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Unravelling the mystery of red flowers in the Mediterranean Basin: How to be conspicuous in a place dominated by hymenopteran pollinators
Functional Ecology ( IF 5.2 ) Pub Date : 2022-08-19 , DOI: 10.1111/1365-2435.14166
Melissa León‐Osper 1 , Eduardo Narbona 1
Affiliation  

1 INTRODUCTION

Plants produce a variety of flower traits such as colour, scent, shape and size to attract pollinators (Fenster et al., 2004). Among these traits, the colour of the flower acts as a lure for pollinators influencing the detectability of flowers and the fitness of the plant (Kantsa et al., 2017). Therefore, flower colour was thought to evolve in response to pollinator selection (Fenster et al., 2004; Trunschke et al., 2021), but other selection agents must also be considered (Dalrymple et al., 2020; Strauss & Whitall, 2006).

Red flower colour has generated a great deal of interest among naturalists and evolutionary biologists due to its striking association with the bird pollination system (Grant, 1966; Raven, 1972; Rodríguez-Gironés & Santamaría, 2004). Among other distinctive floral traits, ornithophilous species tend to show red or red-orange flowers (e.g. Burd et al., 2014), and several hypotheses have been proposed to explain why red flowers are preferentially visited by birds and not by insects (reviewed in Chen et al., 2020; Grant, 1966; Rodríguez-Gironés & Santamaría, 2004). The currently accepted theory applies the niche partition model developed by Possingham (1992) to postulate that red flowers are preferentially visited by birds due to niche differentiation caused by the longer foraging time that bees, the most abundant insect pollinator, would need to exploit red flowers (Rodríguez-Gironés & Santamaría, 2004). This hypothesis stems from the ‘bee avoidance’ hypothesis (Coimbra et al., 2020; Raven, 1972), which predicts that red flowers are less detectable by bees, taking longer time for detection (Chittka & Waser, 1997; Dyer et al., 2011); thus, red bird flowers can avoid bee visitation and originate a private communication channel with birds (Camargo et al., 2019; Lunau et al., 2011). Therefore, this theory is based on the fact that birds and bees have substantially different visual perception of colour. Birds possess a tetrachromatic vision system and perceive light with wavelengths extending from ultraviolet (UV) to red regions (Ödeen & Håstad, 2010). In contrast, those of hymenopterans are commonly trichromatic with a perception from UV to orange-red regions having photoreceptors sensitive to UV, blue and green light (short- medium- and long-wavelength photoreceptor, respectively; Kelber et al., 2003). Honeybees show sensitivity peaks at 344, 436 and 556 nm and most hymenopterans have similar sensitivity maxima, but a few species shown an additional long-wavelength photoreceptor near to 600 nm (Menzel & Backhaus, 1991; Peitsch et al., 1992). Thus, bees are not totally blind for red flowers, especially when using differential conditioning (Reisenman & Giurfa, 2008), but this colour is less discriminable performing more landing mistakes than for other colours such as pink, orange and yellow (Bergamo et al., 2016; Chittka & Waser, 1997; Lunau & Maier, 1995). In this way, Shrestha et al. (2013) proposed that the red colours of Australian flowers show reflectance spectra that would be adapted to the bird visual systems, whereas bee flowers presented colour cues adapted to their visual system. However, not all red flowers are inconspicuous for bees. What humans perceive as red flowers can show three different types of reflectance spectra (Chittka & Waser, 1997; Martínez-Harms et al., 2010): ‘pure red’ flowers reflect light exclusively in the red band of the spectrum, while ‘UV-red’ flowers and ‘blue-red’ flowers show secondary reflectance peaks in the UV and blue bands, respectively. It is demonstrated that in the honeybee colour space using green leaves as background and the half maximal sensitivity of the photoreceptors adapted to the background, only pure red flowers are inconspicuous because secondary reflectance peaks of UV-red and blue-red flowers activate the short-wavelength photoreceptor and increase visibility for bees (Kevan et al., 2001; Lunau et al., 2011). Consequently, most ornithophilous species with red flowers show pure red colours (Camargo et al., 2019; Chen et al., 2020; Coimbra et al., 2020; Lunau et al., 2011; Shrestha et al., 2013).

Ornithophily can be relatively important in regions of the world where pollinating bird species are present, such as in America (Trochilidae), Australia (Meliphagidae, Nectariniidae), and South Africa and Indonesia (Nectariniidae) encompassing more than a thousand species of birds and several thousand plant species (Cronk & Ojeda, 2008; Pauw, 2019). This fact may help explain the considerable number of plant species with red flowers, particularly pure red flowers, in these areas (Chen et al., 2020; Coimbra et al., 2020). However, this fact does not apply to the old world, where there is an absence of bird pollinator species (Cronk & Ojeda, 2008). In this area, ornithophilous species are rare, except for some islands in which ornithophily has secondarily evolved (Ollerton, Cranmer, et al., 2009; Valido et al., 2004) or a few species with a mixed insect-bird pollination system (Ortega-Olivencia et al., 2012).

