Pollination in a new climate:assessing the potential influence of flower temperature variation on insect pollinator behaviour

<div><p>Climate change has the potential to enhance or disrupt biological systems, but currently, little is known about how organism plasticity may facilitate adaptation to localised climate variation. The bee-flower relationship is an exemplar signal-receiver system that may provide important insights into the complexity of ecological interactions in situations like this. For example, several studies on bee temperature preferences show that bees prefer to collect warm nectar from flowers at low ambient temperatures, but switch their preferences to cooler flowers at ambient temperatures above about 30° C. We used temperature sensor thermal probes to measure the temperature of outdoor flowers of 30 plant species in the Southern regions of the Australian mainland, to understand how different species could modulate petal temperature in response to changes in ambient temperature and, potentially, influence the decision-making of bees in the flowering plant’s favour. We found that flower petal temperatures respond in different ways to changing ambient temperature: linearly increasing or decreasing relative to the ambient temperature, dynamically changing in a non-linear manner, or varying their temperature along with the ambient conditions. For example, our investigation of the difference between ambient temperature and petal temperature (<i>ΔT</i>), and ambient temperature, revealed a non-linear relationship for <i>Erysimum linifolium</i> and <i>Polygala grandiflora</i> that seems suited to bee temperature preferences. The temperature profiles of species like <i>Hibertia vestita</i> and <i>H</i>. <i>obtusifolia</i> appear to indicate that they do not have a cooling mechanism. These species may therefore be less attractive to bee pollinators in changing climatic conditions with ambient temperatures increasingly above 30° C. This may be to the species’ detriment when insect-pollinator mediated selection is considered. However, we found no evidence that flower visual characteristics used by bees to identify flowers at close range, such as colour or shape, were straightforward modulators of floral temperature. We could not identify any clear link to phylogenetic history and temperature modulation either. Mapping our test flower distribution on the Australian continent however, indicates a potential clustering that suggests different flower responses may constitute adaptations to local conditions. Our study proposes a framework for modelling the potential effects of climate change and floral temperature on flower pollination dynamics at local and global scales.</p></div

Pollination in a new climate: Assessing the potential influence of flower temperature variation on insect pollinator behaviour - Fig 10

<p><b>a</b>) A representative phylogenetic distribution of flowering plants in our sample following the method of [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.ref084" target="_blank">84</a>] and [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.ref085" target="_blank">85</a>]. A square (solid) represents the relationship between <i>ΔΤ</i> and ambient temperature i.e. NS (non-significant, green), NL (non-linear, magenta), LN (linear negative, blue), LP (linear positive, yellow), and a solid circle represents the hue of the flower colour distribution in bee hexagon colour space following [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.ref074" target="_blank">74</a>]. The colours of these symbols are meant only to be distinguishable and to indicate an approximate radial angle (inset hexagon) consistent with current knowledge of bee colour processing. The short abbreviations represent flower shape (see detail in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.t001" target="_blank">Table 1</a> <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#sec002" target="_blank">Material and Method</a> section). Frequency of ‘hue’ category uses definitions for bee pollinator perception as defined for the hexagon colour space [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.ref074" target="_blank">74</a>]. <b>b)</b> The histogram represents the hexagon sector of our sample data, whereas the red line represents the global pattern of flower colour distribution in each hexagon sector [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.ref032" target="_blank">32</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.ref033" target="_blank">33</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.ref086" target="_blank">86</a>]. Hue = Hue in hexagon sector, shape = flower shape.</p

Predicted effect of ambient temperature (<i>x-</i>axis) on ΔT (primary <i>y-</i>axis: left-hand side) and on bee preference for warmer nectar reward (secondary, <i>y</i>-axis: right-hand side).

<p>The model for ΔT is represented by the solid red line along with its 95% confidence region (shaded blue region). The solid green line represents the preference model along with its 95% confidence region (shaded orange region). Species numbers correspond to those in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.t001" target="_blank">Table 1</a>. Black, dotted lines indicate ΔT values of -1 and 1°C. Refer to Methods sections for details on the bee preference function.</p

Distribution of measured flower samples in Australia based on type of relationship (details on Table 1) between <i>ΔΤ</i> and ambient temperature.

