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Mechanism of Spontaneous Autogamy in the Allogamous Lepidopteran Orchid Gymnadenia Conopsea (L.) R

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Mechanism of Spontaneous Autogamy in the Allogamous Lepidopteran Orchid Gymnadenia Conopsea (L.) R ACTA BIOLOGICA CRACOVIENSIA Series Botanica 57/1: 130–140, 2015 DOI: 10.1515/abcsb-2015-0010 MECHANISM OF SPONTANEOUS AUTOGAMY IN THE ALLOGAMOUS LEPIDOPTERAN ORCHID GYMNADENIA CONOPSEA (L.) R. BR. (ORCHIDACEAE) IZABELA TAŁAŁAJ1* AND MICHAŁ SKIERCZYŃSKI2 1University of Białystok, Institute of Biology, ul. Ciołkowskiego 1J, 15-245 Białystok, Poland 2Adam Mickiewicz University, Institute of Environmental Biology, Department of Behavioural Ecology, ul. Umultowska 89, 61-614 Poznań, Poland Received February 31, 2015; revision accepted March 9, 2015 Studies of plant breeding systems are particularly important when they involve facultative processes, which can be overlooked in natural conditions. This especially applies to species that are considered allogamous, due to their pollination syndrome and floral architecture. We examined the potential level and factors enabling or lim- iting spontaneous autogamy in three populations of the lepidopteran orchid Gymnadenia conopsea. Using a bag- ging experiment, we noted the stages of the anther thecae and the positions of the pollinaria at the five phenologi- cal stages of the flower, as well as the quantity of autogamously set fruits and the number of properly formed seeds. In the studied populations, autogamy represents an accidental character, with a maximum of 3.3% of fruits set spontaneously per analysed sample in a given population, and with seed numbers ranging from 29 to 354. This process is an environmentally dependent co-product of the mechanisms that enable a position appropriate for touching the stigma (bending of the caudicle) and increase male fitness (disintegration of the massulae), preceded by the gradual opening of the anther chambers. Autopollination of G. conopsea may occur in the flowers at various flowering stages (excluding the beginning of anthesis) at each position on the inflorescence. Key words: Anther thecae, bending movement, dehydration, disintegrated pollinium. INTRODUCTION important selective agent on floral traits, inducing the transition from allogamous to pronounced The breeding system is a crucial aspect of species autogamous flowers (Macnair et al., 1989; biology. It is one of the most important factors Squirrell et al., 2002). The low frequency of polli- shaping the demographic and genetic structure of nators (even periodically) may initiate facultative populations, as well as the evolution of genomes autogamy, usually in the final phase of anthesis (Hamrick and Godt, 1989; Charlesworth, 2006). (Kalisz et al., 1999; Suetsugu, 2013). According to The evolution of plant breeding systems is particu- Lloyd and Schoen (1992), autogamy at this period larly evident at the individual level as the adapta- has been commonly called delayed, although in tion to changes in environmental conditions, both reality, autogamous selfing does not fall into strict biotic and abiotic (Kalisz and Vogler, 2003; classes of floral lifespan and is instead continu- Charlesworth, 2006). In general, the reproductive ously distributed (Goodwillie et al., 2005). Because success of entomophilous plants is strongly polli- the possibility of late autogamy is a consequence of nator-limited. Thus, most plants are self-compati- the habitually or temporarily low frequency of pol- ble, which allows them to achieve mixed mating linators and because floral traits related to this (Goodwillie et al., 2005). Simultaneously, a perma- selfing type may change over floral life, the appear- nent or periodic lack of pollen-vectors can also ance and extent of facultative autogamy may vary stimulate a transition to autonomous selfing as between populations of a given species, and even reproductive assurance (Darwin, 1877; Holsinger, between years within the same population, and it 1996). The total lack of pollinators may become an may therefore be overlooked (Kalisz et al., 1999). *e-mail: [email protected] PL ISSN 0001-5296 © Polish Academy of Sciences and Jagiellonian University, Cracow 2015 Autogamy in Gymnadenia conopsea 131 The adaptation of flowers to limited pollinators both in well-lit open habitats and in significantly through autogamy is particularly noticeable in the shaded sites (Vakhrameeva et al., 2008; Sletvold et Orchidaceae. Delayed autogamy may occur in sever- al., 2012). The species is distributed over all of al orchid species (reviewed in Catling, 1990). Europe and a considerable part of Asia (Hultén and Although this process has not been proven empiri- Fries, 1986). Different cytotypes of G. conopsea cally, gynostemium structure and pollination syn- have been recognised, and they often form mixed- drome may indicate the possibility of its