively, depending on the density of There are several species of native birds, including wasps (Harris, 1991). German wasps carry heavier loads kaka and honeyeaters (tui, Prosthemadera novaesee- (5 mg) than common wasps (2 mg; Harris, 1991). landiae, and bellbirds, Anthornis melanura), which utilise Ecological theory predicts that eradication of a prey honeydew as an easily obtained carbohydrate resource. species will occur when the intrinsic rate of increase of Wasps remove so much honeydew for 5 months of the the prey is less than the product of average predator year that there is little left for foraging birds. This may abundance and its per capita predation rate (Holt and lead to a range of responses by birds from simply Lawton, 1994). Wasps are abundant, and very high pre- switching to an alternative food source (if there is one dation rates have been recorded for some species. For available), to reducing reproductive output. Mortality instance, the probability of free-living caterpillars [in this rates may also increase because of insucient food. case Uresiphita polygonalis maorialis (F. & R.), Lepi- Kaka spent about 30% of their foraging time collect- doptera: Cranbidae] that occur at the peak of the wasp ing honeydew when it was available (Beggs, 1988). In season surviving to adults was only 10À78 to 10À40 (Beggs this time, they would have obtained most of their daily and Rees, 1999) and the probability of an orb-web spider energy requirements Ð a net gain of 1400 J minÀ1 Ð [in this case Eriphora pustulosa (Walckenaer), Araneae: but negligible quantities of protein (Beggs and Wilson, Araneidae] surviving to the end of the wasp season was 1991). Males spent at least 30% of their foraging time 10À18 (Toft and Rees, 1998). Thus, ecological theory pre- digging out beetle larvae (Beggs, 1988), which provided dicts that prey species will be at risk of being eradicated by a negligible net energy return but plenty of protein wasps if the prey's intrinsic rate of increase is low. It has (Beggs and Wilson, 1987). It was calculated to be been calculated that to conserve vulnerable species wasp unpro®table energetically for kaka to feed on honeydew abundance needs to be reduced by about 80±90% (Toft when it dropped below 1.4 J dropÀ1, and when wasps and Rees, 1998; Beggs and Rees, 1999). Not all species were abundant it was usually around or less than this will be equally vulnerable to wasp predation, so these value (Beggs and Wilson, 1991). estimates provide a maximum level of control required to The behaviour of kaka changed when it became conserve some species. Achieving a lower level of control unpro®table for them to forage on honeydew. They is likely to be bene®cial to less vulnerable species. were not encountered in the honeydew feeding area J. Beggs / Biological Conservation 99 (2001) 17±28 23 when wasps were numerous. Indeed, they did not return altitudinal transect for 10 years before the arrival of until honeydew had reached an energy value of more common wasps (but not before the arrival of German than 4 J dropÀ1 (Beggs and Wilson, 1991), suggesting wasps). These counts were repeated in 1996, once com- that the 1.4 J dropÀ1 underestimates the ecological mon wasps had been established for about 10 years. threshold below which kaka foraging behaviour alters. Preliminary results indicated that the abundance of Using the renewal rate for the standing crop of honey- many bird species, including insectivorous ones, had dew, it has been estimated that honeydew should not be declined (unpublished data). This is only circumstantial cropped more frequently than every 27 minutes to keep evidence that population changes were due to wasps Ð honeydew at about 1.4 J dropÀ1 (Moller et al., 1996a). indeed it is probable that other variables will also have Using the same relationship in Moller et al. (1996a), in¯uenced bird abundance (e.g. predation, climate). honeydew would need to be cropped no more than Further work is required to determine the e€ect wasps about once every 400 min to maintain 4 J dropÀ1.I are having on birds at the population level. suggest that this higher value is used as an ecological An unquanti®ed impact of wasps on birds is the pre- damage threshold for kaka feeding on honeydew. dation of nestling birds. Wasps have been recorded Tui and bellbirds also changed their behaviour when attacking and killing nestling birds (Moller, 1990), but it honeydew became scarce. Tui spent nearly all their is not known how common this is. Many native species foraging time on honeydew (usually more than 80%) have completed their nesting before wasps become except on days when there was little honeydew available abundant (Heather and Robertson, 1996). However, the (Moller et al., 1996b). They reduced their feeding on chicks of species that produce multiple broods late into honeydew or left beech forest reserves when the stand- summer may be vulnerable to attack by wasps. ing crop of honeydew fell below 2500 J mÀ2 (Moller et al., 1996b). Bellbirds remained