Marco Tschapka’s research while affiliated with Smithsonian Tropical Research Institute and other places

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Publications (205)


Comparative community ecology reveals conserved ectoparasite microbiomes amidst variable host and environment microbiomes
  • Preprint

September 2024

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47 Reads

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Luis Víquez Rodríguez

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Winifred Frick

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[...]

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Susan Perkins

Histogram of silvicultural management intensity index (SMI) across the three regions. Minimum SMI: 0.002, 1st quartile: 0.130, median: 0.210, 3rd quartile: 0.318, maximum: 0.602. The integrated table highlights differences in the proportion of intensively and extensively managed forests between the study plots and forest stands at the national level (BMEL, 2014).
The hypothesized conceptual framework, assuming that silvicultural management intensity indirectly affects acoustic diversity via its effects on forest features and bird species richness and abundance. (1) Direct effect of silvicultural management intensity (SMI) on forest features. (2) Direct effect of forest features on birds. (3) Direct effect of birds on acoustic diversity.
Fitted effects on diurnal and monthly ADI patterns and the influence of SMI (silvicultural management intensity), based on model 1 ( Table 3 ), using “exploration region” as a random factor. Values for this graph were fitted using the Hainich-Dün region as an example. Dark blue line: fitted values for the minimum of the SMI distribution (0.002), light blue line: 1st quartile of the SMI distribution (0.13), light red line: 3rd quartile of the SMI distribution (0.32), and dark red line: maximum of the SMI distribution (0.6). ToD: Time of the day. Vertical lines show the times of sunrise and sunset on the 15th of each month in the Hainich-Dün region (central region).
Structural equation model for direct effects of bird species richness and abundance (mean across 2008 – 2012), as well as indirect effects of silvicultural management intensities (SMI) and forest features on acoustic diversity index (ADI). Standardized coefficients are shown. Black lines represent significant relationships (p < 0.05) and trends (p < 0.1). Significant levels are given as: p < 0.001: “***”, p < 0.01: “**”, p < 0.05: “*”, p > 0.1: “.”. Solid lines represent positive relationships and dashed lines represent negative relationships. Grey solid lines represent hypothesized relationships that were included in the final model but were not significant. The double-headed arrows represent significant correlation among variables. Model fit: Chi-square: 5.001, p-value (Chi-square): 0.209, p-value RMSEA <= 0.05: 0.331, number of observations: 109.
Temporal dynamics of acoustic diversity in managed forests
  • Article
  • Full-text available

September 2024

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278 Reads

Introduction In production forests, management can have cascading effects on biodiversity and ecosystem services. Acoustic diversity reflects the diversity of vocalizing animals and has also considerable recreational value for human well-being, but the relationship between acoustic diversity and forest management remains largely unexplored Method We recorded acoustic diversity on forest plots along a gradient of silvicultural management intensity (SMI) in three regions of Germany. We explored the diurnal and seasonal temporal dynamics in acoustic diversity index (ADI) from March to July using generalized additive mixed models (GAMMs). We further investigated the interrelation between acoustic diversity and silvicultural management intensity, forest structural diversity, as well as tree diversity, bird species richness and abundance using structural equation modeling (SEM). Results Silvicultural management intensity had significant effects on the temporal dynamics of ADI in May and June from dawn till dusk, but variance explained by SMI was low. We confirmed our hypothesis that ADI was reduced by SMI due to its cascading effects on forest structural diversity and bird species richness and abundance. Discussion Acoustic diversity indices can provide valuable insights into how forest management affects the acoustic activity of soniferous communities. We discuss how this can indicate both changes in species diversity as well as their vocal activity. We further address potential implications for forest management.

