bs_bs_banner Botanical Journal of the Linnean Society, 2016, 180, 269–294. With figures Does Traunsteinera globosa (the globe orchid) dupe its pollinators through generalized food deception or mimicry? Downloaded from https://academic.oup.com/botlinnean/article-abstract/180/2/269/2416525 by guest on 26 February 2020 JANA JERSÁKOVÁ1*, JOHANNES SPAETHE2, MARTIN STREINZER2,3, JOHANN NEUMAYER4, HANNES PAULUS5, STEFAN DÖTTERL6 and STEVEN D. JOHNSON7 1Faculty of Science, University of South Bohemia, Branišovská 31, 37005, Cˇ eské Budeˇjovice, Czech Republic 2Department of Behavioral Physiology and Sociobiology, Biozentrum, University of Würzburg, 97074 Würzburg, Germany 3Department of Neurobiology, Faculty of Life Sciences, University of Vienna, 1090 Vienna, Austria 4Obergrubstrasse 18, 5161 Elixhausen, Austria 5Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, 1090 Vienna, Austria 6Department of Ecology & Evolution, University of Salzburg, 5020 Salzburg, Austria 7School of Life Sciences, University of KwaZulu-Natal, 3209 Pietermaritzburg, South Africa Received 13 May 2015; revised 13 October 2015; accepted for publication 6 November 2015 Non-rewarding orchids rely on various ruses to attract their pollinators. One of the most common is for them to resemble flowers sought by insects as food sources. This can range from generalized food deception to the mimicry of specific sympatric food plants. We investigated the basis of pollinator deception in the European food-deceptive orchid Traunsteinera globosa, which has unusually compact flowerheads resembling those of sympatric rewarding species of Knautia and Scabiosa (Dipsacaceae), and Valeriana (Caprifoliaceae). Visual signals of T. globosa are similar in both fly and bee vision models to those of the sympatric food plants used in the choice experiments, but scent signals are divergent. Field experiments conducted in Austria and the Czech Republic showed that both naive and experienced (with respect to visitation of T. globosa) insect species approached the orchids at the same rate as food plants, but direct contact with orchid flowers was taxon specific. Flies were most easily duped into probing the orchid, and, in doing so, frequently received and deposited pollinaria, whereas most bees and butterflies avoided landing on orchid flowers. We conclude that T. globosa is a mimic of a guild of fly-pollinated plants, but the ecological dependence of the orchid on its models remains to be fully tested. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180, 269–294. ADDITIONAL KEYWORDS: Batesian mimicry – floral signals – flower colour – fly pollination – nectar – Orchidaceae – pollination – pollinator efficiency – scent. INTRODUCTION exploit food-seeking behaviour of pollinators (Roy & Widmer, 1999; Schiestl, 2005; Jersáková et al., 2006). Orchids are well known for deploying various systems These systems range from generalized food deception of deception to attract pollinators (Jersáková, that exploits innate food-seeking behaviour of Johnson & Kindlmann, 2006). Most of the c. 8000 animals (Nilsson, 1992; Peter & Johnson, 2013) to orchid species that do not produce floral rewards Batesian food-source mimicry of the signals of par- ticular sympatric rewarding plants (Nilsson, 1983; *Corresponding author. E-mail: [email protected] Dafni, 1984; Johnson, 1994, 2000). Some recent © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180, 269–294 269 270 J. JERSÁKOVÁ ET AL. studies have shown that generalized food-deceptive regardless of whether or not these plant species species may benefit reproductively from the presence co-occur (Fenster et al., 2004). Coincidental similarity of rewarding species of a similar colour (Johnson is less likely an explanation when the traits that et al., 2003a; Pellegrino, Bellusci & Musacchio, 2008). confer resemblance are apomorphic in the lineage of This raises the possibility of a natural continuum interest, thus suggesting evolution for their current between generalized food deception and floral function (Johnson, Alexandersson & Linder, 2003b; mimicry (Jersáková, Johnson & Jürgens, 2009; Ma et al., 2015). As pollinator conditioning should Schiestl & Schlueter, 2009). underlie all cases of Batesian food-source mimicry, Studies of several orchid lineages have suggested choice experiments using the same animal species in Downloaded from https://academic.oup.com/botlinnean/article-abstract/180/2/269/2416525 by guest on 26 February 2020 that floral mimicry systems usually evolve from gen- different contexts can be conducted to infer the impor- eralized food deception (Cozzolino et al., 2001; Kores tance of learned preferences (Jersáková et al., 2012; et al., 2001; Johnson, Hobbhahn & Bytebier, 