in the forest on days 3.5. E€ect of wasps on nutrient cycling when the standing crop of honeydew was low, but reduced the time spent feeding on honeydew (non- Without wasps, a small amount of honeydew is breeding season only); or reduced their non-foraging removed by birds and other insects, but the majority of activities such as singing, ¯ying, social interactions and it falls to the ground around the tree (Moller and Tilley, grooming (during both the breeding and non-breeding 1989). Removal of large quantities of sugary honeydew season; Moller et al., 1996b). Honeydew was maintained by wasps may change the cycling of nutrients in the soil at 2500 J mÀ2 if the ®laments were cropped no more and/or increase the loss of carbon to the tree. Micro- than once every 180 min (Moller et al., 1996a; Fig. 3). organisms are likely to bene®t from the presence of These ecological damage thresholds suggest that wasp honeydew as a source of energy (Dighton, 1978; Stadler densities should not increase above a level where wasps and MuÈ ller, 1996), and this has been shown to a€ect revisit honeydew threads more than once every 180±400 several ecosystem processes (Stadler and Michalzik, min, to avoid behavioural changes in bellbird, tui and 1998; Stadler et al., 1998). kaka. However, it is not known what e€ect these beha- Owen and Wiegert (1976) and Owen (1978) hypothe- vioural changes have on the birds. They could a€ect sised that honeydew-producing aphids may increase breeding success or survival, but the role of wasps in plant ®tness by stimulating free nitrogen ®xation these variables is confounded by the e€ect of other beneath the plant from which sugar is extracted. There introduced predators and competitors. For instance, is con¯icting evidence supporting this hypothesis. introduced stoats (Mustela erminea) killed about half Petelle (1984) found that aphid honeydews do increase the female kaka that attempted to nest, identifying soil non-symbiotic nitrogen ®xation. Furthermore, stoats as an important cause in the decline of kaka Dighton (1978) showed that addition of sugar increased (Wilson et al., 1998). Bellbird and tui produce multiple the biomass of fungi and bacteria. However, Grier and broods, starting in early spring and ®nishing in late Vogt (1990), Stadler and Michalzik (1998), and Michal- summer (Heather and Robertson, 1996). Therefore, the zik et al. (1999), found that honeydew caused a reduc- survival and recruitment of later broods may be a€ected tion in available soil nitrogen. In addition, it has been by a shortage of honeydew. Kaka ¯edglings rely on shown that aphids exert a severe nutrient drain on their their parents for food throughout the wasp season, so host plants, which respond with reduced seed produc- they may also be directly a€ected. This needs to be tes- tion (Choudhury, 1984; Foster, 1984). Honeydew prob- ted by manipulating wasp abundance in the absence of ably a€ects nutrient cycling via a range of complex stoats given that such a high proportion of breeding interactions, and these will be di€erent for di€erent female kaka and chicks were killed by stoats (Wilson et communities. The coevolutionary relationship between al., 1998). the scale insects and beech trees in New Zealand could In addition to honeydew, wasps are likely to compete be di€erent from systems studied in the northern with a range of native birds for invertebrate food. Stan- hemisphere, particularly as honeydew is produced year- dard 5-min bird counts were carried out along a 2-km round in New Zealand whereas it is only produced 24 J. Beggs / Biological Conservation 99 (2001) 17±28 seasonally (May±September; e.g. Stadler and Michalzik, (Beggs et al., 1998). The size of this e€ect will depend on 1998) in Europe. the size of the site poisoned, but since wasps have been If New Zealand beech honeydew does a€ect the recorded foraging up to 4 km from their nest (Coch, metabolism of micro-organisms and hence nutrient 1972), a site would have to be very large (perhaps 2000 cycling in much the same way as in the northern hemi- ha, i.e. 4Â4 km) before reinvasion at the core was not a sphere (Stadler and Michalzik, 1998), then it is likely problem. Some queen wasps are estimated to ¯y up to wasps do have an e€ect. We currently have no data that 30±70 km before establishing a nest (Moller et al., might indicate the magnitude or consequences of such an 1990), although most queens probably do not move as e€ect on the availability of nutrients to micro-organisms far as this. Nevertheless, reinvasion in spring of even or to the trees. However, given estimated reductions in 2000 ha sites would be likely. honeydew yield due to wasps are more than 90% for 5 At times, particularly in non-honeydew beech forest months of the year (Moller et al., 1991a) and about sites, wasps are not greatly attracted to a protein-based 70% of the annual production (Table 1), the loss of bait. Some poison-baiting operations have failed to carbohydrate to micro-organisms on and around hon- reduce wasp abundance