AMERICAN JOURNAL OF UNDERGRADUATE RESEARCH VOL. 2 NO. 2 (2003)

The Relationship of Apis mellifera with Exotic and Native in Boulder County, Colorado

Kira Krend and Christina Murphy Department of Ecology and Evolutionary Biology University of Colorado at Boulder Boulder, Colorado 80309 USA

Received: May 20, 2003 Accepted: August 5, 2003

ABSTRACT

Since honeybees (Apis mellifera) were introduced to North America in the 1600’s, their influence has been profound and widespread. As pollinators, honeybees are extremely valuable economically and are vital to crop pollination. However, their presence has affected native ecosystems, including the plains ecosystem in Colorado. Using recruitment and other unique foraging characteristics, honeybees may be out-competing native pollinators for nectar and pollen resources. Our study was designed to determine if A. mellifera has a preference for exotic or native plants. We observed patches of exotic plants and patches of native plants and recorded the type of bee (exotic or native) that visited each flowering head. We also examined data from Kearns and Oliveras (unpublished), which illustrates that invasive species are also popular with native bees, and may draw vital pollinators away from native plants. Our results indicate that honeybees prefer to visit exotic invasive plant species to native plants. Consequently, honeybees may contribute to the spread of exotic plant species and the decline of native plant species, reducing biodiversity. Thus, native plants are doubly jeopardized. The invasion of exotic flora and fauna into native ecosystems on the plains of Colorado is part of a worldwide phenomenon of species invasion, and researchers must continue to investigate interspecies relationships to minimize the potential negative effects of invasive species.

I. INTRODUCTION mellifera would visit and pollinate exotic plants more than the native plants of the The infiltration of exotic species into an area Front Range. can change ecological processes. Any The honeybee, Apis mellifera, is at disturbances to a food web can affect the the forefront of what ecologists deem a entire ecosystem. Exotics can often out- “pollination crisis:” an imbalance of the compete native species for resources and critical pollination ecosystem of flowering introduce new diseases and parasites [1]. plants [2]. The economic value of flowering Three things are clear about exotics: 1) it is plants is enormous, and most angiosperms impossible to know where an exotic species depend on insect pollinators, such as bees, will become established; 2) when it will for sexual reproduction. Changes in the happen; 3) and how it will affect an populations of pollinating insects directly ecosystem [1]. The effects of introduced affect the plants they pollinate. This shift honeybees on native ecosystems are still could potentially have serious unclear; few studies have been done, and consequences for the world’s food supply. those few found differing levels of effect. Part of a worldwide phenomenon of species The purpose of this project was to examine invasion, A. mellifera has been introduced the attractiveness of exotic and native plants from Eurasia and Africa into most of the rest to the exotic honeybee, Apis mellifera, by of the world [3]. Although introduced looking at visitation rates in Boulder County, honeybees may contribute to the decline of Colorado. Our hypothesis was that A. native pollinators, and consequently native