The relative frequency of red-flowered species in the old world seems to be very low (Chittka et al., 1994), reaching values of about 2% in the flora of Great Britain and Israel (Dafni et al., 1990; Warren & Mackenzie, 2001). In the Mediterranean vegetation of the Iberian Peninsula, red-flowered species are also scarce (1.4%; File S1), but some genus such as Lathyrus (Fabaceae), Serapias (Orchidaceae), Orobanche (Orobanchaceae), Papaver (Papaveraceae) or Adonis (Ranunculaceae) show a considerable number of red-flowered species (File S1). In this region, the most common pollinators are hymenopterans, but other insect groups such as dipterans, coleopterans, and lepidopterans may also play an important role (Kantsa et al., 2017; Reverté et al., 2016). Thus, red-flowered species of Mediterranean flora have evolved in a different pollination scenario than those of other areas with pollinating birds, which could have affected their floral traits (Chittka & Waser, 1997; Cronk & Ojeda, 2008). Here, we propose three nonmutually exclusive hypotheses to explain the presence of red-flowered species in some lineages of the Mediterranean Basin flora. First, if Mediterranean red-flowered species are adapted to the principal pollinator in the area, the hymenopterans, we predict that these species might show UV-red or blue-red flower types, which would allow them to be quite conspicuous for this insect group (Chen et al., 2020; Coimbra et al., 2020). In this way, populations of red-flowered Papaver rhoeas from central Europe have recently been found to show reflectance in the UV region, making these flowers more conspicuous for bees than populations from the eastern Mediterranean lacking UV reflectance (Martínez-Harms et al., 2020). Second, we can also expect that Mediterranean red-flowered species may be mainly pollinated by hymenopterans, but they can show inconspicuous pure red flowers. In this scenario, we predict that these species would show flowers with a colour pattern (i.e. flowers with more than one colour, including UV patterns or floral guides) that help bees to detect flowers against the green background (de Ibarra et al., 2015; Ma et al., 2016; Wester & Lunau, 2017). Lastly, a generalization of the ‘bee avoidance’ hypothesis could be applied to Mediterranean species with red flowers (Coimbra et al., 2020). Based on the spectral sensibility of the Mediterranean Basin pollinators, certain insect groups of coleopterans and lepidopterans can be considered as ‘red sensitive’, while hymenopterans and dipterans have a low sensibility in the red region and can be considered as ‘red insensitive’ pollinators (Martínez-Harms et al., 2012; van der Kooi et al., 2021; Wang et al., 2022). Thus, we predict that species pollinated by red-sensitive insects would show red flowers poorly perceived by red-insensitive pollinators (Camargo et al., 2019; Lunau et al., 2011). This is documented in the East Mediterranean Basin, in which several species of Papaveraceae and Ranunculaceae with red bowl-shaped flowers are pollinated by glaphyrid beetles (Glaphyridae, Coleoptera) (Dafni et al., 1990; Martínez-Harms et al., 2012; Streinzer et al., 2019). In this regard, the diurnal butterfly Aeropetes tulbaghia is the main pollinator of an important number of red-flowered species in South Africa (Johnson, 2010). On the other hand, red flower colour of species of the Mediterranean Basin might not be directly related to pollinator attraction, on the contrary, it could just be the consequence of a specialized pollination system in which colour would not play an important role. For instance, some orchids (Serapias spp.) and irises (Iris section Oncocyclus) with dark red flowers provide protective shelters as a reward to solitary bees that pollinate the flowers (Bellusci et al., 2009; Vereecken et al., 2013). Likewise, some Scrophularia species with red flowers attract wasp pollinators mainly by odour cues (Brodmann et al., 2012), and sapromyiophilous flowers of Amorphophallus konjac may mimic the scent and purple-red colours of animal carcasses (Chen et al., 2015).

In this study, we analysed flower reflectance spectra of red-flowered species from the Mediterranean Basin region distinguishing between areas with different colours. We also analysed flower colour and conspicuousness to pollinators by modelling flower colour in the visual systems of each pollinator functional group, namely hymenopterans, dipterans, coleopterans and lepidopterans. In addition, we examined the match between flower reflectance marker points and colour discrimination ability of red-insensitive hymenopterans and red-sensitive lepidopterans. Finally, we performed a literature review of the potential pollinators of red-flowered species of the Mediterranean Basin.