<p>a) Non-Significant (NS) flowering plants species distribution, b) Non-Linear (NL) flowering plants species distribution, c) Linear-Positive (LP) flowering plants species distribution, or d) Linear-Negative (LN) flowering plants species distribution. <b>Data sources:</b> all the species data co-ordinates have been downloaded from the Global Biodiversity Information Facility (GBIF) (<a href="https://www.gbif.org/" target="_blank">https://www.gbif.org</a>) using the ‘dismo’ package and plotted using “maps” packages in R Version 1.1.423, 2017 [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.ref078" target="_blank">78</a>].</p

Predicted effect of ambient temperature (<i>x-</i>axis) on ΔT (primary <i>y-</i>axis: left-hand side) and on bee preference for warmer nectar reward (secondary, <i>y</i>-axis: right-hand side).

<p>The model for ΔT is represented by the solid red line along with its 95% confidence region (shaded blue region). Solid green line represents the preference model along with its 95% confidence region (shaded orange region). Species numbers correspond to those in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.t001" target="_blank">Table 1</a>. Black, dotted lines indicate ΔT values of -1 and 1°C. Refer to Methods sections for details on the bee preference function.</p

Non-linear, 3-parameter logistic model (solid black) describing the probability of bees choosing a warm nectar feeder rather than an ambient temperature feeder (<i>y</i>-axis) at different ambient temperatures (<i>x</i>-axis) and 95% confidence region (blue shaded area).

<p>Circles represent the data collected by [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.ref052" target="_blank">52</a>].</p

Effect of ambient temperature on <i>ΔT</i> for the 30 sampled flower petals.

<p>Fit type indicates the kind of model that best fitted the data: non-linear (GAM) or linear (GLS). Significance of all models was evaluated at α = 0.05. Details of each fit are available in Figs <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.g005" target="_blank">5</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.g010" target="_blank">10</a>. Flower shape is abbreviated as Boat shape (BS), Open (O), Open tubular (OT), tubular (T) and flower colours in the hexagon colour space are abbreviated as <i>BLUE</i> (G), <i>BLUE-GREEN</i> (BG), <i>GREEN</i> (G), <i>UV-GREEN</i> (UG), <i>ULTRAVIOLET</i> (UV) and <i>UV-BLUE</i> (UB), as defined by [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.ref074" target="_blank">74</a>]. Colour in the table represents non-significant (NS, green), significant non-linear relationship (magenta), significant linear positive (warm-yellow) and significant linear negative (cool-blue). * indicates a short flowering time (ca. 5–9 hours). Species 4 has two parts (4a and 4b) measured and analysed individually.</p

Predicted effect of ambient temperature (<i>x-</i>axis) on ΔT (primary <i>y-</i>axis: left-hand side) and on bee preference for warmer nectar reward (secondary, <i>y</i>-axis: right-hand side).

<p>The model for ΔT is represented by the solid red line along with its 95% confidence region (shaded blue region). Solid green line represents the preference model along with its 95% confidence region (shaded orange region). Species numbers correspond to those in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.t001" target="_blank">Table 1</a>. Black, dotted lines indicate ΔT values of -1 and 1°C. Refer to Methods sections for details on the bee preference function.</p

Predicted effect of ambient temperature (<i>x-</i>axis) on ΔT (primary <i>y-</i>axis: left-hand side) and on bee preference for warmer nectar reward (secondary, <i>y</i>-axis: right-hand side).

<p>The model for ΔT is represented by the solid red line along with its 95% confidence region (shaded blue region). Solid green line represents the preference model along with its 95% confidence region (shaded orange region). Species numbers correspond to those in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0200549#pone.0200549.t001" target="_blank">Table 1</a>. Black, dotted lines indicate ΔT values of -1 and 1°C. Refer to Methods sections for details of the bee preference function.</p

Equipment set up in the field to collect flower temperature readings.

<p>Inset shows the TSM sensor attached to a petal surface.</p