159 Annales Universitatis Paedagogicae Cracoviensis Studia Naturae, 2: 159–169, 2017, ISSN 2543-8832 DOI: 10.24917/25438832.2.12 Samuel Robinson1, William Cetzal-Ix2, Saikat Kumar Basu3* 1Department of Biological Sciences, University of Calgary, Alberta, Canada 2Instituto Tecnológico de Chiná, Tecnológico Nacional de México, Chiná, Campeche, Mexico 3Department of Biological Sciences, University of Lethbridge, Alberta, Canada, *saikat.basu@alumni.uleth.ca Wild bee decline and conservation in North America Pollination by wild bees One of the major challenges of the 21st century will be feeding an increasing number of people on smaller and smaller areas of fertile land. While much of our diet comes from crops which do not require any animal pollination (e.g., wheat, corn, rice), about 35% of global food production depends on pollinating animals, such as bees (Klein et al., 2007). Over 90% of the vitamin C in our diet – as well as a majority of other vitamins, minerals, antioxidants, and micronutrients – come from animal-pollinated crops (Eilers et al., 2011). �is makes animal pollinators an important part of the human food supply and global economy, and conservation of pollinators will be a key factor in managing global food security. Historically, most pollination worldwide has been done by wild bees, and in most undeveloped nations, a majority of pollination is still done by wild pollinators (�ies, moths, butter�ies, bats, and hummingbirds also provide some services). However, developed nations typically rely on large-scale pollination services provided by the European honey bee, Apis mellifera L. Honey bees were brought to North America by European settlers, and they have expanded into a  multi-billion dollar industry over the last 50 years. �e total value of pollination services worldwide is close to $178 billion USD (Gallai et al., 2009). In the United States in 2009, the total value of crop pollination services from honey bees was $11.6 billion, while services from non-hon- ey bees were about $3.4 billion, with much of this value coming from almond, apple, and sun�ower crops, which are all highly pollinator-dependent and grown in large amounts (Calderone, 2012). While much of the general public are aware of honey bees and bumble bees in North America, they are o�en surprised to �nd out that this is a tiny fraction of the to- tal number of bees! Out of the 20.000 species of bees worldwide, there are about 4600 S am ue l R ob in so n, W ill ia m C et za l-I x, S ai ka t K um ar B as u 160 Tab. 1. Common families of bees in the United States, Mexico, and Canada Family Number of genera Number of species Examples Andrenidae 12 1472 Mining bee (Andrena sp., Panurgus sp.) Fairy bee (Perdita sp.) Squash bees (Peponapis sp.) Apidae 83 1305 Honey bee (Apis mellifera) Bumble bee (Bombus sp.) Long-horned bees (Eucera sp., Mellisodes sp.) Carpenter bees (Xylocopa sp.) Stingless bees (Melipona sp., Trigona sp.) Colletidae 9 288 Cellophane bee (Colletes sp., Hylaeus sp.) Halictidae 26 654 Sweat bee (Halictus sp., Lasioglossum sp.)Green bee (Agapostemon sp., Augochlora sp.) Megachilidae 26 791 Leafcutter bee (Megachile sp.) Mason bee (Osmia sp.) Carder bee (Anthidium sp.) Mellitidae 3 28 Mellita sp., Macropis sp. species of bees living in North America (Ascher, Pickering, 2017) (Tab. 1, Appendix – Fig. 1–2), and most of them are in the desert southwest of the United States (Wil- son, Carril, 2016). �is is mainly due to the local diversity of local �owering plants, as high �owering plant diversity generally translates into higher bee diversity (Potts et al., 2003). �ere are 46 species of bumblebee living in North America (Williams et al., 2014), but most wild bees are solitary. Solitary bees do not have a strict caste system with workers, queens, and drones, and can live their lives independently from each other. However, many ‘solitary’ bees will start acting socially (guarding nests, feeding other bees larvae, acting as queens and workers) if enough of them are in the same area (Williams et al., 2014). Pollinator decline Are wild bee populations declining? Because of their large diversity, di�culties in identifying them, and the fact that they are not as well-known