Central place foragers, such as territorial hummingbirds, feed from resources that tend to be constant in space and to replenish with time (e.g. nectar in flowers). The ability to remember both where and when resources are available would allow these animals to forage efficiently. Animals that feed at multiple locations would also benefit from forming routes between these multiple locations. Hummingbirds are thought to forage by repeating the order in which they visit several locations following a route called a “trapline”, although there are no quantitative data describing this behaviour. As a first step to determining how and if wild free living hummingbirds forage by traplining, I decomposed this behaviour into some of its key components. Through five field experiments, where I trained free-living hummingbirds to feed from artificial flowers, I confirmed that territorial hummingbirds will, in fact, trapline. Birds will use the shortest routes to visit several locations and will prioritize those locations that are closest to a usual feeding site. Additionally, even though hummingbirds can learn to use temporal information when visiting several patches of flowers, the spatial location of those patches has a larger influence in how these birds forage in the wild. Since male and female hummingbirds were thought to forage differently I also tested whether there were sex differences in the types of cues they use when foraging. Contrary to expectation, female hummingbirds will also use spatial cues to relocate a rewarded site. Using the foraging ecology of rufous hummingbirds to formulate predictions as to what information these birds should use has lead me to discover that these birds forage in a completely different way than previously thought.

Thesis (Ph.D.)--University of Delaware, 2009. / Principal faculty advisor: Sunil K. Agrawal, Dept. of Mechanical Engineering. Includes bibliographical references.

Title from title page of PDF (University of Missouri--St. Louis, viewed March 8, 2010). Includes bibliographical references.

I tested the twin-threshold model, a risk-sensitive foraging model incorporating both a starvation threshold and a higher reproductive threshold. The model predicts risk-adverse foraging when an animal's energy state is close to the starvation threshold and risk-prone foraging when the animal's energy state is close to the reproductive threshold. Wild rufous hummingbirds (Selasphorus rufus) were presented with a choice of three artificial flower types that had either no, moderate or high variability around a common mean. I manipulated energy state by changing either the mean nectar volume or altering the cost of foraging (long versus short corollas). When the energy state of hummingbirds was close to the reproductive threshold they preferred the variable options. When the energy state of hummingbirds was close to the starvation threshold they preferred the nil option. Hummingbirds responded in a manner consistent with the twin-threshold model. / x, 90 leaves ; 29 cm.

Supplementary food is less variable than natural food. While feeding from constant food sources tends to be preferred by animals they must sometimes forage from more variable resources. However, the ways in which animals deal with the temporal and spatial variability of more natural food is not entirely understood. I investigated the decisions free-living rufous hummingbirds made when foraging from variable resources, where variability was encountered over time or within a bout via four field experiments. In addition, I investigated their use of wild flowers and differences in the use of supplementary food by these birds in different regions using surveys and by manipulating the distribution of feeders at feeding sites. I investigated the possibility of a genetic explanation for any differences in feeder use between regions using analysis of microsatellite DNA and banding data. Hummingbirds seemed to prefer to make foraging decisions based on past behaviour or post-ingestive feedback rather than on sensory information such as taste, which may be harder to assess accurately. Birds choosing between constant and variable rewards with equal means preferred the constant rewards when variability was high but tended to prefer the variable reward when variability was low. This seems to be a result of hidden time and other costs associated with foraging on highly variable resource but not on less variable ones, combined with potential benefits of information seeking from less variable resources. In addition, these preferences between constant and variable resources were affected by preceding foraging conditions. The number of birds using feeders was affected by population density and air temperature. Microsatellite data showed the rufous hummingbird population to have a fairly panmictic population structure. Investigating influences on foraging decisions at a large scale (population density) and small scale (resource variability) has provided a much wider understanding of their foraging behaviour than either could alone.

