Abstract
Beetles of the genus Antherophagus are phoretic organisms that inhabit the nests of Bombus species. They migrate and colonize new nests using the same bumblebees as carriers. Although Antherophagus beetles from temperate Europe and North America are known to use some plant species to move between bumblebees, it is unknown which plants are used as transfer stations by neotropical Antherophagus. Here, we report for the first time how phoretic Antherophagus beetles of an undescribed species use the inflorescences of Chuquiraga jussieui to transfer between individuals of Bombus funebris in the páramos of Central Ecuador. Our observations are the highest records (at 4200 m asl) of a phoretic interaction performed so far.
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Phoresy is an interaction in which an organism (i.e. the phoront) uses another organism (i.e. the host) for dispersal (see Borges 2022). Various bumblebee species have been reported as temporal hosts of phoretic mites and beetles worldwide. However, in the alpine ecosystems of tropical America, only Bombus funebris Smith, 1854 has been reported as a host of both phoretic mites and beetles (Plischuk et al. 2020; Vanegas and Padrón 2022).
Bombus funebris is an Andean species distributed from Colombia to northern Chile (Rasmussen 2003). This bumblebee species is found from 600 up to 4750 m asl (Rasmussen 2003; Pinilla-Gallego et al. 2016). Nevertheless, B. funebris reaches its peak of abundance between 2800 and 3800 m (Pinilla-Gallego et al. 2016), an elevation range that overlaps that of the páramos ecosystems in the northern Andes (usually above 3500 m and below the snowline; Sklenář et al. 2014). Although it is a common bumblebee species in the inter-Andean valleys (Rasmussen 2003), knowledge about its biology and ecological interactions, such as the flowers they pollinate, is still very limited. Our preliminary results of a study on plant-pollinator networks in a páramo of Central Ecuador indicate that B. funebris is the main pollinator of many páramos plant species (Martel unpubl. data) and, therefore, a key pollinator in these ecosystems. This addresses the importance of this kind of study in the conservation of the neotropical páramos.
The páramos harbour a rich biodiversity of plants and animals and are considered the world’s most diverse high-elevation ecosystems (Sklenář et al. 2014). These ecosystems are important water sources and contain large soil carbon. Despite its importance, our knowledge of the ecological interactions of their plants and animals is still poor thus our understanding of the full ecological value of this ecosystem is limited. In the páramos of Ecuador, one common plant species is Chuquiraga jussieui J.F. Gmel. This plant flowers throughout the year (Ezcurra 1985), including during the wet season, when other common páramo species do not bloom. Therefore, this species might be an important source of nectar for pollinating birds and insects, including B. funebris. Bombus funebris queens and workers visit the flowers of C. jussieui to feed on nectar; however, during their visits to the C. jussieui capitula, some unexpected guests “board” the bees.
During fieldwork carried out in the Yanacocha Reserve in Central Ecuador (0.135669°S, 78.575061°W, 4205 m asl; Figure 1) between 28th and 31st October 2023, in a long-term experimental area of a páramo ecosystem, where we have been observing plant-pollinator interactions, we recorded a small beetle on a capitulum of C. jussieui. This beetle had its mandibles wide open and its head pointed up. One day after, we recorded a similar beetle attached to the tarsus of a B. funebris worker, which was collected when approaching a C. jussieui capitulum. Realizing the beetles could have a phoretic association with B. funebris, and this may involve C. jussieui, we inspected the body of 20 B. funebris bumblebees and the capitula of 25 C. jussieui plants to record the occurrence of beetles. As a result, we recorded a C. jussieui capitulum hosting one beetle (Figure 2) and three B. funebris workers bearing a total of five beetles, which were attached to their antennae and legs (Figure 3).
After closer inspection of one collected beetle and the revision of the literature, we identified the beetle as belonging to the genus Antherophagus Dejean, 1821 (Coleoptera: Cryptophagidae). This genus is small and includes only 12 species (Bousquet 1989). In the Americas, five species of Antherophagus have been reported, all of which occur in North America (Evans et al. 2023; Kole and Ivie 2023). Nevertheless, many species remain undescribed in the Neotropical region since Antherophagus beetles have been recorded from Costa Rica to Brazil (Roubik and Wheeler 1982; Bousquet 1989; Chavarría 1994a, b; González et al. 2004; Posada-Flórez and Téllez-Farfán 2021; Vanegas and Padrón 2022). This is the case for the beetles recorded on B. funebris, which belong to a not-yet-described Antherophagus species (Martel unpubl. data).
