New Zealand Journal of Botany
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Assessing the impact of an introduced bee, Anthidium manicatum, on pollinator communities in New Zealand
J Soper & JR Beggs
To cite this article: J Soper & JR Beggs (2013) Assessing the impact of an introduced bee, Anthidiummanicatum, on pollinator communities in New Zealand, New Zealand Journal of Botany, 51:3, 213-228, DOI: 10.1080/0028825X.2013.793202 To link to this article: https://doi.org/10.1080/0028825X.2013.793202
Published online: 18 Jul 2013.
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Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tnzb20 New Zealand Journal of Botany, 2013 Vol. 51, No. 3, 213 228, http://dx.doi.org/10.1080/0028825X.2013.793202
RESEARCH ARTICLE Assessing the impact of an introduced bee, Anthidium manicatum, on pollinator communities in New Zealand J Soper and JR Beggs* School of Biological Sciences, University of Auckland, New Zealand (Received 7 December 2012; accepted 2 April 2013)
Introduced pollinator species may exacerbate the problems faced by pollinator communities, so the detection in 2006 of a new solitary bee, Anthidium manicatum, to New Zealand was concerning. We assess whether establishment of this wool-carder bee presents potential risks to native flora and fauna by recording its current distribution, which plant species it visits, which insects co-occur at these plants, and identifying which species this territorial bee attacks. Anthidium manicatum is now widespread in urban New Zealand. More than 80% of the plants visited by A. manicatum were exotic species (predominantly Lamiaceae and Plantaginaceae), although it also visited native species of Veronica (Plantaginaceae) and Lobelia (Campanula- ceae). Anthidium manicatum primarily interacted with other introduced bees. Native Lasio- glossum bees were seldom attacked and only for short durations. Further research is required, particularly on weeds, but we suggest that A. manicatum does not present a major direct threat to New Zealand’s native flora and fauna. Keywords: alien invasive species; distribution; pollination; pollen load; Anthidium manicatum; wool-carder bee; Lamiaceae; Plantaginaceae; Apis mellifera; Lasioglossum
Introduction Albrecht et al. 2012). This leaves the web still Degradation of the environment has led to well connected, but the species interacting shift the decline of pollinator communities in many from native to exotic. However, not all species parts of the world, coupled with a decline in added to a community are necessarily polylectic, plants reliant on animals for these vital repro- so identifying the range of native and exotic ductive services (Winfree et al. 2009; Potts et al. interactions that a new arrival engages in will 2010). Introduced species may be one of the help to assess the threat it poses to the structure drivers of this pollinator decline, but it is not of the pollinator community. immediately obvious whether an introduced Bees are the most highly adapted of all pollinator will disrupt native plant pollinator insect flower visitors (Kevan & Baker 1983) and interactions, or just seamlessly integrate into are among the most important pollinators of pollinator webs, perhaps even enhancing the many flowering plants including agricultural reproductive success of plants (Tylianakis 2008). crops (Michener 2007). Several species of bee Polylectic exotic pollinator species (species of have been widely introduced outside their bees that take pollen from a wide variety of native range for pollination services, whereas plants), particularly honeybees (Apis mellifera many other species are finding their ways into L., Apidae), tend to end up dominating highly new environments as a result of accidental or invaded pollination webs (Aizen et al. 2008; indirect introductions (Strange et al. 2011).
*Corresponding author. Email: [email protected]
# 2013 The Royal Society of New Zealand 214 J Soper and JR Beggs
Recently there has been increased concern 2011) (Fig. 1). Native to Europe, western Asia regarding the possible impacts of introduced and northern Africa, A. manicatum is a solitary bees, including: competition with native polli- species that has been accidentally introduced nators for floral resources and nest sites, polli- to South America, the USA, Canada, the Canary nation of exotic weeds and disruption of the Islands, Siberia and New Zealand (Proshchalykin pollination of native plants (Goulson 2003; 2007; Gibbs & Sheffield 2009). It was first dis- Paynter et al. 2010). Most research to date covered in Napier and Nelson in 2006 (Donovan has focused on the impacts of managed bees on 2007), adding to New Zealand’s comparatively native bee communities, whereas little is known small bee fauna of 40 species, most of which are about the potential impacts of unintentionally endemic (Donovan 2007; Howlett & Donovan introduced bees (Strange et al. 2011). 2010). In New Zealand, other insect pollinators The wool-carder bee (Anthidium manicatum such as moths, flies and beetles, as well as L., Megachilidae), is globally the most wide- birds, play an important role in pollination spread unmanaged bee species (Strange et al. (Newstrom & Robertson 2005; Kelly et al.
