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Arthropod-Plant Interactions

, Volume 11, Issue 3, pp 403–409 | Cite as

Bee visitors of Centaurea solstitialis L. (Asteraceae) in an urban environment in northwestern Turkey

  • Victor H. GonzalezEmail author
  • Alena Olsen
  • Maija Mallula
  • Aycan Tosunoglu
  • Ibrahim Çakmak
  • John Hranitz
  • John Barthell
Original Paper
  • 506 Downloads

Abstract

Information on the pollination ecology and floral visitors of the noxious weed Centaurea solstitialis is available for several populations in its invasive range, but limited information is available in its native range, with most studies conducted on the Greek island of Lesvos. Herein, we document the visitation pattern of bees and explore the relationship of bee body size and nectar availability in weedy populations of C. solstitialis from an urban environment within its native range in northwestern Turkey. Studies were conducted at patches of C. solstitialis in abandoned lots at the Uludağ University near the city of Bursa. A total of 41 species, including honey bees, belonging to five families and 19 genera were recorded. Small megachilid and halictid bee species were the most common visitors. Average nectar standing crop volume per floret was low (0.003–0.117 μL) and did not significantly vary throughout the day. Average bee head width significantly correlated with average nectar standing crop volume but did not significantly change throughout the day. Analyses of pollen loads as well as direct observations of bee foraging behavior indicate that a large number of bees visit C. solstitialis, primarily in search of nectar while carrying a large percentage of pollen grains of this plant species on their bodies. These results are similar to previous observations on a non-weedy population of C. solstitialis from the island of Lesvos.

Keywords

Body size Nectar standing crop Noxious weed Yellow star-thistle 

Introduction

Yellow star-thistle (Centaurea solstitialis L., Asteraceae) is a common annual to biennial weed of the Mediterranean basin that has received the status of a noxious weed in southern Canada and most of the US (Maddox et al. 1985; Uygur 2004; Uygur et al. 2004; USDA, NRCS 2016). Part of the success of yellow star-thistle as an invasive plant has been attributed to its rapid germination and seedling growth and the overproduction of small, easily dispersed achenes that compensate for the high mortality sustained by the achenes and seedlings (Roché and Thill 2001). The versatile breeding system, plastic phenology, and generalist pollination strategy also confer additional invasive advantages to this plant. Yellow star-thistle exhibits a prolonged flowering period in its invasive range; in its native range it is a late-flowering species, producing flowers in the mid- or late summer when the flowering period of most plant species has ceased; it is facultatively xenogamous with some individuals or populations being obligatory or facultatively autogamous; and attracts a wide array of insect visitors including many bee species (Harrod and Taylor 1995; Sun and Ritland 1998; Roché and Thill 2001; Gerlach and Rice 2003; McIver et al. 2009; Petanidou et al. 2012).

In its invasive range, some populations of C. solstitialis (e.g., Santa Cruz Island) produce relatively high volumes of nectar per floret, on average usually exceeding 0.050 μL (Barthell et al. 2009, 2012) and, although it might be visited by more than 80 species of native bees at a given location, the exotic honey bee (Apis mellifera L.) and introduced leafcutting bee Megachile apicalis Spinola are major pollinators (Thorp et al. 1994; McIver et al. 2009). This relationship between C. solstitialis and both exotic bees, but particularly with honey bees, has been described as “an invasive mutualism” (Barthell et al. 2001). Greater seed production occurs whenever honey bees are present and, because of the high volumes of nectar, managed honey bee colonies produce yellow star-thistle honey, which is commercially available in the northwestern USA (Dalby 2004).

The opposite case regarding nectar volume and visitation by honey bees appears to occur in some populations of C. solstitialis in its native range. On the island of Lesvos (Greece), for example, a small population of C. solstitialis occurring in a semi-natural phrygana scrub (non-weedy population sensu Petanidou et al. 2012), produces low volumes of nectar (never exceeding 0.050 μL). This population is rarely visited by honey bees, even though floral visitors include more than 60 bee species (Barthell et al. 2009, 2012; Petanidou et al. 2012). Contrary to the case in North America, honey designated as coming from yellow star-thistle is virtually unknown in its native range (personal observation). Pollinator interactions also appear to vary across landscapes in its invasive range. For example, in urban areas of California (USA), yellow star-thistle receives a significantly higher number of visits by native bees (non-Apis) than those in natural and agricultural environments; however, pollination efficiency, as indicated by seed production, is lower in urban areas than in other environments, thus suggesting that only a small number of native bees are effective pollinators (Leong et al. 2014). These observations suggest that some environmental factors, including land use at local and continental scales might have an effect on the population’s mating system as well as on its pollinator interactions.

