Insect Flower Visitors of Planted Native Species Within the Arable Landscape

Beneficial Insects 198

agricultural intensification and the paucity of To determine whether native plantings on Insect ower visitors of planted native species within semi-natural habitats can also impact ecosystem arable farms support pollinator diversity the the arable landscape on the Canterbury Plains, service providers like insect pollinators current study, conducted over an entire summer (Morandin & Kremen 2013) and insect pest season, documented insect flower visitors on New Zealand regulators (Davidson et al. 2015; Fontaine et al. eight native tree species planted on three farms. 2006). This information is required to assess whether Franziska G. Schmidlin1,*, Jon J. Sullivan1, Mike H. Bowie1 and Brad G. Howlett2 With the worldwide decline of honey bee such plantings can assist in supporting a diversity populations, thought to be due to a combination of known arable crop pollinators. 1 Agriculture and Life Sciences Division, Lincoln University, PO Box 84, Lincoln 7647, New of habitat loss, agrochemicals, pathogens and Zealand climate change (Potts et al. 2010), the future METHODS 2 e New Zealand Institute for Plant & Food Research Limited (PFR), Private Bag 4704, regarding long-term crop-pollination service is Study system Christchurch Mail Centre, Christchurch 8140, New Zealand uncertain. It is risky to rely on a single species Three farms within 50 km of Rakaia, Canterbury * Corresponding author: [email protected] to pollinate crops and produce food (Klein et al. (43º 33’ 56’’ S, 171º 41’ 35’’ E, 7 m above sea level, 2007; Potts et al. 2010). Preserving landscapes 43º 53’ 39’’ S, 171º 50’ 46’’ E, 21 m, and 43º 53’ Abstract Almost all of the original native vegetation of Canterbury Plains has been replaced that support wild pollinator populations can 32’’ S, 172º 06’ 55’’ E, 172 m) were assessed. All with an arable landscape of managed exotic vegetation. A previous study planted small be regarded as an important, and prudent, three conventionally managed farms had native areas of native trees on arable farms in 2013 to enhance the abundance and diversity of insurance against potential failures in crops biodiverse plantings established in October 2013 beneficial insect crop pollinators. The aim of the current study was to assess insect flower pollinated predominantly by honey bee (and as part of a project funded by the Foundation for visitation at three sites in the fifth year after planting. Weekly standardised surveys of native bumble bee) populations. Native or semi-native Arable Research and the Sustainable Farming flower visitors were conducted between September 2017 and February 2018. A total of 2349 habitats within agricultural landscapes can Fund. All plantings are located in the vicinity of insects from 37 taxa were observed within three native plantings. Native bees (Lasioglossum increase wild bee populations (Jauker et al. 2009; crop fields. In 2017/2018, the adjacent crops were sordidum 20%) and the honey bee, Apis mellifera (19%), were the most common followed Lentini et al. 2012; Ponisio et al. 2016; Venturini seed crops of ryegrass Lolium perenne, mustard by the large hoverfly,Melangyna novaezelandiae (16%). The calliphorid flies, brown blowfly et al. 2017). This can support increased yields or Sinapis alba, red clover Trifolium pratense, and Calliphora stygia (8%) and blue blowfly Calliphora vicina (6%), were also well represented. yield consistency due to their complementarity flax Linum usitatissimum. Spacing between The most abundant insects visited four or more of the eight study plant species. Most (52%) with pollination services, for example through seedlings within the native plantings was 1.5 m of the flower visitors where natives. Many of these insects are known crop pollinators and it diversifying pollen transfer pathways (Garibaldi x 1.5 m throughout. The plantings were between is likely that they assist with crop pollination. et al. 2013), differing activity patterns under 300 m2 and 440 m2 and each consisted of 30–34 variable weather conditions (Howlett et al. species, including 26 species that were shared Keywords: agriculture, ecosystem services, pollination, native restoration, semi-natural 2013a) or seasonal activity (Howlett et al. 2016). across all sites. Eight of these shared species (see habitats, pollinator resource, crop pollination. In a recent analysis of 39 studies conducted in Table 1) were in bloom the season before and several countries across different continents, could, therefore, be tagged as study specimens. Rader et al. (2016) highlighted the significant The plantings were divided into six sections INTRODUCTION a wider range of crops and makes pollination role that non-bee insect pollinators play in global of even size, the midpoint of each section was Little is known about the importance of services more resilient to environmental change crop production. A diversity of insect species selected, then the closest tree to the midpoint perennially flowering woody vegetation in (Rader et al. 2013). The Canterbury Plains has (both bees and non-bees) visit the flowers of of the given species was chosen as marked supporting pollinating insects in New Zealand undergone significant agricultural intensification arable crops on the Canterbury Plains. These specimen. Each marked specimen was visited (Howlett et al 2013a) but such vegetation is since European settlement and is currently crops include pak choi Brassica rapa subsp. and, if in bloom (>20% open flowers per bush), known to support arthropod biodiversity dominated by livestock (particularly dairy) chinensis (Howlett et al. 2009), onion Allium observed weekly. One of the three farms had an (Fukuda et al. 2011). Intensively farmed, large- and arable farming (Dynes et al. 2010) notably cepa (Howlett et al. 2005), carrot Daucus carota apiary of 24 honey-bee colonies permanently scale arable landscapes areas are dominated by oilseed rape, other brassicas, clover, onions, subsp. sativus (Howlett et al. 2015), and radish placed at the edge of the native planting. single mass-flowering crops resulting in large carrots, radishes as well as wind-pollinated Raphanus ativus (Howlett et al. 2013b). Native fluctuations in floral resources during the season. grains and grasses. In such environments, the bees, bumblebees and several fly species have Flower visitor surveys Stavert et al. (2018) showed that agricultural high variation in floral resource availability for been verified as pollinators of pak choi (Howlett Between September 2017 and February 2018, intensification can increase exotic pollinators pollinators is thought to make it difficult for et al. 2011; Rader et al. 2009), onion (Howlett insect observation surveys were conducted (mainly Eristalis tenax) and compensate for large wild populations of pollinators to persist et al. 2017), carrot (Howlett 2012) and other weekly on the eight chosen native plant species. the loss of native pollinators. However, it is a (Dicks et al. 2015). Furthermore, the widespread vegetable seed fields in Canterbury (B. Howlett Two-minute surveys of flower visitors were biodiverse pollinator composition that supports use of pesticides and herbicides associated with unpublished data). conducted on the north and south side of each