Figure 1 Distribution of Anthidium manicatum in New Zealand, July 2012. This bee was first detected at Napier and Nelson in 2006. The most recent detections were at Gisborne and Masterton in 2012. Top right shows three of the five abdominal spines the male wool-carder bee uses to attack other floral visitors. Bottom right shows female bee carding fibre from Stachys sp (lamb’s ear; Lamiaceae) to make her nest. Photos: Eve Manning. Impact of introduced wool-carder bee in New Zealand 215
2006, 2010). Native pollinating insects may general public using websites, newsletters, be particularly vulnerable to disruption by magazines and newspaper articles. New records A. manicatum. were gathered between 2009 and 2012, and Male A. manicatum are territorial and those that were verified (from specimens and aggressively defend patches of flowering plants photographs and/or entomological experts) as mating territories, attacking intruders that were added to our distribution data. enter the territory with their sharp abdominal spines (Wirtz et al. 1988). This bee is described as polylectic, collecting pollen from various kinds Study site of flowers, although the most common plant Observations of A. manicatum behaviour were associations are with members of the Lamia- conducted at the Auckland Botanic Gardens ceae, Scrophulariaceae and Fabaceae (Muller (ABG) in Manurewa, Auckland, New Zealand 1996; Maier 2009). As with other members of the (37.0102298S and 174.907158E). The ABG cover tribe Anthidiini, female A. manicatum engage 64 hectares, containing over 10,000 species of in elaborate nesting behaviours, stripping pub- plants (of which 2357 species are native to escence from the leaves and stems of various New Zealand), and are separated into areas plants, which they roll into balls and carry back containing similar types of plants. This study to pre-existing cavities to construct their nests. was carried out predominantly in the Perennials Anthidium manicatum is in flight over the sum- Garden, the Herb Garden and the New Zealand mer months, during which time there can be a Natives areas, because they were adjacent to second or third generation, and they over-winter each other, easily accessible and contained a as pre-pupae (Payne et al. 2010). range of exotic and native plant species. The main aim of this study was to investi- gate whether the establishment of A. manicatum in New Zealand presents any potential risks to Plant associations of A. manicatum native flora and fauna. To meet this objective, During the time that fieldwork was carried out first we documented the known range of at the ABG, we documented all plants that A. manicatum in New Zealand, incorporating A. manicatum was observed visiting. Addition- new distribution records. Second, we examined ally, weekly examinations were made in sec- whether A. manicatum would be associated with tions of the ABG that were not included in exotic and/or native plant species by under- the study area. New plant associations were taking floral visitor counts at the Auckland also recorded by members of the public and Botanic Gardens. Finally, we observed which entomologists, and those that were verified insect species A. manicatum co-occurred with on were added to our data set. flowers and looked at whether the novel beha- viour of A. manicatum presented any potential risks to the foraging of native bees. Flower visitor community We recorded the floral visitors to a range of native and exotic flowering plants based on the Materials and methods methods developed by the Pollination Biology Distribution Research Group at Landcare Research (www. Existing distribution records of A. manicatum landcareresearch.co.nz/research/biocons/polli in New Zealand were collected from the insect nation/: accessed 29 July 2009). Seven exotic collections of 10 institutes and private indivi- plant species that A. manicatum was known to duals throughout New Zealand in September visit, and 18 native plant species that were 2009. Additionally, new records were solicited in flower (including two Hebe cultivars), were from specialist entomological groups and the selected at random along 38 transects at 216 J Soper and JR Beggs the ABG between 25 November 2009 and 10 allow for comparison of pollen loads between June 2010. Where possible, five replicates of bees collected on native versus exotic plants and each plant species were included, although also to ascertain whether they were collecting when plants had stopped flowering they were pollen from both exotic and native plants in the not always able to be immediately replaced. same pollen-collecting trip. Bees were placed in a We stopped at each plant, chose an area of the container with 1 ml of 75% ethanol, which was plant that was in full sunlight, and recorded gently shaken to remove pollen. The ethanol was the number of flower visitors in a 0.5-m2 area of then poured into an Eppendorf tube and cen- the plant by undertaking a near-instantaneous trifuged at highest speed (16873 g) for 5 min count. (Eppendorf Centrifuge 5418). The pollen pellet Insects were categorized into broad ‘func- was then re-suspended in 10 ml of pollen-staining tional groups’ following the Landcare Research solution (Calberla’s stain*amixtureof5ml protocol; specifically A. manicatum, Apis melli- glycerine, 10 ml 95% ethanol, 15 ml water and fera, bumblebee (Bombus spp., Apidae), native 10 drops basic fuchsin, saturated at 3 mg/ml bee,wasp,largefly,smallfly,beetle,bug, distilled water). butterfly, other. This grouped together species The pollen was identified using a reference that were morphologically very similar, and collection sourced from plants at the ABG. In were therefore likely to be functionally similar addition, Moar (1993) and two online pollen in terms of their mode of pollination. We reference collections: The Australasian Pollen and categorized small house flies as ‘small flies’, Spore Atlas (http://apsa.anu.edu.au) and http:// although in the Landcare Research protocol www.saps.org.uk/library/541 were used to iden- they were counted as a ‘big fly’. Male A. mani- tify pollen