Promoting Bird Functional Diversity on Landscapes with a Matrix of Planted Eucalyptus spp. in the Atlantic Forest.

Promoting the diversity of biological communities in areas of agricultural production is a very current debate since protected areas may not be sufficient to ensure biodiversity conservation. Among the biological communities affected by the production areas are birds, which show rapid responses to changes in the landscape. Here we seek to understand how landscape planning, concerning its composition and configuration, in areas with a matrix of planted Eucalyptus spp. forests influences the functional diversity of bird assemblages in the Atlantic Forest. Our results show that the spatial distribution design of planted forests in terms of age, land cover and clone types have effects on bird diversity with regard to functional divergence, functional evenness and species richness. These results reinforce the importance of good management for the maintenance of bird diversity. We found that bird functional diversity in planted forest matrices increased with the proximity index, proportion of native vegetation and age importance value, and is negatively influenced by edge density and proportion of forest plantation. For bird conservation, it is thus better to associate Eucalyptus spp. with other cover types in the landscape. These results corroborate that, to increase bird functional diversity, it is possible to associate conservation and production in the same landscape. Mosaic landscapes have great potential to contribute to the conservation of bird biodiversity outside protected areas. However, decisions regarding the management of planted forests and planning of improved areas intended for conservation seem to be decisive to ensure the maintenance of bird biodiversity.

Atlantic flower-invertebrate interactions: A data set of occurrence and frequency of floral visits.

Encounters between flowers and invertebrates are key events for the functioning of tropical forests. Assessing the structure of networks composed of the interactions between those partners leads to a better understanding of ecosystem functioning and the effects of environmental factors on ecological processes. Gathering such data is, however, costly and time-consuming, especially in the highly diverse tropics. We aimed to provide a comprehensive repository of available flower-invertebrate interaction information for the Atlantic Forest, a South American tropical forest domain. Data were obtained from published works and "gray literature," such as theses and dissertations, as well as self-reports by co-authors. The data set has ~18,000 interaction records forming 482 networks, each containing between one and 1061 interaction links. Each network was sampled for about 200 h or less, with few exceptions. A total of 641 plant genera within 136 different families and 39 orders were reported, with the most abundant and rich families being Asteraceae, Fabaceae, and Rubiaceae. Invertebrates interacting with these plants were all arthropods from 10 orders, 129 families, and 581 genera, comprising 2419 morphotypes (including 988 named species). Hymenoptera was the most abundant and diverse order, with at least six times more records than the second-ranked order (Lepidoptera). The complete data set shows Hymenoptera interacting with all plant orders and also shows Diptera, Lepidoptera, Coleoptera, and Hemiptera to be important nodes. Among plants, Asterales and Fabales had the highest number of interactions. The best sampled environment was forest (~8000 records), followed by pastures and crops. Savanna, grasslands, and urban environments (among others) were also reported, indicating a wide range of approaches dedicated to collecting flower-invertebrate interaction data in the Atlantic Forest domain. Nevertheless, most reported data were from forest understory or lower strata, indicating a knowledge gap about flower-invertebrate interactions at the canopy. Also, access to remote regions remains a limitation, generating sampling bias across the geographical range of the Atlantic Forest. Future studies in these continuous and hard-to-access forested areas will yield important new information regarding the interactions between flowers and invertebrates in the Atlantic Forest. There are no copyright restrictions on the data set. Please cite this data paper if the data are used in publications and teaching events.

Vertical stratification of insect abundance and species richness in an Amazonian tropical forest.

Tropical forests are among the most biodiverse biomes on the planet. Nevertheless, quantifying the abundance and species richness within megadiverse groups is a significant challenge. We designed a study to address this challenge by documenting the variability of the insect fauna across a vertical canopy gradient in a Central Amazonian tropical forest. Insects were sampled over two weeks using 6-m Gressitt-style Malaise traps set at five heights (0 m-32 m-8 m intervals) on a metal tower in a tropical forest north of Manaus, Brazil. The traps contained 37,778 specimens of 18 orders of insects. Using simulation approaches and nonparametric analyses, we interpreted the abundance and richness of insects along this gradient. Diptera, Hymenoptera, and Coleoptera had their greatest abundance at the ground level, whereas Lepidoptera and Hemiptera were more abundant in the upper levels of the canopy. We identified species of 38 of the 56 families of Diptera, finding that 527 out of 856 species (61.6%) were not sampled at the ground level. Mycetophilidae, Tipulidae, and Phoridae were significantly more diverse and/or abundant at the ground level, while Tachinidae, Dolichopodidae, and Lauxaniidae were more diverse or abundant at upper levels. Our study suggests the need for a careful discussion of strategies of tropical forest conservation based on a much more complete understanding of the three-dimensional distribution of its insect diversity.