2013; Newman, Anderson & Johnson, 2012). Weston et al., 2014). Generalized food-deceptive Few studies of hypothesized cases of floral mimicry orchids usually exploit highly generalist pollinators, have included tests of all, or even most, of the specific such as bees, beetles and small flies (van der Cingel, predictions arising from the hypothesis. Some early 1995, 2001). These insects do not usually select for studies tested for increased reproductive success of a traits related to mimicry as they are unlikely to be species when growing together with its putative solely attracted by the floral signals of a single model (e.g. Dafni & Ivri, 1979, 1981a,b). However, as rewarding plant species. Orchids that deploy gener- the facilitation of reproductive success by rewarding alized food deception also have a tendency to flower plants can also be a feature of generalized floral early in the season when pollinators are less experi- deception and occur through the more general enced and still exploring possible new food sources ‘magnet species’ effect (Johnson et al., 2003a; (Internicola, Bernasconi & Gigord, 2008). These food Pellegrino et al., 2008), these cases remain inconclu- frauds frequently exhibit a high degree of colour or sive. One of the species with an unresolved system of scent polymorphism, possess showy nectar guides and deception is the European globe orchid [Traunsteinera may offer pseudopollen (Moya & Ackerman, 1993; globosa (L.) Rchb.]. A wide range of insects, including reviewed in Jersáková et al., 2009). By contrast, food- Lepidoptera, Hymenoptera, Coleoptera and Diptera, based floral mimicry is likely to evolve when pollina- have been recorded on T. globosa flowers, usually with tors are specialized on particular guilds of plants with no evidence that they act as pollinators (Müller, 1881, specific types of signals, and the mimics will thus be 1883). Reinhard et al. (1991), Vöth (1994, 1999) and under selection to match these signals. In food- Claessens & Kleynen (2011) observed butterflies, hon- deceptive mimicry systems, the most important eybees and bumblebees, empidid flies, syrphids and attractive floral trait seems to be colour, followed by beetles carrying pollinaria of T. globosa, but consid- inflorescence architecture, flower shape and nectar ered them to be occasional visitors and not estab- guide patterns, whereas scent chemistry seems to be lished pollinators. Paulus (2005) suggested Empidiae of lower importance, at least in the systems investi- as the principal pollinators, but Juillet et al. (2007) gated to date (Galizia et al., 2005; Peter & Johnson, and Claessens & Kleynen (2011) did not observe pol- 2008; Jersáková et al., 2012). linarium removal by visiting flies. Pollinator-mediated evolution of floral mimicry is Several co-flowering plant species are strikingly shaped by a combination of innate sensory prefer- similar to T. globosa in its general appearance, colour, ences (receiver biases) and associative learning of habitat and flowering season, and these have been pollinators (Schiestl & Johnson, 2013). To classify a suggested to be putative model plants. Vogel (pers. particular system as floral mimicry, the mimic should comm. in Dafni, 1987) suspected that T. globosa is a occur in sympatry with the model(s), their flowering mimic of Knautia dipsacifolia (Host) Kreutzer in times should coincide and the mimic should resemble Austria. In northern Italy, Dafni (1987) observed the model to the extent that the signal receiver has syrphid flies moving freely between the orchid and difficulties in discriminating between mimic and Valeriana montana L. and Scabiosa columbaria L., model, and thus moves freely between them. The whereas honeybees were seen approaching the orchid resemblance should confer a fitness advantage such flowers without landing. However, Juillet et al. (2007) that the mimic receives more visits and has higher found no relationship between the above-mentioned, fitness in the presence of the model than in its potential model species and fruit set in T. globosa. absence. Such adaptive resemblance is maintained as This would suggest that T. globosa represents a case a result of selection in a local community context, and of generalized food deception. should exclude cases of incidental resemblance or This study aimed to clarify the system of floral floral convergence among unrelated plant species that deception used by T. globosa. If the species employs adapt to the same functional group of pollinators Batesian food-source mimicry, we would expect: (1) © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180, 269–294 GUILD MIMICRY IN TRAUNSTEINERA 271 both naive and conditioned pollinators to have diffi- single globe-like inflorescence