Herein, we document the visitation pattern of bees and explore the relationship of bee body size and nectar availability on a weedy population of C. solstitialis in an urban environment in northwestern Turkey. We sought to answer the following questions. What are the daily changes in nectar standing crop levels? How does bee visitation and body size of visitors change throughout the day? Does body size of bee visitors and nectar standing crop volume vary between patches at different locations within an urban university campus area? Do bees visit C. solstitialis for nectar, pollen, or both? How do these interactions compare with other populations of C. solstitialis?

Materials and methods

Observations were conducted from July 15 to July 17, 2015, at the Görükle Campus of Uludağ University in Bursa, Turkey (40º13′35″N, 28º52′13″E, 56 m). Although plants of C. solstitialis occur throughout the campus, we were only able to find two patches of similar size consisting of more than 20 plants each, nearly all of them in bloom. One patch was located in an unmanaged lot at the periphery of the campus (“Hilltop” patch); the other patch (“Hillside” patch) was located in a rarely managed lot near the center of campus, about 360 meters from the former patch. We measured bee visitation rates, average bee size, and nectar standing crop volume per floret starting at 07:00 on July 15 when we collected bees at the Hilltop patch every 2 h, for 20 min per sampling period, until 19:00. Two collectors captured bees ad libitum using aerial nets for a total of 280 min of collecting effort. We estimated bee size by measuring head width with an ocular micrometer to the nearest 0.1 mm. After each collection event, we measured the nectar standing crop volume per floret on at least ten florets from different plants using 0.25 μL capillary tubes (Kearns and Inouye 1993). We did not bag any of the capitula prior to our observations because we wanted to estimate the available nectar volume to visitors during the sampling period. After removing the nectar, we measured the length of the capillary tube filled with nectar using a digital, hand-held caliper, and converted into μL. We used a new capillary tube each time. Bee specimens are in the Beekeeping Development and Research Center, Uludağ University, Bursa, Turkey.

To determine if bee body size and nectar standing crop volume vary between patches at different locations within the campus, on July 16, we collected bees during 30-min periods at both patches. We collected bees during the peak visitation period, between 12:00 and 14:00, and measured body size as described above. Surveys at each patch were designed to avoid collector bias and conducted simultaneously at 12:00 by two collectors and then exchanged between the two collectors so that each patch was surveyed by each collector once; nectar volumes were taken by each collector prior to each collection event to avoid sampling bias.

To assess whether bees primarily visit C. solstitialis to collect pollen or nectar, on July 17, we observed their behavior at inflorescences and then collected them to analyze their pollen loads. A single collector conducted observations and surveys at Hilltop patch only between 12:00 and 14:00. If a bee approached a floret with its proboscis extended or inserted it into a floret, we recorded the observation as a nectar visit and collected the bee immediately. A pollen visit was recorded when the bee was seen removing the pollen and transferring it onto its body. We collected bees with an aerial net, placed them individually in Eppendorf tubes, and euthanized them on ice. In the laboratory, we kept samples in the freezer at −20 °C until analysis. Then, we added 1 ml of 70% ethyl alcohol to each tube and mixed it with a Vortex. We filtered the mixture through a 250 µ filter, and after the alcohol evaporated, we added glycerin-jelly stained with basic fuchsine (Wodehouse 1965). Finally, we homogenized the sample and prepared three slides for each sample.

We identified and counted pollen grains at ×40 and ×100 magnifications. For each sample, we counted grains at a minimum of five locations randomly on the slide to ensure that at least 500 pollen grains could be identified. We confirmed identifications using a palynological reference collection developed by the Uludağ University Palynology Laboratory, where the samples were later deposited. We calculated percentage of pollen by taxon as the number of pollen grains counted by taxon divided by the sum of all pollen grains counted and multiplied by 100.