5 AMERICAN JOURNAL OF UNDERGRADUATE RESEARCH VOL. 2 NO. 2 (2003) plants, the economic importance of area to area [6]. This evidence suggests honeybees cannot be denied as they honeybees may be poor pollinators of some pollinate a significant proportion of flowering native flora. plants [4]. Yet some research suggests that While the concept that pollinators honeybees may negatively affect the native are more attracted to plants with which they biota [5]. Balancing the economic value and have co-evolved makes intuitive sense, very ecological consequences of honeybees, as few studies have been conducted regarding well as many other species, is a complex this association. In residential areas of issue that has yet to be resolved. Berkeley, California, Frankie et al. [7] found that exotic plants had a low attraction for a. Study Pollinators native bees. The authors believed the low attraction may be attributed to horticultural Apis mellifera is native to Europe, selection where humans have selected for Africa, and northwest Asia. It was first aesthetically pleasing traits, such as showy introduced into North America through petals, and not for large amounts of nectar Jamestown, Virginia, between 1630 and and pollen, resulting in reduced rewards for 1663 [5]. Since that time, honeybees have bees. Additionally, native bees may be less spread to every terrestrial environment in attracted to exotic plants because they did North America and number in the billions. not co-evolve with the exotic plants. Native Honeybees often out-compete other plants were four times more likely than pollinators; however, the extent to which exotic plants to attract native bees. they have replaced native species is Many people think of wax and unclear. Honeybees’ success can be honey production as the primary economic attributed to many factors. First, they find importance of honeybees. However, flowers quickly and promptly determine if the Buchmann and Nabhan [4] estimated that flowers are worth the time to visit. Secondly, honeybee pollination of crops is 50 to 60 if a good source of nectar is found, percent more valuable than their production honeybees can communicate the location of of honey and wax. Unfortunately, many the flowers to the rest of the hive through ecologists believe that both native recruitment, a tactic not used by most native pollinators and honeybees are in rapid pollinators. Consequently, honeybees decline [2]. Some reasons for the drop in harvest nectar and pollen before native honeybee populations include the use of pollinators have a chance [6]. While solitary pesticides and infectious parasitism by mites bees only live for one generation, honeybee [4]. Also, in regions of the United States that colonies are long-lived [6]. Thus, knowledge have been invaded by aggressive of flower patch locations can be used by Africanized bees, many beekeepers have honeybee colonies for generations, while been driven out of business due to rising solitary bees must learn these locations insurance costs against attacks [4]. This independently. decline could mean lower crop yields, with Honeybees are generalists and not serious consequences to the world’s food faithful to any single plant species. This supply; one in every three mouthfuls of food generality is in contrast to many native eaten is pollinated by animals, including pollinators that are specialized visitors of honeybees [4]. certain plants for nectar and pollen [6]. Studies that have attempted to look Additionally, honeybees usually pack their at competition between native bees and A. pollen with nectar and saliva, which limits mellifera have reported mixed results. pollen viability and causes less pollen to fall Some studies argue that honeybees change on a flower’s stigmatic surface [6]. On some the foraging behavior and population size of flowers, honeybees are able to collect pollen native bees [7]. For example, Gross [8] without ever coming into contact with the found that native bees were less likely to flower’s stigma, avoiding pollination of the forage on plants where honeybees are flower. Many ecologists believe that native present. Paton [9] determined that native flower species have not been able to adapt bees of North and South America switch to to honeybees’ particular method of less profitable flower resources when pollination, because a colony’s taste honeybees were present. Though changes from season to season and from honeybees are blamed for out-competing

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native pollinators, not pollinating native results with a broad range of implications, plants effectively, and increasing the which help to illustrate the complexity of success of weeds, Huryn [3] notes that not plant-pollinator relationships. In our study, much data have been collected to support we predicted that A. mellifera would exhibit a these accusations. higher visitation to rate to exotic plant species than native plants. b. Study Plants

All plants in this study are members II. METHODS of the family . The two plant species native to the Front Range that were We examined flower patches of included in this study were golden aster each species, Heterotheca villosa, (Heterotheca villosa) and gumweed Centaurea diffusa, Grindelia squarrosa, and (Grindelia squarrosa). The two exotic Cirsium arvense in the prairie and foothills of o species in the study were Canada thistle Boulder County, (40 00' N latitude, and o o (Cirsium arvense) and diffuse knapweed between 105 20'W and 105 30'W) (Centaurea diffusa). Data were also Colorado, USA. Each species of flower was examined from (but not analyzed, see observed four to six times. Different patches Results) sunflowers ( pumilus, of flowers were observed on different days native) and chicory (Cichorium intybus, for ten-minute periods from July through exotic). Originally a Eurasian immigrant, September 2002. During the study, we Canada thistle is considered a pest in towns, observed approximately equal numbers gardens, fields, and pastures, and is (average 1235 heads) of open flower heads common in the region. Chicory was also available for pollination on each plant imported from Europe and is common on the species. We noted whether each visiting plains, often along roads, fields and ditches bee was a honeybee (A. mellifera) or a from July to October [10]. The third exotic native bee, and attempted to identify the plant, diffuse knapweed, will be elaborated native bee visitors to family. We captured on below, as it is a paradigm of an exotic representative bees after the observation plant species that has invaded an area and period was complete, and later identified may be harming native ecosystems. them to genus. We also recorded the Most invasive plant species are not number of flower heads each bee visited dominant in their natural environment, but during the ten minutes of observation. easily out-compete native species in To supplement this analysis, we environments where they are introduced. used Kearns and Oliveras’ [13] pollination For example, Calloway and Aschehoung database on bee visitors to grassland plants [11] noted that diffuse knapweed (Centaurea from their study on the effects of diffusa) has negatively affected many North urbanization on pollinator diversity. Their American plant species, while it has no research was conducted on 20 grassland negative effect on its native plant neighbors plots in Boulder County, Colorado, USA. We in Eastern Europe and Western Asia. examined the database to determine the Additionally, exotic plant species were number of exotic and native bees that imported without their co-evolved insect landed on exotic and native plants in the herbivores and pathogens. Thus, abiotic Asteraceae, including the four plants in our factors are the only regulators of these study Heterotheca villosa, Centaurea plants, and are often not enough to control diffusa, Grindelia squarrosa, Cirsium their population size [12]. Grasslands that arvense, as well as two more plants, have been invaded by exotic tap-rooted Cichorium intybus, (exotic) and Helianthus weeds such as knapweed have experienced pumilus (native). soil and water losses, consequently harming The data from our study were native plants and reducing biodiversity [12]. analyzed with SAS 8e (1999-2001). The Clearly, understanding the effects procedure used was a logistic analysis with of honeybees on native plants and the Williams adjustment to correct for pollinators is vital to solving the pollination overdispersion. Overdispersion is related to crisis, and more research needs to be the overall variation between individual conducted. Studies have found differing plants.

