Symbiotic bacteria in uropygial secretion of Eurasian Hoopoe may repel blood-feeding flies from nests

José Luis Copete March 12, 2021
Eurasian Hoopoe (Eurasian)Upupa epops [epops Group]

Mosquitoes, black flies, and biting midges eagerly pursue blood meals from a full range of warm-blooded creatures, including birds. Yet exactly how these blood-feeding flies locate their avian hosts remains a mystery, even after decades of research. Knowing how these flies locate a bird in the field can lead to understanding the protective measures birds develop to counteract parasites. In turn, studying birds’ defensive mechanisms against blood-feeding flies could benefit humans as we seek to reduce the transmission of vector-borne diseases by these flies.

Gustavo Tomás and his research team in Spain (Tomás et al. 2020) are tackling this mystery by studying the attraction of blood-feeding flies to the auditory cues produced by begging Eurasian Hoopoe (Upupa epops) nestlings, and the parasites’ attraction to three chemical cues derived from hoopoe nestlings or nests (uropygial secretion, symbiotic bacteria isolated from the secretion, and nest material).

Past research indicates that the odors emitted or derived from a bird’s uropygial gland can attract biting flies. For example, extracts taken from uropygial glands of American Crow (Corvus brachyrhynchus) and Common Loon (Gavia immer) attracted mosquitoes and black flies, respectively. When preening, birds rub uropygial secretion onto their plumage and skin, leaving behind specific odor signatures. This may explain why mosquitoes and black flies also are attracted to chemical cues derived from bird feathers, in combination with CO2.

The Eurasian Hoopoe seems to derive additional and possibly unique benefits from its uropygial secretion. First, its gland is unusually large; and, only for reproducing females and nestlings, the gland produces a dark, pungent, malodorous secretion. This uropygial secretion is unique because it harbors enterococci bacteria which has antibiotic properties. This symbiotic partnership is the only reported example among birds to provide antibiotic protection to the host.

Dr. Tomás and his team deployed insect traps baited with auditory and chemical stimuli at the start and end of the hoopoe breeding season. The abundance of blood-feeding flies varied depending on the habitat and sampling period. Auditory cues of the begging nestlings did not affect the number of flies caught in the traps. However, the chemical stimuli affected the abundance of mosquitoes: fewer were collected in traps baited with enterococci bacteria or nest material than in control traps. In habitats with a higher abundance of biting midges, fewer midges were collected in traps baited with the bacteria and with the secretion. This suggests that the bacteria-harboring uropygial secretion of the hoopoe may repel blood-feeding flies from their nests.

Research by Martín-Vivaldi et al. (2014) indicated that this symbiotic relationship offers further benefit to the hoopoe. Hoopoe eggs change color a few days after being laid; some evidence suggests this is because the incubating female smears her antibiotic secretion on the eggs (a behavior observed by researchers). Martín-Vivaldi’s team studied the microscopic structure of hoopoe eggshells and found features (crypts) that favor the adhesion of uropygial secretion. Their experiments showed that the crypts of the control group were filled with uropygial secretion and that the presence of beneficial bacteria came, at least partially, from the uropygial gland of the incubating female. The existence of specialized crypts on the hoopoe eggshells and the female’s deliberate application of the secretion to the eggs support a strong link between secretion and bacteria on the eggs. Additionally, results showed a positive relationship between the presence of bacteria and hatching success, indicating that the adhesion of the symbiont-carrying uropygial secretion to crypts on the eggshell’s surface protects embryos against infections.

The far-reaching properties of bacteria in the hoopoe’s uropygial secretion reveal complex interactions between bacteria and their feathered host. Serving as parasite repellent and antimicrobial agent, the bacteria protect not only the bird itself, but also the developing embryos within its eggs.

 

References

Martín-Vivaldi, M., J. J. Soler, J. M. Peralta-Sánchez, L. Arco, A. M. Martín-Platero, M. Martínez-Bueno, M. Ruiz-Rodríguez, and E. Valdivia (2014). Special structures of Hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increase hatching success. Journal of Animal Ecology 83:  1289–1301.

Tomás, G., C. Zamora-Muñoz, M. Martín-Vivaldi, M. D. Barón, C. Ruiz-Castellano, and J. J. Soler (2020). Effects of chemical and auditory cues of Hoopoes (Upupa epops) in repellence and attraction of blood-feeding flies. Frontiers in Ecology and Evolution 30. https://doi.org/10.3389/fevo.2020.579667

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