Insect Conservation and Diversity (2018) 11, 13–31 doi: 10.1111/icad.12243
MAJOR REVIEW Insect pollinators collect pollen from wind-pollinated plants: implications for pollination ecology and sustainable agriculture
1,2 MANU E. SAUNDERS 1Institute for Land Water and Society, Charles Sturt University, Albury, NSW, Australia and 2School of Environmental & Rural Sciences/UNE Business School, University of New England, Armidale, NSW, Australia
Abstract. 1. Current research, management and outreach programmes relevant to insect pollinator conservation are strongly focused on relationships between pollinators and insect-pollinated crops and wild plants. 2. Pollinators also visit wind-pollinated plants to collect pollen, or for nest sites and materials, but these interactions are largely overlooked. I review docu- mented records of bee and syrphid fly species collecting pollen from wind-polli- nated plant taxa, including economically important crops, and provide the most comprehensive collation of peer-reviewed records of pollinators visiting wind- pollinated plants to date. I argue for more basic research into functional rela- tionships between insect pollinators and wind-pollinated plants. 3. I found over 200 visitation records for 101 wind-pollinated plant genera in 25 families, including 4 of the 12 gymnosperm families. Almost half the records (49%) were for grasses and sedges (Poales). I also identified records of bees and/or syrphid flies visiting 10 economically important wind-pollinated crop plant species, including three major grain crops (rice, corn, and sorghum). Most records (70%) were from indirect pollen analysis from hives, nest cells or insect bodies, highlight- ing the need for more direct observational studies of plant–pollinator interactions. 4. Insect pollinator communities require resource diversity to persist in a landscape. Hence, researchers and land managers aiming to identify links between pollinators and ecosystem function should also consider broader inter- actions beyond the standard traits of the entomophily syndrome. Key words. Ambophily, anemophily, ecosystem services, functional traits, plant– pollinator interactions, trait linkage.
Introduction can influence plant reproduction and community assem- bly (Moeller, 2004; Biesmeijer et al., 2006; Fontaine Insect pollinators influence the stability, diversity, and et al., 2006). Insect pollinators are under threat from a function of natural and agricultural plant communities variety of human pressures, particularly habitat loss (Tepedino, 1979; Biesmeijer et al., 2006; Garibaldi et al., through land use intensification, and there is an urgent 2011). In agricultural systems, insect pollinators provide need for research and management programmes that ecosystem services by influencing the quality and quan- enhance pollinator populations (Potts et al., 2010; Van- tity of crop yields (Klein et al., 2007; Garibaldi et al., bergen et al., 2013; Archer et al., 2014; Goulson et al., 2013; Rader et al., 2016). In natural systems, pollinators 2015; Manley et al., 2015). However, the success of such programmes is limited by gaps in knowledge of how pol- Correspondence: Manu E. Saunders, School of Environmental linator communities interact with plant communities to & Rural Science/UNE Business School, University of New Eng- influence ecosystem function (Kremen, 2005; De Bello land, Armidale, NSW 2351, Australia. et al., 2010). A particular knowledge gap exists around E-mail: [email protected] the role of wind-pollinated, or anemophilous, plants in
Ó 2017 The Royal Entomological Society 13 14 Manu E. Saunders plant–pollinator communities. Adults of many insect polli- pollen-limited crop varieties that rely on insect pollination nator species visit wind-pollinated plants to collect or feed to produce, or augment, yields (e.g. Aizen et al., 2008; on pollen (hereafter, simply pollen collection) (Fig. 1), and Sheffield et al., 2008; Garibaldi et al., 2011, 2013 and ref- also for non-floral resources, e.g. plant resins or sweet secre- erences therein). In addition, habitat enhancement recom- tions from leaves or stems (Wallace & Trueman, 1995; mendations for supporting pollinator populations (e.g. Nyeko et al., 2002; Leonhardt & Bluthgen,€ 2009), or nest wildflower strips next to crops) mostly focus on nectar- sites and materials (Hurd, 1978; Krombein et al., 1979; rich plants that are attractive to pollinators but rarely Maeta et al., 1985). Yet, much of the recent public dis- promote wind-pollinated plants or trees as potential polli- course around insect pollinator conservation and the man- nator resources (e.g. Haaland et al., 2011; Garbuzov & agement of pollination services has focused on Ratnieks, 2014). Focusing predominantly on pollinator- entomophilous (insect-pollinated) plants as essential attractive plants as essential food resources for insect pol- resources for insect pollinators. linators may make it difficult to convince growers of Wind-pollinated plants, which include at least 10% of wind-pollinated crops to adopt sustainable management angiosperms (i.e. approximately 25 000 species) and most practices that support pollinator conservation in their of the more than 600 gymnosperm species (Faegri & van landscape (e.g. reduced pesticide use, conservation of der Pijl, 1979; Friedman & Barrett, 2009), are rarely con- seminatural habitat). Additionally, if pollen from some sidered as insect pollinator food resources. From a man- wind-pollinated plants is an essential food resource for agement perspective, current knowledge of pollinator pollinators in some regions or seasons, ecological knowl- communities in agroecosystems is dominated by studies of edge of these plant–pollinator relationships needs to be
(a) (b)
(c) (d)
(e) (f)
Fig. 1. Bee and syrphid fly species visit a variety of wind-pollinated plants to collect pollen. (a) European honey bee and (b) Australian syrphid fly collecting hazelnut pollen; (c) Australian Homalictus sp. bee collecting corn pollen; (d) Australian syrphid fly collecting olive pollen; (e) Plantago species are a common pollen source worldwide for bees and syrphid flies; (f) Deciduous trees in temperate regions, such as elms, can be important spring pollen sources for honey bees. Photos: (a, b, d, e) the author; (c, f) Karen Retra. [Colour figure can be viewed at wileyonlinelibrary.com]