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Supporting bird diversity and ecological function in managed grassland and forest systems needs an integrative approach

August 2024

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138 Reads

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1 Citation

In modified production landscapes, biodiversity faces unprecedented pressures from human actions, resulting in significant species declines of plant and animal taxa, including birds. Understanding the underlying mechanisms responsible for such declines is essential to counteract further loss and support practitioners in conserving biodiversity and associated ecosystem function. In this study, we used standardized bird monitoring data collected over 6 years in managed forest and grassland areas across different regions in Germany, Central Europe. We combined these data with morphometric, ecological, behavioral, and acoustic trait data and detailed information on local land use management practices to understand how management decisions affect species and functional diversity, as well as ecological processes shaping local species composition. Our results reveal that the ecosystem and regional context must be considered to understand how management practices affect bird diversity aspects and composition. In forests, regional management decisions related to tree species and stand age affected bird diversity, as well as community and functional composition, and indicated environmental sorting due to ecological and behavioral requirements, biotic interactions, and morphometric constraints. In grasslands, independent of local management practices, increased intensity of land use resulted in an overall loss in bird species richness and functional diversity. Predominantly, constraints due to ecological or behavioral requirements affected bird species assemblage composition. In addition, our results indicated the importance of woody vegetation near managed grasslands and of considering environmental conditions beyond the local scale to support bird diversity and associated ecosystem functions. Our results highlighted that local management decisions can support bird diversity and maintain ecological function. However, this needs a view beyond the local scale of management units. It also demands a joint effort of biologists and land managers to integrate targeted conservation actions into regional management practices and create a network of habitats within production landscapes to protect nature, guard against biotic and functional homogenization, and prevent further degradation of ecosystems in production landscapes.


The resident nectar-feeding bat guild and two key nectar resources
The two resident nectar-feeding bat species, Glossophaga commissarisi (A) and Hylonycteris underwoodi (B), and the pendulous flower of Merinthopodium neuranthum (C) and the horizontally oriented Werauhia gladioliflora (D) at La Selva Biological Station, Costa Rica. When visiting a flower of M. neuranthum, bats (here H. underwoodi) raise their head to the flower above and lap the nectar (E).
Experimental setup in the flight cage
H. underwoodi drinking from the horizontally oriented flower of W. gladioliflora presented in an artificial inflorescence (A) and from the downward-hanging flower of M. neuranthum (B). Both the IR-light-sensor (B) and the reflector (A) are visible in the background.
Comparison of nectar-drinking behavior of the two nectar-feeding bat species at the two resource plants
(A, B) Hovering duration, (C, D) extracted nectar volume, (E, F) standardized nectar extractions efficiency. 9 individuals of H. underwoodi performed 383 drinking events at flowers of M. neuranthum and 5 individuals accomplished 612 drinking events at flowers of W. gladioliflora. For Glossophaga commissarisi, we observed 5 individuals with 272 drinking events at flowers of M. neuranthum and 6 individuals with 653 drinking events at flowers of W. gladioliflora.
Feeding efficiency of two coexisting nectarivorous bat species (Phyllostomidae: Glossophaginae) at flowers of two key-resource plants

June 2024

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51 Reads

Animals should maximize their energy uptake while reducing the costs for foraging. For flower-visitors these costs and benefits are rather straight forward as the energy uptake equals the caloric content of the consumed nectar while the costs equal the handling time at the flower. Due to their energetically demanding lifestyle, flower-visiting bats face particularly harsh energetic conditions and thus need to optimize their foraging behavior at the flowers of the different plant species they encounter within their habitat. In flight cage experiments we examined the nectar-drinking behavior (i.e. hovering duration, nectar uptake, and the resulting feeding efficiency) of the specialized nectar-feeding bat Hylonycteris underwoodi and the more generalistic Glossophaga commissarisi at flowers of two plant species that constitute important nectar resources in the Caribbean lowland rainforests of Costa Rica and compared nectar-drinking behavior between both bat species and at both plant species. We hypothesized that the 1) specialized bat should outperform the more generalistic species and that 2) bats should generally perform better at flowers of the nectar-rich flowers of the bromeliad Werauhia gladioliflora than at the relatively nectar-poor flowers of the Solanaceae Merinthopodium neuranthum that has an extremely long flowering phase and therefore is an extremely reliable nectar resource, particularly for the specialized Hylonycteris. While we did not find substantial differences in the feeding efficiency of the generalist G. commissarisi, we observed an increased feeding efficiency of the specialized H. underwoodi at flowers of the nectar-poor M. neuranthum. This suggests that familiarity and ecological importance are more important determinants of the interaction than just morphological traits. Our results demonstrate that in addition to morphology, behavioral adaptations are also important drivers that determine the fitness of nectar-feeding bats. Both familiarity with and the ecological importance of a resource seem to contribute to shaping the interactions between pollinating bats and their plants.


