Utah State University DigitalCommons@USU All PIRU Publications Pollinating Insects Research Unit 7-23-2018 Co-Dependency Between a Specialist Andrena Bee and Its Death Camas Host, Toxicoscordion paniculatum James H. Cane Utah State University Follow this and additional works at: https://digitalcommons.usu.edu/piru_pubs Part of the Entomology Commons Recommended Citation Cane, James H., "Co-Dependency Between a Specialist Andrena Bee and Its Death Camas Host, Toxicoscordion paniculatum" (2018). All PIRU Publications. Paper 798. https://digitalcommons.usu.edu/piru_pubs/798 This Article is brought to you for free and open access by the Pollinating Insects Research Unit at DigitalCommons@USU. It has been accepted for inclusion in All PIRU Publications by an authorized administrator of DigitalCommons@USU. For more information, please contact [email protected]. Arthropod-Plant Interactions https://doi.org/10.1007/s11829-018-9626-9 ORIGINAL PAPER Co-dependency between a specialist Andrena bee and its death camas host, Toxicoscordion paniculatum James H. Cane1 Received: 11 December 2017 / Accepted: 10 July 2018 © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2018 Abstract Among associations of plants and their pollinating bees, mutually specialized pairings are rare. Typically, either pollen specialist (oligolectic) bees are joined by polylectic bees in a flowering species’ pollinator guild, or specialized flowers are pollinated by one or more polylectic bees. The bee Andrena astragali is a narrow oligolege, collecting pollen solely from two nearly identical species of death camas (Toxicoscordion, formerly Zigadenus). Neurotoxic alkaloids of these plants are implicated in sheep and honey bee poisoning. In this study, T. paniculatum, T. venenosum and co-flowering forbs were sampled for bees at 15 sites along a 900-km-long east–west transect across the northern Great Basin plus an altitudinal gra- dient in northern Utah’s Bear River Range. Only A. astragali bees were regularly seen visiting flowering panicles of these Toxicoscordion. In turn, this bee was never among the 170 bee species caught at 17 species of other prevalent co-occurring wildflowers in the same five state region (38,000 plants surveyed). Our field pollination experiments show that T. panicula- tum is primarily an outcrosser dependent on pollinator visitation for most capsule and seed set. Thus, both A. astragali and two sister species of Toxicoscordion are narrowly specialized and co-dependent on each other for reproduction, illustrating a rare case of obligate mutual specialization in bee–plant interactions. Keywords Apiformes · Breeding biology · Monolecty · Pollination · Oligolecty · Melanthiaceae · Zigadenus Introduction only mustered later by Minckley and Roulston (2006). On the one hand, diverse flowers with complex morphologies Most plant–pollinator interactions include partners that are are typically pollinated by only a few generalist (polylectic) taxonomic generalists, although many also involve special- bees, such as the bumble bees (Bombus) that pollinate the ists. Rarely are both the floral host and its pollinators mutu- asymmetrical flowers of Pedicularis groenlandica (Macior ally specialized. Some brood-site mutualisms exemplify the 1968). Conversely, species of oligolectic bees typically join latter, such as Neotropical figs and their fig wasps, or yuccas generalists in more species-rich floral guilds (e.g. sunflow- and their yucca moths, but these insects actively pollinate ers, blueberries and willows) (reviewed in Wcislo and Cane their hosts (reviewed in Proctor et al. 1996). For bees and the 1996; Minckley and Roulston 2006), although the specialists plants that they passively pollinate while foraging, speciali- are sometimes the superior pollinators (e.g. Larsson 2005). zation seems generally asymmetrical (Vazquez and Aizen Only a few examples represent mutually specialized 2004), although evidence in support of this assertion was bee–flower interactions, wherein a few oligolectic species are the flower’s only visitors. These cases include Macropis bees foraging only at Lysimachia in the Holarctic (Vogel Handling Editor: Kristine Nemec. 