Andréa Cardoso Araujo

Specialization in Plant-Hummingbird Networks Is Associated with Species Richness, Contemporary Precipitation and Quaternary Climate-Change Velocity

Large-scale geographical patterns of biotic specialization and the underlying drivers are poorly understood, but it is widely believed that climate plays an important role in determining specialization. As climate-driven range dynamics should diminish local adaptations and favor generalization, one hypothesis is that contemporary biotic specialization is determined by the degree of past climatic instability, primarily Quaternary climate-change velocity. Other prominent hypotheses predict that either contemporary climate or species richness affect biotic specialization. To gain insight into geographical patterns of contemporary biotic specialization and its drivers, we use network analysis to determine the degree of specialization in plant-hummingbird mutualistic networks sampled at 31 localities, spanning a wide range of climate regimes across the Americas. We found greater biotic specialization at lower latitudes, with latitude explaining 20–22% of the spatial variation in plant-hummingbird specialization. Potential drivers of specialization - contemporary climate, Quaternary climate-change velocity, and species richness - had superior explanatory power, together explaining 53–64% of the variation in specialization. Notably, our data provides empirical evidence for the hypothesized roles of species richness, contemporary precipitation and Quaternary climate-change velocity as key predictors of biotic specialization, whereas contemporary temperature and seasonality seem unimportant in determining specialization. These results suggest that both ecological and evolutionary processes at Quaternary time scales can be important in driving large-scale geographical patterns of contemporary biotic specialization, at least for co-evolved systems such as plant-hummingbird networks.

Spatial organization of a bromeliad community in the Atlantic rainforest, south-eastern Brazil

The habit, shade-tolerance and dispersal agent of 19 bromeliad species were studied in a rainforest community in order to relate specific traits to the spatial occurrence of the species. Highest density was found in riparian forest (RF), followed by restinga scrub (RE), rocky shore (RS) and dense canopy forest (DF). Terrestrial bromeliads occurred in open sites (RE and RS), epiphytes were absent in RS and facultative species occupied all four habitats. Bird-dispersed bromeliads occurred in the upper canopy, whereas those dispersed by mammals were low in the forest profile. Bromeliads which are dispersed by similar fauna fruit sequentially through the year. Differences in traits may allow the sharing of habitats and strata among species.

The assemblage of flowers visited by hummingbirds in the "capões" of Southern Pantanal, Mato Grosso do Sul, Brazil

Summary Flower species visited by hummingbirds were studied over 13 months in 52 forested patches (“capoes”) in the seasonally flooded plains of Southern Pantanal, western Brazil. The size of the surveyed capoes ranged from 0.2 to 3.8 ha and the total sampled area measured 51.6 ha. We recorded 21 plant species, mainly herbs and climbers, whose flowers were visited by hummingbirds. Most of these plant species are regarded as non-ornithophilous (71.4%). The flowering peaks of the hummingbird-visited plants occurred at the end of the dry season and during the rainy season. The density of ornithophilous and non-ornithophilous flowers was higher during the rainy season and the dry season, respectively. Helicteres guazumaefolia is the most frequent ornithophilous species, bearing flowers throughout the year. Four hummingbird species were observed in the capoes. Their mean visiting rates for ornithophilous flowers (x = 0.019 ± 0.01 visits.min −1 .number of flowers −1 ) did not differ (P = 0.09, Kruskal-Wallis) from those for non-ornithophilous flowers (x = 0.025 ± 0.06 visits.min −1 .number of flowers −1 ). The most frequent visitor, Hylocharis chrysura was the only hummingbird recorded every month. It visited 20 plant species, 75% of which were non-ornithophilous, and seems to be the major pollinating bird in the capoes. The availability of H. guazumaefolia flowers throughout the year may favor the residence of this hummingbird in the study area.