Ó 2017 The Royal Entomological Society, Insect Conservation and Diversity, 11, 13–31 Pollinators and wind-pollinated plants 15 incorporated into habitat enhancement programmes for multiple pollination strategies benefit plants and their ani- the persistence of wild pollinator populations. mal visitors. There is an extensive body of literature on how plant– In this review, the aim is to promote recognition of the pollinator interactions influence plant community assem- role of wind-pollinated plants in the natural history of bly (e.g. Waser, 1978; Feinsinger, 1987; Moeller, 2004; insect pollinator species and provide a foundation for fur- Sargent & Ackerly, 2008), but few of these studies have ther research into functional relationships between insect considered the role of wind-pollinated species (e.g. grasses, pollinators and wind-pollinated plants. I review docu- conifers) in structuring plant–pollinator community net- mented interactions between insect taxa known to be works. In addition, many empirical studies of plant–pol- pollinators and plant taxa known or assumed to be wind- linator networks in natural environments are likely to pollinated, which are often overlooked when considering undersample the full suite of plant–pollinator interac- plant resources that insect pollinators rely on for food. I tions in the system (Nielsen & Bascompte, 2007; Chacoff focus on bee (Hymenoptera: Apoidea) and syrphid fly et al.,2012;Rivera-Hutinelet al., 2012; Bartomeus, (Diptera: Syrphidae) species as these are common pollina- 2013) because standard sampling protocols often have a tors encountered in natural and agricultural systems glob- strong focus on flowering plants visible during the survey ally, and both taxonomic groups rely on flowers for food period and rarely observe pollinator visitation across day resources – flies mostly for adult food and bees for both and night, or outside of peak flowering seasons (Waser adult and larval food. I first present results of a system- et al., 1996; Dupont et al., 2003; Bosch et al.,2009; atic review of records of bees or syrphid flies collecting Albrecht et al., 2010). Hence, if pollinator visitation to pollen from wind-pollinated plants that are published in wind-pollinated plants occurs in these systems, it will peer-reviewed journals. I then discuss current knowledge likely be overlooked if floral structures are not obvious, on relationships between insect pollinators and wind-polli- as is often the case with wind-pollinated trees, or if inter- nated plants within the context of pollinator conservation actions occur outside the survey period, e.g. some halic- and agricultural management and identify some key areas tid bees only visit certain grass flowers in the few hours for future research. after sunrise (Adams et al., 1981; Immelman & Eardley, 2000). Wind pollination is thought to have evolved from insect Methods pollination as a response to environmental changes that caused spatial or temporal limitation in pollinator avail- As the first step of the review, I compiled two plant ability (Culley et al., 2002; Friedman & Barrett, 2009). lists. The first list comprised angiosperm and gym- Ambophily (reproduction via a combination of wind and nosperm plant families and genera that are documented insect pollination) has been documented frequently in a as and/or widely considered to be wind-pollinated and variety of plant species (e.g. Sacchi & Price, 1988; Gomez was compiled from Faegri and van der Pijl (1979), & Zamora, 1996; Duan et al., 2009), but it is unclear Eriksson and Bremer (1992) and Ackerman (2000). In whether it indicates the species is in a transitional stage addition to known anemophilous plant families, I between entomophily and anemophily, or whether it is a included commonly known anemophilous genera from reproductive assurance strategy (Culley et al., 2002; De la predominantly entomophilous families (e.g. Populus spp. Bandera & Traveset, 2006). The potential for plant–polli- in the Salicaceae; Fraxinus spp. in the Oleaceae). For nator relationships to vary across time and space is more the recently expanded anemophilous Plantaginaceae, I likely as changes in climate and land use alter global abi- only included the prerevision genera (Bougueria, Lit- otic processes and impact pollinator populations (Mem- torella, Plantago) as the majority of the genera recently mott et al., 2007; Hegland et al., 2009; Potts et al., 2010). added to the family are entomophilous (e.g. Angelonieae Recent evidence has identified insect pollination in plant Martins et al., 2014; Veronica spp. Kampny, 1995). This species presumed to be wind-pollinated, for example the step resulted in a focal list of 1364 plant genera in 50 sedge Rhynchospora ciliata (Vahl) Kukenth€ (Costa & families. The second list consisted of wind-pollinated Machado, 2012), the alpine rush Juncus allioides Franch. crop species that are noted in the literature as being (Huang et al., 2013), and most species in the cycad family wind-pollinated or showing no increase in yield from Zamiaceae (Schneider et al., 2002; Wilson, 2002; Terry insect pollination. This list was compiled from Cunning- et al., 2005). Many gymnosperm taxa have traditionally ham et al. (2002), Abrol (2012), and the supplementary been categorised as wind-pollinated, and are still widely information in Klein et al. (2007). This list comprised considered as such by non-specialists, despite evidence of 23 crop plant species or genera. pollen collection and potential pollination by insects, e.g. As the second step of the review, I conducted separate Thuja occidentalis L. (Avitabile, 1982), Gnetum spp. (Kato database searches of all article fields and all years using et al., 1995; Gong et al., 2016), Ephedra spp. (Niklas, the search term: (bees or syrphid or hover flies or ‘flower 2015; Celedon-Neghme et al., 2016). These examples high- visitors’ or pollinators) + one of the following in each light large gaps in knowledge of plant–pollinator interac- search: (i) plant family name, (ii) all plant genus names tions, particularly how they vary across time and space within each family, (iii) crop species name, and (iv) crop and under different environmental contexts, and how common name. All searches were conducted using the
Ó 2017 The Royal Entomological Society, Insect Conservation and Diversity, 11, 13–31 16 Manu E. Saunders
Web of Science journal database. Searches commenced researchers and managers, rather than a definitive list of in April 2016 and were completed by June 2016. Rele- plant–pollinator interactions. vant papers were also sourced from my personal library and by searching cited literature in papers found during database searches. All studies published Results in peer-reviewed journals or conference proceedings that documented bees or syrphid flies collecting pollen A total of 222 records were found that documented bee from a wind-pollinated plant were included. There is a and/or syrphid fly species collecting pollen from a wind- wealth of anecdotal information available in non-peer- pollinated plant (Table 1). At least 148 wind-pollinated reviewed sources, especially museum catalogues and plant species across 101 genera and 25 families, including collections, but here I restrict my searches to published 4 of the 12 gymnosperm families, were recorded (Table 1). literature available in scholarly databases. I discuss the These families covered a total of 10 plant orders (Data value of these additional sources later in this paper. S1). Almost half the records (108) were for plants in the Many of the search results were pollen analysis studies order Poales (grasses and sedges). Two records were for using samples collected from Apis sp. hives or honey, larval development sites for pollen-feeding larvae in Tox- where individual species are given a ranking based on omerus (Diptera, Syrphidae) species. the proportion of that species’ pollen in the entire pol- Honey bees (Apis spp.) were the most commonly len sample. Because there is potential for honey bees recorded species (114 records), with non-Apis bees (76), to be contaminated with non-target pollen during for- and syrphid flies (26) the next most common. In the non- aging (Rust, 1987; Cane & Sipes, 2006), I did not Apis bee records, 15 documented