Spatio-temporal community characteristics and coronavirus prevalence
Sample sites and sampling regime (A) over a two-year field study in central Ghana. The relative community composition (B), abundance of subadults (C) and coronavirus prevalence (D) of captured bats at the five bimonthly-sampled caves. Map was created with OpenStreetMap and adapted in BioRender.com. Source data are provided as a Source Data file.
Diversity-disease relationship
Spearman-correlation between coronavirus prevalence (alpha-CoV 229E-like, beta-CoV 2b) and Shannon species diversity index (A, B). Solid line and grey band show best fit and 95 percent confidence interval, respectively. Source data are provided as a Source Data file.
Ecological determinants of coronavirus infection likelihood
Coronavirus (CoV) infection probability (alpha-CoV 229E-like, beta-CoV 2b) in relation to the Shannon Diversity Index (A, B), the relative abundance of the most common (n < 50) species Hipposideros (H.) abae (apricot), H. caffer B (light blue), C (yellow), D (dark blue) as well as Coleura (C.) afra (slate grey) and Nycteris (N.) macrotis (orange) (C, D), and the relative abundance of subadults (adults=magenta; subadults=pink) (E, F) in each of the five sampling sites in central Ghana modelled using generalised linear mixed effect models. Solid and dashed lines represent significant (FDR-corrected) and non-significant fitted model curves, respectively, and lightly shaded area the respective 95% confidence interval. Icons were created with BioRender.com. Source data are provided as a Source Data file.
Bat species assemblage predicts coronavirus prevalence

April 2024

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386 Reads

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4 Citations

Anthropogenic disturbances and the subsequent loss of biodiversity are altering species abundances and communities. Since species vary in their pathogen competence, spatio-temporal changes in host assemblages may lead to changes in disease dynamics. We explore how longitudinal changes in bat species assemblages affect the disease dynamics of coronaviruses (CoVs) in more than 2300 cave-dwelling bats captured over two years from five caves in Ghana. This reveals uneven CoV infection patterns between closely related species, with the alpha-CoV 229E-like and SARS-related beta-CoV 2b emerging as multi-host pathogens. Prevalence and infection likelihood for both phylogenetically distinct CoVs is influenced by the abundance of competent species and naïve subadults. Broadly, bat species vary in CoV competence, and highly competent species are more common in less diverse communities, leading to increased CoV prevalence in less diverse bat assemblages. In line with the One Health framework, our work supports the notion that biodiversity conservation may be the most proactive measure to prevent the spread of pathogens with zoonotic potential.


Vertically stratified interactions of nectarivores and nectar-inhabiting bacteria in a liana flowering across forest strata

March 2024

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56 Reads

American Journal of Botany

Premise: Vertical stratification is a key feature of tropical forests and plant-frugivore interactions. However, it is unclear whether equally strong patterns of vertical stratification exist for plant-nectarivore interactions and, if so, which factors drive these patterns. Further, nectar-inhabiting bacteria, acting as "hidden players" in plant-nectarivore interactions, might be vertically stratified, either in response to differences among strata in microenvironmental conditions or to the nectarivore community serving as vectors. Methods: We observed visitations by a diverse nectarivore community to the liana Marcgravia longifolia in a Peruvian rainforest and characterized diversity and community composition of nectar-inhabiting bacteria. Unlike most other plants, M. longifolia produces inflorescences across forest strata, enabling us to study effects of vertical stratification on plant-nectarivore interactions without confounding effects of plant species and stratum. Results: A significantly higher number of visits were by nectarivorous bats and hummingbirds in the midstory than in the understory and canopy, and the visits were strongly correlated to flower availability and nectar quantity and quality. Trochiline hummingbirds foraged across all strata, whereas hermits remained in the lower strata. The Shannon diversity index for nectar-inhabiting bacterial communities was highest in the midstory. Conclusions: Our findings suggest that vertical niche differentiation in plant-nectarivore interactions seems to be partly driven by resource abundance, but other factors such as species-specific preferences of hummingbirds, likely caused by competition, play an important role. We conclude that vertical stratification is an important driver of a species' interaction niche highlighting its role for promoting biodiversity and ecosystem functioning.