grains. Unknown pollen types were catum were recorded as flower visitors when it sorted into morphospecies on the basis of size was clear they were patrolling (see Severinghaus and shape. We did not count pollen types that et al. 1981) the area of plant that was being contributed less than 5% of the total pollen on a observed. slide, because we considered them extraneous and At the start of each transect the date, time of low ecological significance (Westrich 1990). and weather conditions were recorded and a daily flower count was taken for a 0.5-m2 area of each plant. Transects were undertaken on Male territorial behaviour days where there appeared to be little chance of On 6 days between 22 February and 16 March rain and usually on weekdays to reduce human 2011, we watched and recorded the behaviour disturbance at our study site. of a territorial male A. manicatum continuously on a dictaphone. Although individual bees only maintain territories for 4 7 days (Severinghaus Pollen load et al. 1981), as bees were not tagged it was Pollen was removed from female bees (A. mani- not possible to know if we were observing the catum and Lasioglossum sordidum Smith, same male bee on different days. Therefore, we Halictidae) collected on native and exotic treated a bee observed on a different day as plants from the ABG between 7 February and an independent observation. Observations were 8 March 2011. All A. manicatum females that made on sunny days when A. manicatum and were observed on native plants were collected, native bees were co-occurring and when there when possible, and co-occuring L. sordidum was one easily identifiable territorial male bee. individuals were collected from the same native Male bees were identified either by distinctive plants to allow for comparison of pollen loads pollen marks on their thorax, or if they were between the two species. Specimens of A. mani- continuously in the territory and were able to catum were also collected from exotic plants to be constantly observed, then they were known Impact of introduced wool-carder bee in New Zealand 217 to be the same individual bee. Behaviours similar. The SIMPER procedure in PRIMER were classified into seven categories (after was used to calculate the similarity percentage, Severinghaus et al. 1981): patrolling, foraging, which showed the contribution of different resting, interactions with other insect species, insect species to the differences between plant interactions with conspecific males, interactions species and months. Statistical significance for with female A. manicatum (mating or mating all analyses was set at the 95% level. attempts) and out of sight. As it was difficult to Since the data were not normally distributed, time short attacks precisely, all attacks 2 s or a Mann Whitney U-test was used to evaluate shorter were classified as 2 s and longer attacks differences in the number of types of pollen per were timed accordingly. One white ice plant load for A. manicatum and L. sordidum. This (Delosperma ‘Alba’, Aizoaceae) was selected as analysis was performed using the R-statistical the focal plant because this large individual software R version 2.14.0 (2011-10-31). had an abundance of flower visitors including To calculate whether there were differences A. manicatum, Apis mellifera, Bombus spp., in the attack rates on the different types of Lasioglossum spp., flies and other occasional flower-visiting insects by the territorial male flower visitors, such as butterflies. It was located A. manicatum, we fitted a Poisson regression on in the Rock Garden at the ABG. An instanta- the average number of attacks on each species, neous count of all flower visitors was also made with the average number of each species present in the territory at 5-min intervals. in the territory as an offset. An analysis of deviance was then performed to test the over- all significance of the species effect. Pairwise Statistical analyses comparisons were performed by calculating the Differences in the community composition differences in the mean log-counts between were analysed using non-metric multidimen- each of the types of insects. This analysis sional scaling (n-mMDS) based on Bray Curtis was performed using the R statistical software similarity indices. The n-mMDS routines were R version 2.14.0 (2011-10-31). available in PRIMER, a multivariate statistical The non-parametric Kruskal Wallis rank package used for ecological research (Clarke & sum test was used to test for differences in Warwick 2001). The data were square root the lengths of attacks on different insects by the transformed to avoid overweighting the most male A. manicatum, as the data did not meet the abundant species. All ordinations were run from assumption of normal distribution through 100 restarts. Stress values of 0.10 to 0.20 indicate transformations (square root, log, arcsine). that the n-mMDS is a good representation of Tukey Kramer honestly significant difference the relationship between samples (Clarke & was used for pairwise comparisons. These tests † Warwick 2001). were carried out in JMP 10 (SAS Institute Inc. Two-way analyses of similarities (ANOSIM), 2009). a component of the PRIMER package, were used to test whether the assemblages of flower- Results visiting insects were statistically different from one another using plant species and month as Distribution factors. This gave an R-statistic based on the As of July 2012, all confirmed records of rank similarities between samples in a similarity A. manicatum in New Zealand show that this matrix. The R-statistic provides a comparative species is now present in a number of locations measure of the degree of separation of flower from Whangarei to Christchurch, spanning a visitor communities. If the R-statistic equals or distance of 886 km (Fig. 1). The increasing is close to one, the replicates are significantly number of new location records, including the different from each other, whereas at 0 they are discovery of two new locations (Gisborne and 218 J Soper and JR Beggs
Table 1 Plants visited by Anthidium manicatum in New Zealand.
