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Butterfly Pollination and High-Contrast Visual Signals in a Low-Density Distylous Plant

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Butterfly Pollination and High-Contrast Visual Signals in a Low-Density Distylous Plant Oecologia (2003) 136:571–573 DOI 10.1007/s00442-003-1336-y PLANT ANIMAL INTERACTIONS Renee M. Borges · Vinita Gowda · Merry Zacharias Butterfly pollination and high-contrast visual signals in a low-density distylous plant Received: 24 July 2002 / Accepted: 12 June 2003 / Published online: 4 July 2003 Springer-Verlag 2003 Abstract In low-density butterfly-pollinated Mussaenda structures are a vital advertising strategy for this distylous frondosa (Rubiaceae), flowers attract pollinators at short plant, which occurs in very low densities and produces distances while conspicuous, non-rewarding accessory very few open flowers daily. High-contrast visual signals bracts are detectable at long distances by long-ranging have heightened detectability (Lehrer and Bischof 1995; pollinators such as the birdwing butterfly Troides minos Giurfa et al. 1996; Ne’eman and Kevan 2001), facilitating that did not detect flower-bearing plants in the absence of associative learning between signal and reward that is these bracts. However, even in the absence of flowers, the vital for successful advertising. white, ultraviolet-absorbing bracts attracted butterflies that visited flowerless plants. Although flower visits by short-ranging territorial butterflies declined significantly Materials and methods on removal of bracts, they did not cease completely. Nectar-robbing carpenter bees and birds did not change The plant and study site their behaviour following bract removal. Bract removal Mussaenda frondosa is distylous, individual plants bearing either caused a significant decline in fruit set, indicating their long- or short-styled flowers. Fruit is set only with pollen from the importance as visual signals to pollinators. opposite stylar morph, though pollen of both morphs germinates (unpublished data). The plant occurs in extremely low densities Keywords Advertisement · Heterostyly · Reproductive along forest edges (e.g. 15 plants along a 2-km linear edge), producing small, tightly closed, tubular, bright orange flowers. strategy · Spectral reflectance Usually one sepal in a group of flowers is enlarged into a white, leaf-shaped, vertically presented bract (Fig. 1a). Flower longevity is 24 h while individual bracts persist through the flowering season. Introduction The experiments were performed at the edges of a low elevation semi-evergreen forest at Karinja (12520N, 75E) in Karnataka State of the Western Ghats of India. Animal-pollinated plants find mates by attracting polli- nators. Low-density plants can suffer from a minority disadvantage in the pollination market (Silander 1978) Experiments and spectral measurements and may need to increase attractiveness of their floral We obtained a spectral reflectance of bracts and leaves between displays possibly by deploying long-lasting, non-reward- 330 and 721 nm relative to a ceramic, highly ultraviolet-reflecting ing accessory structures as visual signals. white standard under an angle of 45 (minimising surface In butterfly-pollinated Mussaenda frondosa (Rubi- reflection) with a Zeiss spectrophotometer MCS230, using a Zeiss aceae) we show that high-contrast secondary sexual CLXII xenon light source. We conducted experiments in which we removed either bracts or flowers from entire plants and compared visitation rates between R. M. Borges ()) · M. Zacharias pre-treatment (control) and treatment conditions for the same Centre for Ecological Sciences, plants. Plants in the control condition had both bracts and flowers. Indian Institute of Science, We recorded visitation to flowers on plants with and without bracts Bangalore 560 012, India (n=11 plants) for 5 days each in the pre- and post-bract removal e-mail: [email protected] states from 0700 to 1730/1800 hours in 30-min durations and Tel.: +91-80-3602972 similarly to plants with and without flowers (n=12 plants) for 2 Fax: +91-80-3601428 days each in the pre- and post-flower removal states. We used different sets of plants for each experiment, which may explain the V. Gowda difference in visitation rates between the two experiments. We Department of Biological Sciences, pooled data across days for each plant for each experiment, and George Washington University, calculated flower visitation rates (events/min) for each visitor type per plant. A flower visit consisted of probing into or hovering Washington, DC 20052, USA 572 Fig. 1 a The flowers and bracts of Mussaenda frondosa. b Spectral probing — butterflies: 2.70, birdwing butterflies: 2.20, carpenter reflectance of leaves and bracts. c, d Comparison of pre-treatment bees: 0.42, birds: 1.60. d Flower-removal experiment: (n=12 control and treatment observations for