Nectar standing crop volumes were not normally distributed (Goodness of Fit test, P < 0.05) and were transformed using Box-Cox transformation (Box and Cox 1964). Then, we used a one-way ANOVA to detect differences in the average nectar standing crop volume among sampling periods and a two-sample t-test to differences between patches. Bee head widths throughout the day were not normally distributed (Goodness of Fit test, P < 0.05); thus, we used a Kruskal–Wallis test. However, bee head widths from specimens collected from both patches were normally distributed (Goodness of Fit test, P = 0.299), and a two-sample t-test was used to test for differences. We used a Pearson correlation analysis to test for any association between the average standing crop nectar volume and average head width. Averages are provided with standard deviations.

Results

Throughout the day, the average nectar standing crop volume per floret ranged from 0.003 to 0.117 μL (\(\bar{x}\) = 0.023 ± 0.019, n = 71) and there were no differences among sampling periods [one-way ANOVA (F, 6, 64) = 0.84, P = 0.541; Fig. 1]. Bee visitation started as early as 07:00, and peaked between 11:00 and 13:00, with 18 and 14 specimens collected, respectively. Bee head width ranged from 1.471 to 5.150 mm (\(\bar{x}\) = 3.267 ± 1.078, n = 71; Fig. 1), and there was no difference among head widths of bees collected at different sampling periods [Kruskal–Wallis test, H(5) = 8.29, P = 0.141]. However, average bee head width was correlated (r = 0.77; P = 0.043) with average standing crop nectar volume per floret. On a single day, a total of 20 bee species visited a single patch of C. solstitialis; Lasioglossum (str) sp., Lasioglossum (Dialictus) sp., and Lithurgus chrysurus Fonscolombe were the most commonly collected species during that time.
Fig. 1

Daily changes in nectar standing crop volume per floret (n = 71) of Centaurea solstitialis, number of bees recorded (dashed line), and head width of bee visitors (n = 72) at five sampling periods. Boxplots display median, quartiles, and extreme values

No significant difference in the average nectar standing crop volume per floret was found between patches (Hilltop patch: \(\bar{x}\) = 0.012 μl ± 0.011, 0.003–0.033, n = 10; Hillside: \(\bar{x}\) = 0.014 μl ± 0.011, 0.004–0.037, n = 10; two-sample t-test, t = −0.50, df: 17, P = 0.627). Likewise, similar numbers of individuals and species were captured on both patches and Simpson’s indices were the same (Hillside: Richness = 16 spp.; Abundance = 39 specimens; Simpson’s Index of Diversity = 0.92. Hilltop: Richness = 14 spp.; Abundance = 41 specimens; Simpson’s Index of Diversity = 0.92). Nonetheless, average bee head width was greater at the Hilltop patch (\(\bar{x}\) = 3.328 mm ± 0.935, 1.500–5.450, n = 31) than in the Hillside patch (\(\bar{x}\) = 2.654 mm ± 0.933, 1.063–4.450, n = 30, two-sample t test, t = 2.82, df: 58, P = 0.007).

Nectar visits were recorded for 18 of 42 of the total number of bee visits observed during the 2-h survey period at the Hilltop patch. Because visits were very brief or the bees very small, we were not able to determine whether they were searching for nectar or pollen in the remaining visits. As described by Müller and Bansac (2004), we observed two distinct types of pollen-collecting behaviors while megachilid females rapidly inserted their proboscises into the florets in search for nectar: (1) the rapid movement of their abdomen up and down so that pollen grains from anthers were collected on the sternal scopa (e.g., Pseudoanthidium lituratum, Trachusa dumerlei); and (2) the use of their hind legs to comb the pollen grains from the anthers while keeping the abdomen upright (e.g., Megachile apicalis). Other bees, such as andrenids and halictids, appeared to passively collect pollen while also searching for nectar.

In total, we captured and analyzed pollen from 42 bee specimens belonging to 16 species (11 genera of four families). In addition to C. solstitialis, palynological analyses revealed pollen grains from the following nine plant species: Daucus carota L. (Apiaceae), Artemisia sp., Cichorium intybus L., Helianthus annuus L., Sonchus asper (L.) Hill (Asteraceae), Knautia sp., Scabiosa sp. (Caprifoliaceae), Brassica nigra L. (Brassicaceae), and Trifolium sp. (Fabaceae). Except for one sample of a Ceratina sp., which did not have any pollen, all samples contained pollen grains of C. solstitialis and ranged from 28.1 to 100% in abundance. Elven specimens (26.2%) carried pollen grains from other plant species (Table 1).
Table 1

Percentage of pollen types recorded in pollen samples taken from bee specimens collected at capitula of Centaurea solstitialis on the campus of Uludağ University in Bursa, Turkey

Bee species

Visit

n

Plant species

Centaurea solstitialis

Daucus carota

Sonchus asper

Cichorium intybus

Scabiosa sp.