stingless bees (Melipo- include pollen records that the authors noted as rare nini) and the remainder documented other solitary or or uncommon (although see Discussion). I used current social bees. Six observations documented multiple bee accepted botanical names as per The Plant List (www. and/or fly species without providing taxonomic identifica- theplantlist.org). I also searched commonly used syn- tion. onyms of major plant families (e.g. Graminaceae as a A total of 94 records were from natural or seminatural synonym of the accepted family name Poaceae; see systems, 56 were from agricultural systems, 6 were from Data S1). urban non-agricultural locations, and 66 were from multi- Relying only on scholarly database searches can ple or unspecified land use types. The majority were from result in publication bias of results (Pullin & Stewart, temperate regions (114), followed by subtropical (48), 2006), as individual databases usually focus on a spe- tropical (35), semiarid (15), and Mediterranean (12) cialised set of journals depending on institutional regions (two studies covered two bioregions each) (Data access. Hence, I also conducted Google Scholar S1). searches to access a broader range of literature that Only 30% of records were from direct observations. would potentially be available to most researchers The majority (70%) were from indirect analysis, i.e. pollen regardless of institutional affiliations. For these or honey samples collected from Apis spp. hives, stingless searches, I used the same combination of terms for bees bee colonies or solitary bee nest cells (120) or from insect and syrphid flies described above, plus variations of bodies or gut contents (35). A total of 93 of these indirect anemophily or wind-pollinated. I also searched for each records were for Apis, 23 were for Osmia bees, 16 were crop name from the list of wind-pollinated crops as for syrphid flies, 14 for stingless bees, 6 for Andrena bees, described above. I reviewed the first 50 results for each 4 for Bombus species, 2 for Xylocopa nasalis Westwood, search and collated studies that met the search criteria and 1 for multiple bee and fly species. and had not been found in database searches. I also A total of 10 wind-pollinated crop plant species were searched the supplemental list included in Klein et al. visited by bees and syrphid flies for pollen collection: (2007) for additional references for relevant crops that three grain/cereal crops (rice, corn, and sorghum), two oil- did not appear through my database searches. seed crops (jojoba and linseed), and five horticulture crops From each relevant study, I collected information on (olive, pecan, grape, hazelnut, and walnut). The majority the plant species (or genus or family), the insect taxa visit- of these records (66%) were from a location within the ing the plant, the geographical region and the type of native range of the crop species in question, or from a ecosystem. The climate zone of the study region was region with a congeneric species (Data S1). determined from information provided by the authors of the study, or by the Koppen€ –Geiger classification system if not noted in the study (Peel et al., 2007). If more than Discussion one study identified the identical insect–plant species rela- tionship in the same geographical location, the relation- This review shows that bee and syrphid fly species, two of ship was only recorded once. It is important to note that the most important taxonomic groups of pollinators in a my results represent the most comprehensive collation of wide variety of global environments (Ssymank et al., peer-reviewed records of pollinators visiting wind-polli- 2008; Garibaldi et al., 2013; Rader et al., 2016), collect nated plants to date and serve as a starting point for pollen from a broad range of wind-pollinated plant
Ó 2017 The Royal Entomological Society, Insect Conservation and Diversity, 11, 13–31 Ó Table 1. Results of the systematic review of records of bee and syrphid fly species visiting wind-pollinated plant genera. 07TeRylEtmlgclSociety, Entomological Royal The 2017 Direct or Plant family Genus Species Visitor System Reference Location Indirect
Amaranthaceae Achyranthes japonica Bees N Putra & Nakamura (2009) Japan D Alternanthera Apis sp. V Conceicao Silva et al. (2014) Sergipe, Brazil I Meliponini spp. V Vit & Dalbore (1994) Venezuela I Tetragonisca angustula A de Novais et al. (2013) Brazil I Melipona subnitida N Pinto et al. (2014) Brazil I Amaranthus palmeri Melissodes thelypodii A Cane et al. (1992) Arizona, US D thelypodii viridis Tetragonisca angustula A de Novais et al. (2013) Brazil I Celosia argentia Apis cerana, Apis dorsata, V Suwannapong et al. (2013) Thailand I Apis florea Chamissoa altissima Apis mellifera N da Silveira et al. (2012) Sao Paulo, Brazil I Chenopodium Apis mellifera V Wroblewska et al. (2010) Poland I netCnevto n Diversity and Conservation Insect Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Gomphrena Apis mellifera A Alves & dos Santos (2014) Brazil I Iresine celosia Nannotrigona sp., Scaptotrigona V Martinez-Hernandez et al. (1994) Chiapas, Mexico I sp., Plebeia sp., Trigona sp. diffusa Melipona eburnea V Obregon & Nates-Parra (2014) Colombia I Philoxerus Melipona V Vit & Dalbore (1994) Venezuela I Unidentified Apis mellifera V Bilisik et al. (2008) Turkey I Betulaceae Alnus Apis mellifera A Girard et al. (2012) Quebec I Apis spp. A Datta et al. (2008) India I glutinosa Syrphidae V Ssymank & Gilbert (1993) Germany, UK, US I Apis mellifera V Warakomska and Maciejewicz (1992) Poland I incana Bombus & Andrena sp. A Moisan-Deserres et al. (2014) Quebec, Canada I Betula Osmia spp. U MacIvor et al. (2014) Ontario, Canada I ,
11 Osmia spp. A Hansted et al. (2014) Denmark I
13–31 , Apis mellifera V Warakomska and Maciejewicz (1992) Poland I
Carpinus Osmia rufa A Teper & Bilinski (2009) Poland I plants wind-pollinated and Pollinators betulus Syrphidae V Ssymank & Gilbert (1993) Germany, UK, US I Osmia spp. A Hansted et al. (2014) Denmark I Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Corylus avellana Syrphidae V Ssymank & Gilbert (1993) Germany, UK, US I Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Cannabaceae Cannabis sativa Apis cerana, Apis mellifera A Suryanarayana et al. (1992) India I Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Celtis Apis mellifera N Baum et al. (2004) Texas, US I iguanaea Nannotrigona sp., Scaptotrigona V Martinez-Hernandez et al. (1994) Chiapas, Mexico I sp., Plebeia sp., Trigona sp. Trema micrantha Apis mellifera A Simeao et al. (2015) Brazil I micrantha Apis mellifera N Villanueva (2002) Yucatan, Mexico I Cupressaceae Sequoia sempervirens Apis mellifera N Pearson & Braiden (1990) New Zealand I
(continued) 17 Table 1. (continued) 18 auE Saunders E. Manu Direct or Plant family Genus Species Visitor System Reference Location Indirect