Plant family Genus Species/Cultivar Common name Location
Acanthaceae Thunbergia Thunbergia grandiflora Blue trumpet vine Auckland Thunbergia natalensis Natal bluebell ABG Aiozoceae Delosperma Delosperma ‘Alba’ White ice plant ABG Asteraceae Centaurea Centaurea dealbata Cornflower ABG Circium Circium vulgare Scotch thistle Marahau, Nelson Dahlia Dahlia sp. ABG Senecio Senecio mandraliscae Blue finger ABG Balsaminaceae Impatiens Impatiens walleriana Busy Lizzy Auckland Boraginaceae Heliotropium Heliotropium arborescens Cherry pie ABG Campanulaceae Lobelia Lobelia anceps NZ lobelia ABG Caryophyllaceae Dianthus Dianthus sp Whatfield wisp ABG Cleomaceae Cleome Cleome sp ABG Geraniaceae Pelargonium Pelargonium sp Geranium Auckland Iridaceae Moraea Moraea ramosissima Peacock lily ABG Lamiaceae Agastache Agastache foeniculum Anise hyssop ABG Ajuga Ajuga reptans Bugleweed ABG Lamium Lamium purpureum Red deadnettle ABG Lavandula Lavandula dentate Lavender ABG Melissa Melissa officinalis Lemon balm ABG Nepeta Nepeta faassenii Catmint ABG Plectranthus Plectranthus ornatus Dogbane ABG Prunella Prunella vulgaris Self-heal ABG Rosmarinus Rosmarinus officinalis Rosemary ABG Salvia Salvia chamaedryoides Germander sage ABG Salvia greggii Autumn sage ABG Salvia ‘Indigo Spires’ ABG Salvia lyrata Lyre-leafed sage ABG Salvia repens ABG Salvia sylvestris Violet sage ABG Salvia taraxacifolia Dandelion sage ABG Salvia urica Blue bush sage ABG Stachys Stachys byzantina Lamb’s ear ABG Stachys thirkei Dwarf lamb’s ear ABG Thymus Thymus nummularis Thyme ABG Vitex Vitex agnus-castus Chaste tree ABG Plantaginaceae Antirrhinim Antirrhinum spp Snapdragon ABG Cymbalaria Cymbalaria muralis Ivy-leaved toadflax Auckland Digitalis Digitalis purpurea Foxglove ABG Linaria Linaria genistifolia subsp dalmatica Dalmation toadflax ABG Linaria purpurea Purple toadflax ABG Penstemon Penstemon ‘Purple Passion’ ABG Veronica Veronica stricta Koromiko ABG Veronica ‘First Light’ ABG Veronica ‘Totara Blue’ ABG Veronica ‘Westport’ ABG Impact of introduced wool-carder bee in New Zealand 219
Table 1 (Continued )
Plant family Genus Species/Cultivar Common name Location
Veronica ‘Wiri Dawn’ ABG Veronica ‘Wiri Jewel’ ABG Veronica spicata Spiked speedwell ABG Plumbaginaceae Limonium Limonium perezii Perez’s sea lavender ABG Proteaceae Grevillia Grevillia ‘Robyn Gordon’ ABG Scrophulariaceae Nemesia Nemesia denticulata ‘confetti’ ABG
Native plants and native cultivars are shaded. ABG, Auckland Botanic Gardens; other locations listed.
Masterton) in 2012, indicates that A. mani- visitors to approximately half of the native plant catum is continuing to spread in New Zealand. species (Table 2), including V. stricta, poroporo (Solanum laciniatum Aiton, Solanaceae) and Pseudopanax spp. (Araliaceae). Plant associations of A. manicatum The n-mMDS plot shows some differentia- Anthidium manicatum was recorded on 51 plant tion between the flower visitor assemblages species/cultivars from 15 families. Of these, of V. stricta (native) and the three exotic 86% were exotic species and these were pre- plant species (Fig. 2). Overall there was a mod- dominantly members of the Lamiaceae and erate difference in the composition of floral Plantaginaceae families (Table 1). Anthidium visitor communities on the four plants (analysis manicatum was recorded on native plants from of similarities Global R 0.419; P 0.001). two families, Plantaginaceae and Campanu- Pairwise comparisons indicated that the floral laceae. It was recorded twice on koromiko visitor communities of the four plant species (Veronica stricta Benth., Plantaginaceae) plus had a moderate amount of variation with the some Veronica cultivars and Lobelia anceps L.f. exception of the two exotic species, Stachys (Campanulaceae) (Tables 1 and 2). spp. and Penstemon ‘Purple Passion’, whose floral visitor communities were highly simi- lar (Table 3). In the SIMPER, native bees Flower visitor community accounted for 77% of the similarity between In total, 1006 flower visitor counts were made the floral visitor counts on native V. stricta; along transects and 1425 insects were recorded whereas A. manicatum was responsible for most (Table 2). Anthidium manicatum was found to of the similarity between floral visitor counts on most frequently co-occur with Apis mellifera Stachys spp. (96.43%) and Penstemon ‘Purple and Bombus spp., although it co-occurred with Passion’ (84.15%). The native species Lobelia native bees on some native and exotic plants. anceps was not included in the PRIMER Anthidium manicatum made up the highest analysis because there was insufficient data for proportion of visitors to lamb’s ear (Stachys this plant. spp., Lamiaceae), Penstemon ‘Purple Passion’ (Plantaginaceae) and red dead nettle (Lamium purpureum L., Lamiaceae) (Table 2). Male Pollen load A. manicatum were more frequently seen at Overall, A. manicatum carried significantly these exotic plants than females, but female more types of pollen (mean9SEM; 3.2290.28 A. manicatum were frequently seen collecting pollen types per load; n 20) than L. sordidum nest material on Stachys spp. (personal observa- (mean9SEM; 1.3690.20 pollen types per load; tion). Native bees were the predominant flower n 11) (P 0.0002). Where the pollen of the 220 oe n RBeggs JR and Soper J
Table 2 Proportional matrix of near-instantaneous counts of flower visitors to plants observed at the Auckland Botanic Gardens, December 2009 to June 2010.