New Zealand Plant Protection 71: 198-206 (2018) https://doi.org/10.30843/nzpp.2018.71.170 Beneficial Insects 199

New Zealand Plant Protection 71: 198-206 (2018) https://doi.org/10.30843/nzpp.2018.71.170 Beneficial Insects 200

plant. Each week, the order of farm visits was Lasioglossum bees were as abundant as honey 2349 4.3 0.2 3.7 19.2 1.5 0.2 15.5 3.7 3 1.8 6.1 altered. This resulted in varied observation times bees overall and more abundant on some 20.0 Total between 9:00 and 15:00. Observations were not flowers. The hoverfly Melangyna novaezelandiae made unless the wind speed was less than 15 km/h, was the only insect observed visiting all eight temperature was higher than 12ºC and no rainfall tree species. Bees and wasps (Hymenoptera) in tenax tenax 68 5.9 - - 25 11.8 7.4 8.8 - 17.6 - - 20.6 was occurring. total comprised 45.8% of the total flower visitors G.Forst. Phormium Each landing of an insect on an open flower with flies (Diptera) representing 52.4% (Table et J.R.Forst. was recorded. Insect identifications was made by 1). The remainder were Lepidoptera (1.3%) and b one to two researchers trained to recognise the Coleoptera (0.6%) although all surveys were known insect pollinators and common flower diurnal and so did not account for potential Breitw. et Breitw. J.M.Ward (G.Forst.) (G.Forst.) 411 0.7 - 11.9 1 1.5 - 35.8 1.9 0.2 2.9 2.7 visitors. Where possible, unknown flower visitors nocturnal insect activity. Unexpectedly, the site 16.3 leptophyllus Ozothamnus were caught and identified later. Most visitors with nearby honey-bee hives, did not contain the could be identified to species or genus. Tiny highest A. mellifera count but did, however, show insects (<3 mm) such as thrips were not recorded 50% more Lasioglossum spp. than Apis mellifera. nor collected as they have not been shown to be The most abundant flower visitors were 187 - - 1.1 7 - - 52.9 1.6 10.7 2.7 12.9 1.1 scoparium scoparium J.R.Forst. et J.R.Forst. significant pollinators of pak choi (Walker et al. seen at four or more of the eight tree species var. G.Forst. 2009) or onion (Walker et al. 2011) and their surveyed, with four insect taxa visiting 7–8 tree Leptospermum importance as pollinators in other crops has not species (Table 1). All of these insects could be de 93 4.3 - 11.8 4.3 - - 47.3 - 2.2 1.1 1.1 been assessed in New Zealand. considered generalist flower visitors as the eight 20.4 Kunzea Kunzea Toelken Lange et Lange

As the focus of this study was to identify trees represent a range of plant families and serotina the flower-visiting species associated with the floral structures. However, even among the most established native plants on arable farms and generalist insect pollinators (generalists visit species plant Flowering 872 4.8 0.5 2.9 33.5 1.8 - 1.4 7.2 - 1.4 2.3 31.4 G.Forst.