Thuja occidentalis Apis mellifera V Avitabile (1982) US D Unidentified Apis mellifera N Pearson & Braiden (1990) New Zealand I Cyperaceae Carex Apis mellifera A Girard et al. (2012) Quebec, Canada I Apis mellifera A Wroblewska et al. (2010) Poland I Apis mellifera N Baum et al. (2004) Texas, US I Bombus & Andrena spp. A Moisan-Deserres et al. (2014) Quebec I Cyperus Apis cerana, A. mellifera A Suryanarayana et al. (1992) Bihar, India I Eleocharis elegans Syrphidae N Magalhaes et al. (2005) Campinas, Brazil D Lepidosperma Apis mellifera & V Barrett (2013) Australia D Ó non-Apis spp. 07TeRylEtmlgclSociety, Entomological Royal The 2017 Scirpus maritimus Syrphidae V Leereveld et al. (1981) Netherlands D Unidentified Syrphidae V Leereveld et al. (1984) Europe I Syrphidae N Leereveld et al. (1991) Madagascar I Apis mellifera N Pearson & Braiden (1990) New Zealand I Ephedraceae Ephedra Apis mellifera N O’Neal & Waller (1984) Arizona, US I Fagaceae Castanopsis Xylocopa nasalis U Hongjamrassilp & Warrit (2014) Thailand I Fagus Osmia rufa A Hansted et al. (2014) Denmark I Osmia rufa A Teper & Bilinski (2009) Poland I Osmia lignaria A/N Kraemer et al. (2005) Virginia, US I sylvatica Syrphidae V Ssymank & Gilbert (1993) Germany, UK, US I Andrena haemorrhoa, A Chambers (1946) UK I Andrena armata Lithocarpus Xylocopa nasalis U Hongjamrassilp & Warrit (2014) Thailand I Quercus Osmia spp. U MacIvor et al. (2014) Ontario, Canada I Osmia rufa A Teper & Bilinski (2009) Poland I Apis mellifera A Stawiarz (2008) Poland I netCnevto n Diversity and Conservation Insect Osmia lignaria A/N Kraemer et al. (2005) Virginia, US I Osmia tricornis A Vicens et al. (1994) Spain I Apis mellifera N Aronne et al. (2012) Italy I Apis mellifera N Baum et al. (2004) Texas, US I Apis spp. A Datta et al. (2008) North India I Osmia spp. A Hansted et al. (2014) Denmark I Apis mellifera V Warakomska and Maciejewicz (1992) Poland I robur Osmia bicornis A Radmacher & Strohm (2010) Germany I Osmia spp. V Raw (1974) UK I Andrena haemorrhoa A Chambers (1946) UK I Unidentified Apis spp. A Datta et al. (2008) North India I Juglandaceae Carya Apis mellifera N Baum et al. (2004) Texas, US I Juglans Osmia rufa A Teper & Bilinski (2009) Poland I ,
11 Apis mellifera A Wroblewska et al. (2010) Poland I 13–31 , (continued) Ó Table 1. (continued) 07TeRylEtmlgclSociety, Entomological Royal The 2017
Direct or Plant family Genus Species Visitor System Reference Location Indirect
Apis mellifera N O’Neal & Waller (1984) Arizona I regia Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Juncaceae Juncus balticus Bombus N Pojar (1973) Vancouver Is, Canada D Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Myricaceae Myrica Apis spp. A Datta et al. (2008) North India I Nothofagaceae Nothofagus Apis mellifera N Pearson & Braiden (1990) New Zealand I Oleaceae Fraxinus Apis mellifera N Baum et al. (2004) Texas, US I Osmia lignaria A/N Kraemer et al. (2005) Virginia I uhdei Melipona eburnea V Obregon & Nates-Parra (2014) Colombia I Apis mellifera N O’Neal & Waller (1984) Arizona, US I Pinaceae Abies Apis mellifera N O’Neal & Waller (1984) Arizona, US I
netCnevto n Diversity and Conservation Insect Picea Apis mellifera A Girard et al. (2012) Quebec, Canada I Pinus Apis mellifera A Girard et al. (2012) Quebec, Canada I Osmia rufa A Teper & Bilinski (2009) Poland I Apis mellifera N Aronne et al. (2012) Italy I Apis mellifera N Pearson & Braiden (1990) New Zealand I Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Bombus & Andrena spp. A Moisan-Deserres et al. (2014) Quebec, Canada I Apis mellifera V Bilisik et al. (2008) Turkey I Pseudotsuga Apis mellifera N O’Neal & Waller (1984) Arizona I Plantaginaceae Plantago Apis mellifera V Sabugosa-Madeira et al. (2008) Portugal I Apis mellifera A Wroblewska et al. (2010) Poland I media Syrphidae V Leereveld et al. (1976) Netherlands D Syrphidae V Leereveld et al. (1984) Europe I
, maritima Bombus N Pojar (1973) Vancouver Is, Canada D 11 Apis mellifera N O’Neal & Waller (1984) Arizona, US I 13–31 , Apis mellifera V Warakomska and Maciejewicz (1992) Poland I olntr n idpliae plants wind-pollinated and Pollinators Apis mellifera V Bilisik et al. (2008) Turkey I lanceolata Episyrphus balteatus, N Goulson & Wright (1998) UK D Syrphus ribesii Platanaceae Platanus occidentalis Osmia lignaria A/N Kraemer et al. (2005) Virginia, US I Poaceae Acroceras macrum Lipotriches spp. N Immelman and Eardley (2000) South Africa D Agrostis exarata Bombus terricola N Pojar (1973) Vancouver Is, Canada D occidentalis Alloteropsis semialata Nomia spp. N Bogdan (1962) Kenya D Alopecurus pratensis Syrphidae A Orford et al. (2016) UK D Andropogon abyssinicus, amplectens, Apis mellifera & N Bogdan (1962) Kenya D canaliculatus, Nomia spp. chrysostachyus, distachyus
(continued) 19 Table 1. (continued) 20 auE Saunders E. Manu Direct or Plant family Genus Species Visitor System Reference Location Indirect
Lipotriches spp. V Immelman and Eardley (2000) South Africa D Anthephora hochstetteri Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D Arthraxon serrulatus Nomia spp. N Bogdan (1962) Kenya D Aulonemia auristulata Syrphidae N Grombone-Guaratini et al. (2011) Brazil D Bambusa bambos, vulgaris, other Apis cerana, Hallictus N Koshy et al. (2001) India D sp., Trigona biroi Beckeropsis procera, uniseta Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D Brachiaria brizantha, decumbens, Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D dictyoneura, lachnantha, Ó nigropedata, platynota, 07TeRylEtmlgclSociety, Entomological Royal The 2017 ruziziensis, serrata, soluta ruziziensis, nigropedata Lipotriches spp. N Immelman and Eardley (2000) South Africa D ruziziensis Lipotriches spp. N Tchuenguem Fohouo et al. (2004) Cameroon D Cenchrus ciliaris Lipotriches spp. N Immelman and Eardley (2000) South Africa D Chloriis gayana Nomia spp. N Bogdan (1962) Kenya D Cynodon dactylon Apis mellifera N Erickson & Atmowidjojo (1997) Colorado, US I dactylon Apis mellifera N Bogdan (1962) Kenya D Dactylis glomerata Syrphidae A Orford et al. (2016) UK D Deschampsia sespitosa Bombus terricola occidentalis N Pojar (1973) Vancouver Is, Canada D Digitaria didactyla, eriantha Lipotriches spp. N Immelman and Eardley (2000) South Africa D Echinochloa haploclada Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D Eleusine floccifolia, indica, Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D jaegeri Elionurus argenteus Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D Eragrostis Apis mellifera V Villanueva (2002) Yucatan, Mexico I superba Nomia spp. N Bogdan (1962) Kenya D netCnevto n Diversity and Conservation Insect gumniflua Lipotriches spp. N Immelman and Eardley (2000) South Africa D Eremochloa ophiuroides Apis mellifera U Jones (2014) Louisiana, US D Eriochloa meyeriana, stapfiana Lipotriches spp. N Immelman and Eardley (2000) South Africa D Eulalia geniculata Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D Eustachys paspaloides Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D Festuca rubra Bombus terricola occidentalis N Pojar (1973) Vancouver Is, Canada D Fingerhuthia africana Lipotriches spp. N Immelman and Eardley (2000) South Africa D Heteropogon‘ contortus Lipotriches spp. N Immelman and Eardley (2000) South Africa D Hordeum Apis cerana, A. mellifera A Suryanarayana et al. (1992) India I Syrphidae V Ssymank & Gilbert (1993) Germany, UK, US I Hyparrhenia diplandra, dissoluta, Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D hirta, lintonii, papillipes, pilgeriana, ,
11 rufa 13–31 , (continued) Ó Table 1. (continued) 07TeRylEtmlgclSociety, Entomological Royal The 2017
Direct or Plant family Genus Species Visitor System Reference Location Indirect
