Pollinator Effectiveness of a Specialist Bee Exploiting a Generalist Plant
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Pollinator effectiveness of a specialist bee exploiting a generalist plant-tracking pollen transfer by Heriades truncorum with quantum dots Sabine Konzmann, Margareta Kluth, Deniz Karadana, Klaus Lunau To cite this version: Sabine Konzmann, Margareta Kluth, Deniz Karadana, Klaus Lunau. Pollinator effectiveness of a spe- cialist bee exploiting a generalist plant-tracking pollen transfer by Heriades truncorum with quantum dots. Apidologie, 2020, 51 (2), pp.201-211. 10.1007/s13592-019-00700-0. hal-03060427 HAL Id: hal-03060427 https://hal.archives-ouvertes.fr/hal-03060427 Submitted on 14 Dec 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2020) 51:201–211 Original article * The Author(s), 2019 DOI: 10.1007/s13592-019-00700-0 Pollinator effectiveness of a specialist bee exploiting a generalist plant—tracking pollen transfer by Heriades truncorum with quantum dots Sabine KONZMANN, Margareta KLUTH, Deniz KARADANA, Klaus LUNAU Institute of Sensory Ecology, Heinrich Heine University Düsseldorf, Universitätsstr. 1, 40225, Düsseldorf, Germany Received 8 May 2019 – Revised 4 September 2019 – Accepted 9 October 2019 Abstract – Heriades truncorum (Megachilidae) is a specialist bee that forages on Asteraceae and collects pollen by tapping its abdomen on pollen-presenting florets which places the grains directly in the ventral scopa. We tracked pollen transfer by female H . truncorum between conspecific inflorescences of Inula ensifolia and Pulicaria dysenterica by labelling pollen with quantum dots. On average, bees transferred 31.14 (I . ensifolia )and9.96(P. dysenterica ) pollen grains from the last visited inflorescence, 39% and 45% of which were placed on receptive styles. Pollen germination ratio is significantly lower for inflorescences of P. dysenterica visited by one H . truncorum (0.13%) compared with open control inflorescences (0.51%), which suggests that the bees mainly transfer self-pollen of these self-incompatible plants. Thus, a single visit by H . truncorum does not grant the plant high reproductive success, but the bees’ abundance and flower constancy might reduce this disadvantage. Asteraceae / oligolecty / plant–pollinator interaction / pollen germination rate / single-visit deposition 1. INTRODUCTION 1993). In the plant family Asteraceae, the unre- ceptive style brushes or pumps pollen out of the Many mechanisms have evolved in angio- florets through elongation (Erbar and Leins 1995, sperms to secure reproductive success (reviewed 2015). As the circularly arranged disc florets open in Pacini and Hesse 2004; Pacini and Dolferus successively, pollen is available continually and 2016). Entomophilous plants face the dilemma cannot be collected entirely in one flower visit. that bees and other flower-visiting insects not only This pollen portioning strategy leads to more act as pollinators but also as pollen thieves, eating flower visitors collecting and possibly transferring pollen or collecting it to feed their offspring pollen from one inflorescence. The adhesion of (Thorp 1979). One strategy to enhance the chance pollen grains to a flower visitor’sbodyismainly of pollination is secondary pollen presentation, attributable to pollenkitt—a lipid-based substance where pollen is placed on and presented by floral covering pollen of most angiosperms—which al- structures other than the anthers (Howell et al. so grants protection from adverse biotic and abi- otic influences (reviewed in Pacini and Hesse 2005; Hesse 2010). Besides pollenkitt volume, Electronic supplementary material The online version of this article (https://doi.org/10.1007/s13592-019-00700-0) pollen grain size and shape also affect the adhe- contains supplementary material, which is available to sion of entomophilous pollen grains (Lin et al. authorized users. 2013). Corresponding author: S. Konzmann, Oligolectic bees are morphologically and [email protected] behaviourally adapted to effectively collect pollen Manuscript editor: James Nieh on their host plants (reviewed in Thorp 2000). 