for this reason (Spurr, pers. eydew trees could be similar. Conversely, micro-organ- commun.). It is not feasible to use a carbohydrate bait isms associated with wasp nests are likely to gain because of the risk of poisoning honeybees. Even in nutrients. honeydew beech forest, it is dicult to poison wasps It is possible that wasps a€ect beech seed quality by early in the season (before January), probably because interrupting the nutrient cycling processes in the hon- there is such an abundance of prey species that wasps eydew beech forest community. Beggs (1999) found that are not attracted to bait. For these reasons, additional red beech seed was lighter when there were fewer wasps, control tools are required. whereas there was no detectable di€erence for the seed A wasp parasitoid [Sphecophaga vesparum vesparum from silver beech (which is not infested by the scale (Curtis) Hymenoptera: Ichneumonidae] has been insect). This di€erence was not in the expected direction, released in many parts of New Zealand, establishing in perhaps because of the way nutrients are allocated to at least two sites (Moller et al., 1991b; Beggs et al., reproduction when a tree is under stress. A range of 1996). However, despite being established at one site for other seed variables were also measured, but there was more than 10 years, there has been no measurable insucient statistical power to support or reject the reduction in wasp abundance (Beggs et al., 1996; hypothesis that wasps were a€ecting seed quality. unpublished data). Mathematical modelling predicts Wasps could a€ect seed quality via a range of other that nest density could be reduced by up to 25%, but mechanisms, which may not work in the same direction only if the parasitoid kills about 50% of early season as removing honeydew. By reducing the abundance of nests (Barlow et al., 1996; Toft et al., 1999). If fewer caterpillars, wasps may reduce herbivory on trees and early season nests are killed, then the predicted reduc- hence trees would have more nutrients available for seed tion rapidly reduces to around zero (Toft et al., 1999). production. They may also remove large numbers of Two other strains of S. vesparum have been released invertebrates that feed directly on the ¯owers or seed. since 1996, but neither have yet established, and it is not The range of potential interactions is complex and known whether they will have a greater or lesser impact dicult to predict. Nevertheless, the ecological rami®- on wasp populations than the original strain. cations of an e€ect on beech trees, which are the domi- Estimates of ecological damage thresholds suggest nant canopy species, could be very important. Changes that wasp density needs to be reduced by 80±90% to in seed quality may a€ect seed viability and regenera- conserve the most vulnerable native species in honeydew tion potential, and have a ¯ow-on e€ect to the compo- beech forests. There are currently no control tools that sition of the plant community. Furthermore, there may will reduce density by this amount over large areas. The be ¯ow-on e€ects to animal species, particularly those challenge now is to identify and develop additional such as kaka, which in this habitat are dependant on wasp control tools. Pathogens, such as the fungus beech seed for rearing chicks (Wilson et al., 1998). Beauveria bassiana, are showing promise (Harris et al., Beech seed is also a major food source for several 2000) and a technique is being developed to incorporate introduced vertebrate pests (King, 1983; Wilson et al., a pathogen into a bait. The advantage of this over using 1998), so seed quality could have an e€ect on these pests a toxin is that not as much pathogen would have to be and the native species that they impact on. taken back to the nest, so it would work at much lower doses. The potential of genetically modifying microbes 3.6. Wasp control in the gut of wasps to make them pathogenic is also being investigated (Travis Glare, pers. commun.). There Poison-baiting can kill 80±100% of the colonies is still much work to be done, however, and it is likely within a site, but reinvasion by foraging workers means that a range of control tools will be necessary to achieve that total wasp biomass is not reduced by as much an adequate reduction in wasp abundance. J. Beggs / Biological Conservation 99 (2001) 17±28 25