Ischaemum afrum Lipotriches spp. N Immelman and Eardley (2000) South Africa D Merostachys riedeliana Apis mellifera & Trigona N Guilherme and Ressel (2001) Brazil D spinipes Ochlandra ebracteata, scriptoria, Apis cerana, Apis dorsata, N Koshy et al. (2001) India D travancorica Halictus spp., Braunsapis mixta, Braunsapis picitarsis, Ceratina heiroglyphica, Trigona biroi Olyra obliquifolia Toxomerus apegiensis N Reemer and Rotheray (2009) Suriname D Mesograpta croesus, Trigona spp. N Soderstrom & Calderon (1971) S America D Oryza transgene rice Multiple Apoidea & APuet al. (2015) China I
netCnevto n Diversity and Conservation Insect Syrphidae spp. Panicum coloratum, deustum, Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D meyeranium coloratum, infestum, Lipotriches spp. N Immelman and Eardley (2000) South Africa D maxim Apis mellifera N Villanueva (2002) Yucatan I Pariana Trigona spp. N Soderstrom & Calderon (1971) South America D Paspalum dilatatum Dialictus illinoensis N Adams et al. (1981) Oklahoma, US D Apis mellifera V Ramalho et al. (1991) Brazil I Pennisetum catabasis, glabrum, Apis mellifera N Bogdan (1962) Kenya D mezianum, squamulatum, trisetum Phyllostachys nidularia Apis cerana N Huang et al. (2002) China D
, Pogonarthria squarrosa Lipotriches spp. N Immelman and Eardley (2000) South Africa D 11 Schmidtia pappophoroides Lipotriches spp. N Immelman and Eardley (2000) South Africa D 13–31 , Secale Apis mellifera A Wroblewska et al. (2010) Poland I olntr n idpliae plants wind-pollinated and Pollinators Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Sehima nervosum Apis mellifera N Bogdan (1962) Kenya D Setaria atrata, phragmitoides, Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D sphacelata, trinervia incrassatta, sphacelata Lipotriches spp. N Immelman and Eardley (2000) South Africa D Sorghum bicolor arundinaceum Lipotriches spp. N Immelman and Eardley (2000) South Africa D ‘jowar’ Apis cerana, A. mellifera A Suryanarayana et al. (1992) India I Apis mellifera N O’Neal & Waller (1984) Arizona I Sporobolus fimbriatus, marginatus Apis mellifera & Nomia spp. N Bogdan (1962) Kenya D Themeda triandra Lipotriches spp. N Immelman and Eardley (2000) South Africa D Urochloa mosambicensis Lipotriches spp. N Immelman and Eardley (2000) South Africa D Zea Apis mellifera N Baum et al. (2004) Texas, US I Apis mellifera A Danner et al. (2014) Germany I
(continued) 21 Table 1. (continued) 22 auE Saunders E. Manu Direct or Plant family Genus Species Visitor System Reference Location Indirect
Apis mellifera N O’Neal & Waller (1984) Arizona, US I mays Apis cerana, Apis dorsata, V Suwannapong et al. (2013) Thailand I Apis florea Apis mellifera A Wroblewska et al. (2010) Poland I Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Lipotriches spp. N Tchuenguem Fohouo et al. (2004) Cameroon D mays Toxomerus politus N Reemer and Rotheray (2009) US, Venezuela D mays Apis mellifera V Bilisik et al. (2008) Turkey I Zizania aquatica Bombus spp., Toxomerus N Terrell & Batra (1984) Maryland, US D Ó spp., Dialictus spp. 07TeRylEtmlgclSociety, Entomological Royal The 2017 Unidentified Apis mellifera A Simeao et al. (2015) Brazil I Apis mellifera A Alves & dos Santos (2014) Brazil I Apis mellifera N Aronne et al. (2012) Italy I Apis spp. A Datta et al. (2008) India I Syrphidae V Leereveld et al. (1984) var I Syrphidae N Leereveld et al. (1991) Madagascar I Melipona eburnea V Obregon & Nates-Parra (2014) Colombia I Syrphidae V Ssymank & Gilbert (1993) Germany, UK, US I Apis mellifera N O’Neal & Waller (1984) Arizona, US I Apis mellifera N Pearson & Braiden (1990) New Zealand I Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Apis mellifera V Bilisik et al. (2008) Turkey I Melipona subnitida N Pinto et al. (2014) Brazil I Podocarpaceae Podocarpus Frieseomelitta varia U Marques-Souza (2010) Manaus, Brazil I Polygonaceae Rumex acetosella Apis mellifera A Girard et al. (2012) Quebec, Canada I Apis spp. A Datta et al. (2008) India I netCnevto n Diversity and Conservation Insect sanguineus Syrphidae V Ssymank & Gilbert (1993) Germany, UK, US I Apis mellifera V Warakomska and Maciejewicz (1992) Poland I acetosella Bombus spp. & A Moisan-Deserres et al. (2014) Quebec I Andrena spp. Osmia spp. V Raw (1974) UK I crispus Episyrphus balteatus, N Goulson & Wright (1998) UK D Syrphus ribesii Salicaceae Populus tremula Syrphidae V Ssymank & Gilbert (1993) Germany, UK, US I Apis mellifera N O’Neal & Waller (1984) Arizona, US I Apis mellifera V Warakomska and Maciejewicz (1992) Poland I Sapindaceae Acer Osmia rufa A Hansted et al. (2014) Denmark I Apis mellifera V Bilisik et al. (2008) Turkey I negundo Osmia lignaria A Kraemer et al. (2005) Virginia I ,
11 Apis mellifera V Wroblewska et al. (2010) Poland I 13–31 , (continued) Pollinators and wind-pollinated plants 23
species. This is an important result for landscape manage- ment, because wind-pollinated plant taxa are often consid- ered irrelevant to insect pollinator resource needs (e.g. Direct or Indirect Decourtye et al., 2010). Most of the records I found were for Apis bee species and nearly three-quarters of the records were from indirect pollen analysis. More records were from natural or seminatural systems compared to agricultural or urban locations, and 51% of records were from temperate regions. I also found evidence that bee and syrphid fly species visit at least 10 wind-pollinated crop plant species to collect or feed on pollen. m types. Direct or Indirect: D, In this review, I focused on flower visitation for pollen, which is a critical food resource for bee and syrphid fly species. However, it is important to note that bees and syrphid flies also visit wind-pollinated plants for non- floral resources, for example insect honeydew (e.g. Santas, 1983; Koch et al., 2011), plant resins (e.g. Leonhardt & Bluthgen,€ 2009), or resinous/sweet secretions produced (1992) Suriname I (2013) Brazil I (1984) var I (1991) Brazilfrom leaf tissue I (e.g. Warakomska & Maciejewicz, 1992; (2004) Texas, US I (2008)Nyeko Indiaet al., 2002). Other I insect pollinator species also et al. et al. et al. et al. visit wind-pollinated flowers, e.g. bee flies (Bombyliidae) et al. et al. and butterflies (Lepidoptera) visiting Buxus balearica Lam. in the Mediterranean (Lazaro & Traveset, 2005), and moths (Pyralidae, Geometridae) and flies (Lauxani- idae, Drosophilidae, Culicidae) visiting flowers of Gnetum species in south-east Asia (Kato et al., 1995; Gong et al., N Schmidt &A Buchmann (1983)NA Teper &A Bilinski (2009) Baum A Arizona, US Biesmeijer Alves & dos Santos de (2014) Novais I Poland Brazil I I VNV Obregon & Nates-Parra (2014) Villanueva (2002) Ramalho Colombia Yucatan, I Mexico I V Warakomska and Maciejewicz (1992) Poland2016). Pollinators I may also visit non-vascular plants, e.g. bryophytes (e.g. Svetlana & Sabovljevi c, 2008) and fungi (e.g. Oliveira & Morato, 2000), but our understanding of these relationships is more limited. Many pollinator spe- cies also rely on wind-pollinated plants for development sites for pollen-feeding larvae, e.g. Toxomerus spp. (Ree- mer & Rotheray, 2009), or for nest sites and materials; for example, some carpenter bee species preferentially build nests in the stems of bamboo and related plant spe-
