Integrating past and present studies on Ophrys pollination - a comment on Bradshaw et al.

Article (PDF Available)inBotanical Journal of the Linnean Society 165(4):329-335 · March 2011with287 Reads
DOI: 10.1111/j.1095-8339.2011.01112.x
Abstract
In a recent research article in the Botanical Journal of the Linnean Society Bradshaw et al. (2010) provided a detailed and richly illustrated comparative analysis of labellum micromorphology in Ophrys L. They described the variety of epidermal cell types and the different patterns of structural complexity observed in representative species in Ophrys. We agree with Bradshaw et al. that the study of the labellum micromorphology, besides its general significance for plant morphology, is also of interest in the framework of pollinator attraction, as it might influence the optical properties of the labellum and play an important role in directing male insects to the right position for collection or delivery of pollen masses during pseudocopulation. The latter aspect was discovered some 50 years ago by Kullenberg (1956a, b, 1961) and investigated further by Ågren, Kullenberg & Sensenbaugh (1984) (a key reference overlooked by Bradshaw et al.), and the detailed descriptions by the authors shed light on possible directions of phenotypic evolution in Ophrys. However, we think that Bradshaw et al. drew largely unsupported conclusions and overlooked a considerable body of literature when they discussed the role and evolution of other floral traits, including pollinator-attracting signals, patterns of reproductive isolation and speciation in this genus of sexually deceptive orchids. Their view is notably summarized in the abstract of their article, in which they argued that ‘The relative contributions of olfactory, visual and tactile cues to the sophisticated pseudocopulatory pollination mechanism that characterizes Ophrys remain unclear, but the degree of reproductive isolation achieved, and thus the speciation rate, have certainly been greatly exaggerated by most observers’. This statement echoes similar conclusions in other papers (see, for example, Bateman et al., 2003; Pedersen & Faurholdt, 2007; Devey et al., 2008, 2009). Based on a long series of independent past and present studies, we advocate that the view expressed in the last section of their article and in the other works cited below is too simplistic and speculative and misrepresents the current state of understanding of Ophrys ecology and evolution.
    • However, the number of orchid species remains difficult to assess, especially in some groups such as the Mediterranean genus Ophrys, which comprises 19 species according to Blumpers^ (Faurholdt and Perdersen 2007) but more than 250 species according to Bsplitters^ (Delforge 2005). The taxonomy of this genus is indeed extremely controversial, as evidenced by the debate between supporters of Bmorpho-genetically^ versus Beco-ethologically^ based species delimitations (Bateman et al. 2011; Vereecken et al. 2011). This is an important issue since doubts regarding species delimitations often have major implications for conservation (Pillon and Chase 2007).
    [Show abstract] [Hide abstract] ABSTRACT: Several authors have recently stressed the need to develop an integrative approach in taxonomy, but studies applying such an approach to Mediterranean orchids are scarce. In sexually deceptive orchids from the taxonomically difficult genus Ophrys, pollination is specific and performed by male insects attracted to the flowers by sex pheromone-mimicking floral scents. Floral compounds are therefore of primary importance for reproductive isolation and species delimitations in this genus. In the fly orchid group, molecular, morphological, and ecological characters have been extensively studied, but a comprehensive survey of floral scents is still lacking. In the present study, the blends of floral compounds of its three members, Ophrys insectifera, Ophrys aymoninii, and Ophrys subinsectifera, were extracted and analyzed by gas chromatography-mass spectrometry. A total of 107 compounds were found, with a majority of saturated and unsaturated hydrocarbons. Significant differentiation, both qualitative and quantitative, was found among the three taxa. This result, pooled with those from the literature, forms a comprehensive and congruent dataset that allows us to elucidate the taxonomic rank of the three members of the fly orchid group.
    Full-text · Article · Oct 2016
    • This liberal, pollinator-centred and ethological taxonomy, however, was recently criticised and still remains controversial (cf. Bateman et al. 2011; Vereecken et al. 2011). The point of view presented here is clearly intermediate between those of the most extreme splitters and lumpers, respectively Delforge (2005) and Devey et al. (2008) .