their occurrence across the plant species, formal several plant species (Maldonado et al. (2013)), Veronica salicifolia

statistical analyses were not considered necessary some tree species appeared to be favoured. For to achieve this aim. example, while Leioproctus bees visited seven of the eight tree species, most of these visits were 96 1 - - - - - 7.3 1 - 6.2 16.7 54.2 Raoul Discaria Discaria RESULTS to Carmichaelia australis (45.1%) or Veronica toumatou A total of 2,349 flower visiting insects were salicifolia (41.2%). In contrast, while Melangyna counted in the biodiverse plantings across the novaezelandiae visited all tree species, most visits Endl. 563 0.4 - 0.2 19.7 0.9 - 8.3 2.3 6.2 1.2 12.4 three arable farms (Table 1). Bio-status could be were to Ozothamnus leptophyllus (40.4%) or 7.3 australis australis (Forst.f.) (Forst.f.) assigned unambiguously to 97% of the insects; Leptospermum scoparium (27.2%). Cordyline 52.0% of these were natives. The eight most Most tree species attracted a variety of insect abundant flower visitors, that made up 80.4% flower visitors, from five (Carmichaelia australis) R.Br. of all visitors, were, in decreasing abundance, to 25 (Veronica salicifolia) insect taxa (Table 1). 59 78 - - 15.3 - - 3.4 - - - - - Lasioglossum sordidum (native Halictidae), Flies dominated the flower visitors for some tree Carmichaelia australis Apis mellifera (exotic Apidae), Melangyna species, especially Leptospermum scoparium a,n novaezelandiae (native Syrphidae), Calliphora (87.7% Diptera), Ozothamnus leptophyllus a,n

a,e

stygia (exotic Calliphoridae), Calliphora vicina (78.8% Diptera), Cordyline australis (71.4% a,e a,e n a,n a,n (exotic Calliphoridae), Leioproctus species Diptera), and Kunzea serotina (71.0% Diptera). In a,e a,e a,e n spp.

(native Colletidae, a mix of L. pango, L. boltoni, contrast, bees and wasps dominated the visitors spp. and L. fulvescens), Odontomyia spp. (native to Carmichaelia australis (94.9% Hymenoptera), spp. Stratiomyidae), and Eristalis tenax (exotic Veronica salicifolia (72.3% Hymenoptera), and Syrphidae) (Table 1). Phormium tenax (70.6% Hymenoptera). Discaria # visitors: Lasioglossum sordidum Bombus terrestris Melangyna novaezelandiae Eristalis tenax Linnaeus,1758 (Linnaeus,1758) (Linnaeus,1761) 1855) (Macquart, (Linnaeus, 1758) 1848) (Walker, 1826) (Meigen, Leioproctus Bombus hortorum Calliphora vicina Dilophus nigrostigma sericata Lucilia (Linnaeus, 1758) Odontomyia (Smith,1853) Apis mellifera toumatou visitors were 55.2% Hymenoptera and Hylaeus Of the flower visitors, honey bees (Apis 43.8% Diptera. mellifera) was not always the most abundant Flower visitor taxa visitor Flower # visited # visited species: Hymenoptera 7 4 Diptera 8 5 7 1 6 5 5 5 nor generalist pollinator observed (Table 1). 7 Total number of insect flower visitors to eight species of planted native trees at three Canterbury Plains arable farms, and the percentage and the percentage farms, arable Plains at three Canterbury trees native planted speciesof to eight visitors insect flower of number 1 Total Table row on first the Values species”). species (“# visited visited plant of number total is of insectthe each On the left thesetaxon taxon. in each of Otherwise, percentages. all are values species (“# visitors”). plant each visited insects that of number the total are Beneficial Insects 201

their occurrence across the plant species, formal several plant species (Maldonado et al. (2013)), Veronica salicifolia

a,e

s Some tree species attracted many more flower <0.1 0.2 0.2 0.7 0.4 0.9 0.1 3.5 8.3 1.8 1.5 0.8 0.3 0.1 <0.1 <0.1 0.5 0.2 <0.1 1.1 <0.1 <0.1 <0.1 visitors than others, with over half of insect flower visits recorded being on two plant species: Veronica salicifolia (37.1%) and Cordyline australis (24.0%). However, this measure ------2.9 ------combines floral attractiveness and the intensity of flowering in the surveyed season. The latter condition is likely to vary considerably with year and plant age. - - 0.2 3.4 - 2.2 - 9.7 0.2 1.7 4.6 - 0.5 - 0.2 - 1.5 - - 0.2 0.2 - 0.2 DISCUSSION The biodiverse plantings at our study sites supported a diverse range of pollinating insects during the spring and summer months, which are critical flowering periods for seed crops - - - - 3.7 - - 0.5 4.8 - - 0.5 - - - - 0.5 ------that benefit from insect pollination (Howlett et al. 2016). Many of the insects recorded are known crop pollinators and it is plausible that - - - 1.1 - - - 2.2 - 1.1 2.2 ------1.1 - - - - these plantings boost on farm crop-pollinator populations early in the season. The ability of woody plantings to enhance the pollination of adjacent crops has been demonstrated elsewhere - 0.6 0.3 0.1 0.2 0.5 - 1.1 - 3.7 1.6 1.3 0.1 0.3 - 0.1 0.2 - - 2.5 - 0.1 - (e.g. in the Central Valley of California, USA;

