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Floral Visitors to Helianthus Verticillatus, a Rare Sunflower Species in the Southern United States

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Floral Visitors to Helianthus Verticillatus, a Rare Sunflower Species in the Southern United States HORTSCIENCE 55(12):1980–1986. 2020. https://doi.org/10.21273/HORTSCI15394-20 in Madison County; other populations were most likely extirpated due to habitat loss (Ellis et al., 2006; Matthews et al., 2002). Floral Visitors to Helianthus Helianthus verticillatus is a diploid (2n = 2x = 34) perennial species (Ellis et al., 2006). verticillatus, a Rare Sunflower Species Plants can be propagated clonally via rhi- zomes either in the field or in containers in the Southern United States (Edwards et al., 2017), or more efficiently by rooted cuttings until mid-to-late May or early Nicolas C. Strange, John K. Moulton, and Ernest C. Bernard June (Trigiano et al., 2018). Helianthus Department of Entomology and Plant Pathology, University of Tennessee, verticillatus are 2- to 4-m-tall plants that Knoxville, TN 37996-4560 produce flowers from late August or early September to mid-October (Matthews et al., William E. Klingeman, III 2002) or until a killing frost. This sunflower is Department of Plant Sciences, University of Tennessee, Knoxville, TN 37996- a self-incompatible and largely insect- pollinated species (R. Trigiano, unpublished 4561 data) that does not lend itself to wind polli- Blair J. Sampson nation (Mandel, 2010). Pollinators of H. verticillatus and other self-incompatible U.S. Department of Agriculture-Agricultural Research Service, Thad plants are likely restricted to the flight range Cochran Southern Horticultural Laboratory, 810 Highway 26 West, of locally available insect visitors (Ackerman, Poplarville, MS 39470 2000; Faegri and Leendert, 1966). Plants and insects have co-evolved with tightening asso- Robert N. Trigiano ciations between energy expenditures in plants Department of Entomology and Plant Pathology, University of Tennessee, to produce pollen and with the demands of Knoxville, TN 37996-4560 pollinators to obtain nectar and pollen for food (Kevan and Baker, 1983). Because in- Additional index words. Agapostemon species, Bombus species, endangered plant, Halictus sect pollination is of paramount importance species, Lasioglossum/Dialictus species, pollinators to H. verticillatus propagation and crucial to understanding the biology and conservation Abstract. Helianthus verticillatus Small (whorled sunflower) is a federally endangered of this rare plant, it is imperative to identify plant species found only in the southeastern United States that has potential horticultural potentially important pollinator species (Kevan value. Evidence suggests that H. verticillatus is self-incompatible and reliant on insect and Baker, 1983). pollination for seed production. However, the identity of probable pollinators is Flowers of species in the Asteraceae may unknown. Floral visitors were collected and identified during Sept. 2017 and Sept. be visited by only a single species or numer- 2018. Thirty-six species of visitors, including 25 hymenopterans, 7 dipterans, 2 lepidop- ous species of insects (DeGrandi-Hoffman terans, and 2 other insect species, were captured during 7 collection days at a site in and Watkins, 2000; Horsburgh et al., 2011; Georgia (1 day) and 2 locations in Tennessee (6 days). Within a collection day (0745–1815 Robertson, 1922). Species within the bee HR), there were either five or six discrete half-hour collection periods when insects were genera Apis, Bombus, Halictus, and Meliss- captured. Insect visitor activity peaked during the 1145–1215 and 1345–1415 HR periods, odes are among the common hymenopteran and activity was least during the 0745–0845 and 0945–1015 HR periods at all three visitors to sunflowers (DeGrandi-Hoffman locations. Visitors were identified by genus and/or species with morphological keys and and Watkins, 2000; Robertson, 1922). Some sequences of the cox-1 mitochondrial gene. The most frequent visitors at all sites were common families of pollinators in Diptera, Bombus spp. (bumblebees); Ceratina calcarata (a small carpenter bee species) and including Syrphidae and Bombyliidae, also members of the halictid bee tribe Augochlorini were the second and third most common have a significant role in the pollination of visitors at the two Tennessee locations. Helianthus pollen on visitors was identified by some Helianthus spp. (Robertson, 1922). microscopic observations and via direct polymerase chain reaction of DNA using Native bees are the most efficient pollina- Helianthus-specific microsatellites primers. Pollen grains were collected from the most tors of self-incompatible flowers (Free, 1970; frequent visitors and Apis mellifera (honeybee) and counted using a hemocytometer. Greenleaf and Kremen, 2006), and they have Based on the frequency of the insects collected across