PALM S Tucker Lima: Color Vol. 53(4) 2009 Flower Color JOANNA M. T UCKER LIMA School of Natural Resources Variation in and Environment University of Attalea PO Box 110410 Gainesville, FL 32611-0410 USA phalerata [email protected] (Arecaceae)

Over the past few , I have been conducting a phenology study of the arborescent palm Mart. ex Spreng. in southwestern Amazonia. Although botanical records have consistently reported yellow on A. phalerata , I observed multiple cases of non-yellow staminate flowers. Flower color varied from dark purple to violet, or a mixture of yellow- orange to magenta flowers within the same male (Fig. 1; hereafter I refer to non-yellow flowers as purple). This article reports on field observations of flower color polymorphism in A. phalerata and discusses possible explanations for this anomaly.

Field observations the number of sides of the palm crown directly exposed to sunlight (four lateral sides plus top) Phenology (Bechtold 2003). Within old-growth forest, A. phalerata is mainly a lower palm. I monitored flowering phenology of Attalea phalerata in Acre, , between January 2006 Attalea alternate between pistillate, and December 2007. Using binoculars, I staminate, and sometimes hermaphroditic observed flowering from the ground at inflorescences on the same . During 24 monthly intervals at six study sites (three months of observations of 72 A. phalerata actively grazed pastures and three areas of old- palms, I registered only four instances of growth tropical moist forest). At each site I hermaphroditic inflorescences. The remaining observed 12 reproductive palms. Between July inflorescences were either exclusively pistillate to December 2007, observations were reduced or exclusively staminate. The majority of A. to two sites per . For each individual I phalerata staminate inflorescences initiated recorded sex and reproductive phase of all flowering at the beginning of the dry season inflorescences – closed inflorescence buds between May and June, peaked in September (), inflorescences in anthesis (open at the end of the dry season, and dwindled flowers) and dried, post-anthesis inflorescence during the wet season (Fig. 2). Palms growing structures. I also categorized crown illumi- in old-growth forest were more likely to nation on a scale of zero to five by counting suspend inflorescence production for a short

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1. Color variation from yellow to dark purple in Attalea phalerata staminate inflorescences observed in eastern Acre, Brazil. period each between February and April, Flower color variation whereas pasture palms produced inflorescences continuously year-round. Still, pasture palms To my surprise, of 55 male inflorescences mimicked the overall seasonal patterns of observed in anthesis, the majority (55%) flowering peaks and lulls in the forest. produced purple flowers rather than the

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1. ( continued ) Color variation from yellow to dark purple in Attalea phalerata staminate inflorescences.

familiar yellow flowers. During two years of different palms). Some A. phalerata individuals monthly phenological observations, I recorded alternated between purple and yellow flowers, 19 purple staminate inflorescences in anthesis while a few palms (n=5) repeatedly produced in pastures (on 15 different palms) and 11 in purple flowers. Of the 22 A. phalerata forests (on nine different palms). Over the individuals with purple flowers, more than same two-year period, I observed 14 yellow half (n = 12) also produced the better known staminate inflorescences in pastures (on 12 yellow flowers either before or after a purple different palms) and 11 in forest (on ten flowering event, indicating phenotypic 2. Proportion of Attalea phalerata palms with staminate inflorescence and monthly rainfall from January 2006 until December 2007 in pastures and old-growth forests in Acre, Brazil.

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3. Purple coloration of petal tips on flowers of an Attalea phalerata pistillate inflorescence in eastern Acre, Brazil. plasticity within individual palms. In one case, 1). Most flowering anthesis events occurred a single palm exhibited one yellow and one between observation visits, and for these I was purple inflorescence simultaneously. Both unable to determine flower color. yellow and purple inflorescences were Color polymorphism in palms observed in anthesis, and the colors remained constant as they developed. I also observed Flower color polymorphism in is purple coloration at the tips of creamy yellow common in nature and appears within genera, petals of A. phalerata pistillate flowers (Fig. 3), within species, and even within isolated but only three pistillate inflorescences were populations. Several examples from observed in anthesis during the entire study herbaceous and other short-lived plants, both period. wild and cultivated, exist in the research literature (Armbruster 2002). Larry Noblick Staminate flower color variation occurred not (pers. comm.) detected flower color variation only within and among individual palm , between yellow and magenta in Attalea palms but also in both the wet (November to April) near Corumba, Mato Grosso do Sul, Brazil, in and dry seasons (May to October), across the region, but to my knowledge no different (pasture and forest), and on records of within-species color variation in a regional scale dispersed over 100 km 2. Purple palm inflorescences have been published. flowers appeared at various times throughout the year, although mostly during the dry Palms, such as the lipstick palm, season, which corresponds to the peak renda , with its bright red crown shaft, flowering season of A. phalerata (Fig. 2, Tab. epetiolata, with reddish purple underside of