as honey bees, they are less well-sampled in North America, and even less so in Mexico (Freitas et al., 2009). Historical insect collections have proved to be valuable sources of information, as we can compare ‘snapshots’ of bee populations through time at a given location. Unfor- tunately, this has revealed that many wild bee populations are in decline. Cameron et al. (2011) used over 73.000 museum specimens to study 8 common species of bum- blebees across the continental US, and found that 4 out of 8 were in serious decline. �e International Union for Conservation of Nature (IUCN) lists 12 out of 37 North American bumble bees (that we have good data for) as being endangered or vulnera- W ild bee decline and conservation in N orth A m erica 161 ble (IUCN, 2017). Solitary bees do not fare much better in this regard. Biesmeijer et al. (2006) found that there have been declines in wild bee populations across Britain and the Netherlands, and more worryingly, there have also been declines in the plants that are pollinated by these bees! Causes of decline �e factors that contribute to the decline of wild bees can also be complex, but there are some general drivers of pollinator decline: 1. Land use changes Globally, about 40% of land has been converted to agricultural land (Foley et al., 2005). In Mexico, large-scale deforestation for charcoal, cattle, or agricultural expansion has reduced native rainforests to almost 10% of their original extent (Freitas et al., 2009). More than 50% of North American grasslands have been converted to agriculture (Hoekstra et al., 2005), and in some parts of western North America, this number approaches almost 100%, especially for tall-grass prairie (Samson et al., 1998). Habitat destruction has 2 main e�ects on wild bee populations: the reduction of food sources (�owers) and the reduction of nest sites. Wind-pollinated crops, such as corn, provide little nutrition for bees, and even crops like canola or alfalfa (which bees can bene�t from) can be unhelpful in the long run, as the �owers are only available during a few weeks of the summer. Some bee species are only active for a few weeks during the summer, so if their foraging time does not overlap with the �owering of the crop, they have no food! Crop �elds can be dangerous for bees, as tillage and irrigation can destroy nest sites in the ground, and pesticides can injure or confuse bees. Agricultural areas typically have few species of �owering plants present, meaning that generalist bees can persist (Kleijn et al., 2015), but that �oral specialists will be without the �owers that they need. Finally, crop �elds in the US and Canada are o�en very large; small bees o�en only have �ight ranges of a few hundred yards, meaning that �nding areas with both nest habitat and food becomes more and more di�cult as �elds get bigger and bigger. 2. Honey bees Honey bees, while being incredibly useful and pro�table for humans, can put pressure on wild bee populations. �ey do this in two ways: competition for �owering plants, and disease spillover. Honey bee colonies can raise 150–200.000 bees per year (Seeley, 1985), and the sheer number of foraging workers can drain nectar and pollen resourc- es around their hives. �ey can also �y up to 5 km while foraging, while many solitary S am ue l R ob in so n, W ill ia m C et za l-I x, S ai ka t K um ar B as u 162 bees only �y a few hundred meters during their entire lifetime, meaning that honey bees have the potential to compete with many types of wild bees. In Mexico, stingless bees (Melipona beecheii Bennett) can be directly attacked by Africanised honey bees, and declines in native Mayan beekeeping over the last 20 years have been associated with increases in numbers of honey bees (Cairns et al., 2005). Many bumblebee diseas- es are similar to those of honey bees, meaning that disease spillover can occur between them. For example, Fürst et al. (2014) found that both Nosema ceranae I. Fr., F. Feng, J.A. da Silva, S.B. Slemenda & N.J. Pieniazek and deformed wing virus (2 diseases of honey bees) could easily reproduce in bumblebee colonies, and more worryingly, both diseases were found in wild populations of bumblebees across the United Kingdom. Diseases