at the inland site, currently regarded as part of Ozothamnus part as of regarded currently site, the inland leptophyllu at Morandin & Kremen (2013)). It is known that pollinators readily move to and from flowering crops fields (Mesa et al. 2013) and several 1 - - - - 1 - 6.2 1 - - 4.2 ------species (flies and bees) move at least 400 m into the surrounding landscape (Rader et al. 2011). However, insect species would be expected to - - - - - 1.1 0.4 4.1 32.9 0.4 0.2 0.4 0.5 - - - - 0.7 - 0.4 - - - vary in their frequency and distance dispersal out from these native habitats, depending on their life cycles, behaviour and the attractiveness of nearby crops outside of native plantings. It is notable that several of the insect species - - - - 1.7 ------1.7 ------recorded in the current study were at least as abundant and generalised in their utilisation n

e of flowering plant species as honey bees. Such

e e

e insects have the potential to provide valuable e a,e Ozothamnus vauvilliersii Ozothamnus the taxon includes a,n

spp. pollination to crop fields, augmenting and e

a,e n

n e

n complementing the pollination provided by a,n managed honey bees. At this point in time, the spp. spp management of wild pollinating species has been poorly explored in New Zealand, although one other Coleoptera other other Lepidoptera other other Tachinidae other other Syrphidae other other Hymenoptera Hymenoptera other (wasps) Helophilus seelandicus other Calliphoridae other Melanostoma Melanostoma fasciatum varia Oxysarcodexia Calliphora quadrimaculata Musca domestica Pollenia Hydrotaea rostrata Protohystricia Coccinella undecimpunctata itea Vanessa Pales usitata Asilidae Pieris rapae Hermetia illucens Hermetia Scaptia Calliphora stygia Muscidae other (Fabricius, 1794) (Fabricius, 1850) (Macquart, 1836) (Walker, 1787) (Swederus, Linnaeus, 1758 1901) (Hutton, (Linnaeus, 1758) 1790 Gmelin, Linnaeus, 1758 (Fabricius, 1775) (Fabricius, (Robineau-Desvoidy, (Robineau-Desvoidy, 1830) (Linnaeus 1758) bee species Leioproctus huakiwi Donovan, 2007 (Donovan et al. 2010) has been successfully established at a site located on The New Zealand exotic or native native or exotic Ozothamnus leptophyllus

recognised crop pollinator pollinator recognised crop 1 1 2 3 3 1 (G.Forst.) Breitw. & J.M.Ward (Breitwieser & Ward 1997). & Ward (Breitwieser & J.M.Ward Breitw. (G.Forst.) 4 4 4 4 3 2 1 1 Coleoptera 5 Lepidoptera 3 1 1 1 1 1 4 Other unidenti ed species to 6 a b e/n Institute for Plant & Food Research Limited farm Beneficial Insects 203

e of flowering plant species as honey bees. Such e e

e insects have the potential to provide valuable e a,e Ozothamnus vauvilliersii Ozothamnus the taxon includes a,n

spp. pollination to crop fields, augmenting and e a,e n n e n complementing the pollination provided by a,n managed honey bees. At this point in time, the spp. spp management of wild pollinating species has been poorly explored in New Zealand, although one other Coleoptera other other Lepidoptera other other Tachinidae other other Syrphidae other other Hymenoptera Hymenoptera other (wasps) Helophilus seelandicus other Calliphoridae other Melanostoma Melanostoma fasciatum varia Oxysarcodexia Calliphora quadrimaculata Musca domestica Pollenia Hydrotaea rostrata Protohystricia Coccinella undecimpunctata itea Vanessa Pales usitata Asilidae Pieris rapae Hermetia illucens Hermetia Scaptia Calliphora stygia Muscidae other (Fabricius, 1794) (Fabricius, 1850) (Macquart, 1836) (Walker, 1787) (Swederus, Linnaeus, 1758 1901) (Hutton, (Linnaeus, 1758) 1790 Gmelin, Linnaeus, 1758 (Fabricius, 1775) (Fabricius, (Robineau-Desvoidy, (Robineau-Desvoidy, 1830) (Linnaeus 1758) bee species Leioproctus huakiwi Donovan, 2007 (Donovan et al. 2010) has been successfully established at a site located on The New Zealand exotic or native native or exotic Ozothamnus leptophyllus