Robust evidence for bats as reservoir hosts is lacking in most African virus studies: a review and call to optimize sampling and conserve bats

November 2023

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469 Reads

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9 Citations

Africa experiences frequent emerging disease outbreaks among humans, with bats often proposed as zoonotic pathogen hosts. We comprehensively reviewed virus–bat findings from papers published between 1978 and 2020 to evaluate the evidence that African bats are reservoir and/or bridging hosts for viruses that cause human disease. We present data from 162 papers (of 1322) with original findings on (1) numbers and species of bats sampled across bat families and the continent, (2) how bats were selected for study inclusion, (3) if bats were terminally sampled, (4) what types of ecological data, if any, were recorded and (5) which viruses were detected and with what methodology. We propose a scheme for evaluating presumed virus–host relationships by evidence type and quality, using the contrasting available evidence for Orthoebolavirus versus Orthomarburgvirus as an example. We review the wording in abstracts and discussions of all 162 papers, identifying key framing terms, how these refer to findings, and how they might contribute to people's beliefs about bats. We discuss the impact of scientific research communication on public perception and emphasize the need for strategies that minimize human–bat conflict and support bat conservation. Finally, we make recommendations for best practices that will improve virological study metadata.


Black cuboidal boxes with small protruding opening (A) were presented as novel food source on an array inside the experimental cage (B)
To allow a clear differentiation of bats from the video footage, focal bats (left) were marked with a reflective stripe on their back
Learning time until bats first fed from the novel food source. In the social transmission situation, focal bats learned significantly faster than in the control situation (Wilcoxon rank sum test with continuity correction, W = 101, p < 0.01 (α = 0.05)). Solid lines depict medians and different symbols of demonstrator bats represent individuals
Social information facilitates learning about novel food sources in adult flower-visiting bats

July 2023

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83 Reads

Animal Cognition

Incorporating novel food sources into their diet is crucial for animals in changing environments. Although the utilization of novel food sources can be learned individually, learning socially from experienced conspecifics may facilitate this task and enable a transmission of foraging-related innovations across a population. In anthropogenically modified habitats, bats (Mammalia: Chiroptera) frequently adapt their feeding strategy to novel food sources, and corresponding social learning processes have been experimentally demonstrated in frugivorous and animalivorous species. However, comparable experiments are lacking for nectarivorous flower-visiting bats, even though their utilization of novel food sources in anthropogenically altered habitats is often observed and even discussed as the reason why bats are able to live in some areas. In the present study, we investigated whether adult flower-visiting bats may benefit from social information when learning about a novel food source. We conducted a demonstrator–observer dyad with wild Pallas’ long-tongued bats (Glossophaga soricina; Phyllostomidae: Glossophaginae) and hypothesized that naïve individuals would learn to exploit a novel food source faster when accompanied by an experienced demonstrator bat. Our results support this hypothesis and demonstrate flower-visiting bats to be capable of using social information to expand their dietary repertoire.


MHC class II genes mediate susceptibility and resistance to coronavirus infections in bats