spp. V Raw (1974)cies, UK e.g. the neotropical I Xylocopa subgenus Stenoxylocopa spp. A Datta (Hurd, 1978) and the Asian subgenus Biluna (Maeta Osmia SyrphidaeSyrphidaeApis mellifera Apis mellifera Tetragonisca angustula V V Leereveld Ssymank & Gilbert (1993) Germany, UK, US I Apis mellifera Apis mellifera SyrphidaeApis mellifera et al. V, 1985). Ssymank & Gilbert (1993) Krombein Germany,et UK, US al. (1979) I notes North Ameri- can carpenter bee species that preferentially nest in trunks or branches of native wind-pollinated trees, e.g. Xylocopa tabaniformis orpifex Smith. in Alnus rhombifolia Nutt., Juniperus spp., Populus spp., Pseudotsuga menziesii (Mirb.) Franco, and others; and Xylocopa californica cali- fornica Cresson. in Sequoia sempervirens D. Don Endl. and Sequoiadendron giganteum (Lindl.) Buchholz. mutisiana, peltata Melipona eburnea Mutualism or consumer–resource interaction? (continued) The traditional conceptual approach to plant–pollinator interactions focuses on mutualisms (++), where both par- Simmondsia chinensisCecropia Apis mellifera Apis mellifera Table 1. Typha latifolia Sparganium Ulmus Osmia rufa UrticaUnidentified dioica ties benefit from Apis the interaction. Some studies have con- sidered antagonistic (+ À) plant–pollinator interactions where the pollinator benefits from floral resources at the expense of the plant’s fitness or reproduction; for exam- ple, nectar/pollen theft without pollinating (Inouye, 1980; Hargreaves et al., 2009; Irwin et al., 2010). However, + Simmondsiaceae Urticaceae Plant family Genus Species Visitor System Reference Location Typhaceae Ulmaceae See Data S1 fordirect full observation; references I, and indirect details pollen of analysis each from record. hives, System: nest A, cells agricultural; or N,understanding insect natural/semi bodies. natural; U, urban; V, multiple unidentified syste of commensal relationships ( 0) between
Ó 2017 The Royal Entomological Society, Insect Conservation and Diversity, 11, 13–31 24 Manu E. Saunders insect pollinators and plants is more limited. Most wind- sedges (Poales: Poaceae, Cyperaceae). The records came pollinated plants have a very high pollen-to-ovule ratio from 33 separate studies, most of which (65%) were the and limited pollen viability compared to animal-pollinated results of hive, honey or gut samples, so information on plants (Ackerman, 2000; Culley et al., 2002) and many habitat structure was not available. Of the remaining 11 wind-pollinated species may be pollen-limited, especially observational studies, seven were conducted in relatively in fragmented habitats (Koenig & Ashley, 2003; Davis open environments (e.g. savannah, river floodplain), et al., 2004; Jump & Penuelas,~ 2006; Labouche et al., where wind-pollinated plant species are more likely to be 2016). It is likely that most interactions between insect found. Only two studies were of bees visiting flowers in pollinators and wind-pollinated plants would be commen- tropical forested environments, both for bamboo species: sal or antagonistic, depending on how much viable pollen Merostachys riedeliana Rupr. ex Doll€ in Brazil (Guilherme is removed from the plant. However, some wind-polli- & Ressel, 2001), and multiple Bambusa and Ochlandra nated plant species may benefit from enhanced dispersal species in southern India (Koshy et al., 2001). Most of by insects, although the extent of this relationship is the observations in these studies were from seminatural unknown (see Discussion of ambophily below). managed environments on cultivated plants, for example In my review, the majority of records were from tem- a seed-stock nursery (Immelman & Eardley, 2000), test perate bioregions, where the proportion of wind-polli- plots at a grassland research station (Bogdan, 1962), and nated species in plant communities is highest (Whitehead, botanical garden (Koshy et al., 2001). Clifford (1964) sug- 1969; Regal, 1982). Wind-pollinated species, particularly gests that insect pollination could be more common in trees, tend to flower earlier than animal-pollinated species tropical grasses than temperate grasses, because a higher (Bolmgren et al., 2003). Hence, these species often provide proportion of tropical and subtropical grass species have critical nutrients for pollinators in temperate regions dur- pigmented flowers compared to temperate grass species. ing periods of poor pollen availability, i.e. early spring However, 48% of grass taxa visitation records in my before the spring-summer floral resource peaks. For review were from tropical and subtropical regions, while example, Batra (1985) observed multiple species of bees, 43% were from temperate regions, and the remainder flies, and wasps visiting red maple Acer rubrum L. flower- were from semiarid or Mediterranean regions. ing in March–April in Maryland, USA, with numerous individuals of both sexes foraging on male and female flowers. The curious case of ambophily Many of the records from my search were results of pollen analysis from hive or honey samples, rather than Stelleman (1984) called attention to ambophily, where direct observations, and these studies did not provide plants rely on both wind and insects for pollination, over information on whether bees also visited female wind-pol- three decades ago. Yet, it remains unclear whether the linated flowers during foraging. It is possible that anemo- strategy represents a stable, flexible state for plants in philous pollen found in honey or hive samples could be a variable environments, or a transition state between polli- result of contamination from pollen blowing onto flowers nation syndromes (Friedman, 2011). or insect bodies, rather than from direct collection of pol- Many examples are documented in the literature across len by insects (Cane & Sipes, 2006). However, the level of a variety of plant families and geographical locations, e.g. anemophilous pollen species present in bee hives is not Salix lasiolepis Benth. in Arizona, United States visited by always correlated with high levels of that pollen type in Bombus, Andrena, Agapostemon, Dialictus, and Sphecodes the environment (Sabugosa-Madeira et al., 2008) and ane- bees, and calliphorid, syrphid, and tachinid flies (Sacchi & mophilous pollen blown into hives naturally is usually a Price, 1988); Hormathophylla spinosa Kupfer€ in the Sierra very small fraction compared to the pollen brought to the Nevada, Spain, visited by over 70 insect species in five hives by bees (Bryant & Jones, 2001). In addition, Vil- orders, mostly Diptera and Hymenoptera (Gomez & lanueva-Guti errez and Roubik (2016) analysed pollen Zamora, 1996); Thalictrum polygamum Muhl. (also Thalic- occurrence in Centris and Megachile nests in Mexico and trum pubescens) in the United States, visited by Syrphidae, concluded that rare pollen was seldom a result of contam- Muscidae, Membracidae, Coleoptera and Bombus species ination and was more likely to indicate bees were using (Kaplan & Mulcahy, 1971); Amborella trichopoda Baill. in multiple resources in their foraging environment. New Caledonia, visited by cerambycid beetles, chalcid and I found the second highest number of visitation records braconid wasps, and gall midges (Thien et al., 2003). (almost as many as temperate regions) from tropical and Pojar (1973) observed regular pollen collection (he docu- subtropical bioregions combined. Wind-pollinated plant ments it as pollination but did not confirm seed set) of species are less common in tropical environments, espe- several salt marsh species on Vancouver Island (e.g. Plan- cially forests (Whitehead, 1969; Regal, 1982; Ollerton tago maritima L., Juncus balticus Willd., Festuca rubra et al., 2011), as wind pollination is generally thought to L. and others) by the bumble bee Bombus occidentalis be an adaptation to conditions of low humidity, low rain- Greene (see Table 1). Evidence of insect pollination has fall and open or deciduous vegetation (Culley et al., 2002; also been found in some aquatic plant species traditionally Rech et al., 2016). Over half of the plant records from thought to be pollinated by wind or water (Cook, 1988; tropical and subtropical regions (55%) were grasses and Barrett et al., 1993), and bees and flies have been recorded