ATLANTIC POLLINATION: a data set of flowers and interaction with nectar-feeding vertebrates from the Atlantic Forest.

Flowering plant species and their nectar-feeding vertebrates exemplify some of the most remarkable biotic interactions in the Neotropics. In the Brazilian Atlantic Forest, several species of birds (especially hummingbirds), bats, and non-flying mammals, as well as one lizard feed on nectar, often act as pollinators and contribute to seed output of flowering plants. We present a dataset containing information on flowering plants visited by nectar-feeding vertebrates and sampled at 166 localities in the Brazilian Atlantic Forest. This dataset provides information on 1902 unique interactions among 515 species of flowering plants and 129 species of potential vertebrate pollinators and the patterns of species diversity across latitudes. All plant-vertebrate interactions compiled were recorded through direct observations of visits, and no inferences of pollinators based on floral syndromes were included. We also provide information on the most common plant traits used to understand the interactions between flowers and nectar-feeding vertebrates: plant growth form, corolla length, rate of nectar production per hour in bagged flowers, nectar concentration, flower color and shape, time of anthesis, presence or absence of perceptible fragrance by human, and flowering phenology as well as the plant's threat status by International Union for Conservation of Nature (IUCN) classification. For the vertebrates, status of threat by IUCN classification, body mass, bill or rostrum size are provided. Information on the frequency of visits and pollen deposition on the vertebrate's body is provided from the original source when available. The highest number of unique interactions is recorded for birds (1771) followed by bats (110). For plants, Bromeliaceae contains the highest number of unique interactions (606), followed by Fabaceae (242) and Gesneriaceae (104). It is evident that there was geographical bias of the studies throughout the southeast of the Brazilian Atlantic Forest and that most effort was directed to flower-hummingbird interactions. However, it reflects a worldwide tendency of more plants interacting with birds compared with other vertebrate species. The lack of similar protocols among studies to collect basic data limits the comparisons among areas and generalizations. Nevertheless, this dataset represents a notable effort to organize and highlight the importance of vertebrate pollinators in this hotspot of biodiversity on Earth and represents the data currently available. No copyright or proprietary restrictions are associated with the use of this data set. Please cite this data paper when the data are used in publications or scientific events.

Negative impacts of dominance on bee communities: Does the influence of invasive honey bees differ from native bees?

Invasive species can reach high abundances and dominate native environments. One of the most impressive examples of ecological invasions is the spread of the African subspecies of the honey bee throughout the Americas, starting from its introduction in a single locality in Brazil. The invasive honey bee is expected to more negatively impact bee community abundance and diversity than native dominant species, but this has not been tested previously. We developed a comprehensive and systematic bee sampling scheme, using a protocol deploying 11,520 pan traps across regions and crops for three years in Brazil. We found that invasive honey bees are now the single most dominant bee species. Such dominance has not only negative consequences for abundance and species richness of native bees but also for overall bee abundance (i.e., strong "numerical" effects of honey bees). Contrary to expectations, honey bees did not have stronger negative impacts than other native bees achieving similar levels of dominance (i.e., lack of negative "identity" effects of honey bees). These effects were markedly consistent across crop species, seasons and years, and were independent from land-use effects. Dominance could be a proxy of bee community degradation and more generally of the severity of ecological invasions.

Forest and connectivity loss simplify tropical pollination networks.

Mutualistic interactions between plants and pollinators play an essential role in the organization and persistence of biodiversity. The structure of interaction networks mediates the resilience of local communities and ecosystem functioning to environmental changes. Hence, network structure conservation may be more critical for maintaining biodiversity and ecological services than the preservation of isolated species in changing landscapes. Here, we intensively surveyed seven 36 km2 landscapes to empirically investigate the effects of forest loss and landscape configuration on the structure of plant-pollinator networks in understory vegetation of Brazilian Atlantic Forest. Our results indicate that forest loss and isolation affect the structure of the plant-pollinator networks, which were smaller in deforested landscapes, and less specialized as patch isolation increased. Lower nestedness and degree of specialization (H'2) indicated that the remaining plant and bee species tend to be generalists, and many of the expected specialized interactions in the network were already lost. Because generalist species generate a cohesive interaction core in these networks, these simplified networks might be resistant to loss of peripheral species, but may be susceptible to the extinction of the most generalist species. We suggest that such a network pattern is an outcome of landscapes with a few remaining isolated patches of natural habitat. Our results add a new perspective to studies of plant-pollinator networks in fragmented landscapes, showing that those interaction networks might also be used to indicate how changes in natural habitat affect biodiversity and biotic interactions.

