Competition between exotic honey bees (Apis mellifera) and native pollinators on late-blooming desert scrub

Janelle M. Osteen1, Alexis M. Necarsulmer2, Jessica J. Fan Brown2, Nhung H. Nguyen3

1University of California, Berkeley; 2University of California, Santa Cruz; 3University of California, Los Angeles

ABSTRACT

Pollinators are essential to worldwide biodiversity. This study focuses on pollinator communities on Isocoma acradenia, a late blooming shrub in the Colorado desert. We hypothesize that late in the flowering season, exotic honey bees and native pollinators experience increased competition for floral resources. We surveyed pollinator species richness, abundance, and competitive interactions. Our results reveal that honey bee presence does not have effects, competitive or otherwise, on native pollinators. Continuing to research exotic and native pollinator dynamics will provide insight into understudied desert ecosystems.

Keywords: pollinator competition, Apis mellifera, Isocoma acradenia, desert, limiting resources

INTRODUCTION utilizes non-native honey bees (Vandenberg 2013). Even though a diverse pollinator 1.1 Pollination community yields more sustainable crops, $215 billion is spent annually on introducing Pollinators are a crucial component of European honey bees to promote global biodiversity because they provide agricultural pollination (Vandenberg 2013). cross-pollination, promoting genetic diversity in wild plant populations (Cane and 1.2 Honey Bee Effects on Native Pollinators Tepedino 2001, Steffan-Dewenter and Westphal 2008). Insect pollinators have Compared to other invertebrates, loss of been experiencing a global decline due to native bees is likely to have the most habitat fragmentation, use of herbicides, detrimental effects on pollination in North climate change, introduction of invasive America (Cane and Tepedino 2001). species, and many more anthropogenic Introduced honey bees compromise native disturbances (Vandenberg 2013). These pollinator communities because they pressures on pollinator communities compete for about 25% of the same wild jeopardize crucial ecosystem services. The resources (Minckley et al. 2003). Honey bees most important of these services is (Apis mellifera) are thought to be superior agricultural pollination, which exclusively competitors to solitary bees because of their

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high nectar and pollen requirements and 1.4 Isocoma as the Ideal Study Species their use of communication to locate and exploit productive patches of flowers more Isocoma acradenia (alkali goldenbush, efficiently (Steffan-Dewenter and hereafter referred to as Isocoma), is one of Tscharntke 2000). Additionally, large honey the only angiosperms still blooming in Anza bees have disproportionately greater Borrego Desert State Park during late fall. foraging distances than smaller native bees Calflora shows Isocoma in a patchy, narrow (Greenleef et al. 2007). Longer foraging distribution near riparian zones. Most desert distances allow honey bees to utilize the honey bee populations are also found near most energetically productive patches of riparian zones (Minckley 2003). Although A. plants in a given area (Schaeffer et al. 1979, mellifera is the most common visitor to 1983 and Ginsberg 1983). By practicing nest Isocoma in Anza Borrego, at least 20 native thermoregulation, honey bees access species also utilize Isocoma, making it the resource-rich areas earlier in the day than ideal study species to test for increased native species (Jones et al. 2004). Honey resource competition. bees also actively thermoregulate during foraging, so they might prefer different sun 1.5 Hypotheses exposure levels (Roberts and Harrison 1998). We hypothesize that greater honey bee Honey bee foraging habits, such as temporal presence negatively affects native pollinator and climactic preferences, may also have species richness. Additionally, honey bee major effects on native pollinators. Because visitation rates will be greatest in the honey bees have naturalized across many morning, whereas native visitation rates will habitats, it is especially important to be greatest in the afternoon when honey examine their impacts in understudied bee abundance decreases. Periods of environments, such as deserts. greatest visitation will yield the most visitor 1.3 Desert Communities interactions, indicating increased resource competition. Honey bee distribution will be In many desert communities, peak equally spread across all sun exposures pollination occurs in the spring and little to because they actively thermoregulate. In no pollinator competition has been comparison, native visitors will be found in observed. In fact, during peak bloom, sunny areas due to their adaptions to desert Minckley et al. (2003) found no relationship climates. between number of honey bees and native bee species richness and abundance on the METHODS most common shrub in the Sonoran Desert, 2.1 Study System Larrea tridentata. However, later in the flowering season, honey bees and native Our research was based in Anza Borrego pollinators may experience increased Desert State Park and was conducted competition for floral resources, possibly between November 2–7. Our study site was leading to aggressive interactions. at Yaqui Wells (33.13948, -116.38779), selected due to the abundance of Isocoma.