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III. RESULTS common for a single bee to move between flowering heads in the observed patch while Exotic plants were more likely than data were being collected. native plants to be visited by the exotic bee, Unpublished data from an ongoing A. mellifera (Wald Chi square p=0.0559; study by Kearns and Oliveras [13] (Table 3) Table 1). With the Williams adjustment indicate similar trends to those found in our applied to correct for overdispersion, the study. We did not conduct a statistical probability of an exotic bee visiting an exotic analysis of these data, since we lumped plant was 7.8 times greater than that of an data from many dates and sites. However, exotic bee visiting a native plant. However, the raw data help illustrate that exotic bees the number of native bees present was 7-8 were much more likely to be captured while times greater than the number of honeybees visiting an exotic plant than while visiting a on both exotic and native plants. We did not native plant. The data also show that exotic observe any interactions between individual plants are popular with both native and bees while visiting the study plants. It was exotic bees.

Heterotheca villosa (native) 1330 flowering heads observed

Native bees Exotic bee (A. mellifera)

Total number of visiting bees 48 2

Total landings on flowering heads 547 8

Grindelia squarrosa (native) 1090 flowering heads observed

Native bees Exotic bee (A. mellifera)

Total number of visiting bees 96 0

Total landings on flower heads 419 0

Cirsium arvense (exotic) 1250 flowering heads observed

Native bees Exotic bee (A. mellifera)

Total number of visiting bees 93 13

Total landings on flower heads 195 32

Centaurea diffusa (exotic) 1270 flowering heads observed

Native bees Exotic bee (A. mellifera)

Total number of visiting bees 73 10

Total landings on flower heads 407 53

Table 1. Total number of bees and bee landings observed on study plants during data collection periods. Statistical analysis was performed on the total number of landings on each study plant. Data are from the present study (Krend and Murphy).

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IV. DISCUSSION Plant species Genera of The data from our study indicate native bees that A. mellifera is much more likely to visit observed an exotic study plant than a native study plant. Exotic plants in the study also appear Grindelia squarrosa Agapostemon to be utilized by native bees. Unpublished (native) Lasioglossum data from Kearns and Oliveras [13] seem to Megachile indicate a similar trend. While our study was Melissodes short-term, collected over a period of three Hoplitis months, Kearns and Oliveras’ data are being Andrena collected over three years. Our study Dianthidium focused on observing bees on flowering Anthidum heads, while Kearns and Oliveras’ study Bombus involves collecting the bees. However, both studies indicate the above trends. The repercussions of these trends could Heterotheca Hylaeus potentially be widespread for both native villosa Agapostemon plants and native pollinators. The (native) Melissodes reproductive success of exotic plants, due to Halictus pollination by exotic bees, may displace Megachile native plants, consequently reducing Heterosaurus biodiversity. Additionally, if pollinators visit Panurginus