Antherophagus beetles inhabit and develop in bumblebee nests, where they feed on organic detritus acting as scavengers (Wheeler 1919; Frison 1921; Chavarria 1994a), in a sort of commensalistic relationship. However, since Antherophagus beetles have also been frequently recorded attached to different bumblebee species in Europe and North America (Wheeler 1919; Frison 1921; von Frisch 1952), they are considered phoretic on Bombus and not to be detrimental to the bumblebee colonies (Frison 1921). However, some bumblebees might be negatively impacted by the weight of carrying several beetles, especially those occurring at higher elevations where it is more energetically costly to fly due to the low air density and low oxygen levels occurring at high altitudes (Halloy 1989). For instance, we have recorded one B. funebris worker carrying three beetles resting on the grass before taking off (Figure 3), and Posada-Flórez and Téllez-Farfán (2021) recorded a B. pauloensis Friese, 1913 worker on the ground carrying six beetles in Colombia at 2600 m. The presence of the beetles may also reduce the capacity of the bumblebee to access nectar and pollen, carry the floral reward to the nest and ultimately pollinate the plants. Thus, this phoretic Antherophagus-Bombus relationship can deviate periodically into a parasitic relationship, which is expected to evolve over time in phoretic interactions (White et al. 2017). However, whether Bombus species from high elevations are particularly susceptible to being affected by Antherophagus needs to be explored.
In the neotropical region, there are four Bombus species (B. ephippiatus Say, 1837, B. funebris, B. pauloensis, B. pullatus Franklin, 1913) reported as hosts of phoretic Antherophagus beetles in the cloud forests of Costa Rica and Colombia and páramo remanents of Ecuador (Roubik and Wheeler 1982; Chavarría 1994a, b; Posada-Flórez and Téllez-Farfán 2021; Vanegas and Padrón 2022). Although Antherophagus beetles were already reported on B. funebris bumblebees (at 3845 m; Vanegas and Padrón 2022), our report was made at a higher elevation (4200 m) and in a well-preserved páramo, in which we could identify the plant species used by the Antherophagus beetles as transfer stations (i.e. Chuquiraga jussieui). It was suggested that Antherophagus beetles occur and use flowers to move between bee hosts in North America (Parks 2016) and the Neotropics (Roubik 1989); however, knowledge about which flowers are being used by these beetles in these regions has remained elusive. Therefore, to our knowledge, C. jussieui is the first plant recorded as a bumblebee transfer station for any New World Antherophagus species. The orange colouration of the capitula of C. jussieui and the diameter of the tubular flowers, similar in size to the beetle height, may help Antherophagus beetles to camouflage and stay undetected by an approaching bumblebee (see Figure 2). An additional observation of a Bombus-Antherophagus interaction in the neotropics can be found on iNaturalist (https://www.inaturalist.org/observations/174133066), in a photo taken at around 2700 m in a cloud forest in northern Ecuador, where a beetle was attached to a bumblebee similar to B. robustus Smith, 1854. Thus, in the Andean páramos, there are so far only two reports of phoretic Antherophagus on Bombus species, all from the western Andes of Ecuador (Figure 1). Further studies would better inform the extent of this interaction and the ecological implications of this phoretic relationship on neotropical bumblebees.
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Acknowledgements
We would like to thank Roxana Rojas for preparing the map shown in Figure 1. We also thank the support of the Royal Society (RGS\R1\231379) from the UK and the Universidad de Las Americas (DIV.FCC.23.01) that allowed us to conduct fieldwork in our study. We would like to express our gratitude to the Jocotoco Foundation, owners of the Yanacocha Reserve, where our passive warming experiment has been established since 2012. We also thank two anonymous reviewers whose comments helped improve the manuscript. This study was carried out under the research permit No. MAATE-DBI-CM-2021-0187 (Caracterización de la diversidad filogenética funcional y ecosistémica en el Ecuador).
Funding
This work was supported by a research grant from the Royal Society to CT (RGS\R1\231379) and from Universidad de Las Americas to FC (DIV.FCC.23.01).
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All authors conceived the study. CM and LC collected the material. CM performed the analysis and wrote the paper. All authors participated in the revision, read and approved the final manuscript.
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Martel, C., Cifuentes, L., Cuesta, F. et al. Scientific note: Phoretic interaction between Antherophagus (Coleoptera) and Bombus funebris (Hymenoptera), using Chuquiraga jussieui (Asteraceae) as transfer stations in the páramos. Apidologie 55, 32 (2024). https://doi.org/10.1007/s13592-024-01075-7
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DOI: https://doi.org/10.1007/s13592-024-01075-7