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Scent Chemistry Is Key in the Evolutionary Transition Between Insect and Mammal Pollination in African Pineapple Lilies

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Scent Chemistry Is Key in the Evolutionary Transition Between Insect and Mammal Pollination in African Pineapple Lilies Research Scent chemistry is key in the evolutionary transition between insect and mammal pollination in African pineapple lilies Petra Wester1,2,3 , Steven D. Johnson1 and Anton Pauw2 1School of Life Sciences, University of KwaZulu-Natal Pietermaritzburg, Private Bag X01, Scottsville 3209, South Africa; 2Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Stellenbosch 7602, South Africa; 3Institute of Sensory Ecology, Heinrich-Heine-University, Universit€atsstr. 1, 40225 Dusseldorf,€ Germany Summary Author for correspondence: Volatile emissions may play a key role in structuring pollination systems of plants with mor- Petra Wester phologically unspecialised flowers. Here we test for pollination by small mammals in Eucomis Tel: +49 1729590360 regia and investigate whether its floral scent differs markedly from fly- and wasp-pollinated Email: [email protected] congeners and attracts mammals. Received: 22 August 2018 We measured floral traits of E. regia and made comparisons with insect-pollinated con- Accepted: 31 December 2018 geners. We observed floral visitors and examined fur and faeces of live-trapped mammals for pollen. We determined the contributions of different floral visitors to seed set with selective New Phytologist (2019) 222: 1624–1637 exclusion and established the breeding system with controlled pollination experiments. Using doi: 10.1111/nph.15671 bioassays, we examined whether mammals are attracted by the floral scent and are effective agents of pollen transfer. Key words: Asparagaceae, Eucomis regia, Eucomis regia differs from closely related insect-pollinated species mainly in floral scent, nectar, nonflying mammal pollination, polli- with morphology, colour and nectar properties being similar. We found that mice and ele- nator group, pollinator shift, scent, sulphur phant-shrews pollinate E. regia, which is self-incompatible and reliant on vertebrates for seed compounds. production. Mammals are strongly attracted to the overall floral scent, which contains unusual sulphur compounds, including methional (which imparts the distinctive potato-like scent and which was shown to be attractive to small mammals). The results highlight the important role of scent chemistry in shifts between insect and mammal pollination systems. 2015; Hobbhahn et al., 2017). It has been suggested that these Introduction plants rely mainly on deployment of scent cues to attract pollina- Specialised pollination systems are mostly characterised by flow- tors (Wester et al., 2009; Johnson et al., 2011). This is well sup- ers with complex architecture, allowing only a specific group of ported by studies of bat pollination systems in South America flower visitors access to rewards (Johnson & Steiner, 2000). where various aliphatic compounds and the sulphur compound However, there is increasing evidence that the chemistry of scent dimethyl disulphide (DMDS) emitted by flowers have been and nectar can mediate specialisation in pollination systems by shown to be attractive to flower-visiting bats (Knudsen & functioning as highly specific cues or filters (Johnson et al., 2006; Tollsten, 1995; von Helversen et al., 2000). There is still limited Nicolson et al., 2015; Sch€affler et al., 2015). These chemical traits evidence for a role of scent in pollination systems involving appear to be particularly important in determining the visitor ground-dwelling mammals. These pollination systems are partic- fauna in morphologically unspecialised flowers that potentially ularly well developed in Australia (involving mainly marsupials) allow a broad range of animal visitors to reach nectar. Evolution- and South Africa (involving mainly rodents and elephant-shrews) ary transitions in scent chemistry may, even in the absence of (Rourke & Wiens, 1977; Carthew & Goldingay, 1997; Letten & morphological changes, result in an evolutionary change in the Midgley, 2009; Wester et al., 2009; Wester, 2010, 2011). In a pollinator fauna with important implications for the evolution of study of the African parasitic plant Cytinus visseri (Cytinaceae) it reproductive isolation and for speciation (Peakall et al., 2010; was shown that a volatile ketone (3-hexanone) plays an important Waterman et al., 2011; Okamoto et al., 2015). role in attraction of mice to the flowers (Johnson et al., 2011), Flowers pollinated by mammals often have relatively open but no comparisons were made among related species to establish morphology owing to the lack of specialised mouthparts of these if this compound is uniquely associated with mammal animals. They are mostly pollinated at night and have drab col- pollination. oration (Rourke & Wiens, 1977; Johnson et al., 2001; Wester The African genus Eucomis L’Her. (Asparagaceae, previously et al., 2009; Wester, 2010, 2011; Zoeller et al., 2017; but see Hyacinthaceae) consists of 12 species characterised by structurally Johnson & Pauw, 2014; Johnson et al., 2011; Melidonis & Peter, unspecialised greenish flowers with easily accessible nectar 1624 New Phytologist (2019) 222: 1624–1637 Ó 2019 The Authors www.newphytologist.com New Phytologist Ó 2019 New Phytologist Trust New Phytologist Research 1625 (Zonneveld & Duncan, 2010). Previous studies have revealed the Study sites existence of scent-mediated specialisation for insect pollination in Eucomis. Species pollinated by spider-hunting wasps (Pompili- Observations and experiments took place between 2009 and dae) differ in scent from those pollinated by carrion flies, but 2014 at 16 sites that were selected to span the natural distribution wasp- and fly-pollinated species are otherwise very similar in of the two subspecies of E. regia (Table S2; Fig. 1). terms of floral morphology, colour and nectar properties (Shut- tleworth & Johnson, 2009, 2010). Addition of sulphur com- Pollinator observations pounds (DMDS and dimethyl trisulphide (DMTS)) to flowers of the wasp-pollinated species resulted in pollination by carrion We used both direct observations and videography to observe flies (Shuttleworth & Johnson, 2010). pollinator visits. Direct observations of small groups of flowering Eucomis regia (L.) L’Her. is the only Eucomis species in the E. regia plants were made among boulders on a dolerite ridge at winter-rainfall region of South Africa (Zonneveld & Duncan, the Nieuwoudtville site (7 h, about 20 plants) and in Renoster- 2010). Flowers of this species are very similar in appearance to veld vegetation at the Overberg site (14 h, about 50 plants; see those of other Eucomis species known to be pollinated by insects. Table 1 for details). To avoid disturbing mammals, plants were However, during preliminary observations we noticed that flow- illuminated with a flashlight covered with red plastic film. Video ers of E. regia have a highly distinctive potato-like scent and are observations were made at the Windhoek farm site. Five plants not visited by insects. The peculiar scent, along with the presence growing among boulders were monitored with three video cam- of fresh mammal faeces on leaves, led us to hypothesize that an corders (HDR-XR520, HDR-XR550; Sony, Tokyo, Japan) evolutionary transition in scent chemistry has occurred in con- using infrared lights (one to three 1-A SMD LEDs emitting junction with an ecological shift to pollination by small ground- 940 nm light), using 12 V/18 A.h lead-acid batteries as a power dwelling mammals. source. Camcorders and light sources operated continuously for The aims of this study were: to identify the pollinators of 6–13 h (86 h in total) and were placed 70–100 cm from the near- E. regia; to determine the breeding system in order to establish if est plants (see Table S2 for details). the plants depend on pollinators for reproduction; to evaluate Foraging behaviour of captured mammals was observed in ter- whether selective exclusion of vertebrates results in reduced seed raria (13 animals for c. 38 h in total, see Table S2 for details). production; to determine floral morphology, colour, nectar and Each terrarium was equipped with sand, stones as shelter, food, scent properties and compare these to those of insect-pollinated water, one animal and one to two flowering E. regia plants. congeners; and to experimentally test whether the overall scent and individual compounds are attractants for small mammals. Pollen transfer simulation Experiments were conducted using living mice to test whether Materials and Methods they could effect pollen transfer between E. regia inflorescences. Two E. regia inflorescences, one of which had anthers dusted Study taxa with dye powder, were placed in terraria with one live mammal E. regia is native to the winter rainfall zone of the Cape Floral at a time (three Namaqua rock mice Micaelamys namaquensis, Region of South Africa (Northern and Western Cape; Zonneveld four Four-striped field mice Rhabdomys pumilio, one Cape rock & Duncan, 2010). It occurs as two subspecies with E. regia (L.) elephant-shrew Elephantulus edwardii; Table S2). The stigmas of Gawl. ex Reyneke ssp. regia in the north, flowering from August flowers of undyed inflorescences were subsequently inspected for until October, and E. regia ssp. pillansii (L. Guthrie) Reyneke in the presence of dye powder. the south of its distribution area, flowering from July until September (Fig. 1; Reyneke, 1972; Crouch, 2010). The inflores- Trapping of mammals and pollen loads cences of E. regia ssp. pillansii are taller than those of ssp. regia (20 vs. 10 cm), but the subspecies have very similar flower dimen- To investigate which small mammal species occur near the sions (Supporting
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