an invasive plant species more frequently than a native plant, indigenous plants are Centaurea Ceratina left with fewer pollinators to facilitate sexual diffusa Dialictus reproduction. (exotic) In the United States, information on the abundance and diversity of native bee species before the introduction of Cirsium Sphecodes honeybees is almost non-existent. This lack arvense Lasioglossum of information makes the effects of (exotic) Bombus honeybees difficult to assess, and few Melissodes studies have addressed this question. In Colletes Australia, where honeybees were introduced Hylaeus only in the last 150 years, more studies have Dialictus been conducted. The sources of nectar and Andrena pollen used by A. mellifera in Australia Halictus overlap with those of native bird and bee Svastra pollinators, resulting in competition. One Australian study showed that Table 2. Genera of native bees observed honeybees begin foraging in the early on native and exotic plant species. The only morning when most flowers have the most exotic bee observed was A. mellifera. Data resources, while native Australian bees are are from the present study (Krend and most active in the middle of the day [9]. Murphy). Another study illustrated that honeybees

temporarily reduced the foraging success of nectar from bird-pollinated flowers. Also, native bees by depleting mutual resources New Holland honeyeaters were much less [14]. Honeybees also out-competed native likely to visit flowers when the honeybee bees by foraging over greater areas, and by population was high, and avoided flowers their ability to move their colonies [5]. where honeybees were present. When At least one study indicated that honeybees replace native honeyeaters as honeybees affected the New Holland plant pollinators, plant fitness may decrease. honeyeater (Phylidonyris novaehollandiae) On one Australian plant, Callistemon in Australia [9]. This study estimated that rugulosus (Myrtaceae), nectar harvesting honeybees removed more than 90% of the

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conducted on the pollination efficiency of Plant Number Number of honeybees on individual plant species, both species of native A. mellifera native and exotic. bees (exotic) Although our study found that honeybees visit exotic plants more than Heterotheca 95 1 native plants, many more native bees were villosa observed overall (on both exotic and native (native) study plants) than honeybees. As such, native bees may also be contributing to the Grindelia 10 0 spread of exotic plants. However, the squarrosa influence of any species of bee on the (native) success of invasive plants may be overrated because plants’ ability to reproduce Helianthus 50 0 asexually. According to a study by Huryn pumilus and Moller [15], honeybees might not play a (native) large role in the overall success of invasive

plants since most problematic weeds tend to Centaurea 39 33 diffusa have plastic reproduction, such as self- (exotic) pollination, unspecialized pollination, high germination rates, specialized seed

dispersal, or vegetative spread. Huryn and Cirsium 11 14 arvense Moller [15] found that in New Zealand, only (exotic) one out of 29 problem weeds studied was ‘highly influenced’ by honeybees. Thus, this Cichorium 19 11 study indicated that most weeds would intybus probably still be successful without (exotic) honeybees, and the influence of A. mellifera is probably minimal for most problem weeds. Table 3. The numbers of native and exotic Researchers have not yet determined how (A. mellifera) bees collected on native and successful invasive species such as exotic plants. Data are from Kearns and knapweed would be on the prairie without Oliveras [13]. the facilitation of sexual reproduction by honeybees and other bees. The influence of A. mellifera on honeybees only struck the stigma on 4.4% native pollinators is complex. Honeybees’ of visits, while its native pollinator, the New system of recruitment and other unique traits Holland honeyeater, struck the stigma more may help them out-compete native than 50% of the time [9]. Presently, pollinators. Since honeybees target exotic researchers do not know if a similar trend is plants, native bees may still have plenty of occurring with native bees and honeybees in nectar and pollen available for consumption the United States. from native plants. However, native Despite negative effects, removing pollinators might have their own interspecific honeybees completely may be detrimental competition on native plants, causing some to native plants that have lost their natural native bees to move to exotic plants and pollinators or are inadequately pollinated by compete with honeybees. Whether the native fauna. For example, honeybees are actually taking away Orthrosanthus multiflorus (Iridaceae) is only resources from native bees and forcing them in flower for a single day. Honeybees were to visit fewer plants and/or plants with able to pollinate O. multiflorus effectively, depleted nectar and pollen has yet to be while native pollinators were not always as conclusively determined. efficient [9]. Thus, honeybees are effective From studies in the United States, pollinators for some native plants such as O. as well as Australia and New Zealand, A. multiflorus but certainly not all flowering mellifera is clearly affecting native plants, as illustrated by its low pollination ecosystems. Yet how detrimental A. rate of Callistemon rugulosus [9]. On the mellifera is in specific situations remains to Colorado prairie, more research needs to be be determined. While researchers do not