Impacts of deforestation on plant-pollinator networks assessed using an agent based model.

Plant-pollinator networks have been widely used to understand the ecology of mutualistic interactions between plants and animals. While a number of general patterns have been identified, the mechanisms underlying the structure of plant-pollinator networks are poorly understood. Here we present an agent based model (ABM) that simulates the movement of bees over heterogeneous landscapes and captures pollination events, enabling the influence of landscape pattern on pollination networks to be explored. Using the model, we conducted a series of experiments using virtual landscapes representing a gradient of forest loss and fragmentation. The ABM was able to produce expected trends in network structure, from simulations of interactions between individual plants and pollinators. For example, results indicated an increase in the index of complementary specialization (H2') and a decline in network connectance with increasing forest cover. Furthermore, network nestedness was not associated with the degree of forest cover, but was positively related to forest patch size, further supporting results obtained in the field. This illustrates the potential value of ABMs for exploring the structure and dynamics of plant-pollinator networks, and for understanding the mechanisms that underlie them. We attribute the results obtained primarily to a shift from specialist to generalist pollinators with increasing forest loss, a trend that has been observed in some field situations.

Influence of landscape structure on Euglossini composition in open vegetation environments / Influência da estrutura da paisagem na composição de Euglossini em ambientes com vegetação aberta

Abstract The fauna of Euglossini bees is poorly known in savanna regions, making it difficult to understand how these bees use open vegetation environments. The aim of this study was to evaluate the influence of landscape structure on species abundance and composition of Euglossini bees in naturally heterogeneous savanna landscapes. Nine sites were sampled monthly using six traps with chemical baits. Three aromatic essences (eucalyptol, methyl salicylate and vanillin) were used to attract the Euglossini. Surrounding environmental conditions were measured using three independent variables, calculated in multiple scales: index of local vegetation and two landscape indices (Shannon Diversity and area-weighted shape). We compared the competing hypotheses through model selection based on Second-order Akaike Information Criterion (AICc). The four competing hypothesis were: (1) The local vegetation complexity favors Euglossini bees species richness and/or abundance (local vegetation hypothesis); (2) The proportion of the native vegetation types favors Euglossini bees species richness and/or abundance (habitat amount hypothesis); (3) Higher landscape diversity shall increase species richness of Euglossini bees (landscape heterogeneity hypothesis); (4) More complex landscape configuration shall favor the Euglossini bees richness and/or abundance (landscape heterogeneity hypothesis). We sampled 647 individuals belonging to six species of two distinct genera. Our results support the habitat amount hypothesis since bees’ abundance was strongly related with the proportion of habitat in the surrounding landscape. This may be related to the availability of floral and nesting resources in some types of savanna vegetation.

Resumo A fauna das abelhas da tribo Euglossini é pouco conhecida em regiões de savana, tornando difícil a compreensão de como essas abelhas usam ambientes com vegetação aberta. O objetivo desse estudo foi avaliar a influência da estrutura da paisagem na abundância e composição de espécies de abelhas Euglossini em paisagens naturalmente heterogêneas de savana. Nove locais foram amostrados mensalmente utilizando seis armadilhas com iscas químicas. As essências eucaliptol, salicilato de metila e vanilina foram utilizadas para atrair os machos de Euglossini. As condições ambientais foram medidas usando três variáveis, calculadas em múltiplas escalas: índice de vegetação local e dois índices de paisagem (diversidade de Shannon e o índice de forma ponderado pela área). Através da seleção de modelos baseada no critério de informação de Akaike de segunda ordem (AICc) comparamos as hipóteses alternativas: (1) Vegetação local mais complexa favorece as abelhas Euglossini (hipótese da vegetação local); (2) A proporção dos tipos de vegetação nativas favorece as abelhas Euglossini (hipótese da quantidade habitat); (3) A diversidade da paisagem favorece a riqueza de espécies de abelhas Euglossini (hipótese da heterogeneidade da paisagem); (4) Configuração mais complexa da paisagem favorece a riqueza e/ou abundância de abelhas Euglossini (hipótese da heterogeneidade paisagem). Nós amostramos 647 indivíduos pertencentes a seis espécies de dois gêneros distintos. Nossos resultados apoiam a hipótese de quantidade de habitat já que a abundância das abelhas foi fortemente relacionada com a proporção de habitat nas paisagens circundantes. Esses resultados podem estar relacionados com a disponibilidade de recursos florais e substratos para nidificação em alguns tipos de savana.