May 2023

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87 Reads

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8 Citations

Molecular Ecology

Understanding the immunogenetic basis of coronavirus (CoV) susceptibility in major pathogen reservoirs, such as bats, is central to inferring their zoonotic potential. Members of the cryptic Hipposideros bat species complex differ in CoV susceptibility, but the underlying mechanisms remain unclear. The genes of the major histocompatibility complex (MHC) are the best understood genetic basis of pathogen resistance, and differences in MHC diversity are one possible reason for asymmetrical infection patterns among closely related species. Here, we aimed to link asymmetries in observed CoV (CoV-229E, CoV-2B and CoV-2Bbasal) susceptibility to immunogenetic differences amongst four Hipposideros bat species. From the 2072 bats assigned to their respective species using the mtDNA cytochrome b gene, members of the most numerous and ubiquitous species, Hipposideros caffer D, were most infected with CoV-229E and SARS-related CoV-2B. Using a subset of 569 bats, we determined that much of the existent allelic and functional (i.e. supertype) MHC DRB class II diversity originated from common ancestry. One MHC supertype shared amongst all species, ST12, was consistently linked to susceptibility with CoV-229E, which is closely related to the common cold agent HCoV-229E, and infected bats and those carrying ST12 had a lower body condition. The same MHC supertype was connected to resistance to CoV-2B, and bats with ST12 were less likely be co-infected with CoV-229E and CoV-2B. Our work suggests a role of immunogenetics in determining CoV susceptibility in bats. We advocate for the preservation of functional genetic and species diversity in reservoirs as a means of mitigating the risk of disease spillover.


Citations (69)


... Furthermore, the localities in which the bats were captured, which are close to human settlements (Fig. 1), have experienced a reduction in forest cover in recent years due to anthropogenic factors, including livestock farming, fires, and land use 96 . The loss of natural ecosystems and the ability of bats to adapt to different ecosystems would increase the probability of spillover processes occurring from bats to other hosts (humans or domestic animals/livestock), potentially affecting their health through the transmission of these zoonotic microbes 21,22 . Therefore, we emphasise the necessity of further research to understand the frequency of associated zoonotic diseases to these microbes, the dispersal of vectors, the microbial ecology in these reservoirs and other associated hosts, and the transmission efficiency. ...

Reference:

Microbial community dynamics in blood, faeces and oral secretions of neotropical bats in Casanare, Colombia
Bat species assemblage predicts coronavirus prevalence

... One Health, which recognizes that animal, human, and environmental health are interdependent and must be promoted simultaneously, can be used to promote biophilia, or a desire to connect with nature. As the world emerges from the COVID-19 pandemic, bat and biodiversity conservation must be promoted writ large to reduce zoonotic spillover risks and prevent pandemics before they begin (Eby et al., 2023;Weber et al., 2023;Plowright et al., 2024;Reaser et al., 2024). Protecting bat populations and their habitats offers significant co-benefits for people and bats; these activities reduce stress and viral shedding in bats while also reducing human-bat interactions. ...

Robust evidence for bats as reservoir hosts is lacking in most African virus studies: a review and call to optimize sampling and conserve bats

... In contrast, we found that specific functional variants (ST3, ST7 and ST5) underlie the MHC-mediated effects on fitness. Specific MHC supertypes have previously been associated with resistance or susceptibility to infection in a broad range of vertebrate species, including humans Homo sapiens (Trachtenberg et al. 2003), fat-tailed dwarf lemurs Cheirogaleus medius (Schwensow et al. 2007), Hipposideros bats (Schmid et al. 2023), red deer Cervus elaphus (Buczek et al. 2016), common frogs Rana temporaria (Teacher, Garner, and Nichols 2009), great tits Parus major (Sepil et al. 2013), Galápagos mockingbirds Mimus (Vlček and Štefka 2020) and Australian tawny dragon lizards Ctenophorus decresii (Hacking et al. 2018). However, few studies have observed associations between specific MHC supertypes and individual fitness (Ferreira et al. 2024;Sepil, Lachish, and Sheldon 2012). ...

MHC class II genes mediate susceptibility and resistance to coronavirus infections in bats
  • Citing Article
  • May 2023

Molecular Ecology

... However, studies focusing on the actual interactions among taxa across the vertical gradient are scarce. For plant-frugivore interactions, for instance, it was shown that networks differ profoundly among strata in terms of mutual specialization and interaction frequency and community composition of frugivores (Shanahan and Compton, 2001;Schleuning et al., 2011;Thiel et al., 2023). Few studies have examined the vertical stratification of interactions among plants and nectarivores although there are known differences in strata use among taxa. ...