Ó 2017 The Royal Entomological Society, Insect Conservation and Diversity, 11, 13–31 Pollinators and wind-pollinated plants 25 visiting flowers of aquatic wind-pollinated plant species have widespread benefits across the landscape. Plant den- (e.g. Osborn & Schneider,1988; Gumbert & Kunze, 1999). sity is also known to influence pollinator visitation and Recent evidence has also highlighted facilitative benefits seed set in many plants (e.g. Kunin, 1993; Steven et al., of insect activity on wind-pollinated plants, whereby 2003; Dauber et al., 2010), but no published studies have insect activity on flowers may assist wind pollination by tested whether wind-pollinated plants are more likely to releasing pollen grains for easier dispersal, e.g. Chamae- be visited by pollinators when cultivated in high densities dorea pinnatifrons (Listabarth, 1993); Brassica napus as in commercial crop fields. L. (Pierre et al., 2010); Crateva adansonii DC. (Mangla & Pollinator conservation strategies for farm systems (e.g. Tandon, 2011). Timerman et al. (2015) recently identified the planting of wildflower strips) usually focus on plants the mechanical properties of stamens that enable turbu- that are rich in floral rewards, i.e. nectar, and therefore lence-driven pollen shedding in wind-pollinated Plantago attractive to, and pollinated by, insects (Haaland et al., lanceolata, and it is likely that insects have the capacity to 2011; Pywell et al., 2011). A focus on these types of flow- facilitate this process. ers is also promoted in urban environments (Garbuzov & Many insect-pollinated plant species may also benefit Ratnieks, 2014; Hicks et al., 2016) and through general from wind pollination because pollen vectors commonly conservation extension and outreach organisations (e.g. vary through space and time; hence, it is likely that dual The Royal Horticultural Society, 2016; Xerces Society, pollination strategies are more widespread than is cur- n.d.). This means that most wind-pollinated plants, which rently accepted (Totland & Sottocornola, 2001; De la provide pollen but no nectar, are overlooked. However, Bandera & Traveset, 2006). For example, most willow as pollen is more important for reproduction, particularly species (Salix spp.) benefit from both wind and insect pol- for bees (Sheffield et al., 2008), there is potential for lination, but some species are almost completely ento- wind-pollinated plants to also fill those needs. While some mophilous, some predominantly anemophilous, and authors do acknowledge that grasses are also visited by others rely equally on both pollination strategies (Peeters pollinators, grass species (or other wind-pollinated taxa) & Totland, 1999; Totland & Sottocornola, 2001; Karren- are rarely included in analyses or management recommen- berg et al., 2002; Hopley & Young, 2015). This genus dations (Haaland et al., 2011; Hicks et al., 2016; Orford appears to be an important source of pollen for early et al., 2016) and statements that grasses are of no value spring bees and other pollinators; for example, Krombein to bees and other pollinators appear regularly in relevant et al. (1979) lists over 200 North American bee species literature (e.g. Decourtye et al., 2010). Orford et al. (2016) and a wasp that visit Salix flowers for pollen. studied pollinator visitation to flowers of common grass- land/pasture plant species and noted that grass species were commonly visited by pollinator taxa, but did not Implications for food production and pollinator conservation specifically compare grasses and flowering plants. Recent in agroecosystems evidence has shown that cultivated wildflower plantings are not visited by pollinators as often as wild plants, and Pollinator conservation practices are not only important may do little to support the persistence of local pollinator for insect-pollinated crop systems that receive direct bene- populations (e.g. Wood et al., 2017). This may be one rea- fits from insect visitation through fruit or seed set. Insect son why many studies find that the effectiveness of on- pollinators are commonly found in agroecosystems domi- farm conservation measures (e.g. wildflower strips) is nated by wind-pollinated crops, particularly cereal crops influenced by the amount of natural or seminatural habi- (e.g. Bowie et al., 2001; Holzschuh et al., 2007; Rundlof€ tat in the surrounding landscape (Scheper et al., 2013; et al., 2008; Kovacs-Hosty anszki et al., 2011; Raymond Batary et al., 2015; Campbell et al., 2017). Given the et al., 2014), and bee and syrphid fly species collect pollen number of wind-pollinated plants used by insect pollina- from flowers of some of these crops. However, high pesti- tors for food or nesting resources, a focus on habitat that cide use in wind-pollinated crop systems may have serious includes diverse plants regardless of pollination syndrome impacts on local pollinator populations (Krupke et al., is more useful for enhancing the persistence of pollinator 2012; Hladik et al., 2016). Some pollinator species may populations. feed on aphid honeydew in wheat crops, presenting another pathway for pesticide exposure in cereal crops (Shires et al., 1984; Oliver et al., 2015). Recent evidence Future directions has shown that some crops traditionally assumed to be wind-pollinated or self-compatible do benefit from Identifying the outcomes of interactions between polli- enhanced pollination by insects, e.g. oilseed rape Brassica nators and wind-pollinated plants from both perspectives napus L. (Bommarco et al., 2012) and robusta coffee, Cof- (i.e. the plant and the pollinator) will build knowledge of fea canephora Pierre (Ngo et al., 2011). In addition, land- how these interactions influence ecosystem function. Plant scape-scale management practices, rather than local reproduction can be influenced by pollinator visitation to measures, are important for the sustainability of produc- co-flowering plant species and these interactions are a key tion landscapes (Concepcion et al., 2012), so managing a driver of plant community structure (e.g. Robertson, wind-pollinated crop system to support pollinators can 1895; Mosquin, 1971; Heinrich, 1975; Waser, 1978;
Ó 2017 The Royal Entomological Society, Insect Conservation and Diversity, 11, 13–31 26 Manu E. Saunders