Trifolium sp.

Artemisia sp.

Brassica nigra

Helianthus annuus

Knautia sp.

Andrena limata Smith

N

 

79.1

    

20.9

    

Andrena sp. 1

?

 

89.2

10.8

        

Andrena sp. 1

?

 

28.1

7.02

 

34.8

   

30.1

  

Ceratina sp. 1

N

 

100.0

         

Ceratina sp. 1

N

 

         

Ceratina sp. 2

?

 

100.0

         

Eucera sp. 7

?

2

100.0

         

Halictus sp. 7

?

 

100.0

         

Halictus sp. 7

?

 

88.5

  

7.6

3.9

     

Halictus sp. 7

?

 

94.1

  

0.8

5.1

     

Halictus sp. 7

N

 

36.9

  

51.0

    

8.9

3.1

Halictus sp. 7

N

 

86.4

  

13.6

      

Halictus sp. 4

?

 

100.0

         

Lasioglossum (Dialictus) sp.

?

4

100.0

         

Lasioglossum (Evylaeus) sp.

?

 

100.0

         

Lasioglossum (str) sp. 1*

?

 

100.0

         

Lasioglossum (str) sp. 1

N

 

100.0

         

Lasioglossum (str) sp. 1

?

 

71.1

4.4

    

24.6

   

Lasioglossum (str) sp. 1

?

3

100.0

         

Lasioglossum (str) sp. 1

?

 

86.8

 

11.1

 

2.1

     

Heriades crenulatus Nylander

?

 

100.0

         

Lithurgus chrysurus Fonscolombe*

N

6

100.0

         

Megachile apicalis Spinola*

?

 

91.9

    

8.1

    

Megachile apicalis

N

 

96.5

   

3.5

     

Osmia bidentata Morawitz

N

2

100.0

         

Pseudoanthidium lituratum (Panzer)

?

2

100.0

         

Trachusa dumerlei (Warncke)*

N

3

100.0

         

Visit: N = nectar; ? = undetermined; * = male; n = number of specimens of the same species with same information

A total of 41 species belonging to five families and 20 genera (n = 197 specimens) were recorded as flower visitors of C. solstitialis on the Uludağ University campus (Table 2). Most species belonged to the families Halictidae and Megachilidae.
Table 2

Bee genera and number of species recorded visiting capitula of Centaurea solstitialis on the campus of Uludağ University in Bursa, Turkey, during July of 2015

Taxa

# Species

Family Andrenidae

 

