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Memory, Learning and Floral Characteristics in Foraging Patterns of Eupetomena Macroura, a Neotropical Hummingbird

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Memory, Learning and Floral Characteristics in Foraging Patterns of Eupetomena Macroura, a Neotropical Hummingbird Revista de Etologia 2001, Vol.3, N°2,Memory 77-88 and learning in a neotropical hummingbird Memory, Learning and Floral Characteristics in Foraging Patterns of Eupetomena macroura, a Neotropical Hummingbird CARLOS B. CARVALHO AND REGINA H. MACEDO Universidade de Brasília Some studies suggest that hummingbirds associate floral characteristics with resources, and remember this through time, but there is controversy regarding which floral characteristics are more attractive. We used artificial feeders to analyze flower choice patterns of one hummingbird species, Eupetomena macroura, from the “cerrado” region of Brazil, regarding perception of flower color, shape and odor, and tested if associative memory was retained over time. Natural sucrose odor had little influence overall, but individuals showed a marked preference for flat-shaped corollas, a characteristic that is opposed to the tubular flowers typically exploited by hummingbirds. Contrary to expectations, hummingbirds did not exhibit short-term memory for association between resources and morphological floral characteristics (color and shape). However, over a short time-span, they did associate the resource with a strong artificial vanilla scent. Long-term memory was not evident when the resource was associated with red flowers, but occurred when flower corollas were flat. Due to the high diversity of flower types in the Neotropics, it may be more advantageous for hummingbirds to use explorative and flexible searching strategies without forming strong associations for specific floral characteristics. Index terms: Memory. Learning. Hummingbirds. Nectarivory. Eupetomena macroura. Memória, aprendizado e características florais nos padrões de forrageamento de Eupetomena macroura, um beija-flor neotropical. Alguns estudos sugerem que beija-flores associam características florais com o recurso (néctar), e que retêm essa memória através do tempo, embora hajá controvérsia sobre quais caracte- rísticas florais seriam mais atrativas. Utilizamos alimentadores artificiais para analisar padrões de escolha de flores em uma espécie de beija-flor, Eupetomena macroura, na região do Cerrado brasileiro. Consideramos a percepção de cor, formato e odor florais, e testamos se a memória associativa ficaria retida ao longo do tempo. O odor da solução de sucrose natural teve pouca influência de modo geral, mas indivíduos mostraram uma preferência marcante por flores com corolas achatadas, uma característica floral oposta àquela normalmente encontrada em flores exploradas por beija-flores, usualmente de formato tubular. Contráriamente às expec- tativas, beija-flores não exibiram memória à curto prazo da associação estabelecida entre recurso e caracterís- ticas florais morfológicas (cor e formato). Entretanto, por um período curto de tempo as aves associaram o recurso com um odor artificial de baunilha. A memória à longo prazo não ficou evidenciada quando o recurso estava associado a flores vermelhas, mas ocorreu quando as corolas das flores eram achatadas. Devido à alta diversidade de tipos florais nos neotrópicos, talvez seja mais vantajoso para beija-flores utilizarem estratégias de busca que sejam exploratórias e flexíveis do que formarem associações fortes a partir de características florais muito específicas. Descritores: Memória. Aprendizagem. Beija-flores. Nectarivoria. Eupetomena macroura. Carlos B. Carvalho, Universidade de Brasília, Pós- For comments on the manuscript we are indebted to Graduação em Biologia Animal, Depto. de Ciências Guarino Colli, Maria Alice Alves and Ivone Diniz. For Fisiológicas, C.P. 04457, Brasília, D.F. 70919-970. E- an in-depth and very helpful review of the paper we mail: humming@unb. Regina H. Macedo Depto. de thank Lee Gass. The Conselho Nacional de Desen- Zoologia – IB, Universidade de Brasília, Brasília, D.F. volvimento Científico e Tecnológico - CNPq provided 70910-900. E-mail: [email protected] financial support through a graduate scholarship for C. B. Carvalho and a research fellowship for R. H. Macedo. 