Johnson et al., 2003; Moeller, 2004; Lazaro et al., 2009). for non-Apis bee species, many of which were not found Yet, most studies that consider these effects focus on pol- in my formal review, e.g. Hylaeus panamensis Michener linator competition or facilitation between insect-polli- and Perdita larreae Cockerell collected pollen from nated plant species, rather than broader community Dicraurus spp.; Ashmeadiella californica florissantensis interactions, such as those involving wind-pollinated plant Michener visits flowers of Chrysolepis spp. These cata- species (Feinsinger, 1987; Mitchell et al., 2009). From the logues are limited in detailed information about geo- pollinator’s perspective, identifying the costs and benefits graphical locations of individual plant–pollinator of foraging for anemophilous pollen versus entomophilous interactions, but provide a valuable starting point for pollen will increase understanding of the relative ecologi- hypothesis generation. cal and evolutionary importance of these two food In addition, social media are an unconventional but sources (Baker & Baker, 1979; Roulston et al., 2000). valuable source of validated natural history observations. Most studies of pollen nutrition for insect pollinators have For example, in my literature search I did not find any been conducted on honey bees (Apis mellifera L.), or in records for the grass genus Chrysopogon. However, a controlled laboratory feeding experiments. Therefore, record of regular visitation to Chrysopogon fallax S.T. more research on non-Apis pollinator species is needed, as Blake by a native stingless bee species is published on a are more field-based studies of how anemophilous pollen blog maintained by an Australian conservation group complements entomophilous pollen in pollinator diets (Land for Wildlife Top End, 2016). Similarly, Ginkgo across geographical ranges and seasons. biloba L. is a wind-pollinated gymnosperm that few people In agroecosystems, the current research focus on pol- would consider relevant to insect pollinators (but see Sch- len-limited crops that require insect pollinators limits glo- malzel, 1980). I found no records for ginkgo visitation in bal understanding of how agroecosystems can be my review, but I have recorded an observation of syrphid managed to support pollinator communities for land- flies and honey bees visiting reproductive parts of male and scape-wide benefits, rather than ecosystem services on female G. biloba trees in temperate south-eastern Australia individual farms. In addition, the growing literature of on my blog (Fig. 2; Saunders, 2016). Other social media trait-based analyses linking biodiversity to ecosystem that promote photo sharing, such as Twitter, Flickr, and function would benefit from broader ecological knowl- Instagram, are also valuable untapped resources for col- edge. For example, studies that aim to identify links lecting data on natural interactions (Sonter et al., 2016). between pollinator and plant communities should consider The limitations of my review do not limit the value of the role of unconventional plant traits beyond the stan- its results, which highlight the complexity of natural inter- dard ones that are assumed to have most influence over actions involved in the structure of plant–pollinator net- pollinator communities (e.g. Pakeman & Stockan, 2013). works. There are large knowledge gaps in the natural The recorded interactions between insect pollinators history and functional ecology of many of the thousands and wind-pollinated plant species I found in my review of insect pollinator species globally. Building knowledge are likely only a small proportion of actual interactions of these species, particularly how they interact with plant between pollinators and wind-pollinated plants. I focused communities beyond the plant species they pollinate, will on searching peer-reviewed journals for records of a list increase understanding of how pollinator communities of commonly known wind-pollinated plant families. Yet, influence ecosystem function in natural and agricultural the reproductive strategies of many of the world’s plant systems. species are still undescribed, and it is likely that many plant families considered to contain mostly insect-polli- nated species also contain wind-pollinated species (e.g. Cook, 1988). In addition, many regional natural history journals and museum catalogues are not indexed in jour- nal databases and may be difficult to locate outside of the relevant region, but are likely to be a rich source of observational accounts not recorded in peer-reviewed journals. For example, Houston’s (2000) catalogue of native bee visitation records to western Australian wild- flowers, collated from data labels in the Western Aus- tralian Museum collections, documents non-Apis bee visitation to nine wind-pollinated plant genera in five families. Visitation records for one of these plant families (Haloragaceae) and six genera (Amaranthaceae: Aerva, Ptilotus, Rhagodia; Casuarinaceae: Allocasuarina; Halor- agaceae: Glischrocaryon; Poaceae: Triodia) were not found in my systematic search of the peer-reviewed literature. Fig. 2. Common hover flies (Diptera: Syrphidae) collecting pollen Similarly, Krombein et al.’s (1979) catalogue of North from a male Ginkgo biloba tree in Albury, Australia. Photo: the American Hymenoptera contains pollen collection records author. [Colour figure can be viewed at wileyonlinelibrary.com]
Ó 2017 The Royal Entomological Society, Insect Conservation and Diversity, 11, 13–31 Pollinators and wind-pollinated plants 27
Acknowledgements Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemuller,€ R., Edwards, M., Peeters, T., Schaffers, A.P., Potts, S.G., Kleuk- I thank Gary Luck for helpful comments on an earlier ers, R., Thomas, C.D., Settele, J. & Kunin, W.E. (2006) Paral- version of this manuscript and Karen Retra for conversa- lel declines in pollinators and insect-pollinated plants in Britain 313 – tions about bees visiting wind-pollinated plants. I formu- and the Netherlands. Science, , 351 354. Bogdan, A.V. (1962) Grass pollination by bees in Kenya. Pro- lated the ideas behind this paper during regular ceedings of the Linnean Society of London, 173,57–61. observational surveys of insect pollinators collecting Bolmgren, K., Eriksson, O. & Linder, H.P. (2003) Contrasting hazelnut pollen at Happy Wombat Hazelnuts (I thank flowering phenology and species richness in abiotically and Bindi Vanzella and Craig Anderson for giving me access biotically pollinated angiosperms. Evolution, 57, 2001–2011. to their farm). I thank Laurence Packer and anonymous Bommarco, R., Marini, L. & Vaissi ere, B. (2012) Insect pollina- reviewers who provided constructive comments that tion enhances seed yield, quality, and market value in oilseed helped me improve the quality of this manuscript. rape. Oecologia, 169, 1025–1032. Bosch, J., Mart ın Gonzalez, A.M., Rodrigo, A. & Navarro, D. (2009) Plant–pollinator networks: adding the pollinator’s per- Ecology Letters 12 – Supporting Information spective. , , 409 419. Bowie, M.H., Gurr, G.M. & Frampton, C.M. (2001) Adult and lar- val hoverfly communities and their parasitoid fauna in wheat in Additional Supporting Information may be found in the online New South Wales, Australia. New Zealand Entomologist, 24,3–6. version of this article under the DOI reference: doi: 10.1111/ Bryant, V.M. Jr. & Jones, G.D. (2001) The r-values of honey: icad.12243: pollen coefficients. Palynology, 25,11–28. Data S1. 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