1976); Brazilian Ancyloscelis gigas bees at Eichhornia Electronic supplementary material The online version of this azurea (Alves dos Santos and Wittmann 2000); Brazilian article (https ://doi.org/10.1007/s1182 9-018-9626-9) contains Ceblurgus longipalpis bees at Cordia (Milet-Pinheiro and supplementary material, which is available to authorized users. Schlindwein 2010); several Euryglossa (Euhesma) bee spe- Verticordia * James H. Cane cies at Australian (Houston et al. 1993), and in [email protected] South Africa; Rediviva bee species at Diascia (Vogel and Michener 1985) or certain orchids (Pauw 2006). Half of 1 USDA-ARS Pollinating Insect Research Unit (PIRU), Utah these examples involve bees specialized to collect (Neff State University, Logan, UT 84322-5310, USA Vol.:(0123456789)1 3 J. H. Cane and Simpson 1981) and metabolize floral oils, although are combined herein. Both species are herbaceous, bulb- some oil-collecting bees are more taxonomically versatile forming perennial geophytes. By May or June, depending (Schlindwein 1998). These narrow oligoleges are expected on elevation, both species send up a single columnar pani- to be effective pollinators of their singular hosts, but evi- cle crowded with tiny, white, mostly hermaphroditic flowers dence is sparse (Milet-Pinheiro and Schlindwein 2010). with conspicuous tepal glands (Emms 1993; McNeal and A tantalizing additional example involves two intergrad- Zomlefer 2012). ing species of death camas, Toxicoscordion paniculatum (Nuttall) Rydberg and T. venenosum (S. Watson) Rydberg Breeding biology (Zomlefer and Judd 2002). These are visited by a non-social bee species with the unfortunate epithet of Andrena (Euan- Wild populations of T. paniculatum growing up Logan drena) astragali Viereck and Cockerell (Tepedino 2003). Canyon (Cache Co, Utah, USA) were used for experimental Pollen loads taken from female A. astragali in the PIRU manual pollinations. During May and June, budded pani- museum collection invariably consisted of Toxicoscordion cles were enclosed in fine mesh bags and each assigned a pollen but never included Astragalus pollen; that host record pollination treatment. Two manual pollination treatments— is only known from Cockerell’s single holotype specimen geitonogamy (transfer of self pollen) and xenogamy (out- (Tepedino 2003). This bee’s apparent pollen specificity is crossing)—were applied thrice weekly to all open flowers consistent with it being an oligolege of Toxicoscordion, of tagged panicles. By repeatedly hand-pollinating flowers although it might instead merely reflect strong floral con- on the same panicles over multiple days, we should have stancy for Toxicoscordion, the plant at which all the females accommodated their protandrous tendencies (Emms 1993). had been collected. For the plant’s part, its dependence on Geitonogamous pollination involved manually rubbing pollinators cannot be concluded, as the breeding biology recipient virgin stigmas with anthers of a flower clipped low of T. paniculatum is poorly known. Its pollen–ovule ratios on the same panicle. Donor flowers for xenogamy were taken suggest substantial outcrossing (Tepedino 1981), but most from other plants in the local population. Optical visors were of the pollination trials in that study were lost to livestock necessary to magnify all manipulations. Control panicles trampling. Frost damaged Emms’ (1993) experimental pani- limited to autogamy remained bagged during bloom, while cles, leaving only 10–15 hand-pollinated flowers to evalu- openly pollinated panicles were tagged but not bagged. ate. Hence, the pollination needs of T. paniculatum remain Flowers were too small to emasculate in the field, so we unknown, and so its need for pollinators. cannot rule out the possibility of some geitonogamy result- The three objectives of this research were (1) to experi- ing from stigmas inadvertently contacting pollen rubbed on mentally characterize the breeding biology of T. panicula- the bagging fabric. Once seeds were nearing maturity, but tum (and so it’s need for pollinators); (2) to assess the strict before capsules had fully opened, each panicle’s capsules dependence of the bee A. astragali on T. paniculatum and T. were counted, harvested and returned to the laboratory to venenosum, to the exclusion of other abundant co-flowering count their complements of plump brown seeds. species used by other bee species in the same Intermountain Treatments were compared for proportions of panicles wildflower communities; and (3) to document the geographi- producing no capsules using logistic regression. This first cal extent of their specialized relationship in the U.S. Inter- analysis was necessary because some treatments, especially mountain Region using field surveys at bloom. autogamy, seldom yielded capsules. The excess of zero val- ues (no capsules) resulted in hopelessly non-normal data that precluded an ANOVA. Convergence criteria were met Materials and methods for the logistic regression, however, and the proportional odds assumption accepted. The Wald test was the appropri- Systematics and natural history ate overall statistical test in this logistic analyses, given the sample sizes. The taxonomic history of Toxicoscordion has been com- Reproductive responses of plants to the three manipu-