occurrence. ploidy populations (Marhold et al., 2005; Jersáková A very simple type of gynostemium may cause a et al., 2010; Stark et al., 2011). The generative shoot large number of its morphological variations to lead forms a fairly dense inflorescence, consisting of to facultative autogamy as a minor adaptation to 27–70 and as many as 87 flowers (Vakhrameeva et al., local pollinator availability, especially when derived 2008; personal observation). Flowers are small, pink- from a generalised pollination system resulting from ish or reddish lilac, with narrow spurs of 11–18 mm Hymenoptera and Diptera visits (Squirrell et al., long, containing a large amount of nectar 2002; Tałałaj and Brzosko, 2008). A more specialised (Stpiczyńska and Matusiewicz, 2001; Bell et al., architecture that is adapted to flower pollination by 2009, Jersáková et al., 2010). During both day and Lepidoptera significantly reduces the probability of night, flowers emit a weak vanilla-like but slightly autogamy (reviewed in Claessens and Kleynen, 2011). unpleasant scent (Marhold et al., 2005), which is Flower features and pollination syndrome are very produced in osmophores on the surface of the label- often the basis for speculation about the possibility of lum and lateral sepals (Stpiczyńska, 2001). Sletvold autogamy for the specified orchid, and such informa- et al. (2012) present this species as an orchid with a tion is used in many fields of plant science. Thus, semi-generalised pollination system because it there is a significant need for research on the breed- receives visits from a large number of species, ing system potential of orchids. though most of them are lepidopteran (listed in In the present study, we examine the potential Claessens and Kleynen, 2011). In other populations, for spontaneous autogamy in lepidopteran distinct differences in pollination efficiency between Gymnadenia conopsea (L.) R. Br., a species widely butterflies and moths have been observed (Vöth, regarded as allogamous and which is currently the 2000; Meyer et al., 2007; Sletvold et al., 2012), as subject of intensive research (Jersáková et al., 2010; this species may represent an intermediate stage in Stark et al. 2011; Trávnícek et al., 2012; Meekers the adaptation to diurnal versus nocturnal pollina- and Honnay, 2011; Sletvold and Ågren, 2011; tors (Claessens and Kleynen, 2011). The fruiting Sletvold et al., 2012). The common view is that this level varies significantly between different sites and plant is self-compatible but depends on pollinators ranges from 23% to 95.5% (compiled in Claessens (Gustafsson, 2000; Huber et al., 2005; Jersáková et and Kleynen, 2011). al., 2010; Sletvold and Ågren, 2011; Sletvold et al., The gynostemium of G. conopsea is very short, 2012) and that under pollinator deficiency, selfing is massive and deflexed. The anther is joined to the conducted via geitonogamy (Meekers and Honnay, gynostemium above the rostellum, close to the stig- 2011). Meanwhile, during research on the breeding ma base. The anther contains two parallel chambers system of orchids in Poland, fruits of G. conopsea covered by thin-walled, attenuated and partially free were found after an experiment on spontaneous anther thecae at the base, which open by a slit autogamy (I. Tałałaj, unpubl. data). Thus, in the (Szlachetko and Rutkowski, 2000; Box et al., 2008). present work, we specifically (1) evaluate the poten- Each chamber contains one pollinarium with a tial level of spontaneous autogamy under pollinator clearly distinguishable sectile pollinium (formed by limitation, (2) investigate the mechanism of auto- the pollen tetrads, bound together by elastic gamy in this species, and (3) examine whether the threads in the massulae) and a long caudicle, autogamous fruits contain properly formed seeds. which is attached to a sticky viscidium (Darwin, Based on the allogamous architecture of the flowers 1877; Freudenstein and Rasmussen, 1997; and the pollination syndrome of G. conopsea, we Claessens and Kleynen, 2011). Caudiculae exhibit hypothesise that autogamy, if it occurs, is possible at the ability of a bending movement when the viscid- the end of flowering. ium adheres to a pollinator's proboscis which brings the pollinia into the appropriate position for touching the stigma (Darwin, 1877). The stigma in MATERIAL AND METHODS G. conopsea is located ventral to the anther thecae and consists of three lobes. The two lateral lobes STUDY SPECIES are confluent, each with a flat receptive surface. The basal part of the median lobe is also likely to Gymnadenia conopsea (L.) R. Br. is a perennial be fertile, but it is covered with an almost pendant, species occurring on calcareous soils in grazed remnant rostellum (Szlachetko and Rutkowski, meadows and in the margins of marshes and fens, 2000; Box et al., 2008). 132 Tałałaj and Skierczyński STUDY SITES At fruit maturation, we recorded the number
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