Nocturnal bees exploit but do not pollinate flowers of a common bat-pollinated tree

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Nocturnal bees exploit but do not pollinate flowers of a common bat‑pollinated tree Fernanda Figueiredo de Araujo1 · Priscila de Cássia Souza Araújo2 · Estefane Siqueira3 · Isabel Alves‑dos‑Santos4 · Reisla Oliveira3,5 · Stefan Dötterl6 · Clemens Schlindwein7  Received: 7 May 2020 / Accepted: 12 September 2020 © Springer Nature B.V. 2020

Abstract Some species of bees restrict foraging to the twilight period before sunrise or after sunset. Among the plants sought by these nocturnal bees are species described as chiropterophilous, such as Caryocar brasiliense. The flowers of this species open in the evening and provide resources until dawn. We determined the pattern of flower visitation by nocturnal bees and their role in pollination and fruit set of C. brasiliense and evaluated its importance as floral resource for nocturnal bees. We analyzed the pollen composition of cell provisions of nocturnal bees of Ptiloglossa (Colletidae) and compared its scent with floral scent compounds of C. brasiliense. Moreover, we conducted a pollinator exclusion experiment to determine the contribution of nocturnal bees to its fruit set. Disregarding bats, Ptiloglossa latecalcarata and two species of Megalopta (Halictidae) were consistent nectar and pollen gathering visitors, along with some social diurnal bees. The visitor exclusion experiment revealed that bee visits do not result in fruit set, which only occurs through visits by bats. The flowers supply a significant amount of pollen for nocturnal bees, as demonstrated through pollen analysis of brood cells and scopa loads. This interaction, therefore, is only beneficial to the commensalist bees. The scent collected from brood cells was dominated by hexanoic acid and 1-hexanol and differed strongly from the floral scent of C. brasiliense. These results substantiate that bat-pollinated flowers are an important part of the food niche of nocturnal bees, which implies that they are sensorially equipped to recognize floral traits shaped by bats. Keywords  Caryocar brasiliense · Caryocaraceae · Cerrado · Food niche · Dim-light foraging · Crepuscular bees · Megalopta · Ptiloglossa · Pollen loads

Handling Editor: Heikki Hokkanen. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1182​9-020-09784​-3) contains supplementary material, which is available to authorized users. 5



Programa de Pós‑Graduação Em Biologia Vegetal, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil

Departamento de Genética, Ecologia e Evolução, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, Pampulha, Belo Horizonte, Minas Gerais 31270‑901, Brazil

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Programa de Pós‑Graduação Em Zoologia, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil

Department of Biosciences, Plant Ecology, Paris-Lodron University of Salzburg, Hellbrunnerstr. 34, 5020 Salzburg, Austria

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Departamento de Botânica, Laboratório Plebeia–Ecologia de Abelhas e da Polinização, Universidade Federal de Minas Gerais