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201 PALM S Tucker Lima: Attalea Flower Color Vol. 53(4) 2009 young (Blanco & Martén-Rodríguez to deter pollinators. Further research may help 2007), and various palm genera with purple determine if purple staminate flowers (e.g., , , Butia , ), negatively affect fertilization, set and testify to widespread anthocyanin production reproductive success in A. phalerata . within . Anthocyanins (a flavonoid Associations between anthocyanins in sub-group) are responsible for most orange, vegetative organs and flowers and environ- red, purple and blue flower colors and occur mental stresses may also help explain flower in almost all vascular plants (Grotewold 2006). color variation in A. phalerata . In vegetative Harborne et al. (1974) found flavonoid organs, plants manufacture anthocyanins to pigments (glycosides) specifically in the flowers protect against environmental stresses, such of ten different palm species, and a few studies as herbivory (Fineblum & Rausher 1997), have identified other types of flavonoids in photo-damage (Close & Beadle 2003) and the vegetative structures of Attalea and other drought (Levin & Brack 1995). Plants also cocosoid palm species (Williams et al. 1983, synthesize pigments in response to extreme Williams et al. 1985). Still, the question environmental conditions, such as cold remains as to what drives flower color variation temperatures (Stiles et al. 2007) and nitrogen in A. phalerata . deficiency (Bonguebartelsman & Phillips Possible explanations for color poly- 1995). Finally, Armbruster (2002) found morphism in Attalea phalerata flowers linkages between anthocyanins in vegetative organs and their presence in flowers. Selection To try and uncover the reasons for flower color pressures related to environmental hetero- variation in A. phalerata , I used Pearson’s Chi- geneity and stress tolerance may be responsible squared Test to examine relationships between for plant anthocyanin production in general, flower color and four variables: (1) habitat (old- helping maintain flower color polymorphism growth forest versus pasture) ( χ2 = 1.01 , d.f. within and among species (Warren & = 1, p = 0.32), (2) season (wet versus dry) ( χ2 MacKenzie 2001). = 0.799 , d.f. = 1, p = 0.37), (3) year (2006 versus 2007) ( χ2 = 1.84 , d.f. = 1, p = 0.17), and Final Considerations (4) crown illumination ( χ2 = 10.67, d.f. = 5, p Until now, A. phalerata inflorescence color in = 0.06). Results revealed no significant southwestern Amazonia has been reported associations with flower color. Crown only as yellow or cream-colored (Evandro illumination, or light availability, was Ferreira, pers. comm.). Anthocyanins present marginally significant, but the absence of an in the plant to various degrees likely account association between habitat and flower color for the various shades of purple observed. The precluded any strong linkage between crown question remains as to what provokes the illumination and flower color, since the two differences in anthocyanins seen in these habitats we compared – pasture and forest – palms. Flower color is not genetically fixed in represent two extremes in light availability. A. phalerata , since yellow inflorescences often A common explanation for color variation followed the production of purple inflo- within and among species is pollinator rescences on the same plant. If environmental selective pressures (Hannan 1981). Pollinators stress is responsible for flower color variation respond to various floral signals – color, shape, in A. phalerata , three sources of stress come to size, fragrance, temperature – and these mind: (1) Intermittent cold fronts pass through preferences exert selective pressures on the the region each year during the early dry plant to optimize reproductive success (Levin season, dropping temperatures into the lower & Brack 1995, Meléndez-Ackerman et al. 1998). teens ( ºC) (cf . Stiles et al. 2007); (2) A severe Studies of A. phalerata are scarce; drought in 2005 induced soil moisture stress however, nitidulid beetles from the and could have indirectly augmented Mystrops are most likely the principal susceptibility to herbivory or pathogen attack; pollinators (Moraes et al. 1996). Beetles and (3) Extensive fires during the 2005 drought respond to floral signals of increased killed a large number of pollinators, and palms temperature and fragrance, rather than color, may have reacted with a different flower color and Attalea flowers are known to mature to attract alternative pollinators. Attalea quickly, heating up before anthesis (Henderson phalerata is a broadly distributed species, found 2002). I observed insects, apparently throughout the southern and western pollinators, actively feeding on purple periphery of the Amazon region, including inflorescences, so purple flowers do not appear Brazil, and Peru, as well as the planalto