    [Show abstract] [Hide abstract] ABSTRACT: Recently published botanical floras provided an opportunity to develop operational systems for identifying in the field in France of species of the difficult genus Ophrys. Its specific and infra-specific taxonomy is extremely complex because of conflicting points of view and/or insufficient knowledge about specific biological features. In order to produce an identification key based on observable morphological criteria we developed a pragmatic taxonomy suitable for non-expert botanists, which includes “morphospecies” that are unambiguously identifiable based on a number of unique or a combination of diagnostic criteria and “subspecies” that are sets of populations sharing the same geographical and ecological adaptations but not distinctly differing morphologically. The taxonomic scheme reviewed here for the section Pseudophrys is well correlated with the floral chemical signatures of all the French taxa. This intermediate position, between splitters (mainly orchidologists) and lumpers (mainly geneticists), will hopefully enable us to revise the taxonomy of this genus at the Euro- Mediterranean level.
    Full-text · Article · Dec 2015
    • Rather, it is clear that the optical, tactile and even olfactory stimuli to potential pollinating insects are, at best, only moderately effective (cf. Paulus & gack 1983; BateMan et al. 2011; Vereecken et al. 2011).
    Full-text · Article · Aug 2015 · New Phytologist
    • Although authors as early as Linnaeus noted the visual similarity to insects, it was not suggested to be a form of pseudocopulation until the early 20th century (Pouyanne, 1917).[. The role of pheromones in the process was only identified somewhat later (e.g.Kullenberg, 1950;, and details of the compounds involved and the responses of the insects have been revealed through the elegant studies of Schiestl and colleagues (seeVereecken & Schiestl, 2009;Vereecken et al., 2011, and references therein.) and others. In the case of Ophrys insectifera, the pollinators are, at least predominantly, male digger wasps (Argogorytes species, primarily A.mystaceus in Britain).
    [Show abstract] [Hide abstract] ABSTRACT: Ophrys insectifera L., fly orchid is described and illustrated. Details of its relationships, pollination biology, distribution and conservation status are presented. Possible reasons for its ongoing decline in the UK are suggested. Cultivation and propagation are discussed.
    Article · Feb 2015
    • Das zeigt, dass die bisher angewendeten molekular-genetischen Methoden in falschen Ebenen gesucht haben und daher bislang keine nennenswerten Trennungen gefunden werden konnten (devey et al. 2008; BateMan et al. 2003). Auf alle diese Dinge haben wir schon früher ausführlich hingewiesen (vereecken et al. 2011).
    [Show abstract] [Hide abstract] ABSTRACT: It is demonstrated, that the biological species concept of the genus Ophrys is identical with the general concepts of Ernst Mayr. By the example of two near related forms of the fusca group in Andalucia it is shown how to understand the different criteria of the biospecies concept. One of these criteria is the high specifity of attraction fol lowed by a complex pseudocopulation behaviour which enable the correct pollen transfer only within the species. The high specifity is caused by a perfect imitation of the sexual pheromones of the mimicked female of the pollinator. Sexual pheromones of animals act as high intraspecific signals which result in attractions of only males of the same species. Exactly this specific behaviour is released by the Ophrys species, too. This high specifity is selected by the pollinator males by pollinating only those plant individuals which have the correct mixture of the pheromone molecules. To be successfully the, pollinating males also select other characters of the Ophrys flower as labellum size, colour, labellum hair characters, phenology and possibly habitat selections etc. As in the sexual reproduction behaviour of the male insects these pollinator males act as pregamic isolation mechanisms for the given Ophrys like for their own female. In observations at the growing sides of the Ophrys species and numerous field experiments, mainly choice experiments, we could confirm the high specifity, this in contrary to the assertions of Hennecke & Munzinger. Their arguments are that there are many different pollinator species listed in literature for a given Ophrys species. But they took it upon from literature without any critical improvements of the reliability of these citations. For this they have had to read the primary literature and not only the secondary ones like Delforge or others. Therefore they rehash many of the old mistakes in wrong identifications of the bees or even the Ophrys taxon which are long corrected. Especially a mixture of old and actual names of the same species in different combinations is especially annoying