the three sites and on the mean co-evolved with sunflowers, which are native number of pollen grains carried on the body of the insects, Bombus spp., Halictus ligatus to North America (Hurd, 1980). Despite this (sweat bee), Agapostemon spp., and Lasioglossum/Dialictus spp., collectively, are the most co-evolution, honeybees, which are not na- probable primary pollinators of H. verticillatus. tive to North America, have been reported to be the most efficient pollinators of commer- The whorled sunflower, Helianthus verti- cial sunflowers (McGregor, 1976). In con- cillatus Small, is a rare and federally endan- trast, Parker (1981) claimed that two oligolectic native bees, Andrena helianthi Received for publication 26 Aug. 2020. Accepted gered plant (U.S. Fish and Wildlife Service, and Melissodes agilis, were much more effi- for publication 28 Sept. 2020. 2014) found in only a few locations in the cient pollinators. A combination of both na- Published online 2 November 2020. southern United States. This plant was de- tive and domesticated bees provided efficient We thank David Paulsen of University of Tennes- scribed in 1892 by Samuel Bain (Ellis et al., see for assistance identifying bee and fly speci- pollination of hybrid commercial sunflowers mens, Kevin Hoyt and his staff at Utah Arboretum 2006; Mandel, 2010; Matthews et al., 2002; (DeGrandi-Hoffman and Watkins, 2000; for plot development and maintenance, and Nature Small, 1898) from collections obtained in Greenleaf and Kremen, 2006). Conservancy for access/permission to work at the Chester County, TN. The species was not There has not been a study of floral Cave Spring, GA site. This research was supported collected again until 1993, when it was dis- visitors of H. verticillatus; therefore, an inte- by funding from USDA Agreement 58-6062-6 covered in Floyd County, GA (Matthews gral part of its reproductive biology is un- Grant and USDA NIFA, Hatch project TEN00494. et al., 2002). A regional census was conduct- known. The goals of this study were as R.N.T. is the corresponding author. E-mail: rtrigian@ ed several years later, and an additional utk.edu. follows: to identify and catalog the diversity This is an open access article distributed under the population was discovered in Cherokee of potential pollinators visiting whorled sun- CC BY-NC-ND license (https://creativecommons. County, AL (Matthews et al., 2002). In flower inflorescences at diverse locations org/licenses/by-nc-nd/4.0/). Tennessee, wild plants are now located only using morphological keys and sequences of 1980 HORTSCIENCE VOL. 55(12) DECEMBER 2020 the cox-1 mitochondrial gene; to verify the insects concurrently in sweep nets. When of Entomology and Plant Pathology Insect pollen composition carried by captured in- sweep netting, specimens could become Museum. sects via DNA amplification with H. annuus cross-contaminated with pollen from other Polymerase chain reactions (PCRs) for primers; and to determine loads of pollen plants, and pollen could potentially be col- the cox-1 mitochondrial gene contained 36 grains carried on captured insects. lected from disturbed flower heads. Second, mL of sterile distilled water, 5 mLof10· sweeping a net over the tops of the inflores- TaKaRa Taq buffer, 2.3 mL MgCl2 (50 mM), Materials and Methods cences would likely capture many flying 3.5 mL dNTPs (10 mM), 0.2 mL TaKaRa hot insects, some of which that may not have start Ex Taq, 3 mLof10mM aliquots of Study sites. Three locations with popula- visited flowers, thus possibly confusing them forward and reverse primers (Table 1), and 1 tions of H. verticillatus were used to assess with potential pollinators. Third, H. verticil- mL of DNA template (various concentra- potential insect pollinators: a rural location latus can grow to a height of 4 m, which is too tions). A touchdown amplification program where the sunflower naturally occurs (native) tall for the practical use of standard sweep (Senatore et al., 2014) was used with the in Cave Spring, GA; plantings at a suburban nets unless the operation is performed using a following modifications: 95 °C for 1 min, 10 garden site (suburban) in Maryville, TN; and ladder. Fourth, moving a net over and around cycles of 96 °C for 15 s, 58 °C for 20 s, 72 °C a controlled field trial location at the Univer- these plants could destroy flower heads and for 1 min; 10 cycles of 96 °C for 15 s, 50 °C sity of Tennessee Forest Resources Research degrade the plants at the location. Potential for 20 s, 72 °C for 1 min; and 40 cycles of and Education Center Arboretum (semirural) biases using vials for capture were also 96 °C for 15 s, 45 °C for 20 s, 72 °C for 1 min, in Oak Ridge, TN. introduced, including the following: capture and 72 °C for 5 min. PCR products were The rural location is a forested site on a skill among collectors could vary greatly; a separated on a 1% agarose gel (120 V/cm2 for prairie remnant near Cave
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