No. of Total A. Honey- Bumble- Native Big Small Family Species Origin plants insects manicatum bee bee bee Wasp Ant fly fly Butterfly Other
Araliaceae Pseudopanax Native 6 102 0.000 0.137 0.000 0.539 0.019 0.030 0.216 0.059 0.000 0.000 spp. Asteraceae Olearia albida Native 2 10 0.000 0.200 0.000 0.300 0.000 0.000 0.300 0.200 0.000 0.000 var. angulata Olearia Native 1 5 0.000 0.000 0.000 0.200 0.200 0.000 0.200 0.400 0.000 0.000 paniculata Campanulaceae Lobelia anceps Native 1 12 0.417 0.250 0.000 0.167 0.000 0.000 0.000 0.000 0.167 0.000 Fabaceae Carmichaelia Native 1 1 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 1.000 muritai Hemerocallidaceae Hemerocallis sp. Exotic 3 3 0.000 0.000 0.000 0.000 0.670 0.000 0.330 0.000 0.000 0.000 Phormium spp. Native 6 67 0.000 0.045 0.000 0.343 0.016 0.597 0.000 0.000 0.000 0.000 Lamiaceae Lamium Exotic 1 17 0.647 0.058 0.000 0.118 0.118 0.000 0.000 0.006 0.000 0.000 purpureum Stachys spp. Exotic 7 175 0.708 0.109 0.154 0.000 0.006 0.000 0.017 0.006 0.000 0.000 Salvia Exotic 2 21 0.809 0.143 0.048 0.000 0.000 0.000 0.000 0.000 0.000 0.000 chaemaedryoides Salvia ‘Indigo Exotic 5 332 0.090 0.558 0.346 0.003 0.000 0.000 0.000 0.003 0.000 0.000 Spires’ Thymus Exotic 4 66 0.015 0.167 0.015 0.015 0.000 0.000 0.788 0.000 0.000 0.000 nummularius Table 2 (Continued )
No. of Total A. Honey- Bumble- Native Big Small Family Species Origin plants insects manicatum bee bee bee Wasp Ant fly fly Butterfly Other
Myrtaceae Kunzea ericoides Native 4 17 0.000 0.000 0.000 0.059 0.294 0.235 0.000 0.118 0.000 0.294 Leptospermum Native 5 19 0.000 0.053 0.053 0.316 0.368 0.000 0.053 0.157 0.000 0.000 scoparium Metrosideros Native 7 42 0.000 0.524 0.024 0.381 0.024 0.047 0.000 0.000 0.000 0.000 excelsa Metrosideros Native 2 35 0.000 0.400 0.057 0.257 0.000 0.200 0.086 0.000 0.000 0.000 perforate Nyctaginaceae Pisonia Native 1 4 0.000 0.500 0.000 0.000 0.000 0.000 0.000 0.500 0.000 0.000 brunoniana
Plantaginaceae Penstemon Exotic 8 87 0.540 0.254 0.138 0.057 0.011 0.000 0.000 0.000 0.000 0.000 Zealand New in bee wool-carder introduced of Impact ‘Purple Passion’ Veronica Native 5 37 0.000 0.514 0.000 0.000 0.000 0.216 0.216 0.054 0.000 0.000 bishopiana Veronica ‘First Cultivar 2 72 0.028 0.042 0.139 0.666 0.000 0.000 0.097 0.028 0.000 0.000 Light’ Veronica stricta Native 6 169 0.024 0.112 0.130 0.497 0.000 0.053 0.071 0.065 0.018 0.030 Veronica Native 1 10 0.000 0.000 0.000 0.400 0.000 0.000 0.300 0.200 0.000 0.100 salicifolia Veronica ‘Wiri Cultivar 2 53 0.057 0.131 0.403 0.264 0.000 0.063 0.057 0.027 0.000 0.000 Dawn’ Solanaceae Solanum Native 10 35 0.000 0.029 0.029 0.629 0.000 0.143 0.000 0.114 0.000 0.056 laciniatum Violaceae Melicytus Native 1 5 0.000 0.200 0.000 0.800 0.000 0.000 0.000 0.000 0.000 0.000 ramiflorus
Proportions higher than 0.3 are highlighted with grey shading (where plants recorded B10 insect visitors, these were not shaded). 221 222 J Soper and JR Beggs
whereas one A. manicatum individual captured in the Edibles garden on the exotic herb basil (Ocimum basilicum L., Lamiaceae) was carrying Lobelia anceps pollen, which was only available in the native area.
Male territorial behaviour Figure 2 Non-metric multidimensional scaling plot Over a 6-day period, 300 min were spent showing the similarity of flower visitor assemblages recording the behaviour of territorial male from transect counts during December 2009 to June 2010 at the Auckland Botanic Gardens. The stress A. manicatum on Delosperma ‘Alba’. Through- value of 0.18 indicates that the graph is a good out this time, 416 attacks were observed on representation of the multidimensional ordination. conspecific males (33.65%), Apis mellifera The native plant species Veronica stricta is shown in (37.02%), Bombus spp. (17.55%), Lasioglossum black; all three exotic plant species are shown in spp. (6.97%), flies (4.57%); plus a single attack grey. on an unidentified moth (0.22%). There was a highly significant difference host plant could be identified, L. sordidum in the attack rates on different types of insects carried a higher percentage of pollen from the in the territory (analysis of deviance 35.225; host plant in comparison to A. manicatum P ( Chi) 0.0000013). Pairwise comparisons (Table 4). Four A. manicatum individuals cap- showed that the territorial A. manicatum male tured in the native area were carrying 5% attacked native Lasioglossum bees significantly pollen from plants in the Lamiaceae family, less frequently than Apis mellifera, Bombus which were not present in the native area; spp. and conspecific males, when compared
Table 3 Results of analysis of similarities pairwise tests for differences between plant species groups with R value and significance level.