 Genus Andrena

4

Family Apidae

 Genus Apis

1

 Genus Bombus

1

 Genus Ceratina

3

 Genus Eucera

1

 Genus Xylocopa

1

Family Colletidae

 Genus Hylaeus

1

Family Halictidae

 Genus Halictus

6

 Genus Lasioglossum

6

Family Megachilidae

 Genus Anthidium

1

 Genus Anthidiellum

1

 Genus Heriades

2

 Genus Hoplosmia

2

 Genus Lithurgus

1

 Genus Megachile

4

 Genus Osmia

2

 Genus Pseudoanthidium

1

 Genus Rhodanthidium

1

 Genus Stelis

1

 Genus Trachusa

1

Total: 20 genera

41 species

Discussion

The short-term duration of the experiment and small sample sizes make inferences on the bee visitors preliminary in nature. However, our brief observations are still valuable because they represent the only information available on the floral visitors of C. solstitialis in its native range outside the island of Lesvos, Greece. Our observations on the nectar availability, composition, and visitation pattern of bees on the weedy population of C. solstitialis at the Uludağ University largely agree with those of Barthell et al. (2009) on a non-weedy population of this plant from Lesvos. At both sites standing crop nectar volume, on average, is relatively low, inflorescences are visited by a large number of bee species, and honey bees are uncommon visitors relative to the western USA (Barthell et al. 2001). At our study sites, honey bees were always present in great numbers at flowers of other plants because at least a dozen hives were located within a 5 km radius, yet they did not frequently visit our observational patches. We do not know if honey bees were simply drawn away from C. solstitialis by higher flower rewards from some plants purposely kept on campus either as bee food (Lamiaceae) or as ornamentals, nor whether this is a common local pattern. In addition, we do not know the phenologies of the plants in the study area, including that of C. solstitialis. Some bee species that visited our patches were also commonly collected on Lesvos, namely Lithurgus chrysurus, Megachile albisecta (Klug), M. lefebvrei (Lepeletier), Osmia bidentata (Morawitz), Rhodanthidium septemdentatum (Latreille), Trachusa dumerlei (Warncke), and Xylocopa iris (Christ). Halictidae and Megachilidae were also the most species-rich families and average bee head width was comparable between both sites, not exceeding 4.0 mm (Barthell et al. 2012). The total number of bee species (41 spp.) collected at inflorescences of C. solstitialis on the Uludağ campus is high considering the short period of the study and that it represents about 40% of the total number of bees known from the area during mid-summer (Gonzalez et al. unpublished manuscript). In addition, even though most bees appear to be searching for nectar at the florets, the palynological analyses indicate that they are also carrying pollen of C. solstitialis with some of them exhibiting specialized pollen-collecting behaviors (Müller and Bansac 2004).

Daily fluctuations in the available nectar volume were also similar to those reported from Lesvos and, on average, did not exceed 0.05 μL (Barthell et al. 2009). Although average bee head width was similar throughout the day, it was correlated with average nectar standing crop volume, which might be related to differences in foraging energetics among bees (reviewed in McCallum et al. 2013). Patch location and surrounding vegetation appear to be important factors in determining the composition of the bee visitors. Larger scale comparisons of C. solstitialis visitation on Lesvos and Santa Cruz Island (USA) show a different pattern that may relate to the flight ranges of foraging bees and their fidelity to nest sites. The patches on the Uludağ University campus have similar standing crop nectar volumes and the composition of the bee visitors was also similar in terms of their richness, abundance, and diversity. However, large-bodied bees such as Bombus spp. and X. iris were only collected at the Hilltop patch, which is located farther away, at the periphery of the campus. This area is characterized by the presence of dense patches of oak forests and cultivated pine trees that might provide suitable nesting places for these bees in comparison to other areas on campus. Likewise, patch size and capitula density might affect the composition of visitors as well as visitation rates in C. solstitialis as observed in other plants (e.g., Dauber et al. 2010).

The significant relationship between the volume of nectar produced by florets and the average size of bees visiting those florets is consistent with other studies. Schaeffer et al. (1979) described a tendency for larger bodied and social bees (including honey bees) to exploit higher nectar standing crops. A related study also demonstrated that when competitors are removed from such systems, nectar levels increase and honey bees may return to exploit it (Schaffer et al. 1983). Similarly, Roubik (1980) reported the abandonment of feeders during relatively low periods of nectar flow. Such interrelationships of nectar usage by bee species may explain distinctions made in the literature between “small” and “large” bee pollinated plant communities (Frankie et al. 1983), and may be the result of exploitative forms of competition that occurs among other species (e.g., bumble bees and hummingbirds) as well (Laverty and Plowright 1985). We hope these observations draw more attention to and encourage future studies on the foraging dynamics of pollinators at this and other invasive plant species.

Notes

Acknowledgements

We dedicate this paper to the memory of Charles D. Michener (1918–2015), friend and mentor who always encouraged and inspired us throughout his teachings and papers to learn something more about bees and their behavior on plants. We are indebted to two anonymous reviewers for comments and suggestions that improved this manuscript. This work was supported by the National Science Foundation’s REU program (DBI 1263327).

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Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Victor H. Gonzalez
    • 1
    Email author
  • Alena Olsen
    • 2
  • Maija Mallula
    • 1
  • Aycan Tosunoglu
    • 3
  • Ibrahim Çakmak
    • 3
  • John Hranitz
    • 4
  • John Barthell
    • 5
  1. 1.Undergraduate Biology Program and Department of Ecology and Evolutionary BiologyUniversity of KansasLawrenceUSA
  2. 2.University of MichiganAnn ArborUSA
  3. 3.Beekeeping Development-Application and Research CenterUludağ UniversityBursaTurkey
  4. 4.Biological and Allied Health SciencesBloomsburg UniversityBloomsburgUSA
  5. 5.Department of Biology and Office of Provost & Vice President for Academic AffairsUniversity of Central OklahomaEdmondUSA

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