and seems to demonstrate that the authors are not really fit in the nomenclature of Ophrys. Their pollinator lists are completely worthless without a critical sifting of the actual literature. This is demonstrated on some examples which are very confusing without knowledge of the bees. That these authors do not know any of these bee is seen in such cases where a 3-4 mm bee (Andrena hesperia) should be an alleged pollinator of a 20 mm labellum of a large Ophrys omegaifera species. But there are some cases with more than one pollinator. Besides the main pollinator the others I call them “secondary pollinators” who in those cases we could check their pollination contribution in the population is very weak. In many cases these secondary visitors are mainly pollinaria thieves because they will be attracted, they try to copulate. But they seem to learn very quickly that this Ophrys is not a true female and will never visit another flower. In some quantitative field experiments (with Eucera nigrescens/longicornis on Ophrys holosericea) we could confirm it. The conclusion of the two authors Ophrys species are not species-specific attractively does not agree with the field finding,, not agree to the olfactory compound investigations with its biotests, does not agree with the molecular data of population biology and does not agree with the genetic analyses. To confirm or not the authors should make experiments with the pollinator bees. The other proof the authors used in their argumentations are the supposed frequency of hybrids. But this is also a spurious argument. Hybrids are only frequent in literature and not in nature. The main aim of the two authors is to reduce the many species within Ophrys because they are unable to distinguish them. But this is a worthless argument because there are many groups of insects where specialists only are able to distinguish them. Nobody would conclude that these species do not exist. The next step in their argumentation is to make a new systematic without any biological background. But they are not alone in the field of botanists. Botanical systematic use very often a complete anthropomorphic typological systematic like the “Index of accepted plant names” of the Kew Gardens. But this is in the 21. Century, 150 years after Darwin, a kind of middle age taxonomy. They use a quite typological morphospecies concept like in the book of Pederson & Faurhold (2007). But it does not fit with nature. If you pay attention to the different criteria of the biospecies concept within the genus Ophrys then you will recognise all the many species which the genus makes so interestingly.
    Full-text · Article · Jan 2015 · New Phytologist
    • This isolation mechanism has been shown to provide a nearly perfect barrier (floral isolation) to gene flow between closely related sympatric sexually deceptive orchids (Xu et al., 2011b; Whitehead & Peakall, 2014). Species numbers in Ophrys have been the subject of extensive debate, focusing on the different species concepts adopted and the weight given to the diagnosability of characters (see Bateman et al., 2011; Vereecken et al., 2011). Accordingly, estimates range from 10 macrospecies recognized on the basis of internal transcribed spacer (ITS) DNA sequencing (Devey et al., 2008), to 19 subspecies with 75 subspecies based on a herbarium morphological approach (Pedersen & Faurholdt, 2007), up to > 250 species when a more ethological/geographical approach is adopted (Delforge, 2006).
    [Show abstract] [Hide abstract] ABSTRACT: Episodes of rapid speciation provide unique insights into evolutionary processes underlying species radiations and patterns of biodiversity. Here we investigated the radiation of sexually deceptive bee orchids (Ophrys). Based on a time-calibrated phylogeny and by means of ancestral character reconstruction and divergence time estimation, we estimated the tempo and mode of this radiation within a state-dependent evolutionary framework. It appears that, in the Pleistocene, the evolution of Ophrys was marked by episodes of rapid diversification coinciding with shifts to different pollinator types: from wasps to Eucera bees to Andrena and other bees. An abrupt increase in net diversification rate was detected in three clades. Among these, two phylogenetically distant lineages switched from Eucera to Andrena and other bees in a parallel fashion and at about the same time in their evolutionary history. Lack of early radiation associated with the evolution of the key innovation of sexual deception suggests that Ophrys diversification was mainly driven by subsequent ecological opportunities provided by the exploitation of novel pollinator groups, encompassing many bee species slightly differing in their sex pheromone communication systems, and by spatiotemporal fluctuations in the pollinator mosaic.
    Full-text · Article · Dec 2014
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