Os beija-flores, por serem aves altamente especializadas na exploração de néctar e possuírem uma das maiores taxas metabólicas dentre os endotermos, são altamente dependentes de estratégias que otimizem a utilização dos recursos disponíveis no meio. Depreende-se, assim, que uma memória detalhada dos diferentes aspectos de seus recursos alimentares seja um importante componente do seu sucesso alimentar. Estudos recentes têm mostrado que alguns animais não humanos exibem a capacidade de lembrar \"onde\" e \"quando\" eventos específicos (\"o quê\") ocorreram. Considera-se que o conhecimento concomitante sobre \"o quê\", \"onde\" e \"quando\" caracteriza um tipo de memória denominada \"memória episódica\", considerada, até então, privativa de seres humanos. A proposta do presente trabalho foi avaliar (1) a preferência de beija-flores das espécies Amazilia lactea e Eupetomena macroura por duas concentrações de solução de sacarose (\"o quê\"); na espécie E. macroura (2) sua memória espacial (\"onde\") e sua memória sobre pistas intrínsecas associadas à fonte alimentar (\"o quê\"); e (3) sua capacidade de se recordar da hora do dia (\"quando\") associada à localização espacial (\"onde\") e à cor de alimentadores (\"o quê\"). Os resultados mostraram que os beija-flores são capazes de processar informações sobre \"o quê\", \"quando\" e \"onde\" de seus recursos alimentares e que utilizam essas informações flexivelmente quando confrontados com diferentes situações experimentais, exibindo, assim, conhecimento sobre os principais elementos que caracterizam uma memória do tipo-episódica. / Hummingbirds are highly specialized for nectar consumption as a main food source. Since these animals exhibit one of the highest metabolic rates among endoterms, they depend on strategies that optimize the use of the available food resources. Therefore, a detailed memory for the location, quality and time of food availability is likely to be an important component of their feeding strategies and success. Recent studies have shown that some non-human animals exhibit the capacity of remembering \"where\" and \"when\" specific events (\"what\") occurred. Simultaneous recalling of \"what\", \"where\" and \"when\" specific events occurred characterizes a kind of memory known as \"episodic-memory\", considered, until recently, exclusive to humans. This study aimed at evaluating (1) the preference for either 20 or 40% sucrose solutions (\"what\") by exemplars of Amazilia lactea and Eupetomena macroura hummingbirds, (2) the memory for spatial locations (\"where\") and for intrinsic cues (\"what\") associated with food resources by exemplars of E. macroura, and (3) the ability of exemplars of E. macroura to learn an association including the time of day (\"when\") spatial locations (\"where\") offered profitable colored feeders (\"what\"). The results showed that the hummingbirds are capable of memorizing information about \"what\", \"when\" and \"where\" food resources are available and of using this information flexibly. Therefore, these results clearly indicate that hummingbirds exhibit an episodic-like type of memory.

"Why have separate sexes?" is a fundamental question in biology and has been investigated intensively since Darwin first proposed two hypotheses: Separate sexes evolve 1) to avoid detrimental effects of self-fertilization or 2) to improve allocation of scarce resources to each sex's reproductive function. In animal-pollinated plants dioecy is hypothesized to be favored when small, generalized pollinators predominate because they increase self-fertilization rates of plants. I concurrently tested Darwin's hypotheses using Echinocereus coccineus (Cactaceae). I found, as predicted, when specialized pollinators (hummingbirds) were excluded from plants and only generalized pollinators (bees) visited, selfing rates of plants increased 238%. High selfing rates produced by bees, along with high levels of inbreeding depression in E. coccineus populations, were sufficient to select for dioecy, even in absence of any reallocation of resources by the plants. Hummingbirds may also maintain high levels of gene flow among E. coccineus populations: populations blooming synchronously with the hummingbird migration had lower FST values (i.e. less genetic divergence) than asynchronously blooming populations. Population genetic data also suggest frequency of dioecious populations should be negatively correlated with both hummingbird abundance and elevation. Structural equation models of effects of hummingbird abundance, elevation and annual rainfall (resources) on dioecy across the range of E. coccineus supported this hypothesis. All predictor variables were either directly or indirectly negatively correlated with dioecy. Only models with hummingbird abundance as a direct predictor of dioecy significantly fit the data. Darwin's first hypothesis was again supported: as hummingbird abundance declines (and selfing rates increase), the incidence of dioecious populations increases. Finally, to determine how changes in pollinator type may be globally influencing the evolution of dioecy, I conducted a literature survey of studies noting changes in pollinator types along elevation gradients and compared these to studies of dioecy along elevation gradients. The abundance of specialized insect pollinators declines with elevation, often leaving only generalized pollinators at the highest elevations: Proportion of dioecious species in communities increases accordingly with elevation. I propose elevation may be useful as a worldwide predictor of dioecy because it effects pollinator community composition and amount of inbreeding depression expressed in plant populations.