Spatial heterogeneity regulates plant-pollinator networks across multiple landscape scales.

Mutualistic plant-pollinator interactions play a key role in biodiversity conservation and ecosystem functioning. In a community, the combination of these interactions can generate emergent properties, e.g., robustness and resilience to disturbances such as fluctuations in populations and extinctions. Given that these systems are hierarchical and complex, environmental changes must have multiple levels of influence. In addition, changes in habitat quality and in the landscape structure are important threats to plants, pollinators and their interactions. However, despite the importance of these phenomena for the understanding of biological systems, as well as for conservation and management strategies, few studies have empirically evaluated these effects at the network level. Therefore, the objective of this study was to investigate the influence of local conditions and landscape structure at multiple scales on the characteristics of plant-pollinator networks. This study was conducted in agri-natural lands in Chapada Diamantina, Bahia, Brazil. Pollinators were collected in 27 sampling units distributed orthogonally along a gradient of proportion of agriculture and landscape diversity. The Akaike information criterion was used to select models that best fit the metrics for network characteristics, comparing four hypotheses represented by a set of a priori candidate models with specific combinations of the proportion of agriculture, the average shape of the landscape elements, the diversity of the landscape and the structure of local vegetation. The results indicate that a reduction of habitat quality and landscape heterogeneity can cause species loss and decrease of networks nestedness. These structural changes can reduce robustness and resilience of plant-pollinator networks what compromises the reproductive success of plants, the maintenance of biodiversity and the pollination service stability. We also discuss the possible explanations for these relationships and the implications for landscape planning in agricultural areas.

Assessing the utility of statistical adjustments for imperfect detection in tropical conservation science.

1. In recent years, there has been a fast development of models that adjust for imperfect detection. These models have revolutionized the analysis of field data, and their use has repeatedly demonstrated the importance of sampling design and data quality. There are, however, several practical limitations associated with the use of detectability models which restrict their relevance to tropical conservation science. 2. We outline the main advantages of detectability models, before examining their limitations associated with their applicability to the analysis of tropical communities, rare species and large-scale data sets. Finally, we discuss whether detection probability needs to be controlled before and/or after data collection. 3. Models that adjust for imperfect detection allow ecologists to assess data quality by estimating uncertainty and to obtain adjusted ecological estimates of populations and communities. Importantly, these models have allowed informed decisions to be made about the conservation and management of target species. 4. Data requirements for obtaining unadjusted estimates are substantially lower than for detectability-adjusted estimates, which require relatively high detection/recapture probabilities and a number of repeated surveys at each location. These requirements can be difficult to meet in large-scale environmental studies where high levels of spatial replication are needed, or in the tropics where communities are composed of many naturally rare species. However, while imperfect detection can only be adjusted statistically, covariates of detection probability can also be controlled through study design. Using three study cases where we controlled for covariates of detection probability through sampling design, we show that the variation in unadjusted ecological estimates from nearly 100 species was qualitatively the same as that obtained from adjusted estimates. Finally, we discuss that the decision as to whether one should control for covariates of detection probability through study design or statistical analyses should be dependent on study objectives. 5.Synthesis and applications. Models that adjust for imperfect detection are an important part of an ecologist's toolkit, but they should not be uniformly adopted in all studies. Ecologists should never let the constraints of models dictate which questions should be pursued or how the data should be analysed, and detectability models are no exception. We argue for pluralism in scientific methods, particularly where cost-effective applied ecological science is needed to inform conservation policy at a range of different scales and in many different systems.

Singing in the rain forest: how a tropical bird song transfers information.

How information transmission processes between individuals are shaped by natural selection is a key question for the understanding of the evolution of acoustic communication systems. Environmental acoustics predict that signal structure will differ depending on general features of the habitat. Social features, like individual spacing and mating behavior, may also be important for the design of communication. Here we present the first experimental study investigating how a tropical rainforest bird, the white-browed warbler Basileuterus leucoblepharus, extracts various information from a received song: species-specific identity, individual identity and location of the sender. Species-specific information is encoded in a resistant acoustic feature and is thus a public signal helping males to reach a wide audience. Conversely, individual identity is supported by song features susceptible to propagation: this private signal is reserved for neighbors. Finally, the receivers can locate the singers by using propagation-induced song modifications. Thus, this communication system is well matched to the acoustic constraints of the rain forest and to the ecological requirements of the species. Our results emphasize that, in a constraining acoustic environment, the efficiency of a sound communication system results from a coding/decoding process particularly well tuned to the acoustic properties of this environment.