中文翻译:

揭开地中海盆地红色花朵的神秘面纱:如何在膜翅目传粉者占主导地位的地方显眼

1 简介

植物产生多种花性状,例如颜色、气味、形状和大小以吸引传粉者(Fenster 等人,  2004 年)。在这些性状中,花的颜色作为传粉媒介的诱饵,影响花的可检测性和植物的适应性(Kantsa 等人,  2017 年)。因此,人们认为花色会随着传粉媒介的选择而演变(Fenster 等人,  2004 年;Trunschke 等人,  2021 年),但也必须考虑其他选择剂(Dalrymple 等人,  2020 年;Strauss & Whitall,  2006 年) )。

由于与鸟类授粉系统的显着关联,红色花朵引起了博物学家和进化生物学家的极大兴趣(Grant,  1966 年;Raven,  1972 年;Rodríguez-Gironés & Santamaría,  2004 年)。在其他独特的花卉特征中,鸟类物种往往会开出红色或橙红色的花(例如 Burd 等人,  2014 年),并且已经提出了几个假设来解释为什么鸟类优先访问红色花朵而不是昆虫(综述于Chen 等人,  2020 年;Grant,  1966 年;Rodríguez-Gironés 和 Santamaría,  2004 年)。目前公认的理论应用了 Possingham 开发的生态位划分模型(1992 年)假设由于蜜蜂(最丰富的昆虫传粉者)需要利用红色花朵的较长觅食时间引起的生态位分化,鸟类优先访问红色花朵(Rodriguez-Gironés & Santamaría,  2004 年)。这一假设源于“蜜蜂回避”假设(Coimbra 等人,  2020 年;Raven,  1972 年),该假设预测红色花朵不易被蜜蜂检测到,需要更长的时间才能检测到(Chittka 和 Waser,  1997 年;Dyer 等人。 ,  2011 ); 因此,红色的鸟花可以避免蜜蜂的来访,并与鸟类建立私人交流渠道(Camargo et al.,  2019 ; Lunau et al.,  2011)。因此,这一理论是基于鸟类和蜜蜂对颜色的视觉感知存在显着差异这一事实。鸟类拥有四色视觉系统,可以感知波长从紫外线 (UV) 延伸到红色区域的光 (Ödeen & Håstad,  2010 )。相比之下,膜翅目昆虫通常是三色的,感知从紫外线到橙红色区域,具有对紫外线、蓝光和绿光敏感的光感受器(分别为短中波和长波光感受器;Kelber 等人,  2003 年)。蜜蜂在 344、436 和 556 nm 处显示出灵敏度峰值,大多数膜翅目昆虫具有相似的灵敏度最大值,但少数物种在 600 nm 附近显示出额外的长波长感光器 (Menzel & Backhaus,  1991; Peitsch 等人,  1992 年)。因此,蜜蜂对红色花朵并非完全失明,尤其是在使用差异调节时(Reisenman & Giurfa,  2008 年),但与粉色、橙色和黄色等其他颜色相比,这种颜色在着陆错误方面更难辨别(Bergamo 等人,2008 年)。 ,  2016 年;Chittka 和 Waser,  1997 年;Lunau 和 Maier,  1995 年)。这样,Shrestha 等人。( 2013) 提出澳大利亚花朵的红色显示出适合鸟类视觉系统的反射光谱,而蜜蜂花则呈现出适合其视觉系统的颜色线索。然而,并不是所有的红色花朵对蜜蜂来说都不显眼。人类感知为红色花朵的东西可以显示三种不同类型的反射光谱(Chittka & Waser,  1997 ; Martínez-Harms et al.,  2010):“纯红色”花朵仅在光谱的红色波段反射光,而“UV-红色”花朵和“蓝红色”花朵分别在 UV 和蓝色波段显示二次反射峰。结果表明,在以绿叶为背景的蜜蜂色彩空间中,光感受器适应背景的最大灵敏度的一半,只有纯红色的花朵不显眼,因为紫外红色和蓝红色花朵的二次反射峰激活了短-波长感光器并增加蜜蜂的能见度(Kevan 等人,  2001 年;Lunau 等人,  2011 年)。因此,大多数有红色花朵的鸟类物种呈现纯红色(Camargo 等人,  2019 年;Chen 等人,  2020 年;Coimbra 等人, 2020 年;Lunau 等人,  2011 年;Shrestha 等人,  2013 年)。

鸟类在世界上存在授粉鸟类的地区可能相对重要,例如美洲(Trochilidae),澳大利亚(Meliphagidae,Nectariniidae)以及南非和印度尼西亚(Nectariniidae),包括一千多种鸟类和几种千种植物(Cronk 和 Ojeda,  2008 年;Pauw,  2019 年)。这一事实可能有助于解释在这些地区有相当数量的红色花朵,特别是纯红色花朵的植物物种(Chen 等人,  2020 年;科英布拉等人,  2020 年)。然而,这一事实不适用于没有鸟类传粉者物种的旧世界(Cronk & Ojeda,  2008)。在该地区,鸟类很少见,除了一些岛屿发生了二次进化(Ollerton, Cranmer, et al.,  2009 ; Valido et al.,  2004)或少数具有混合昆虫-鸟类授粉系统的物种( Ortega-Olivencia 等人,  2012 年)。