Floral traits are typically associated with specific groups of pollinators. Yet, many flowering plants are pollinated by more than one group of pollinators. To explore the influence of multiple effective pollinators on floral traits, I examined how the pollinator assemblage of Polemonium brandegeei affects pollen movement and selection on floral traits. I documented phenotypic and genetic variation in floral traits, and quantified the effectiveness of floral visitors. In natural populations, I quantified pollen removal and deposition over two consecutive flowering seasons. I then performed a pair of novel array experiments to estimate selection through female (seeds set) and male (seeds sired) function on floral traits by two important pollinators, hawkmoths and hummingbirds. My analysis of field populations demonstrated that height and relative positioning of sex organs were important for the removal and deposition of pollen. Individuals of P. brandegeei displayed a large degree of continuous and heritable variation, particularly in the relative positioning of sex organs. Plants in the same population displayed stigmas recessed below (reverse herkogamy), or exserted above anthers (approach herkogamy). My array experiments determined that variation in herkogamy is likely maintained through contrasting selection, because hawkmoths selected for recessed stigmas but hummingbirds selected for exserted stigmas. While my results were the first to detect selection for reverse herkogamy by hawkmoths, I also identified selection for traits that are typically associated with both pollinators. For example, hawkmoths selected for narrow corolla tubes, and hummingbirds selected for longer corolla tubes. The selection I detected on floral traits through female function was generally stronger than through male function, which runs counter to traditional theory of gender-biased selection. My findings indicate that floral traits can conform to intermediate dimensions between the optima of two pollinators (herkogamy), or appear specialized to one pollinator (tube length). Therefore, cumulative arrangements of floral traits (floral design) can effectively function under pollination by two pollinators that exert different selection pressures on traits.

Floral traits are typically associated with specific groups of pollinators. Yet, many flowering plants are pollinated by more than one group of pollinators. To explore the influence of multiple effective pollinators on floral traits, I examined how the pollinator assemblage of Polemonium brandegeei affects pollen movement and selection on floral traits. I documented phenotypic and genetic variation in floral traits, and quantified the effectiveness of floral visitors. In natural populations, I quantified pollen removal and deposition over two consecutive flowering seasons. I then performed a pair of novel array experiments to estimate selection through female (seeds set) and male (seeds sired) function on floral traits by two important pollinators, hawkmoths and hummingbirds. My analysis of field populations demonstrated that height and relative positioning of sex organs were important for the removal and deposition of pollen. Individuals of P. brandegeei displayed a large degree of continuous and heritable variation, particularly in the relative positioning of sex organs. Plants in the same population displayed stigmas recessed below (reverse herkogamy), or exserted above anthers (approach herkogamy). My array experiments determined that variation in herkogamy is likely maintained through contrasting selection, because hawkmoths selected for recessed stigmas but hummingbirds selected for exserted stigmas. While my results were the first to detect selection for reverse herkogamy by hawkmoths, I also identified selection for traits that are typically associated with both pollinators. For example, hawkmoths selected for narrow corolla tubes, and hummingbirds selected for longer corolla tubes. The selection I detected on floral traits through female function was generally stronger than through male function, which runs counter to traditional theory of gender-biased selection. My findings indicate that floral traits can conform to intermediate dimensions between the optima of two pollinators (herkogamy), or appear specialized to one pollinator (tube length). Therefore, cumulative arrangements of floral traits (floral design) can effectively function under pollination by two pollinators that exert different selection pressures on traits.