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No studies have been completed on interaction was characterized as aggression. Isocoma, although it provides valuable All observations were repeated at each bush resources for desert pollinators at the end of during each time block. the season. We surveyed twelve bushes in two-hour time blocks from 8 am to 4 pm, 2.4 Statistical Methods observing each bush during each block, to record how species richness, abundance, A linear regression model was used to test and competition changed throughout the the effect of time of day on species richness, day. total species visitation rates, and honey bee visitation rates. To see how the pollinator 2.2 Species Richness and Honey Bee community changed throughout the day we Abundance ran a discriminate analysis on the four time blocks. To test the effect of sun exposure on Species richness was documented through honeybee and native visitor activity, an group observation. At every bush, we ANOVA was performed. All statistical recorded each visiting species seen on analysis was completed on JMP 14. Isocoma flowers until three minutes elapsed without seeing a new species, ensuring that RESULTS all frequent visitors were included. We counted honey bees in three quadrats on 3.1 Species Richness and Honey Bee each bush to get an average measure of Abundance honey bee abundance. Finally, sun exposure Overall species richness remained for each bush was categorized into shade, constant throughout the day (N= 48, partial shade, and sun. All observations were r2<0.001 p = 0.48). However, different repeated at each bush during each time pollinator species were recorded foraging at block. different times (Figure 1). For example, 2.3 Visitor Interactions common morning pollinators were honey bees, flies (Copestylum sp., Nannocyropogon We observed 10-25 inflorescences from sp., syrphids, and muscids), wasps the same twelve bushes for fifteen minutes. (Podalonia sp. and Priocnemis sp.), and a Each branch was defined as one butterfly (Strymon sp.). Afternoon inflorescence. We tallied the number of pollinators often included solitary bees visitations and interactions per species. If a (Colletes sp. and Megachile sp.), flies visitor joined an inflorescence occupied by (Bombylius sp. and Geron sp.), wasps another visitor and neither left for at least (Steniola sp. and Ammophila sp.), and a three seconds, this interaction was butterfly (Plebejus sp.). There was no pattern characterized as tolerance. However, if one associated with honey bee abundance and visitor flew away within three seconds, the time of day (N= 48, r2=0.02, p= 0.31).

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Figure 1. Discriminate analysis of temporal taxon shifts in the pollinator community. Twenty common diurnal pollinators, identified to families or genera, are unequally represented across four different time blocks. There are distinct changes between which pollinators are present during each time block. The 8 am–10 am and 2 pm–4 pm time blocks show the least overlap in pollinator communities.

Figure 2. Effects of sun exposure status on European honeybee density. Vertical bars represent ± one Figure 3. Effect of time of day on total visitation rate. standard error. Honey bees were most likely to occur Military time is shown on the x-axis and log(total on Isocoma bushes in the sun. Honey bee visits) per hour are shown on the y-axis. Total microhabitat preference for sun could be behavioral visitations on Isocoma decrease from morning to thermoregulation. Native visitor sample size was too afternoon. small to show microhabitat preference (p>0.3).

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3.2 Visitation and Interactions has partitioned foraging times to minimize direct competition, especially when Total visitation rate decreased throughout resources are limiting (Stone et al 1996). the day. (N= 48, p = 0.04, r2= 0.08; Figure 2). Although species richness did not change, Honey bee visitation rate followed a total visitation on Isocoma declined decreasing trend throughout the day (N= 48, throughout the day. Decreasing visits can be p= 0.11, r2= 0.85). There were not enough explained by nectar and pollen depletion of total interactions observed to conclude any Isocoma flowers caused by heavy morning temporal effects on insect interactions. foraging (Roubik and Buchmann 1984). A Throughout the study, honeybees had a possible explanation for decreased visitation total of 158 tolerance interactions and 47 is honey bee heat exhaustion. However aggression interactions with other average peak temperature during this study honeybees. Between honey bees and native period never reached 35°C, the temperature species, 12 tolerance interactions and 6 at which honey bees stop foraging (Cooper aggression interactions were observed. and Schaffer 1984). However, cooler morning temperatures may be favorable for 3.3 Sun Exposure pollinators trying to maximize energy function. Honey bee presence was associated with Both tolerance and aggression decreased sunny bushes (Nsun= 32, Nshade= 5, Npartial= 11, over time, but this could be a result of the F = 4.53, p = 0.02; Figure 3). Unlike honey bee overall decrease in Isocoma visitations. Our presence, there was no difference in native prediction that the most interactions would species presence between bushes in the sun be observed at the highest visitation time or shade (Nsun= 32, Nshade= 5, Npartial= 11, F= was supported. We observed surprisingly 0.97, p= 0.39). few interactions between honey bees and DISCUSSION native visitors. Ginsburg (1983) and Schaffer et al. 1979 have found minimal evidence for Overall, we did not find evidence for honey aggression between honey bees and native bee competition with native visitors on pollinators. While aggression may not be Isocoma. Because honey bee visitation occurring, daily nectar depletion in Isocoma showed a decreasing trend throughout the could lead to a “first come, first serve” day, we expected that native pollinator scenario, known as scramble competition, richness would increase in the afternoon. instead of direct competition as we had However, species richness remained hypothesized. European honey bees constant, disproving our hypothesis. The monopolize plants high in resources (Kearns constant species richness reflects and Inouye 1997). Honey bees can also have conclusions by Minckley et al. 2013 that an advantage over native bees by arriving honey bee presence does not affect native earlier and in high abundance to the species richness. Although richness did not flowering plant (Greenleaf et al. 2007). change, different genera were observed Native pollinators could avoid competition foraging at different parts of the day. This by utilizing bushes less favored by honey could suggest that the pollinator community bees. European honey bees prefer bushes in