recognised crop pollinator pollinator recognised crop 1 1 2 3 3 1 4 (G.Forst.) Breitw. & J.M.Ward (Breitwieser & Ward 1997). & Ward (Breitwieser & J.M.Ward Breitw. (G.Forst.) 4 4 4 3 2 1 1 Coleoptera 5 Lepidoptera 3 1 1 1 1 1 4 Other unidenti ed species to 6 a b e/n Institute for Plant & Food Research Limited farm Beneficial Insects 204 near Christchurch, Canterbury, New Zealand. REFERENCES native flower visitors to onions. New Zealand from main habitat. Landscape Ecology 24(4): Considerable variation in the size and Breitwieser I, Ward JM 1997. Transfer of Cassinia Plant Protection 58: 213-218. 547-555. composition of the pollinator communities leptophylla (Compositae) to Ozothamnus. Howlett BG, Walker MK, Newstrom-Lloyd LE, Klein A, Vaissière B, Cane J, Steffan-Dewenter across the different tree species was documented. New Zealand Journal of Botany 35(1): 125- Donovan BJ, Teulon, DAJ 2009. Window I, Cunningham S, Kremen C, Tscharntke T This study suggests that there is potential for 128. traps and direct observations record similar 2007. Importance of pollinators in changing enhancing crop pollination through increased Davidson MM, Howlett BG, Butler RC, Taylor arthropod flower visitor assemblages in two landscapes for world crops. Proceedings. pollinator diversity resulting from the presence NM, Walker MK 2015. The influence of mass flowering crops. Journal of Applied Biological Sciences, 274(1608): 303-13. of native biodiverse plantings on arable farms. In shelterbelts in arable farmland on beneficial Entomology, 133(7): 553-564. Lentini, PE, Martin, TG, Gibbons P, Fischer addition to pollinating insects, these plantings and pest invertebrates. New Zealand Plant Howlett BG, Walker MK, Rader R, Butler RC, J, Cunningham SA 2012. Supporting wild may also provide other ecosystem services to Protection 68: 367-372. Newstrom-Lloyd LE, Teulon DAJ 2011. Can pollinators in a temperate agricultural cropping systems such as supporting arthropods Dicks, LV, Baude M, Roberts SPM, Phillips insect body pollen counts be used to estimate landscape: Maintaining mosaics of natural that predate on pest insects (Howlett et al. J, Green M, Carvell, C 2015. How much pollen deposition on pak choi stigmas? New features and production. Biological 2013a). However, our understanding of the flower-rich habitat is enough for wild Zealand Plant Protection 64: 25-31. Conservation 149(1): 84-92. factors that could significantly influence species pollinators? Answering a key policy question Howlett BG 2012. Hybrid carrot seed crop Maldonado MB, Lomáscolo SB, Vázquez composition and distribution of arthropod with incomplete knowledge. Ecological pollination by the fly Calliphora vicina DP 2013. The importance of pollinator assemblages on arable farms remains limited. Entomology 40: 22-35. (Diptera: Calliphoridae). Journal of Applied generalization and abundance for the The full economic and non-economic value Donovan BJ, Howlett BG, Walker MK 2010. Entomology 136(6): 421-430. reproductive success of a generalist plant. of such plantings requires further study. This Relocation and establishment of nesting Howlett BG, Davidson MM, Mathers D, Pyke PLoS ONE. 2013:8(10):e75482. includes the diversity of native and exotic insect populations of the native bee Leioproctus NB 2013a. Hedgerow plants to support crop Mesa LA, Howlett BG, Grant JE, Didham RK arthropods they support, aesthetic values, the huakiwi Donovan (Hymenoptera: Colletidae). pollination and pest management. The Weta 2013. Changes in the relative abundance value and consistency of ecosystem services they New Zealand Entomologist 33: 109-113. 46: 3-12. and movement of insect pollinators during deliver to the farm and surrounding land uses. Dynes RA, Burggraaf VT, Goulter CG, Dalley Howlett BG, Butler RC, Nelson WR, Donovan the flowering cycle of Brassica rapa crops: This knowledge is essential to provide grower DE 2010. Canterbury farming: production, B 2013b. Impact of climate change on crop implications for gene flow. Journal of Insect or community incentive to establish similar processing and farming systems. pollinator activity in New Zealand. MPI Science 13: 13. plantings in the future. https://www.grassland.org.nz/publications/ Technical Paper No: 2013/30, Ministry Morandin LA, Kremen C 2013. Hedgerow nzgrassland_publication_5.pdf (accessed 13 for Primary Industries. www.mpi.govt.nz/ restoration promotes pollinator populations ACKNOWLEDGEMENTS April 2018). document-vault/4101 (accessed 13 April and exports native bees to adjacent fields. We are grateful to John Evans, David Ward, and Fontaine C, Dajoz I, Meriguet J, Loreau, M 2006. 2018). 