10 AMERICAN JOURNAL OF UNDERGRADUATE RESEARCH VOL. 2 NO. 2 (2003) yet know if the presence of honeybees 3. Huryn, V.M. 1997. Ecological impacts causes the decrease in native bees present, of introduced honey bees. The honeybees are clearly affecting the Quarterly Review of Biology 72:275-297. pollination of plants on the prairie. The 4. Buchmann, S.L. and G.P. Nabhan. introduction of honeybees to the North 1996. The pollination crisis: the plight of American continent has led to both the honeybee and the decline of other detrimental and beneficial consequences. pollinators imperils future harvests. The Although they could be facilitating the Sciences. 36:22-28 spread of exotic plants, and possibly 5. Hubbell, S. 1997. Trouble with causing the decline of native pollinators, the Honeybees. Natural History. 106:32- contribution of the honeybee to the food 43. supply through crop pollination is of vital 6. Westerkamp, C. 1991. Honeybees are economic importance [4]. poor pollinators-why? Plant The introductions of invasive plants, Systematics and Evolution 177:71-75. such as diffuse knapweed, and of animals, 7. Frankie, G.W., R.W. Thorp, M.H. such as the honeybee, have many Schindler, B. Ertter and M. Przybylski. implications to the native plains ecosystem. 2002. Bees in Berkeley? Fremontia. Ecologists recognize these introductions as 30:50-58. part of a worldwide phenomenon of exotic 8. Gross, C.L. 2001. The effect of species invasion. The potential introduced honeybees on native bee consequences of exotic introductions are visitation and fruit-set in Dillwynia shifts in the delicate relationships between juniperina (Fabaceae) in a fragmented species in the native ecosystems. Though ecosystem. Biological Conservation nearly all ecosystems on Earth have already 102:89-95. experienced invasion of exotic species, 9. Paton, D.C. 1993. Honeybees in the research must continue in order to Australian environment. Bioscience understand intricate interspecies 43:95-103. relationships to help minimize the potential 10. Guennel, G.K. 1995. Guide to Colorado negative effects of invasive species. Wildflowers. Westcliffe Publishers, Inc. Englewood, Colorado. ACKNOWLEDGEMENTS 11. Callaway, R.M. and E.T. Aschehoung. We would like to thank Carol Kearns and 2000. Invasive plants versus their new Diana Oliveras of the Baker Residential and old neighbors: a mechanism for Academic Program, University of Colorado exotic invasion. Science 290:521-523. at Boulder, for their guidance and support. 12. Beck, K.G. 1994. How do weeds affect We would also like to thank Bill Oliver for his us all? Abstract, Leafy Spurge assistance with statistical questions, Pablo Symposium. Bozeman, ; July Weaver for assisting in the editing process, 26-29, 1994. http://www.team.ars.usda. and three anonymous reviewers for gov/ symposium/1994/one.html. providing constructive comments on drafts Accessed 13 July 2002. of this paper. The Undergraduate Research 13. Kearns, C. and D. Olivias (private Opportunities Program at the University of communication) Colorado at Boulder funded this research. 14. Sugden, E.A. and G.H. Pyke. 1991. Effects of honey bees on colonies of REFERENCES Exoneura asimillima, and Australian

1. Bright, C. 1995. Bio-invasions: the native bee. Australian Journal of spread of exotic species. World Watch. Ecology 16:171-181. July/Aug:10-18. 15. Huryn, V.M. and H. Moller. 1995. An 2. Kearns, C.A., D.W. Inouye and N.M. assessment of the contribution of honey Waser. 1998. Endangered mutualisms: bees to weed reproduction in New the conservation of plant-pollinator Zealand protected natural areas. New interactions. Annual Reviews of Zealand Journal of Ecology 19:111- Ecology and Systematics 29:83-112. 121.

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