202 PALM S Tucker Lima: Attalea Flower Color Vol. 53(4) 2009 of Brazil, Bolivia and (Henderson et FINEBLUM , W.L. AND M.D. R AUSHER . 1997. Do al . 1995). More detailed studies of this species’ floral pigmentation genes also influence flowering phenology and variation in flower resistance to enemies? The W locus in color over its geographical range are warranted Ipomoea purpurea . Ecology 78: 1646–1654. to understand what triggers deviations in A. GROTEWOLD , E . 2006. The genetics and phalerata flower color and how flower color biochemistry of floral pigments. Annual variation affects the ecology of this species. Review of Plant Biology 57: 761–780. Acknowledgments HANNAN , G.L . 1981. Flower color Research in Brazil was funded in part by the polymorphism and pollination biology of United States Environmental Protection Platystemon californicus Benth. (Papa- Agency (EPA) under the Science to Achieve veraceae). American J. Bot. 68: 233–243. Results (STAR) Graduate Fellowship Program. HARBORNE , J.B., C.A. W ILLIAMS , J. G REENHAM AND Additional funding for field work was provided P. M OYNA . 1974. Distribution of charged by two generous grants from the International flavones and caffeylshikimic acid in Palmae. Palm Society in 2005 and 2007. Research was Phytochem. 13: 1557–1559. carried out in collaboration with the at the Parque Zoobotânico – Federal HENDERSON , A. 2002. Evolution and Ecology of University of Acre in Brazil (PZ-UFAC), and Palms. The New York Press, their logistic support made this research Bronx, New York. possible. I wish to sincerely thank Professors HENDERSON , A., G. G ALEANO AND R. B ERNAL . 1995. Karen A. Kainer (University of Florida) and Field Guide to the Palms of the Americas. Evandro J. Linhares Ferreira (PZ-UFAC), for Princeton University Press, Princeton, New their valuable advice and guidance throughout Jersey. this research, and I especially thank José Evandro Santos Lima, who was indispensable LEVIN , D.A. AND E.T. B RACK . 1995. Natural as my field assistant. I am also very grateful to selection against white petals in Phlox . Larry Noblick, Francis E. Putz, Wagner Evolution 49: 1017–1022. Vendrame and two additional anonymous MELÉNDEZ -A CKERMAN , E. AND D.R. C AMPBELLL . reviewers for their helpful reviews and 1998. Adaptive significance of flower color comments on this manuscript. and inter-trait correlations in an Ipomopsis hybrid zone. Evolution 52: 1293 –1303. LITERATURE CITED MORAES , M., F. B ORCHSENIUS AND U. B LICHER - ARMBRUSTER, W.S. 2002. Can indirect selection MATHIESEN . 1996. Notes on the biology and and genetic context contribute to trait uses of the motacú palm ( Attalea phalerata , diversification? A transition-probability Arecaceae) from Bolivia. Economic Botany study of blossom-colour evolution in two 50: 423 –428. genera. J. Evolutionary Biol. 15: 468–486. STILES , E.A., N.B. C ECH , S.M. D EE AND E.P. L ACEY . BECHTOLD, W.A . 2003. Crown position and light 2007. Temperature-sensitive anthocyanin exposure classification – an alternative to production in flowers of Plantago lanceolata . field assigned crown class. Northern J. Appl. Physiologia Plantarum 129: 756–765. Forestry 20: 154–160. WARREN , J. AND S. M AC KENZIE . 2001. Why are all BLANCO, M.A. AND S. M ARTÉN RODRÍGUEZ. 2007. colour combinations not equally represented The stained-glass palm, Geonoma epetiolata . as flower-colour polymorphisms? New Palms 51: 139–146. Phytol. 151: 237–241.

BONGUEBARTELSMAN , M. AND D.A. P HILLIPS. 1995. WILLIAMS , C.A., J.B. H ARBORNE AND S.F. G LASSMAN . Nitrogen stress regulates gene expression on 1983. Flavonoids as taxonomic markers in enzymes in the flavonoid biosynthetic some cocosoid palms. Plant Syst. Evol. 142: pathway of tomato. Plant Phys. Biochem. 157–169. 33: 539–546. WILLIAMS , C.A., J.B. H ARBORNE AND S.F. G LASSMAN . CLOSE , D.C. AND C.L. B EADLE . 2003. The 1985. Further flavonoid studies on Attalea ecophysiology of foliar anthocyanin. The species and some related cocosoid palms. Botanical Review 69: 149–161. Plant Syst. Evol. 149: 233–239.

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