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No Evidence of Flowering Synchronization Upon Floral Volatiles

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No Evidence of Flowering Synchronization Upon Floral Volatiles Fricke et al. BMC Ecol (2019) 19:29 https://doi.org/10.1186/s12898-019-0245-9 BMC Ecology RESEARCH ARTICLE Open Access No evidence of fowering synchronization upon foral volatiles for a short lived annual plant species: revisiting an appealing hypothesis Ute Fricke1,2,3, Dani Lucas‑Barbosa2,4 and Jacob C. Douma1,2* Abstract Background: Self‑incompatible plants require simultaneous fowering mates for crosspollination and reproduc‑ tion. Though the presence of fowering conspecifcs and pollination agents are important for reproductive success, so far no cues that signal the fowering state of potential mates have been identifed. Here, we empirically tested the hypothesis that plant foral volatiles induce fowering synchrony among self‑incompatible conspecifcs by accelera‑ tion of fowering and fower opening rate of non‑fowering conspecifcs. We exposed Brassica rapa Maarssen, a self‑ incompatible, in rather dense patches growing annual, to (1) fowering or non‑fowering conspecifcs or to (2) foral volatiles of conspecifcs by isolating plants in separate containers with a directional airfow. In the latter, odors emitted by non‑fowering conspecifcs were used as control. Results: Date of frst bud, duration of frst fower bud, date of frst fower, maximum number of open fowers and fower opening rate were not afected by the presence of conspecifc fowering neighbors nor by foral volatiles directly. Conclusions: This study presents a compelling approach to empirically test the role of fower synchronization by fo‑ ral volatiles and challenges the premises that are underlying this hypothesis. We argue that the life history of the plant as well as its interaction with pollinators and insect herbivores, as well as the distance over which volatiles may serve as synchronization cue, set constraints on the ftness benefts of synchronized fowering which needs to be taken into account when testing the role of foral volatiles in synchronized fowering. Keywords: Flowering synchronization, Flowering onset, Phenology, Plant–plant communication Background [3]. Te most important exogenous signals are tempera- Te transition from the vegetative to fowering stage is ture, light conditions (such as photoperiod) and water irreversible and its timing is crucial [1, 2]: environmental availability [4]. For example, prolonged drought can be conditions should be favorable, and for obligate outcross- associated with accelerated fowering [5]. Shade and light ing species, fowering conspecifcs and pollinating agents quality can both play a role in fowering onset accelerat- to transfer pollen need to be present in the environment. ing and delaying fowering, depending on the plant spe- Tus, fowering synchronization is critical for outcross- cies [3]. Furthermore, fungal, viral and bacterial pathogen ing species. infection as well as herbivore attack can alter fowering Te fowering phenology of a plant depends on the phenology [6]. Endogenous factors that play a role in interplay of endogenous signals and exogenous signals fowering phenology are plant hormones, sugar levels and the genetic makeup of the plant [3]. Diferences in the genetic makeup may lead to variation in the indi- *Correspondence: [email protected] vidual timing of fowering within a population [7], while 1 Centre for Crop Systems Analysis, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands exogenous biotic and abiotic signals and their interac- Full list of author information is available at the end of the article tions may constrain fowering time of populations [6]. © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Fricke et al. BMC Ecol (2019) 19:29 Page 2 of 9 Te intraspecifc variation in fowering onset can be P = 0.210]. Te frst fower opened at about large [8] and constrains pollen transfer between individu- 47.4 ± 4.7 days from sowing [ANOVA, F(1,38) = 1.385, als. Given the need of pollen from conspecifcs, cues that P = 0.247]. As in the neighboring experiment, the traits signal the presence of fowering mates might have estab- related to fowering phenology measured in the two- lished to tune fowering among mates [9, 10]. cylinder experiment were similar irrespectively of the Floral volatiles are outstanding candidate cues to signal foral volatiles exposure [ANOVA, E: F(1,25) = 0.008, the presence of fowering mates, for a number of reasons. P = 0.931; FB: F(1,24) = 1.704, P = 0.204; duration of First, foral volatiles are known to afect the physiology of frst fower bud (FD): F(1,24) = 2.544, P = 