旧世界红花物种的相对频率似乎非常低(Chittka 等,  1994),在英国和以色列的植物群中达到约 2% 的值(Dafni 等,  1990;Warren &麦肯齐,  2001 年)。在伊比利亚半岛的地中海植被中,红花物种也很稀少(1.4%;文件 S1),但一些属如Lathyrus(豆科)、Serapias(兰科)、Orobanche(Orobanchaceae)、罂粟(Papaveraceae)或Adonis(毛茛科)有相当数量的红花品种(文件S1)。在该地区,最常见的传粉媒介是膜翅目昆虫,但其他昆虫群,如双翅目、鞘翅目和鳞翅目也可能发挥重要作用(Kantsa 等人,  2017 年;Reverté 等人,  2016 年)。因此,地中海植物群的红花物种在授粉场景中的进化与其他有授粉鸟类的地区不同,这可能影响了它们的花卉特征(Chittka & Waser,  1997 ; Cronk & Ojeda,  2008)。在这里,我们提出了三个非互斥的假设来解释地中海盆地植物群的某些谱系中红花物种的存在。首先,如果地中海红花物种适应了该地区的主要传粉媒介膜翅目昆虫,我们预测这些物种可能会表现出紫外红色或蓝红色的花型,这将使​​它们在这个昆虫群中非常显眼(Chen 等人,  2020 年;科英布拉等人,  2020 年)。通过这种方式,最近发现来自中欧 的红花罂粟种群在紫外线区域具有反射率,这使得这些花对蜜蜂来说比缺乏紫外线反射率的地中海东部种群更显眼(Martínez-Harms 等人, 2020)。其次,我们也可以期待地中海红花物种可能主要由膜翅目昆虫授粉,但它们可以开出不起眼的纯红色花朵。在这种情况下,我们预测这些物种会展示具有颜色图案的花朵(即具有多种颜色的花朵,包括紫外线图案或花卉指南),这有助于蜜蜂在绿色背景下检测花朵(de Ibarra et al.,  2015;Ma 等人,  2016 年;Wester 和 Lunau,  2017 年)。最后,“蜜蜂回避”假设的推广可以应用于开着红色花朵的地中海物种(Coimbra et al.,  2020)。根据地中海盆地传粉媒介的光谱敏感性,某些昆虫群的鞘翅目和鳞翅目可以被认为是“红色敏感的”,而膜翅目和双翅目在红色区域的敏感性较低,可以被认为是“红色不敏感”的传粉媒介。 Martínez-Harms 等人,  2012 年;van der Kooi 等人,  2021 年;Wang 等人,  2022 年)。因此,我们预测由对红色敏感的昆虫授粉的物种会表现出红色不敏感的传粉者难以感知的红色花朵(Camargo et al.,  2019 ; Lunau et al.,  2011)。这在东地中海盆地有记载,其中几种罂粟科和毛茛科的红色碗状花由鳞甲虫(Glaphyridae,鞘翅目)授粉(Dafni 等人,  1990 年;Martínez-Harms 等人,  2012 年; Streinzer 等人,  2019 年)。在这方面,昼夜蝴蝶Aeropetes tulbaghia是南非许多重要红花物种的主要传粉者(Johnson,  2010)。另一方面,地中海盆地物种的红色花朵颜色可能与传粉者的吸引力没有直接关系,相反,它可能只是特殊的授粉系统的结果,颜色不会发挥重要作用。例如,一些带有深红色花朵的 兰花( Serapias spp.)和鸢尾花(Iris section Oncocyclus )提供保护性庇护所,作为对给花朵授粉的孤独蜜蜂的奖励(Bellusci 等人, 2009 年;Vereecken 等人,  2013 年)。同样,一些开有红色花朵的玄参物种主要通过气味线索吸引黄蜂传粉者(Brodmann 等人,  2012 年),而魔芋可能会模仿动物尸体的气味和紫红色(Chen et al., 2015)。

在这项研究中,我们分析了地中海盆地地区红花物种的花卉反射光谱,以区分不同颜色的区域。我们还通过对每个传粉媒介功能组(即膜翅目、双翅目、鞘翅目和鳞翅目)的视觉系统中的花色进行建模,分析了花色和对传粉者的显着性。此外,我们检查了红色不敏感膜翅目昆虫和红色敏感鳞翅目昆虫的花反射标记点与颜色辨别能力之间的匹配。最后,我们对地中海盆地红花物种的潜在传粉媒介进行了文献综述。

更新日期:2022-08-19
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