Orientadores: Marlies Sazima, Paulo Eugênio de Oliveira / Tese (doutorado) - Universidade Estadual de Campinas, Instituto de Biologia / Made available in DSpace on 2018-08-16T21:04:45Z (GMT). No. of bitstreams: 1 Araujo_FranciellePaulinade_D.pdf: 3543401 bytes, checksum: b7273cb58849233b7256545072adbb93 (MD5) Previous issue date: 2010 / Resumo: O estudo da interação entre flores e beija-flores oferece diversas informações a respeito da estruturação das comunidades bem como de processos coevolutivos. Para a região do Cerrado quase não há informações em nível de comunidades sob este enfoque, portanto o presente estudo teve como objetivos obter informações sobre a florística, fenologia e atributos florais das plantas visitadas por beija-flores em diversas fisionomias do Cerrado na Estação Ecológica do Panga, Uberlândia, MG. Além de fornecer estimativas da disponibilidade de néctar e capacidade suporte da área, fornece dados da quantidade de energia que os beija-flores podem encontrar no Cerrado ao longo do ano. O estudo também descreve o comportamento alimentar do beija-flor Phaethornis pretrei, fornecendo dados a respeito do fluxo de pólen proporcionado por este beija-flor. Por fim, este estudo discute aspectos ecológicos como o mimetismo, facilitação e efeito "magnético" em plantas sincronopátricas que compartilham o mesmo polinizador. Foi registrado um total de 46 espécies de plantas que podem ser utilizadas por beija-flores. A diversidade de habitats e espécies que podem ser utilizadas por beija-flores no Cerrado é semelhante à de outros biomas como a Mata Atlântica. Mesmo não tendo grande número de espécies ornitófilas o Cerrado oferece condições propícias para a permanência destas aves. A aparente falta de recursos para beija-flores é compensada com o uso de outras plantas nectaríferas não ornitófilas. O estudo confirmou que Phaethornis pretrei é residente e utiliza 21 espécies de plantas ao longo do ano. Este beija-flor é o visitante exclusivo de duas espécies e o responsável por mais de 90% das visitas em outras quatro. Foi confirmado que P. pretrei é trapliner, retornando sempre às mesmas flores em intervalos regulares. Phaethornis pretrei representa alto potencial de fluxo de pólen para esta comunidade vegetal, pois além de ser vetor de pólen de muitas espécies, transporta grandes quantidades e percorre longas distancias. Neste estudo também foi demonstrado que as espécies Ruellia brevifolia (Pohl) Ezcurra, Geissomeria longiflora Lindl., Dicliptera squarrosa Nees, Cuphea melvilla Lindl e Manettia cordifolia Mart., são sincronopátricas (exibindo sobreposição espacial e em seus períodos de floração), apresentam atributos florais similares e são visitadas principalmente pelo beija-flor Phaethornis pretrei. Análises morfológicas das flores demonstraram que estas espécies diferem na localização dos estames e estigmas, sugerindo que utilizam diferentes partes da cabeça ou bico dos beija-flores para o transporte do pólen. Análises de cargas de pólen retiradas dos beija-flores também demonstraram que há estratificação horizontal da localização do pólen no beija-flor. Este conjunto de espécies pode ser considerado um anel mimético Mülleriano, uma vez que as flores enviam sinais similares para os beija-flores e todas as espécies fornecem néctar, fato que reforça o comportamento de visitação. A floração sincronizada destas espécies é uma resposta coletiva que atrai os polinizadores para o interior da mata por um breve, porém importante período. Esta atração depende não só de uma única espécie de planta, mas da combinação das interações ecológicas como a facilitação, o mimetismo e o efeito magnético destas espécies. / Abstract: The study of the interactions between flowers and hummingbirds offers diverse information regarding the structure of the communities as well as information of coevolutive processes. For the Cerrado region, there is a lack of information on interactions at community level, thus the purpose of this study is to obtain information on floristic composition, phenology and floral attributes of the species visited by hummingbirds in diverse physiognomies of the Cerrado at 'Estação Ecológica do Panga', Uberlândia, MG. Besides providing estimates of nectar availability and carrying capacity of the area, it also gives quantitative data of the amount of energy hummingbirds can find in the Cerrado throughout the year. The study also describes the foraging behaviour of the hummingbird Phaethornis pretrei, and gives information about the pollen flow provided by this hummingbird. Finally, the study discusses ecological aspects such as mimicry, facilitation and "magnet" effect in synchronopatric plants that share the same pollinator. A total of 46 plant species that can be used by hummingbirds was recorded. The diversity of habitats and species that can be used by hummingbirds in the Cerrado is similar to other biomes as the Atlantic Forest. Despite having a low number of ornithophilous species, the Cerrado offers appropriate conditions for the permanence of these birds. The apparent lack of resources for hummingbirds is counterbalanced by the use of other non-ornithophilous nectariferous species. The results of this study confirmed that Phaethornis pretrei is resident and uses 21 plant species throughout the year. This hummingbird species is the exclusive visitor of two species and is responsible for more than 90% of the visits of other four species. It was confirmed that P. pretrei is a trapliner, returning to the same flowers at regular intervals. P. pretrei represents a high potential of pollen transport for this plant community, not only because it carries pollen from many species, but also carries high amounts of it and travels great distances. This study also demonstrated that the species Ruellia brevifolia (Pohl) Ezcurra, Geissomeria longiflora Lindl., Dicliptera squarrosa Nees, Cuphea melvilla Lindl and Manettia cordifolia Mart. are synchronopatric (spatial and flowering overlap), they present similar floral attributes, and they are visited mainly or almost exclusively by the hummingbird Phaethornis pretrei. Morphological analysis of the flowers showed that they differ in the location of the stamens and stiles suggesting that they might use different parts of the hummingbirds' bill or head for pollen transportation, avoiding overlap of pollen placement. The analysis of pollen loads from the hummingbirds also demonstrate a horizontal stratification of pollen placement on the hummingbirds, although some overlap occurred. This group of species can be considered a Mullerian mimicry "ring" as their similar colors send uniform signals to the hummingbirds, and their tubular corollas require similar handling techniques. The synchronized flowering of the studied species is a collective response that attracts pollinators into the forest for a brief but important period. This shift into the forest depends not only on the characteristics of a single plant host species, but rather on a combination of ecological interactions as facilitation, mimicry, and magnet-species effects associated to these species. / Doutorado / Ecologia / Doutor em Ecologia