0.124; FF: neighboring plants, e.g. by inhibiting root growth [11]. F(1,24) = 0.415, P = 0.526]. Importantly, no interactions Second, plant volatiles can promote defenses and growth were found between the trial number and the tested in neighboring plants [12–15]. Tird, foral volatiles are traits, but the traits related to fowering phenology dif- often produced in higher quantity than leaf volatiles fered between trials in the neighboring experiment on which makes them likely detectable by nearby conspecif- average up to 8.5 days. In the two-cylinder experiment ics [16]. Finally, foral volatiles are a reliable cue exploited only FD and FF difered between trials by an average of by pollinators to locate fowers [17–19]. Floral volatile up to 2.5 days. Most of the traits related to fowering emission is often highest when a fower is ready for pol- phenology had slightly lower values in the two-cylin- lination, which makes unfertilized fowers particularly der experiment when compared with the neighboring attractive to pollinators [20, 21]. Unfertilized fowers are, experiment presented above. therefore, more attractive to pollinating agents than ferti- When modeling the number of open fowers over time, lized fowers and indeed foral scent changes or levels of the exposure to fowering or non-fowering (1) neighbor- after fertilization [22, 23]. ing plants or (2) their odors only did not add explanatory Whether cues of conspecifcs directly afect fower- value to the model [lr-test: (1) P = 0.627, (2) P = 0.818]. ing time has never been investigated, although there is Both groups of B. rapa plants, exposed to fowering some indirect evidence that supports this idea [10]. For and non-fowering neighboring conspecifcs, reached instance, butterfy egg deposition on Brassica nigra sped an equal maximum number of open fowers [Asym, (1) up fowering [24] and seed production of herbivore- P = 0.687, (2) P = 0.468], started fowering at a similar infested plants and its non-infested neighbors, whereas time [xmid, (1) P = 0.226, (2) P = 0.639] and opened their foral volatile composition was changed upon exposure fowers similarly quickly [scal, (1) P = 0.558, (2) P = 0.706] to butterfy eggs and caterpillars [16, 25]. Tus, additional (Fig. 1; Additional fle 1). However, the onset of fowering foral volatile-based mechanisms may underlie fowering difered between the two subsequent trials in both exper- phenology. iments [xmid, (1) P < 0.001, (2) P = 0.007]. A model on the In this study, we explored for the frst time whether fo- neighboring experiment data that included trial number ral volatiles can change fowering phenology of younger in scal and the other parameters led to ftting problems, conspecifcs, i.e. whether foral volatiles can afect the wherefore the covariate trial number was excluded from onset of fowering and the rate of fower opening. We the explanation of scal in the neighboring experiment revisited the hypothesis by [10] of fower synchronization model. In case of the (2) two-cylinder experiment, these and challenged its premise that it is benefcal for veg- observations were made under consideration of a fac- etative plants to advance the onset of fowering and the tor describing the number of plants elongated prior to fower opening rate in response to foral volatiles. exposure (preE). Tis factor was added as plants, which just had started to elongate, were used in the experiment Results due to a shortage of not yet elongated plants. A model Te traits related to fowering phenology days from with preE as explanatory factor was preferred (lr-test: sowing until stem elongation (E), days from sow- P < 0.001). Plants showing elongated stems at the initia- ing until the frst fower bud (FB) and days from sow- tion of the experiment tended to reach a higher NOF max ing until the frst fower opening (FF, fowering time) than plants initiating stem elongation later (P = 0.074). were not afected by the exposure to fowering or Maximum fower opening rate (MFR) was simi- non-fowering neighboring conspecifcs (neighbor- lar between plants exposed to (odors of) fowering or ing experiment). Stem elongation manifested on non-fowering emitters in both experiments (Fig. 2). In average 38.3 5.1 (mean SD) days from sowing the neighboring experiment MFR reached on average ± ± about 6.4 1.4 (mean SD) fowers per day [ANOVA, [ANOVA, F(1,41) = 0.214, P = 0.646]. Te frst fower ± ± bud appeared at about 42.1 5.3 days from sow- F(1,37) = 0.014, P = 0.905], while in the two-cylinder ± experiment a maximal rate of average about 11.5 5.7 ing [ANOVA, F(1,41) = 0.002, P = 0.967] and lasted ± for about 6.1 ± 1.1 days [ANOVA, F(1,38) = 1.629, Fricke et al.
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