Groups R statistic Significance level (p)
Veronica stricta, Stachys spp. 0.556 0.001 Veronica stricta, Penstemon ‘Purple Passion’ 0.305 0.001 Veronica stricta, Salvia ‘Indigo spires’ 0.564 0.001 Stachys spp., Penstemon ‘Purple Passion’ 0.096 0.001 Stachys spp., Salvia ‘Indigo spires’ 0.597 0.001 Penstemon ‘Purple Passion’, Salvia ‘Indigo spires’ 0.452 0.001
Table 4 Mean% pollen load of Anthidium manicatum and Lasioglossum sordidum captured on plants at the Auckland Botanic Gardens. Native plants are shaded.
No. of Mean percentage (%) Mean number of types of Bee species Plant captured on bees pollen from capture plant pollen grains ( 5%)
L. sordidum Lobelia anceps 9 71.94 (912.07 SEM) 1.56 (90.24 SEM) A. manicatum Lobelia anceps 4 33.29 (917.63 SEM) 3.00 (90.71 SEM) A. manicatum Lamium purpureum 8 45.73 (910.53 SEM) 3.38 (90.56 SEM) A. manicatum Ocimum basilicum 2 31.96 2 33.43 4 Impact of introduced wool-carder bee in New Zealand 223
Table 5 Pairwise comparisons of the rate of attacks by the territorial male Anthidium manicatum on different insect visitors to Delosperma ‘Alba’.
Estimate SED z value p value Ratio LL95 UL95
BB-HB 0.4605 0.4676 0.9849 0.3247 0.6310 0.2477 1.6074 NB-HB 2.4154 0.6947 3.4768 0.0005 0.0893 0.0223 0.3585 Fly-HB 1.0618 0.7964 1.3333 0.1824 0.3458 0.0703 1.7006 Male-HB 0.4656 0.3926 1.1859 0.2357 1.5930 0.7264 3.4932 NB-BB 1.9549 0.7464 2.6190 0.0090 0.1416 0.0318 0.6300 Fly-BB 0.6013 0.8419 0.7143 0.4751 0.5481 0.1018 2.9519 Male-BB 0.9261 0.4782 1.9370 0.0528 2.5246 0.9701 6.5699 Fly-NB 1.3536 0.9863 1.3723 0.1700 3.8712 0.538 27.8316 Male-NB 2.8810 0.7019 4.1044 4.05E 05 17.8318 4.3803 72.5910 Male-Fly 1.5274 0.8027 1.9029 0.0571 4.6063 0.9250 22.9382
The category ‘Other’ has been excluded because other species were rarely seen in the territory. HB, honeybee; BB, bumblebee; NB, Lasioglossum spp; Male, male A. manicatum. with their abundance in the territory (Table 5; percentage of short attacks on Apis mellifera Fig. 3). Although native bees (Lasioglossum (51.57%) was lower compared with the percen- spp.) were the most frequent floral visitors tage for Bombus spp. (67%), flies (89.5%), (36.81%), they received only 6.97% of the attacks. Lasioglossum spp. (93%) and other A. mani- There was a significant difference in the catum males (66.2%). Attacks on Lasioglossum length of attacks by the male A. manicatum on spp. and flies were never longer than 4 s, different types of flower visitors (x2 26.0232; whereas attacks on Apis mellifera, Bombus spp. d.f. 4; PB0.0001). Pairwise comparisons and other A. manicatum males were frequently showed that the mean length of attacks was longer than 4 s, with the longest recorded significantly different between Apis mellifera attack 20 s on one individual of Apis mellifera. and Lasioglossum spp. and flies (Fig. 4). Most attacks were short (2 s or less), although the
Figure 4 Mean (9SEM) length of attacks on honey- Figure 3 Mean attack rate (closed circle) of territor- bees (HB), bumblebees (BB), native Lasioglossum ial Anthidium manicatum male on Delosperma ‘Alba’ spp. (NB), flies (Fly) and conspecific males (Male at the Auckland Botanic Gardens. Error bars WCB) by territorial male Anthidium manicatum on indicate the lower and upper 95% confidence inter- Delosperma ‘Alba’. Bars not connected by the same vals for the means. HB, honeybee; BB, bumblebee; letter are significantly different (Tukey Kramer NB, Lasioglossum spp; Male, male A. manicatum. honestly significant difference) (P 0.05). 224 J Soper and JR Beggs
Lasioglossum spp. were never seen to be chased by human-mediated dispersal (Severinghaus out of A. manicatum territories. In contrast, we et al. 1981; Suarez et al. 2001; Ward et al. recorded instances of displacement from terri- 2006) and this is most likely the case for tories for all other types of flower visitors. A. manicatum. In the USA, 16 of the 17 acci- Two native bees captured on Delosperma dentally introduced bee species (including ‘Alba’ were identified as Lasioglossum cogna- A. manicatum) are cavity-nesting bees (Ascher tum. However, as it was not possible to identify 2001), demonstrating how easily these species all individual native bees by eye while observa- are moved around by humans and also how tions were taking place, they continued to be important it is to detect them at the border. referred to as Lasioglossum spp. The relatively fast spread and establishment of A. manicatum in New Zealand, combined with our temperate climate and the wide availability Discussion of its food plants in urban environments, Anthidium manicatum does not appear to pre- suggest that this species will soon become a sent a major threat to New Zealand’s native common sight in urban parks and gardens flora and fauna as it mostly interacts with across most of New Zealand. However, we exotic species. It was predominantly found to think it unlikely that this species will become be associated with exotic plant species in abundant within most native New Zealand eco- the Lamiaceae and Plantaginaceae families, systems because these will not contain adequate although it was also recorded on two native food resources for this bee. genera, Veronica (Plantaginaceae) and Lobelia Anthidium manicatum was a major compo- (Campanulaceae). It was primarily found shar- nent of the floral visitor assemblage at some ing floral resources with other introduced bees, exotic plant species in the ABG. It accounted Apis mellifera and Bombus spp., and less fre- for more than half of the floral visitors to quently with native New Zealand Lasioglossum Penstemon ‘Purple Passion’ and Stachys spp. spp. Furthermore, although Lasioglossum spp. and accounted for most of the similarity bet- were the most frequent floral visitors in our ween the floral visitor communities of these two study, they received fewer attacks