Distyly and sequential pollinators of Psychotria nuda (Rubiaceae) in the Atlantic rain forest, Brazil

Abstract.Reciprocal herkogamy is known to promote intermorph-pollination in distylous species, which are generally self- and intramorph-incompatible. Legitimate crossing rates are also influenced by pollinator foraging strategy, which determines most of the pollen flow in natural populations. This study reports on the floral morphology, compatibility relations and pollination biology of Psychotria nuda (Cham. and Schltdl.) Wawra in the Atlantic rain forest, southeastern Brazil, based on floral measurements, hand-pollination experiments and focal observation of floral visitors. It was found that P. nuda does not present an exactly reciprocal herkogamy, however, this morphological trait in P. nuda is as good as in most of Rubiaceae. Reproductive experiments showed compatibility relations similar to those frequently observed in distylous species. The hummingbirds Ramphodon naevius and females of Thalurania glaucopis were the main pollinators of P. nuda, presenting the traplining foraging strategy, which seems to maximize intermorph crosses in P. nuda flowers. These hummingbirds pollinated P. nuda flowers sequentially throughout the flowering period.Reciprocal herkogamy is known to promote intermorph-pollination in distylous species, which are generally self- and intramorph-incompatible. Legitimate crossing rates are also influenced by pollinator foraging strategy, which determines most of the pollen flow in natural populations. This study reports on the floral morphology, compatibility relations and pollination biology of Psychotria nuda (Cham. and Schltdl.) Wawra in the Atlantic rain forest, southeastern Brazil, based on floral measurements, hand-pollination experiments and focal observation of floral visitors. It was found that P. nuda does not present an exactly reciprocal herkogamy, however, this morphological trait in P. nuda is as good as in most of Rubiaceae. Reproductive experiments showed compatibility relations similar to those frequently observed in distylous species. The hummingbirds Ramphodon naevius and females of Thalurania glaucopis were the main pollinators of P. nuda, presenting the traplining foraging strategy, which seems to maximize intermorph crosses in P. nuda flowers. These hummingbirds pollinated P. nuda flowers sequentially throughout the flowering period.

Pollen Analysis Reveals Plants Foraged by Africanized Honeybees in the Southern Pantanal, Brazil

The pollen diet of Africanized honeybees Apis mellifera L. was studied during seven months (October 2006 to April 2007) in a natural forest fragment in the southern Pantanal, sub-region of Abobral, Mato Grosso do Sul. The analysis of the pollen diet was based on direct observations of the bees visiting flowers as well as through the use of a pollen trap installed in a wild colony in a tree hole in the same forest fragment. The total of 28 species in 15 botanical families were observed as potential sources of pollen for A. mellifera, with visits registered in 24 of these species in 13 botanical families. In the pollen trap we recorded 25 pollen types. This study is the first report to use this type of trap for pollen collection in the Neotropical region and aimed to identify the polliniferous bee plants of Brazilian Pantanal.

Flowering phenology and pollination of ornithophilous species in two habitats of Serra da Bodoquena, Mato Grosso do Sul, Brazil

The aim of this study is to describe interactions between hummingbirds and ornithophilous species at Serra da Bodoquena in midwest Brazil, with focus on flowering phenology and pollination of these plant species. In two habitats, gallery forest and semi-deciduous forest, data on flowering phenology of ornithophilous species were collected monthly over 14 months. In addition, data on morphology and floral biology, as well as visitor frequency and hummingbird behavior, were recorded. The studied community contained eight ornithophilous plant species and six hummingbird species. The ornithophilous species flowered throughout the year, and the greatest abundance of flowers was at the end of the rainy season and the beginning of the dry one. The herit huingbird Phaethornis pretrei and feales of Thalurania furcata, were the most similar in floral resource use. Acanthaceae is the most representative family of ornithophilous plant species in Serra da Bodoquena and, thus, represents the main food source for hummingbirds. Ruellia angustiflora is especially important because it flowers continuously throughout the year and is a significant food resource for P. pretrei, which is the main visitor for this plant guild.