4. Discussion (Mayr)] is of concern. These ants are already known to have major detrimental impacts on native invertebrates The ecological impact of introduced wasps in about 1 in other countries (HoÈ lldobler and Wilson, 1990), par- million ha of honeydew beech forests is pervasive. The ticularly isolated islands with a depauperate ant fauna. high numbers and polyphagous habit of these invaders For example, introduced ants have destroyed most of mean that they are able to monopolise the honeydew Hawaii's endemic lowland arthropod fauna (Zimmer- resource for 4 months of the year, maintain high pre- man, 1978; Reimer, 1994). Should such ants invade dation rates on several groups of native invertebrates, honeydew beech forests in New Zealand, their popula- and a€ect native vertebrates. This potentially leads to a tions would be supported by large quantities of honey- cascade of events, including competition for carbohy- dew year-round. I predict that the impact of some drate and protein resources with native birds, ¯ow-on invasive ants in this ecosystem will be devastating. e€ects to the invertebrate food-web, and disruption of There are about 15 000 species of Hymenoptera in the nutrient cycling in the beech forest community. world (Hurd, 1955), although most of these are solitary, More than a decade of research on the impact of ino€ensive insects. However, there are a number of wasps in beech forest communities has yielded some social wasp species throughout the world that have not good measurements of the reduction in the honeydew yet established in New Zealand, but which are con- resource caused by wasps (Beggs and Wilson, 1991; sidered to be pests in other countries. Social wasps are Moller et al., 1991a) and wasp predation rates on some excellent invaders, and New Zealand is at risk from invertebrates (Toft and Rees, 1998; Beggs and Rees, additional arrivals. For instance, North America has at 1999). What is not known is whether wasps have an least 16 species belonging to the sub-family Vespinae, e€ect on any native species at the population level, and many of which are pests (Akre et al., 1981). It is this is crucial if we are to understand the magnitude of unknown what e€ect the arrival of any of these pest the impact of this invasive species. Demonstrating such species would be in New Zealand. Some of them may an e€ect is likely to be dicult given the complexity of add to the problem, or some of them may simply dis- the beech forest community. The abundance of some place the existing species. For example, in the late 1970s species may decrease, but equally the abundance of V. pensylvanica spread to several Hawaiian islands and other species may increase. We may never know if increased in density (Chang, 1988), eventually displa- invertebrate species have been eliminated, as our cing V. vulgaris on some islands and increasing the wasp knowledge of what should be present is so limited. problem (Dave Foote; pers. commun.). This suggests Manipulative experiments of wasp abundance are di- that if V. pensylvanica established in New Zealand it cult because it is not possible to eradicate wasps from might displace V. vulgaris and increase the threat to sites, and even low densities of wasps lead to high pre- native communities. dation rates on some species. For example, the prob- Specimens of other social wasps have been recorded ability of an orb-web spider surviving the entire wasp in New Zealand, including the American bald-faced season was still unlikely (3Â10À5) even in sites which hornet (Dolichovespula maculata) and the yellow Orien- had been poisoned (Toft and Rees, 1998). No-one has tal paper wasp (Polistes olivaceus; Harris 1979, 1984). It determined whether wasps a€ect ecosystem processes, is likely that social wasps are continually arriving in or even if honeydew does. Further research on the e€ect New Zealand, but failing to establish. For instance, of wasps on ecosystem processes and ¯ow-on e€ects each year, on average, the Ministry of Agriculture and would add to our knowledge of wasp impacts. Forestry Quarantine Service detect two live and several Despite the lack of knowledge about impacts at the empty nests of the Asian paper wasp in shipments of community or ecosystem level, what we do know pro- cars and car parts arriving in New Zealand (Rose, vides some timely warnings of other potential invaders. 1999). Most Vespinae are morphologically similar to Wasps removed large quantities of honeydew (240 l each other, and to the species already in New Zealand haÀ1 seasonÀ1) at high wasp densities (Harris, 1991). (Akre et al., 1981). This similarity, coupled with the However, it has been estimated in central European abundance of social wasps already present in New forests that ants (Formica polyctena) collected about Zealand, is likely to make it dicult to detect the arrival 4800 l haÀ1 yearÀ1 (MuÈ ller, 1956). Ants are assumed to of a new species. New Zealand needs to remain vigilant consume about two-thirds of the honeydew resource in to reduce the risk of more invasions, and to detect if European forests (Stadler, pers. commun.). such an invasion occurs. While the conservation threat of social wasps in New Zealand may be large, the impact of introduced ants that forage on honeydew may be greater because they Acknowledgements are present throughout the year. The recent arrival in New Zealand of the tramp species Pheidole megacephala Many people, too numerous to list, have contributed (Fab.) and the Argentine ant [Linepithema humile to the wasp research programme in the last decade. 26 J. Beggs / Biological Conservation 99 (2001) 17±28

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