from terri- plants. The close association of A. manicatum torial males than Apis mellifera, Bombus spp. with plants in the Lamiaceae and Planta- and conspecific males, and the attacks on ginaceae (many of which were formerly Scro- Lasioglossum spp. and flies were significantly phulariaceae) is well-documented, both in its shorter than attacks on Apis mellifera. native and introduced ranges (Muller 1996; The range of A. manicatum in New Zealand Schick & Sukopp 1998; Payette 2001; Maier has continued to increase because it was first 2009). Female A. manicatum have a specialized detected in 2006 and is now present in a wide pollen-collecting apparatus on their face, which range of locations from Whangarei to Christch- is used to enhance pollen release from the urch. As we did not systematically survey for nototribic flowers of these families and their this species, it is likely A. manicatum is present pollen plays an important role in larval nour- in other locations in New Zealand. It is unlikely ishment (Muller 1996). This suggests that these that the spread of A. manicatum in New Zealand ornamental plants play a key role in the dis- is the result of natural dispersal because, in tribution of A. manicatum (Schick & Sukopp general, bees are not good at crossing major 1998; Strange et al. 2011). barriers (Michener 1974) and A. manicatum Anthidium manicatum was rarely found visit- would have had to cross large tracts of unsui- ing native plant species in our study. As table habitat to reach new locations. Species A. manicatum is frequently associated with plants that associate closely with humans and nest in in the Plantaginaceae, it was not surprising to moveable objects are commonly moved around find it on the native V. stricta, along with some Impact of introduced wool-carder bee in New Zealand 225
Veronica cultivars. Likewise, A. manicatum plants that it requires for nectar, pollen and is known to visit plants in the Lobelia genus nest material, which are typically found in (R. Toft, Entecol Ltd, and J. Dugdale, pers. parks and gardens in urban areas. However, comm. 2 February 2010), and as the flowers of the close association of A. manicatum with Lobelia also have nototribic pollen presentation the Plantaginaceae, and to a lesser degree the (Macior 1967), this indicates that these plant Fabaceae and Asteraceae, may possibly aid its species may be favoured by A. manicatum as spread into natural areas. Nevertheless, many a source of pollen. Foraging from flowers with native New Zealand plants flower during the a similar morphology is known to result in a winter, so flowering does not coincide with the higher foraging efficiency (Westerkamp & November May flight period of A. manicatum Classen-Bockhoff 2007). In the USA, A. (Soper 2011). For example, ko¯whai (Sophora manicatum has only been recorded on one native microphylla Aiton, Fabaceae) flowers from plant species, roundhead lespedeza (Lespedeza August to October and pu¯riri (Vitex lucens capitata Michx., Fabaceae) (Maier 2009) and Kirk, Lamiaceae) flowers from May to October collecting nest material from another, eastern (New Zealand Plant Conservation Network cottonwood (Populus deltoides W. Bartram ex 2012). Also, many native plants that may be Marshall, Salicaceae) (Kurtak 1973 in Strange et attractive to A. manicatum, such as the nation- al. 2011). Instead it is most frequently associated ally critical New Zealand skullcap (Scutellaria with plants of European and Asian origin (Gibbs novae-zelandiae Hook.f., Lamiaceae), have & Sheffield 2009). Similarly, A. manicatum was restricted ranges limiting their availability as a not recorded on any native plants in the food plant. Christchurch Botanic Gardens, where instanta- The spread of exotic weeds is a major neous counts on native and exotic plant species problem in New Zealand and exotic bee species included six native Veronica species and two are believed to play a major role in the pollina- native Asteraceae species (Webber et al. 2012). tion of some weed species (Newstrom & Anthidium manicatum may visit other native Robertson 2005). For example, the introduced New Zealand plants that were unavailable in bee Apis mellifera is the most important polli- our study area. The most likely candidates are nator of wild broom (Cytisus scoparius L, those in families with which the bee has a close Fabaceae) in New Zealand (Paynter et al. association elsewhere, such as the five native 2010), and the naturalized solitary orchid bee species of Lamiaceae. Plant species in the Euglossa viridissima Friese (Apidae) was the Fabaceae are known to be an important source main pollinator of the invasive shrub Solanum of pollen for A. manicatum (Muller 1996), but torvum Sw. (Solanum) at a forest site in Florida there were no exotic Fabaceae species present (Liu & Pemberton 2009). Anthidium manicatum at the ABG (Yvonne Baker, Botanical Records has been recorded on at least eight plant species Officer, ABG, pers. comm. 18 July 2011) and that are categorized as weeds (Roy et al. 2004), native Fabaceae were only present in low suggesting that this recently introduced polli- numbers (one individual of coastal tree broom nator may have the potential to contribute to was included in the transects but it was in the spread of exotic weeds in New Zealand. For flower for only a short time). Novel plant example, it is known to visit purple loosestrife associations in New Zealand may also be (Lythrum salicaria L, Lythraceae) (Payette possible if plants offer suitable nesting material. 