45 pp. Ecological Applications 23(4): 829-839. Ian Marr for access to their farms. Celine Proirier Functional diversity of plant–pollinator Howlett BG, Lankin-Vega GO, Pattemore DE Ponisio LC, M’Gonigle LK, Kremen, C 2016. provided invaluable assistance with the field work. interaction webs enhances the persistence of 2015. Native and introduced bee abundances On-farm habitat restoration counters biotic Sam Read (PFR) assisted with project logistics and plant communities (pollinator diversity and on carrot seed crops in New Zealand. New homogenization in intensively managed insect identification. Thanks to Melanie Davidson ecosystem sustainability). PLoS Biology 4(1). Zealand Plant Protection 68: 373-379. agriculture. Global Change Biology: 22(2). (PFR) for her valuable inputs in experiment Fukuda Y, Moller H, Burns B 2011. Effects of Howlett BG, Davidson MM, Pattemore DE, 704-715. design. We also thank the Foundation for Arable organic farming, fencing and vegetation Walker MK, Nelson WR 2016. Seasonality Potts SG, Biesmeijer JC, Kremen C, Neumann Research who provided critical support for the origin on spiders and beetles within of calliphorid and sarcophagid flies P, Schweiger O, Kunin WE 2010. Global establishment of the Biodiverse plantings on shelterbelts on dairy farms. New Zealand across Canterbury arable farms requiring pollinator declines: trends, impacts and arable farms. We acknowledge the New Zealand Journal of Agricultural Research 54(3): 155- pollinators. New Zealand Plant Protection drivers. Trends in Ecology & Evolution 25(6): Organisms Register (www.nzor.org.nz/) and 176. 69: 290-295. 345-353. NatureWatch NZ (www.naturewatch.org.nz/) Garibaldi LA, Steffan-Dewenter I, Winfree R, Howlett BG, Evans LJ, Pattemore DE, Nelson WR Rader R, Howlett B, Cunningham S, Westcott as good resources for insect nomenclature and Aizen MA, Bommarco R, Cunningham SA, 2017. Stigmatic pollen delivery by flies and D, Newstrom-Lloyd L, Walker M, Teulon D, identification. This study was supported by the Kremen C, Carvalheiro LG, Harder LD, Afik bees: Methods comparing multiple species Edwards W 2009. Alternative pollinator taxa programme Ministry of Business, Innovation O and others 2013. Wild pollinators enhance within a pollinator community. Basic and are equally efficient, but not as effective as the and Employment C11X1309. fruit set of crops regardless of honey-bee Applied Ecology 19: 19-25. honeybee in a mass flowering crop. Journal of abundance. Science 339: 1608-1611. Jauker F, Diekötter T, Schwarzbach F, Wolters V Applied Ecology 46: 1080-1087. Howlett BG, Donovan BJ, McCallum JA, 2009. Pollinator dispersal in an agricultural Rader R, Edwards W, Westcott D, Cunningham Newstrom LE, Teulon DAJ 2005. Between matrix: opposing responses of wild bees and S, Howlett B 2011. Pollen transport differs and within field variability of New Zealand hoverflies to landscape structure and distance among bees and flies in a human-modified Beneficial Insects 205 near Christchurch, Canterbury, New Zealand. REFERENCES native flower visitors to onions. New Zealand from main habitat. Landscape Ecology 24(4): Considerable variation in the size and Breitwieser I, Ward JM 1997. Transfer of Cassinia Plant Protection 58: 213-218. 547-555. composition of the pollinator communities leptophylla (Compositae) to Ozothamnus. Howlett BG, Walker MK, Newstrom-Lloyd LE, Klein A, Vaissière B, Cane J, Steffan-Dewenter across the different tree species was documented. New Zealand Journal of Botany 35(1): 125- Donovan BJ, Teulon, DAJ 2009. Window I, Cunningham S, Kremen C, Tscharntke T This study suggests that there is potential for 128. traps and direct observations record similar 2007. Importance of pollinators in changing enhancing crop pollination through increased Davidson MM, Howlett BG, Butler RC, Taylor arthropod flower visitor assemblages in two landscapes for world crops. Proceedings. pollinator diversity resulting from the presence NM, Walker MK 2015. The influence of mass flowering crops. Journal of Applied Biological Sciences, 274(1608): 303-13. of native biodiverse plantings on arable farms. In shelterbelts in arable farmland on beneficial Entomology, 133(7): 553-564. Lentini, PE, Martin, TG, Gibbons P, Fischer addition to pollinating insects, these plantings and pest invertebrates. New Zealand Plant Howlett BG, Walker MK, Rader R, Butler RC, J, Cunningham SA 2012. Supporting wild may also provide other ecosystem services to Protection 68: 367-372. Newstrom-Lloyd LE, Teulon DAJ 2011. Can pollinators in a temperate agricultural cropping systems such as supporting arthropods Dicks, LV, Baude M, Roberts SPM, Phillips insect body pollen counts be used to estimate landscape: Maintaining mosaics of natural that predate on pest insects (Howlett et al. J, Green M, Carvell, C 2015. How much pollen deposition on pak choi stigmas? New features and production. Biological 2013a). However, our understanding of the flower-rich habitat is enough for wild Zealand Plant Protection 64: 25-31. Conservation 149(1): 84-92. factors that could significantly influence species pollinators? Answering a key policy question Howlett BG 2012. Hybrid carrot seed crop Maldonado MB, Lomáscolo SB, Vázquez composition and distribution of arthropod with incomplete knowledge. Ecological