202 S. Konzmann et al. Their foraging behaviour is fine-tuned to their Andrenidae) are thought to solely act as pollen host plants, e.g., adapted to continuous or syn- thieves on their only host plant, Passiflora lutea chronous pollen presentation (Schlindwein (Passifloraceae) (Neff and Rozen 1995). Visita- 2000), and the degree of specialisation can depend tion frequency alone is no measure for pollination on the composition of plant species at a given effectiveness of a flower visitor, but tracking the locality (Schlindwein et al. 2009). In contrast to single-visit deposition (SVD) of conspecific pol- corbiculate bees (honey bees, bumble bees, sting- len grains is a suitable means to provide informa- less bees, and orchid bees) which use regurgitated tion on pollinator effectiveness of any bee species nectar to form pollen pellets attached to their hind (King et al. 2013). legs, non-corbiculate bees transport pollen either As H . truncorum is morphologically and in their crop or in their scopa, a brush-like struc- behaviourally adapted to efficiently collect pollen ture on their abdominal venter or long hairs on from inflorescences of Asteraceae, we expected their hind legs (Michener 2007). Scopal pollen the bees to transfer scarcely any pollen to recep- can be moistened or glazed, but is most often tive styles. The objective of our study was to test dry (Portman and Tepedino 2017). Apart from pollinator effectiveness of female H . truncorum the fact that corbicular pollen is rather unlikely foraging on inflorescences of Inula ensifolia and to detach from the compressed pellet, these modes Pulicaria dysenterica (tribe Inuleae, Asteraceae) of pollen storage (wet and compacted vs. dry and by tracking pollen grains labelled with quantum loose) affect pollen functionality differently: man- dots (Minnaar and Anderson 2019). Detecting ual transfer of corbicular pollen of Apis and marked pollen grains on the bees allowed identi- Bombus results in significantly lower seed num- fication of body sites that are potentially suitable bers than scopal pollen of oligolectic bees, sug- for transferring pollen. Likewise, location of pol- gesting that enveloping the grains with moisture len placement on different floral structures could might also affect pollen viability (Parker et al. be specified after H . truncorum had visited an 2015). inflorescence with marked pollen grains. Viability Foraging on plants of the family Asteraceae, of transferred pollen grains was measured by pol- some oligolectic bees are known to collect pollen len tube germination. with an abdominal drumming, tapping, or wiping technique (Cane 2016). While contacting the 2. MATERIALS AND METHODS pollen-presenting styles with the abdomen, pollen grains are directly placed into the scopa All experiments were conducted in the (Figure 1). The large-headed resin bee, Heriades Botanical Garden of the Heinrich Heine Uni- truncorum (tribe Osmiini, Megachilidae), is a versity Düsseldorf from June to July 2018. In solitary bee which is endemic to central Europe the vicinity of a nesting aid for wild bees and active from summer until early autumn that several females of Heriades truncorum (Westrich 1989). It forages exclusively on were using, we placed ten abundantly Asteraceae (Praz et al. 2008a) and collects pollen flowering plants of each tested species, Inula via abdominal drumming, a rapid dorso-ventral ensifolia and Pulicaria dysenterica movement (Cane 2016; see supplementary (Asteraceae). The average disc diameter was material, Video S1, S2). Considering that this 9.95 mm (± 2.41 mm SD, n = 10) for I . specialised behaviour is an adaptation for effec- ensifolia and 9.69 mm (± 1.25 mm SD, n = tive pollen collection from disc florets of 10) for P. dysenterica . Prior to testing, some Asteraceae, the effectiveness of pollen transfer to inflorescences were covered with mesh fabric receptive stigmas is questionable. Although to prevent insect visits. Digital photographs oligolectic bees may be more efficient pollinators and videos in the field were taken using a than honey bees and bumble bees (e.g., Parker camera with a close-up lens (PEN E-PL7, 1981), the complete opposite can also be the case. M.Zuiko Digital ED 60 mm 1:2.8 Macro, For instance, pollen-foraging females of the pas- Olympus, Japan). Seventeen video recordings sion flower bee (Anthemurgus passiflorae , with a frame rate of 30 frames/second were Pollinator effectiveness of a specialist bee exploiting a generalist plant—tracking pollen transfer 203 Figure 1. Female Heriades truncorum simultaneously drinking nectar and collecting pollen on inflorescences of Asteraceae. Pollen of (A ) Pulicaria dysenterica and (B ) Inula ensifolia is actively accumulated in the ventral scopa, but also clumps on legs and mouthparts while scattered grains can be found all over the bee’sbody.(C ) Abdominal drumming of H . truncorum is specifically aimed at the circle of pollen-presenting florets in the male phase of anthesis (arrow 1), while receptive stigmas