2001; Maier 2009), which is a pest plant banned We only detected female A. manicatum collect- from propagation and sale in New Zealand ing nesting material from Stachys spp. at the (MAF Biosecurity New Zealand 2008). ABG. In general, there is not a lot of cross-over The spread of A. manicatum into natural between native and exotic plant pollinator areas may be restricted by the availability of the webs. In our study, native bees were the most 226 J Soper and JR Beggs frequent floral visitors to most native plants, of pollinators (King & Sargent 2012). If A. mani- and they only occasionally visited exotic plants catum has a different level of floral constancy along the transects. Similarly, at the Christch- than native pollinators, then it may alter the urch Botanic Gardens, Webber et al. (2012) reproductive success of plants. We found that found that native insects accounted for 70.1% A. manicatum carried significantly more types of the visitors to native plants, whereas exotic of pollen than L. sordidum, and less pollen from insects were predominantly found on exotic the plant on which they were captured, suggest- plant species (70.4%). We did observe native ing that the Lasioglossum bees in our study Lasioglossum bees and A. manicatum sharing displayed higher floral constancy and that they floral resources on some exotic plant species, were potentially a more reliable pollinator of although this was infrequently recorded during Lobelia anceps,incomparisontoA. manicatum. our transect counts. In other locations there However, as A. manicatum was not displacing the may be a greater degree of overlap with native native pollinator in this case, it seems unlikely bees, such as with Halictinae females, which are that it would have a measurable effect on the known to forage on a wide range of native and reproductive success of Lobelia anceps.Consid- exotic flowering plant species (Donovan 2007). erably more research is required to evaluate these Although male A. manicatum did attack less obvious impacts on other species, but in any native Lasioglossum bees in our study, they case it would only be a problem where there was attacked conspecific males, Apis mellifera and significant overlap and displacement of native Bombus spp. more frequently. In a similar study pollinators. in Germany, Wirtz et al. (1988) found that The introduction of a new pollinator can although Halictidae bees represented 18.1% of be beneficial, detrimental or neutral for native the floral visitors, they received only 1.5% of plants, and if a new species is an effective the attacks, whereas A. mellifera represented pollinator, then it can provide additional polli- 42.3% of the floral visitors and received 80.2% nation services. Many native New Zealand of the attacks. Lasioglossum spp. may be plants are at risk, because of the loss of native ‘overlooked’ by the territorial male because of pollinators and competition from exotic weeds, their small size and/or may not be seen as such for example the nationally vulnerable napuka a threat to the territory holder as larger intru- (Veronica speciosa A. Cunn. Andersen, Planta- ders. As A. manicatum and Lasioglossum spp. ginaceae) (Armstrong & de Lange 2005). The did not co-occur in high numbers and attacks introduction of A. manicatum into the New on native bees were less frequent than those on Zealand environment may provide benefits for other bee species, it is unlikely that there were pollination systems in New Zealand should any substantial negative impacts on the fora- it prove to be an effective pollinator of native ging of native Lasioglossum bees. However, species. However, the preference of A. mani- these observations were only undertaken on a catum for visiting ornamental plants from single plant in a single location and further the Lamiaceae and Plantaginaceae families in observations, particularly on some of New urban environments, suggests that this new Zealand’s larger native bees, would be neces- pollinator may provide few benefits to native sary to extend the validity of this conclusion. plants. Should A. manicatum be found to Experiments that remove the territorial male contribute to the spread of invasive weeds in A. manicatum would also be useful to explore New Zealand, it may further contribute to the differences in the floral visitor community with decline of some native plants. Although further and without the presence of the male. work is required in other locations, at this point The presence of introduced species in a we conclude that A. manicatum is unlikely to pollinator web can disrupt pollination services pose a major direct threat to New Zealand’s to native plants by altering the floral fidelity native flora and fauna because it is mostly Impact of introduced wool-carder bee in New Zealand 227 interacting with a restricted range of exotic bee and interpretation. 2nd edition. Plymouth, PRI- and exotic plant species. MER-E. p.1-1 17-17. Donovan BJ 2007. Apoidea (Insecta:Hymenoptera). Fauna of New Zealand 57: 1 295. Acknowledgements Gibbs J, Sheffield CS 2009. 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Thorpe for help with identifying native bees; Sandra Kelly D, Robertson AW, Ladley JJ, Anderson SH, Anderson for assistance with fieldwork and pollen McKenzie RJ 2006. Relative (un)importance of classification; Kelly Booth for assisting with PRI- introduced animals as pollinators and dispersers MER and laboratory work; Vivian Ward for assis- of native plants. Ecological Studies 186: 227 245. tance with the figures and Kathy Ruggiero and Kelly D, Ladley JJ, Robertson AW, Anderson SH, James Russell for assistance with statistics. We are Wotton DM, Wiser SK 2010. Mutualisms with- in the wreckage of an avifauna: the status of grateful to everyone from around New Zealand who bird pollination and fruit dispersal in New sent A. manicatum specimens, photographs and new Zealand. New Zealand Journal of Ecology 34: location and/or plant association information and to 66 85. Barry Donovan for answering our bee questions. Kevan PG, Baker, HG 1983. 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