pollination by the fly Calliphora vicina DP 2013. The importance of pollinator assemblages on arable farms remains limited. Entomology 40: 22-35. (Diptera: Calliphoridae). Journal of Applied generalization and abundance for the The full economic and non-economic value Donovan BJ, Howlett BG, Walker MK 2010. Entomology 136(6): 421-430. reproductive success of a generalist plant. of such plantings requires further study. This Relocation and establishment of nesting Howlett BG, Davidson MM, Mathers D, Pyke PLoS ONE. 2013:8(10):e75482. includes the diversity of native and exotic insect populations of the native bee Leioproctus NB 2013a. Hedgerow plants to support crop Mesa LA, Howlett BG, Grant JE, Didham RK arthropods they support, aesthetic values, the huakiwi Donovan (Hymenoptera: Colletidae). pollination and pest management. The Weta 2013. Changes in the relative abundance value and consistency of ecosystem services they New Zealand Entomologist 33: 109-113. 46: 3-12. and movement of insect pollinators during deliver to the farm and surrounding land uses. Dynes RA, Burggraaf VT, Goulter CG, Dalley Howlett BG, Butler RC, Nelson WR, Donovan the flowering cycle of Brassica rapa crops: This knowledge is essential to provide grower DE 2010. Canterbury farming: production, B 2013b. Impact of climate change on crop implications for gene flow. Journal of Insect or community incentive to establish similar processing and farming systems. pollinator activity in New Zealand. MPI Science 13: 13. plantings in the future. https://www.grassland.org.nz/publications/ Technical Paper No: 2013/30, Ministry Morandin LA, Kremen C 2013. Hedgerow nzgrassland_publication_5.pdf (accessed 13 for Primary Industries. www.mpi.govt.nz/ restoration promotes pollinator populations ACKNOWLEDGEMENTS April 2018). document-vault/4101 (accessed 13 April and exports native bees to adjacent fields. We are grateful to John Evans, David Ward, and Fontaine C, Dajoz I, Meriguet J, Loreau, M 2006. 2018). 45 pp. Ecological Applications 23(4): 829-839. Ian Marr for access to their farms. Celine Proirier Functional diversity of plant–pollinator Howlett BG, Lankin-Vega GO, Pattemore DE Ponisio LC, M’Gonigle LK, Kremen, C 2016. provided invaluable assistance with the field work. interaction webs enhances the persistence of 2015. Native and introduced bee abundances On-farm habitat restoration counters biotic Sam Read (PFR) assisted with project logistics and plant communities (pollinator diversity and on carrot seed crops in New Zealand. New homogenization in intensively managed insect identification. Thanks to Melanie Davidson ecosystem sustainability). PLoS Biology 4(1). Zealand Plant Protection 68: 373-379. agriculture. Global Change Biology: 22(2). (PFR) for her valuable inputs in experiment Fukuda Y, Moller H, Burns B 2011. Effects of Howlett BG, Davidson MM, Pattemore DE, 704-715. design. We also thank the Foundation for Arable organic farming, fencing and vegetation Walker MK, Nelson WR 2016. Seasonality Potts SG, Biesmeijer JC, Kremen C, Neumann Research who provided critical support for the origin on spiders and beetles within of calliphorid and sarcophagid flies P, Schweiger O, Kunin WE 2010. Global establishment of the Biodiverse plantings on shelterbelts on dairy farms. New Zealand across Canterbury arable farms requiring pollinator declines: trends, impacts and arable farms. We acknowledge the New Zealand Journal of Agricultural Research 54(3): 155- pollinators. New Zealand Plant Protection drivers. Trends in Ecology & Evolution 25(6): Organisms Register (www.nzor.org.nz/) and 176. 69: 290-295. 345-353. NatureWatch NZ (www.naturewatch.org.nz/) Garibaldi LA, Steffan-Dewenter I, Winfree R, Howlett BG, Evans LJ, Pattemore DE, Nelson WR Rader R, Howlett B, Cunningham S, Westcott as good resources for insect nomenclature and Aizen MA, Bommarco R, Cunningham SA, 2017. Stigmatic pollen delivery by flies and D, Newstrom-Lloyd L, Walker M, Teulon D, identification. This study was supported by the Kremen C, Carvalheiro LG, Harder LD, Afik bees: Methods comparing multiple species Edwards W 2009. Alternative pollinator taxa programme Ministry of Business, Innovation O and others 2013. Wild pollinators enhance within a pollinator community. Basic and are equally efficient, but not as effective as the and Employment C11X1309. fruit set of crops regardless of honey-bee Applied Ecology 19: 19-25. honeybee in a mass flowering crop. Journal of abundance. Science 339: 1608-1611. Jauker F, Diekötter T, Schwarzbach F, Wolters V Applied Ecology 46: 1080-1087. Howlett BG, Donovan BJ, McCallum JA, 2009. Pollinator dispersal in an agricultural Rader R, Edwards W, Westcott D, Cunningham Newstrom LE, Teulon DAJ 2005. Between matrix: opposing responses of wild bees and S, Howlett B 2011. Pollen transport differs and within field variability of New Zealand hoverflies to landscape structure and distance among bees and flies in a human-modified Beneficial Insects 206