Vertically stratified frugivore community composition and interaction frequency in a liana fruiting across forest strata
  • Citing Article
  • March 2023

Biotropica

... When foraging in clutter, insectivorous bats have been found to shift to increased reliance on vision (Ekl€ of et al., 2002), and nectar bats will shift to greater reliance on scent (Muchhala & Serrano, 2015), in line with the idea that echolocation becomes a less reliable sensory modality in such situations. Interestingly, rather than moving the flower away from its vegetative parts, another evolutionary approach to reduce clutter echoes found in batpollinated cacti is the evolution of wooly hairs around the flowers that absorb ultrasound, thus making the floral echoes more apparent (Simon et al., 2023). ...

An ultrasound absorbing inflorescence zone enhances echo-acoustic contrast of bat-pollinated cactus flowers

Journal of Experimental Biology

... This dynamic creates a highly competitive environment among floral species for pollen transfer by bats, as all species exhibit coinciding anthesis periods. These periods begin in the late afternoon or early evening and last until early morning, with the majority of pollen being dispersed during the early hours of the night [53,54]. For the selection of chiropterophilous plant species included in the fundamental inaccuracy, our inclusion criterion was a minimum population of 15 accessible individuals, enabling the measurement of intrapopulational phenotypic variation. ...

A Negative Association Between Nectar Standing Crop And Pollen Transfer Suggests Nectar Function As A Manipulator Of Pollinating Bats
  • Citing Article
  • December 2022

Annals of Botany

... Some of the ES included in climate adapta2on and sustainable produc2on such as greenhouse gas emissions were not considered to primarily depend on patch area, and thus modelled as simple lookup tables without spaOal mechanisms, resulOng in insensiOvity to landscape configuraOon. This could be improved in future studies, as landscape configuraOon has been shown to also impact these ES either directly (Didham et al., 2015) or indirectly through effects on supporOng soil biota (Le Provost et al., 2022). SOll, these ES varied across restoraOon scenarios, mostly due to changes in land cover proporOons as the scenarios prioriOsed different areas of the landscape, and thus different land covers, for restoraOon (Richards et al., 2024). ...

The supply of multiple ecosystem services requires biodiversity across spatial scales

Nature Ecology & Evolution

... Mount Meru is also a recharge zone, providing fresh water to the Arusha region in the foothills 23 . Landsat imagery has shown that forest bridges between Mounts Kilimanjaro and Meru once served as a corridor for arthropod dispersal and mammal and reptile migration, but these biogeographically important bridges have disappeared over time due to human settlement and agricultural expansion 19,24 . The Arusha region which encompasses Mount Meru has a population of around 2.3 million 20 . ...

Potential of Airborne LiDAR Derived Vegetation Structure for the Prediction of Animal Species Richness at Mount Kilimanjaro

... Importantly, in several vertebrates including humans, different characteristics of the MHC class II genotype are associated with inter-individual differences in the microbiota [36][37][38][39][40]. For instance, certain MHC class II motifs are specific to certain bacteria of the gut microbiota of sticklebacks (Gasterosteus aculeatus), reddish-grey mouse lemurs (Microcebus griseorufus) and neotropical bats (Artibeus jamaicensis) [41][42][43]. In addition, individuals with higher MHC class II diversity have lower gut microbiota diversity in sticklebacks and lemurs [41,42]. ...

Interaction between MHC diversity and constitution, gut microbiota and Astrovirus infections in a neotropical bat
  • Citing Article
  • May 2022

Molecular Ecology

... The nectar secretion pattern of H. neesianus matches those of many other bat-pollinated plants that commonly peak between 2000 and 2200 h and decrease after 0200 h, and which have been associated with the activity of nectarivorous bats (Ramirez et al., 1984;Fischer, 1992;Tschapka et al., 1999;Slauson, 2000;Rivera-Marchand and Ackerman, 2006;Rocha et al., 2007;Tschapka and von Helversen, 2007;Aguilar-Rodríguez et al., 2022). There is no nectar reabsorption since we did not register a decrease in nectar accumulated in bagged flowers before flower abscission (Pyke et al., 2020b). ...

Intraspecific variability of nectar attracts different bats: the case of Pseudalcantarea viridiflora, a bromeliad with crepuscular anthesis

Acta Botanica Brasilica