of solitary bees are not well-studied, but chalkbrood fungus from honey bees (Ascosphaera aggregata Skou) can also infect leafcutter bees (Goulson, 2003). Finally, beekeepers provide help to honey bees by controlling their pests and diseases, and by feeding them during �ower-free periods. �is make sense, given that their livelihoods are based on having a large worker force, but this can put wild bees at a distinct disad- vantage when it comes to surviving alongside honey bees. 3. Insecticides Large amounts of attention have been devoted to the e�ect of pesticides on honey bees. In particular, neonicotinoid insecticides have been implicated in honey bee deaths. �ere is far less data examining the e�ects of pesticides on wild bees, but research does show that insecticides can change foraging behaviour and can cause increased rates of mortality in bumblebees. For example, Laycock et al. (2014) found that bumblebees fed small amounts of pesticides in their diet tended to live shorter lives. Sandrock et al. (2014) showed that mason bees (Osmia bicornis L.) can also be a�ected, as they tended to produce less o�spring when fed small doses of pesticides throughout their lives. However, it is far less clear whether these small-scale e�ects of pesticides are causing reductions in wild bee populations, and it is more likely that a combination of land use changes, diet changes, and pesticide usage are driving declines in wild bee populations (Goulson et al., 2015). 4. Mitigation Clearly, there are many things that threaten the existence of wild bee populations. But how can we help encourage robust wild bee populations, and lessen risks of extinc- tion? Even more importantly, how do we balance our desire for agriculture and urban development while still conserving wild bees? To do this, we need to move beyond the “only honey bees” mentality. We suggest that both individuals and local governments should work to establish wild bee habitats in order to preserve local species diversity and abundance. W ild bee decline and conservation in N orth A m erica 163 While we recognise that honey bees are extremely practical in the modern agricul- tural setting, we encourage people to begin thinking beyond just honey bees, and to consider wild pollinators as valuable parts of our ecosystems. Worldwide, the number of pollinator-dependent crops have grown more than 300% in the last 50 years, while the number of honey bee colonies has only grown by 45% (Aizen, Harder, 2009). �is means that the number of honey bees has not kept pace with our growing demand for pollination, and this ‘pollination gap’ will continue to increase into the future. Wild pollinators also provide insurance against honey bee die-o�s, which have increased in severity in many parts of the United States. Additionally, honey bees are not necessar- ily the best pollinators for all crops! Garibaldi et al. (2013) found that in over 41 worldwide crop types, wild pollinators increased yield across all fruit, nut, and seed crop types, but that honey bees only in- creased yield in 14% of the crop types. In other words, honey bees can supplement, but not replace, pollination by wild pollinators. Greenleaf and Kremen (2006) found that the yield of hybrids sun�owers was increased in �elds located close to natural areas, and that honey bees switched between �owers more frequently if there were wild bees present, meaning that wild bees can actually increase the e�ciency of honey bee pol- lination! In this way, wild pollinators have the potential to work alongside introduced pollinators if they establish stable populations. Bee habitats should provide a  diverse set of food resources and stable year-to- year nesting sites for wild pollinators. �ese areas can extend the bee foraging period beyond the �owering crop season (Basu, Cetzal-Ix, 2017) and provide undisturbed nesting sites so that populations can more easily persist from year-to-year. Plant seed mixtures could include native wild�owers, grasses, and legumes, as well as �owering trees and shrubs. Priority should be given to native plants, as they generally bene�t wild pollinators more than introduced plant species. �e plant species included in the mixture should be