landscape. Diversity and Distributions 17: 519-529. Does pasture plant diversity inuence abundance and Rader R, Reilly J, Bartomeus I, Winfree R 2013. diversity of lacewings and Hymenopteran parasitoids? Native bees buffer the negative impact of climate warming on honey bee pollination Philippa J. Gerard*, Derrick J. Wilson and Anastazia L. Docherty of watermelon crops. Global Change Biology 19: 3103-3110. AgResearch, Ruakura Research Centre, Private Bag 3123, Hamilton, New Zealand Rader R, Bartomeus I, Garibaldi LA, Garratt *Corresponding author: [email protected] MPD, Howlett BG, Winfree R et al. 2016. Non-bee insects are important contributors Abstract The lack of plant biodiversity in New Zealand pastoral ecosystems may limit to global crop pollination. Proceedings of the the abundance and diversity of generalist parasitoids and predators, predisposing these National Academy of Sciences 113(1): 146- ecosystems to pest outbreaks. To test this hypothesis, patches of turf were established in 151. existing pasture during spring 2016. Four treatments of increasing plant complexity were Stavert JR, Pattemore DE, Bartomeus I, Gaskett established, commencing with ryegrass alone, and increasing exponentially up to eight AC, Beggs JR 2018. Exotic flies maintain species of forage plant per patch. In the summer of 2017, insects were collected from the pollination services as native pollinators patches and control plots using suction to assess whether or not plant diversity had influenced decline with agricultural expansion. Journal the abundance and diversity of lacewings and parasitic Hymenoptera aggregating in the of Applied Ecology, 1-10. patches. Plant species richness had no impact on lacewing abundance but fewer parasitic Venturini EM, Drummond FA, Hoshide AK, Hymenoptera were recovered from the ryegrass-only plots compared with more species rich Dibble AC, Stack LB 2017. Pollination plots. Also, a wider range of parasitoid families were represented in the more diverse plant reservoirs for wild bee habitat enhancement treatments compared with the less diverse treatments. Such diversity may have beneficial in cropping systems: a review. Agroecology impacts on the stability of pasture ecosystem and the risk of pest outbreaks. and Sustainable Food Systems 41(2): 101-142. Walker MK, Howlett BG, McCallum JA, Wallace Keywords Biodiversity, pasture, Micromus tasmaniae, parasitoid AR, Teulon DAJ 2009. Small arthropods as pollinators in a New Zealand pak choi field trial New Zealand Plant Protection 62: 92-98. Walker MK, Howlett BG, Wallace AR, McCallum INTRODUCTION main drivers (Tozer et al. 2016). However, there JA, Teulon DAJ 2011. The diversity and Most lowland pastures in New Zealand are based is limited research on terrestrial biodiversity in abundance of small arthropods in onion, on perennial ryegrass (Lolium perenne L.) and production landscapes and how it may impact Allium cepa, seed crops, and their potential white clover (Trifolium repens L.). Ecological on agroecosystem communities and resilience role in pollination. Journal of Insect Science theory suggests that such simple agroecosystems (Moller et al. 2008). Indeed, the lack of plant 11: 98. are inherently unstable, and vulnerable to diversity in pastures is postulated to underlie the invasions (Kennedy et al. 2002) and pest loss of efficacy of Microctonus hyperodae Loan outbreaks (Murdoch 1975). This is supported (Hymenoptera: Braconidae); the biocontrol by long-term international studies which have agent introduced to control the Argentine shown that grassland plant species richness stem weevil (Listronotus bonariensis (Kuschel) strongly affects the colonisation of new species (Coleoptera: Curculionidae) (Goldson et al. 2014; into the community (Weisser et al. 2017) and Tomasetto et al. 2017). The potential benefits of that reductions in plant diversity shift arthropod increasing pasture plant diversity on invertebrate communities from being predator/parasitoid- community composition were demonstrated in dominated to herbivore-dominated (Haddad et a study by Tozer et al. (2016) across five regions al. 2009). in New Zealand. They found that although the Poor pasture persistence is ranked as one of inclusion of the forage herbs chicory (Cichorium the most important factors currently limiting intybus L.) or plantain (Plantago lanceolata L.) farm economic performance in New Zealand, in a grass–legume pasture had no impact on with drought and insect pests implicated as the herbivorous invertebrates, it resulted in a 65%

©2018 New Zealand Plant Protection Society (Inc.) www.nzpps.org Refer to http://www.nzpps.org/terms_of_use.html New Zealand Plant Protection 71: 207-213 (2018) https://doi.org/10.30843/nzpp.2018.71.185