Pollination biology and reproduction of Seemannia sylvatica (Kunth) Hanstein(Gesneriaceae) in the Serra da Bodoquena National Park, Mato Grosso do Sul

In Brazil, the family Gesneriaceae is represented by 23 genera and approximately 200 species. Seemannia sylvatica is an herb that occurs in dense populations in the riverbeds at Serra da Bodoquena. Goals of this study were to report the floral biology (on the first five days of anthesis), as well as to determine the breeding system and the pollinators of S. sylvatica. Data collection was conducted from June 2005 to July 2006 through monthly field trips, lasting for five days. Data on floral biology, breeding system and on the floral visitors were taken from individuals located along a track 2500 m long, in riparian forest of Salobrinha river. Flowers of S. sylvatica are tubular, red, with no perceptive odor and lasted more than five days (ca. 10 - 20 days in individuals transferred to an urban garden and kept in vases). Seemania sylvatica is protandrous, and the male phase occurred between the first and the fourth days of anthesis, while the female one started in the fifth day. Mean nectar volume secreted was 4.77 ± 3.2 µl, with a significative variation among flowers of different ages. Otherwise, nectar concentration average was 9.71 ± 4.41%, and did not varied significantly in flowers of different ages. The flowers of S. sylvatica were pollinated mainly by the hummingbirds Phaethornis pretrei and Thalurania furcata, and pierced by the bee Ceratina chloris. The butterfly Parides anchises orbygnianus was considered an occasional pollinator of these flowers. Seemannia sylvatica is self-compatible, since fruit set occurred on the experiments of spontaneous self-pollination, manual self-pollination, cross-pollination and open pollination (control). The protandry, coupled with the pattern of nectar production, characterized by low volume and solute concentration, which induces the pollinators to visit different flowers in a given circuit foraging, act maximizing the likelihood of cross-pollination in S. sylvatica. Moreover, the high proportion of fruit set by autogamy is an important strategy considering that S. sylvatica is visited by few species, being pollinated mainly by P. pretrei. Therefore, in the absence of these visitors, the formation of fruits may be achieved.

Bees (Hymenoptera: Apoidea) and flowers in natural forest patches of southern Pantanal

This is the first systematic survey of bees in the Pantanal wetland, Brazil. We recorded bee species and their floral resources within grassland and natural forest edge habitats in the Pantanal. Surveys were conducted during two to four-days per month, for a total of 12 months. Overall, we recorded 56 bee species visiting a total of 63 flowering plants. Asteraceae and Fabaceae presented the highest number of visited species, however Hyptis suaveolens (Lamiaceae) was the plant most visited by different bee species (18). The most generalist native bee was Trigona fuscipennis visiting a total of 17 flowering plant species. Apis mellifera, an exotic bee, visited 27 species. We also report the overlap (37.5%) in the use of floral resources between the exotic bee Apis mellifera and native bee species. Our updated bee checklist here presented includes 10 new records for the State of Mato Grosso do Sul. These data will support management strategies targeting the conservation of plant-pollinator interactions in the Pantanal ecosystem.

Flowers visited by hummingbirds in an urban Cerrado fragment, Mato Grosso do Sul, Brazil

Hummingbirds are the main vertebrate pollinators in the Neotropics, but little is known about the interactions between hummingbirds and flowers in areas of Cerrado. This paper aims to describe the interactions between flowering plants (ornithophilous and non-ornithophilous species) and hummingbirds in an urban Cerrado remnant. For this purpose, we investigated which plant species are visited by hummingbirds, which hummingbird species occur in the area, their visiting frequency and behavior, their role as legitimate or illegitimate visitors, as well as the number of agonistic interactions among these visitors. Sampling was conducted throughout 18 months along a track located in an urban fragment of Cerrado vegetation in Campo Grande, Mato Grosso do Sul, Brasil. We found 15 species of plants visited by seven species of hummingbirds. The main habit for ornithophilous species was herbaceous, with the predominance of Bromeliaceae; among non-ornithophilous most species were trees from the families Vochysiaceae and Malvaceae. Hylocharis chrysura was the hummingbird that visited the largest number of plant species and also attended the greater number of agonistic events. The high proportion (66.7%) of non-ornithophilous species visited by hummingbirds in the present study was similar to that found in other communities analyzed in Brazil. The fact that ornithophilous species in the area does not offer resources continuously throughout the year should induce hummingbirds to search for alternative resources, and contribute to the high proportion of non-ornithophilous species visited. In general, the floral form was not a barrier to floral visits by hummingbirds, although morphological characteristics of flowers from some plant species may be restrictive. Tabebuia aurea, for example, presents flowers with long corollas, hindering the access to floral resources by the pollinators, what may favor the occurrence of illegitimate visits by hummingbirds. Despite of being a small fragment of Cerrado vegetation, the studied remnant can be considered an important refuge, sheltering a great richness of hummingbird species comparable to several forested areas in Brazil.