selected so that they do not all �ower simultaneously, but are spread across the �owering season so that they bene�t the widest range of pollinators (Basu, Cetzal-Ix, 2017). Hedgerows or other pollinator habitats will need to be tailored speci�cally for each region in which they are planted, and the Xerces Society (http:// xerces.org/guidelines/) provides recommendations for planting pollinator habitats, including lists of plant species across the continental United States and Canada. But will creating new pollinator habitats take away farmland or urban areas and create ‘o�-limit’ zones for human development or activity? Not necessarily, because many unused areas already exist in urban and rural environments where these pol- linator habitats could be established. Habitats could be established along fence lines, wind breaks, irrigation canals, highways, sections of golf courses, and municipal parks and gardens (Basu, 2017; Basu, Cetzal-Ix, 2017). Pollinator habitats can have positive impacts on the richness and abundance of wild bee species, and they can provide S am ue l R ob in so n, W ill ia m C et za l-I x, S ai ka t K um ar B as u 164 bene�ts to farmers growing pollinator-dependent crops. For instance, Kremen and M’Gonigle (2015) found that planting hedgerows (lines of �owering shrubs and bush- es) in the highly cultivated Napa Valley in California increased the abundance of both common and rare pollinators. Not only did these hedgerows increase abundance and diversity locally, but they acted as sources of wild pollinators for the surrounding ad- jacent �elds, as �elds planted next to hedgerows tended to have higher numbers of pollinators present in them (Morandin, Kremen, 2013). 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Diversity of �ora of Mexico pollinated by di�erent species of bees. Bees: A–E – Apis mellifera L., F – Scaptotrigona sp., G – Bombus sp., H – Euglossa viridissima Friese. Plants: A – Capraria mexicana Moric. ex Benth. (Scrophulariaceae)., B – species from the family of grass- es (Poaceae), C – Ximenia americana L. (Olacaceae), D – Ruellia nudi�ora (Engelm. & A. Gray) Urb. (Acanthaceae), E – Okenia hypogaea Schltdl. & Cham. (Nyctaginaceae), F – Lu�a aegyptiaca Mill. (Cu- curbitaceae), G – Catasetum integerrimum Hook. (Orchidaceae), H – Notylia barkeri Lindl. (Orchidace- ae) (Photo. W. Cetzal-Ix) S am ue l R ob in so n, W ill ia m C et za l-I x, S ai ka t K um ar B as u 168 Fig. 2. Some common western North American bee species. Bees: A – Apis mellifera L., B – Osmia lignaria Say provisioning their nests in a bee block, C – Bombus ternarius Say, D – Halictus sp., E – Agopostemon virescens Abrams & Eickwort, F – Andrena lupinorum Cockerell, G – Bombus borealis Kirby, H – Halictus spp. Plants: A – Medicago sativa L. (Fabaceae), C – Syringa vulgaris L. (Oleaceae), D, H – Taraxicum o cinale F. H. Wigg. (Asteraceae), E – Gaillardia aristata Pursh (Asteraceae), F – Brassica napus L. (Brassicaceae) (Photo. S. Robinson and P. Birch) A ppendix 1 169 Zanikanie i ochrona dzikich pszczół w Ameryce Północnej Streszczenie Pszczoły – to niezwykle różnorodna i  ważna grupa owadów; około 4600 gatunków pszczół występuje w Ameryce Północnej. Dzikie pszczoły „świadczą usługi” w zakresie zapylania roślin, a ich działalność jest prawdopodobnie nawet więcej warta niż działalność pszczół miodnych na całym świecie. Są one słabo zba- dane na większości obszarów, ale na terenach, dla których mamy wiarygodne dane, liczebność ich popu- lacji obniża się. Wynika to głównie z  przekształcania obszarów półnaturalnych w  grunty rolne, a  nowsze dane wskazują również, że pszczoły miodne mogą także wpływać na ich populacje. Aby zachować istniejące populacje pszczół, należy ustalić siedliska zapylaczy, w celu zachowania różnorodności dzikich zapylaczy w  krajobrazach wiejskich i  miejskich. W  miarę jak populacja ludzi rośnie wraz z  zapotrzebowaniem na produkcję rolną, musimy znaleźć sposoby „współpracy” z dzikimi zapylaczami i sposoby zachowania dla przyszłych pokoleń tysięcy gatunków pszczół, które żyją w Ameryce Północnej i w innych częściach świata. Key words: causes of decline, conservation, diversity, wild bee Received: [2017.08.25] Accepted: [2017.11.10]