77 Carlos B. Carvalho and Regina H. Macedo Resources, such as food for animals, are remembering them, most of these focus upon not found homogeneously, but vary in quality, spatial memory ability. Hummingbirds quantity and availability over an animal’s home apparently are capable of finding resources range (Sutherland & Gass, 1995). The capacity based upon their location (Cole, Hainsworth, of animals to learn about resources in their Kamil, Mercier, & Wolf, 1982; Healy & Hurly, environment may affect the way in which they 1995; Hurly & Healy, 1996), with or without search for and choose among available resources visual cues (Brown & Gass, 1993; Miller, Tamm, (Bell, 1991), and remembering this information Sutherland, & Gass, 1985), and can establish is potentially important to long-term foraging spatial associations. They also remember the success. Conditioned responses are forms of position of resources and continue to visit them learning that involve the establishment of as long as these are adequate (Gass & associations between some reinforcement Sutherland, 1985; Miller et al., 1985) and, (whether positive or not) and the animal’s furthermore, they avoid visiting flowers which response (Carthy, 1980). Operational or instru- they have depleted recently (Healy & Hurly, mental conditioning, wherein the reinforcement 1995). Even after resources have changed depends upon voluntary responses of animals places, the birds will persist in visiting previous (Carthy, 1980), have been analyzed through locations for some time, indicating the influence experiments involving rats that learn to obtain of memory upon foraging patterns (Sutherland rewards by pressing levers (Carthy, 1980; & Gass, 1995). Pearce, 1997), or pigeons that obtain rewards by pecking disks illuminated with certain While it is clear from a host of wavelengths (Carthy 1980). observations and experimental evidence that hummingbirds clearly use spatial memory to There are apparently two phases during locate their flowers, it is less evident what they the acquisition of memory: (1) short-term remember and how this memory is being used memory, where information about an event is during foraging (Hurly & Healy, 1996). Two kept for a short period; and (2) long-term types of information may be useful for memory, where the physical trace of the memory hummingbirds as they return to a resource: the is permanently fixed for future access (Milinski, specific characteristics of flowers of certain 1994). Animals that feed upon renewable species and/or the position of the site with resources can explore these more readily if they respect to more general patterns of the remember their locations and refill rates (Hurly landscape (Hurly & Healy, 1996). There has & Healy, 1996). been a large amount of controversy regarding which floral characteristics (such as color or Hummingbirds are the smallest of all flower shape) are more attractive to birds and, consequently, have very hummingbirds. The efficient location of flowers highmetabolic rates (Hainsworth & Wolf, 1972, by hummingbirds may be based upon their 1977). Additionally, they have elevated energetic highly developed visual acuity. They see not only costs associated with their hovering flight wavelengths visible to humans, but also those (Hainsworth & Wolf, 1977). Because in the near ultraviolet range (Bleiweiss, 1994; hummingbirds obtain the greatest part of their Goldsmith, 1980). Some authors have food from flowers that renew nectar standing speculated that hummingbirds prefer longer crop, sometimes visiting hundreds of flowers wavelengths, particularly the color red (Pickens, each day, they can potentially obtain energetic 1930; Ruschi, 1953), which is more conspicuous benefits by knowing where to find and how to in contrast to green vegetation (Snow, 1994). recognize the most rewarding flowers (Healy & However, other authors suggest that Hurly, 1995; Hurly, 1996; Hurly & Healy, 1996). hummingbirds may be conditioned to the colors of local flowers (Bené, 1941; Sick, 1997; Snow, Although several studies show that 1994), and that the quality of the nectar is a hummingbirds are capable of establishing more important factor than the color (Stiles, associations and then subsequently 1976). 78 Memory and learning in a neotropical hummingbird Despite the existence of some controversy beginning of the rainy season; the other two regarding the evolutionary processes that were conducted between March and June 1998, shaped flower and pollinator morphologies at the end of the rainy season. (Nilsson, 1998; Wasserthal, 1997), it is generally Each experiment had two phases (A and assumed that some species of plants may have B), each phase conducted in three places at least co-evolved with certain hummingbird species, 1.5 km apart and lasting 15 days (Table 1). At since the corolla shape is compatible with the each place we used a 3 X 3 m vertical grid with bill morphology of these birds (Sick, 1997; Snow, nine plastic feeding bottles (each one with three 1994). Thus, flowers pollinated by identical “flowers”) separated from each other hummingbirds generally exhibit a tubular by one meter. During each experiment, eight corolla (Pickens, 1930; Snow, 1994). feeders in the grid had identical flowers and contained only water, and one feeder had Another characteristic typical of flowers distinct floral characteristics and contained a visited by hummingbirds is the absence of odor 25% sugar water solution, that is, 25g of sugar (Bené, 1945; Snow, 1994). Apparently, per
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