Bat and bee pollination in Psittacanthus mistletoes, a genus regarded as exclusively hummingbird‐pollinated

Mistletoes are aerial parasitic plants of the sandalwood order (Santalales), composed of ~1,500–1,600 species worldwide (Nickrent et al. 2010). Some temperate European and North-American species are folkloric and mystic, but the beauty of colors and the variety of forms are almost exclusively found in the tropical species in South and Central Americas, Africa, Australia, and New Zealand. Loranthaceae, the showy mistletoes, is the largest family on these continents. Within it, Psittacanthus is one of the most spectacular and species-rich genus (~119 species), occurring from Baja California, Mexico to northern Argentina (Kuijt 2009). The large radiation of species within Psittacanthus has been related to interactions with birds, as the genus is regarded as entirely hummingbird-pollinated and bird-dispersed (Restrepo et al. 2002, Vidal-Russell and Nickrent 2008). Nonetheless, while studying the pollination of Psittacanthus species in the Brazilian Pantanal and Amazon, we found P. acinarius and P. eucalyptifolius to be batand bee-pollinated, respectively (Fig. 1). Flower characteristics of these species do not provide cues for hummingbird pollination, such as a narrow and long tubular corolla, absence of odor, and a combination of red, yellow, and orange colors. Instead, P. acinarius has brush flowers that exhale an unpleasant odor and are inconspicuously greenish and P. eucalyptifolius has curved buds and slightly zygomorphic flowers, sweetly scented and vividly yellow. Based on these floral traits, bat pollination in P. acinariuswas previously assumed by Araujo and Sazima (2003) and suspected by Kuijt (2009), who also pointed out the potential of bat pollination in P. macrantherus and insect pollination in P. eucalyptifolius. Throughout several years of continuous fieldwork in the region of Pantanal of Miranda (19°340 S; 57°000 W), we found P. acinarius individuals flowering yearly from January to August (Araujo and Sazima 2003). Each plant produced ~1–10 inflorescences and 10–150 buds in total, and opened 1–20 flowers per night. Because its buds and pedicels are thicker, inflorescences are stronger than those of other Psittacanthus species that are pollinated by hummingbirds. P. acinarius flowers open at early evening (18:30–19:00) when the six petals (60 mm length) separate, exposing the central style (55 mm length) with a simple stigma. One stamen is attached to each petal, so the six anthers are peripheral and introrse (dehiscence facing inward). These traits contrast with hummingbird-pollinated Psittacanthus species whose petals often curl in open flowers and stamens are central with extrorse anthers (facing outward). On April 27, 2000, between 19:00 and 20:00, we extracted an average of 15.2 lL of nectar with a mean sugar concentration of 16.5% from each of four flowers of different P. acinarius individuals. This is a sugar concentration expected for bat-pollinated flowers in the Neotropics (Ornelas et al. 2007). On three P. acinarius individuals, we observed (on different nights, 21 h total) short hovering visits (<1 s; n = 118) by small bats throughout the night and, at the beginning of anthesis, longer perching visits (>1 s; n = 5) by large bats. On other nights, we mist-netted bats nearby these plants and captured the nectar-feeding bats Glossophaga soricina (14 g) and Phyllostomus discolor (34 g), which typically hover and perch, respectively, when visiting flowers (Fischer 1992). On two further occasions, we programed a camera to take one picture per minute throughout the night focused on P. acinarius flowers, and recorded visits of G. soricina (Fig. 1; see also Fischer et al. 2013: Fig. 2b). To drink nectar, both bat species inserted the head into the flower and contacted anthers and stigma with their anterior parts (head, neck, thorax, and shoulders). Furthermore, pollen of P. acinarius has been found in feces of G. soricina and P. discolor, as well as of Platyrrhinus lineatus, Carollia perspicillata, and Phyllostomus