Efficiency of playback for assessing the occurrence of five bird species in Brazilian Atlantic Forest fragments.

Playback of bird songs is a useful technique for species detection; however, this method is usually not standardized. We tested playback efficiency for five Atlantic Forest birds (White-browed Warbler Basileuterus leucoblepharus, Giant Antshrike Batara cinerea, Swallow-tailed Manakin Chiroxiphia caudata, Whiteshouldered Fire-eye Pyriglena leucoptera and Surucua Trogon Trogon surrucura) for different time of the day, season of the year and species abundance at the Morro Grande Forest Reserve (South-eastern Brazil) and at thirteen forest fragments in a nearby landscape. Vocalizations were broadcasted monthly at sunrise, noon and sunset, during one year. For B. leucoblepharus, C. caudata and T. surrucura, sunrise and noon were more efficient than sunset. Batara cinerea presented higher efficiency from July to October. Playback expanded the favourable period for avifaunal surveys in tropical forest, usually restricted to early morning in the breeding season. The playback was efficient in detecting the presence of all species when the abundance was not too low. But only B. leucoblepharus and T. surrucura showed abundance values significantly related to this efficiency. The present study provided a precise indication of the best daily and seasonal periods and a confidence interval to maximize the efficiency of playback to detect the occurrence of these forest species.

Efficiency of playback for assessing the occurrence of five bird species in Brazilian Atlantic Forest fragments

Playback of bird songs is a useful technique for species detection; however, this method is usually not standardized. We tested playback efficiency for five Atlantic Forest birds (White-browed Warbler Basileuterus leucoblepharus, Giant Antshrike Batara cinerea, Swallow-tailed Manakin Chiroxiphia caudata, Whiteshouldered Fire-eye Pyriglena leucoptera and Surucua Trogon Trogon surrucura) for different time of the day, season of the year and species abundance at the Morro Grande Forest Reserve (South-eastern Brazil) and at thirteen forest fragments in a nearby landscape. Vocalizations were broadcasted monthly at sunrise, noon and sunset, during one year. For B. leucoblepharus, C. caudata and T. surrucura, sunrise and noon were more efficient than sunset. Batara cinerea presented higher efficiency from July to October. Playback expanded the favourable period for avifaunal surveys in tropical forest, usually restricted to early morning in the breeding season. The playback was efficient in detecting the presence of all species when the abundance was not too low. But only B. leucoblepharus and T. surrucura showed abundance values significantly related to this efficiency. The present study provided a precise indication of the best daily and seasonal periods and a confidence interval to maximize the efficiency of playback to detect the occurrence of these forest species.

A técnica de play-back é muito útil para a detecção de aves, mas este método geralmente não é padronizado. Sua eficiência em atestar a ocorrência de cinco espécies de aves da Mata Atlântica (Pula-pula-assobiador Basileuterus leucoblepharus, Batará Batara cinerea, Tangará Chiroxiphia caudata, Olho-de-fogo Pyriglena leucoptera e Surucuá-de-barriga-vermelha Trogon surrucura) foi analisada de acordo com o horário do dia, estação do ano e abundância das espécies na Reserva Florestal do Morro Grande (São Paulo, Brasil) e em treze fragmentos florestais de uma paisagem adjacente. Gravações das vocalizações foram emitidas mensalmente ao amanhecer, meio do dia e entardecer, durante um ano. Para B. leucoblepharus, C. caudata e T. surrucura, o amanhecer e o meio do dia apresentaram-se mais eficientes que o entardecer. Batara cinerea apresentou maior eficiência de julho a outubro. O uso do play-back aumentou o período de maior eficiência dos levantamentos de aves em matas tropicais, comumente restrito ao período da manhã durante a estação reprodutiva. A técnica utilizada foi eficiente na detecção da ocorrência de todas as espécies, salvo quando sua abundância se apresentou muito baixa. Porém, apenas B. leucoblepharus e T. surrucura apresentaram abundância significativa e positivamente relacionada com essa eficiência. O presente estudo proporciona uma indicação precisa sobre o melhor horário do dia e época do ano, assim como um intervalo de confiança, com o intuito de aumentar a eficiência do play-back em detectar a ocorrência dessas espécies.