visitation rates (flower plants). Z-values for Wilcoxon matched pairs signed ranks tests. probing or hovering) by each group of visitors to plants Flower probing — butterflies: 3.06, birdwing butterflies: 2.20, (means€SD) using a matched pairs test. Control plants have both carpenter bees: 2.66. Hovering — butterflies: 0.75, birdwing bracts and flowers. *P<0.05, **P<0.01. Butterflies Butterflies butterflies: 2.36, carpenter bees: 1.09. Solid triangles represent excluding the birdwing. c Bract removal experiment: (n=11 plants). values=0 by definition, but shown to indicate that probing visits to Z-values for Wilcoxon matched pairs signed ranks tests. Flower flowers in control state were significantly greater than 0 around (measured only in the flower removal experiment) flowers birdwing Troides minos, which we placed in a separate or former flower locations. Extremely low plant densities con- category because it is a long-ranging canopy butterfly, strained sample sizes. We recorded the number of open flowers on the experimental plants each day and morphometric parameters of which descended to feed on flowers. all bracts harvested from experimental plants in the bract removal Following bract removal, visitation by all butterflies to experiment. flowers on such plants declined significantly. However, territorial butterflies continued to visit such bractless plants, whereas long-ranging birdwing butterflies made Results no visits to such plants, suggesting that they did not detect them in the absence of bracts (Fig. 1c). Flower visitation Plants presented very few flowers (mean€SD=7.7€5.2, by nectar-robbers was not significantly affected by bract n=11 plants) but many bracts (mean€SD=49.4€35.4, removal (Fig. 1c). Birds did not visit the set of plants n=11 plants) per day. Average (SD; maximum) measure- chosen for the flower removal experiment; consequently ments of individual bracts per plant (n=11 plants) were: their response to flower removal is unknown. Importantly, length 7.2 cm (0.9; 10.2), width 4.2 cm (1.1; 7.0), contour fruit set (% flowers setting fruit) of plants with bracts outline or perimeter 18.5 cm (3.8; 27.5) and area 20.2 cm2 (mean€SD=71.3€32.6%) was significantly higher than (4.3; 29.5). The bracts absorb ultraviolet (Fig. 1b). that of those without bracts (mean€ SD=24.3€18.1%) Butterflies, carpenter bees (Xylocopa sp.) and sunbirds (Wilcoxon matched pairs signed ranks test; Z=2.49, (Nectarinia zeylonica) visited the flowers. Butterflies, P<0.05; n=10), indicating the importance of bracts as representing 57.4% of visits, were legitimate visitors; the pollinator signals. Territorial butterflies continued to others with 36.1% and 6.5% of visits respectively were hover over plants from which flowers had been removed nectar robbers. Most butterflies were territorial under- and birdwing butterflies also visited these plants (Fig. 1d), storey species, which made 65.3% of visits. The other showing that bracts were effective signals for birdwing 34.7% of butterfly visits were made by the southern butterflies. 573 Discussion which the flowers alone would not have been able to achieve. Low-density plants must be individually conspicuous as they cannot rely on the combined advertisement of Acknowledgements We thank Andreas Gumbert for the spectral neighbours. Low-density Mussaenda frondosa advertises reflectance measurements; Veena C.P. for field assistance; Lars Chittka, Andreas Gumbert, Natalie Hempel de Ibarra, Almut using non-rewarding bracts that increase reproductive Kelber, Peter Kevan, Michiyo Kinoshita, Doekele Stavenga and success indicated by the significant decline of fruit set in Misha Vorobyev for useful suggestions; and Almut Kelber, Natalie bractless plants. Although sterile accessory structures can Hempel de Ibarra, and the reviewers for valuable comments on the increase attractiveness (Bell 1985; however see Herrera manuscript. This research was funded by the Department of 1997), we demonstrate differential responses of various Science and Technology, Government of India. flower visitors to their removal. Birdwing butterflies did not visit flowering bractless plants although they visited flowerless plants with intact bracts. Since butterflies are References capable of associative learning (Papaj 1986; Weiss 1995), Bell G (1985) On the function of flowers. Proc R Soc Lond Ser B this could be because of a learned association between 224:223–265 bracts and flowers. Territorial, short-ranging butterflies, Giurfa M, Vorobyev M, Kevan PG, Menzel R (1996) Detection of however, continued to visit flowers of bractless plants coloured stimuli by honeybees: minimum visual angles and although such visits declined significantly, suggesting that receptor specific contrasts. J Comp Physiol A 178:699–710 Herrera J (1997) The role of colored accessory bracts in the they use other cues (Stanton 1984), or trapline (Waller
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