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full sun over those in partial or total shade. want to thank Krikor Andonian, Tim Miller, Honey bees may prefer sunnier areas due to Kate Melanson, and the California Ecology behavioral microhabitat selection to and Conservation program for the regulate heat transfer (Roberts and Harrison opportunity to think wide and push limits in 1998). Native visitors had a sample size too field research and foster an environment for small to determine preference for sun or continuous growth. shade. However, shaded flowers may provide essential foraging opportunities for REFERENCES native species. Cane, J. H., and V. J. Tepedino. 2001. Causes and Our results align with prior research that extent of declines among native North American honey bee presence does not have dramatic invertebrate pollinators: Detection, evidence, and effects on native desert pollinators, even consequences. Conservation Ecology 5:341–363. when resources are limiting (Minckley et al. 2013). Even though we did not detect direct Ginsberg, H. 1983. Foraging ecology of bees in an old field. Ecology 64:165–175. competition, we still think honey bees are having negative impacts. We propose that Greenleaf, S., N. M. Williams, R. Winfree, and C. trials excluding honey bees and quantifying Kremen. 2007. Bee foraging ranges and their nectar depletion would be useful in relationship to body size. Oecologia 153:589–596. detecting scramble competition. If honey Huryn, V. 1997. Ecological impacts of introduced bee exclusion increases native pollinator honey bees. The Quarterly Review of Biology visitation, then scramble competition is 72:275–297. likely. European honey bees have other poorly researched impacts on native desert Jones, J., M. R. Myerscough, S. Graham, and B. P. pollinator populations, such as increased Oldroyd. 2004. Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404. pathogen transmission and alterations in plant communities (Butz Hurn 1997). Minckley, R. L., J. H. Cane, L. Kervin, and D. Yanega. Understanding how pollinator relationships 2003. Biological impediments to measures of are affected by anthropogenic disturbances competition among introduced honey bees and is crucial because other important desert bees (Hymenoptera: Apiformes). Kansas Entomological Society 76:306–319. interactions could be occurring. Minckley, R., and Ascher, J. 2013. Preliminary survey ACKNOWLEDGMENTS of bee (Hymenoptera: Anthophilia) richness in the northwestern Chihuahuan Desert. USDA Forest We want to extend our gratitude to the Service Proceedings 67:138-143. Steele/Burnand Anza-Borrego Desert Research Center doi:10.21973/N3Q94F for Roberts, S., and Harrison J. 1998. Mechanisms of thermoregulation in flying bees. American providing a facility to conduct and analyze Zoologist 38:492–502. our research. Many thanks to Jim Dice and Elaine Tulving for hosting our stay and Schaffer, W. M, D. B. Jensen, D. E. Hobbs, J. Gurevitch, providing enriching opportunities for us to J. R. Todd, and M. V. Schaffer. 1979. Competition, expand our knowledge of Anza, its history foraging energetics, and the cost of sociality in three species of bees. Ecology 60:976–987. and sights. Finally, with big gratitude, we

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Schaffer, W. M, D. W. Zeh, S. L. Buch, S. Kleinhans, and Vandenberg, A. 2013. Threats to an ecosystem J. Antraian. 1983. Competition for nectar between service: pressure on pollinators. Frontiers in introduced honey bees and native North American Ecology and the Environment 11:251–259. bees and ants. Ecology 64:564–577. Waddington, K D. 1983. Foraging behavior of Steffan-Dewenter, I. and Tscharntke, T. 2000. pollinators. Annals of the Missouri Botanical Resource overlap and possible competition Garden 95:213–239. between honey bees and wild bees in Central Europe. Oecologia 122:288–296 .

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