This project examines the evolution of multimodal signals based on behavior experiments at Schönbrunn Zoo and in the wild. Beyond the well-known acoustic signaling in frogs, the foot-flagging species also use visual signals to communicate. The conspicuous leg waving, in which the light-colored web is briefly presented to rivals, is considered to be an agonistic signal. This special adaptation to rapidly flowing, loud streams has since been documented in several species from a range of families in Southeast Asia and South Africa. In frogs, this winking signal behavior has evolved several times independently.
Aim
The combination of studies in the wild and research in zoos yields insights into the actual quality and function of these signals. The visual signaling behavior probably requires the precise coordination of various neuronal circuits and muscle groups. Because this visual signal is specifically applied in fights between males, the hypothesis assumes that hormones modulate signal complexity. The expectation is that the movement patterns provide information about the size and/or weight of the signaler and thus influence the rival.
Relevance
The focus of this research is on the transmission, recognition, reception and integration of these visual signals. This encompasses the underlying mechanism and therefore all the communication modalities that impact the recipient. The development of a signal can be influenced both by the receiver and by competing signalers, with the physical environment also playing a role. For the first time, researchers can draw further-reaching conclusions about the origin, modification and loss of adaptive movement patterns in signals.
Method
Physiological investigations with androgens were conducted at Schönbrunn Zoo in order to test how this affects the frequency and motion of waving signals. Male foot-flagging frogs were separated into two: one received testosterone, the other a saline solution. The behavior of the animals was then filmed and analyzed. The treatment substances are non-toxic and in no way impact the health or further development of the animals.
Another facet involves comparing the waving movements of the zoo-reared foot-flagging species from Borneo with three frog species from India. Video-documentation (slow motion) combined with color measurements of the feet are expected to reveal the commonalities and differences in the communication of these unrelated foot-flagging frogs.
Results
The research showed that the feet of the foot-flagging frog species held at the zoo first take on their bright white coloration over the course of their first year of life: the juveniles are still well camouflaged.
Another result was that the frogs treated with testosterone waved considerably more than the control group (Figure 1). Foot-flagging frogs generally have ten times more androgen receptors in their leg musculature than frog species that do not wave. The researchers suspect that the increased number of androgen receptors in the leg muscles has also led to changes in the circuitry of the spinal cord and brain.
Associated researchers:
Dr. Matthew Fuxjager
Brown University, Dept. of Ecology and Evolutionary Biology, 171 Meeting Street, Providence, Rhode Island, USA
Email: matthew_fuxjager@brown.edu
Website: https://www.fuxjagerlab.com/
Dr. Lisa Mangiamele
Smith College, Department of Biological Sciences, 44 College Ln, Northampton, MA 01063
Email: lmangiamele@smith.edu
Website: http://www.science.smith.edu/mangiamele/
References
Mika A Holtz, Riccardo Racicot, Doris Preininger, Adam M M Stuckert, Lisa A Mangiamele, Genome assembly of the foot-flagging frog, Staurois parvus: a resource for understanding mechanisms of behavior, G3 Genes|Genomes|Genetics, 2023;, jkad193, https://doi.org/10.1093/g3journal/jkad193
Love, N., D. Preininger & M. J. Fuxjager (2023): Social regulation of androgenic hormones and gestural display behavior in a tropical frog. Hormones and Behavior, 155 105425. https://doi.org/10.1016/j.yhbeh.2023.105425
Nigel K. Anderson, Sarah E. Goodwin, Eric.R. Schuppe, AllexAndrya Dawn, Doris Preininger, Lisa A. Mangiamele, Matthew J. Fuxjager (2022): Activational vs. organizational effects of sex steroids and their role in the evolution of reproductive behavior: Looking to foot-flagging frogs and beyond. Hormones and Behavior, Volume 146, 105248, ISSN 0018-506X, https://doi.org/10.1016/j.yhbeh.2022.105248.
Smith, S. M., A. R. Eigerman, K. M. LeCure, E. Kironde, A. G. Privett-Mendoza, M. J. Fuxjager, D. Preininger and L. A. Mangiamele (2021). Androgen Receptor Modulates Multimodal Displays in the Bornean Rock Frog (STAUROIS PARVUS). Integrative and Comparative Biology, Volume 61, Issue 1, Pages 221–230, https://doi.org/10.1093/icb/icab042
Anderson, N., E. Schuppe, K. V. Gururaja, P. Hebbar, L. Mangiamele, J. C. C. Martinez, R. v. May, D. Preininger and M. Fuxjager (2021). A common endocrine signature marks the convergent evolution of an elaborate dance display in frogs The American Naturalist, Volume 198, Number 4, https://doi.org/10.1086/716213
Anderson, N., M. Grabner, L. Mangiamele, D. Preininger and M. Fuxjager (2021). Testosterone amplifies the negative valence of an agonistic gestural display by exploiting receiver perceptual bias. Proc Biol Sci B., Volume 288 ,Issue 1963, https://doi.org/10.1098/rspb.2021.1848
Anderson, N. K., Gururaja, K. V., Mangiamele, L. A., Netoskie, E. C., Smith, S., Fuxjager, M. J., & Preininger, D. (2021). Insight into the Evolution of Anuran Foot Flag Displays: A Comparative Study of Color and Kinematics. Ichthyology & Herpetology, 109(4), 1047-1059. https://doi.org/10.1643/h2020160
Grosjean, Stéphane & Preininger, Doris. (2020). Description of two Staurois tadpoles from Borneo, Staurois parvus and Staurois tuberilinguis (Anura: Ranidae). Zootaxa. 4896. 523-534. 10.11646/zootaxa.4896.4.4.
Preininger D., Weissenbacher A., Wampula T. and W. Hödl. 2012. The conservation breeding of two foot-flagging frog species from Borneo, Staurois parvus and Staurois guttatus. Amphibian and Reptile Conservation 5(3):45-56(e51)
http://www.redlist-arc.org/Article-PDFs/ARC_5(3)_45-56_e51_high_res.pdf
Preininger D., Boeckle M., Freudmann A., Starnberger I., Sztatecsny M., and W. Hödl. 2013. Multimodal signaling in the Small Torrent Frog (Micrixalus saxicola) in a complex acoustic environment. Behavioral Ecology and Sociobiology 67: 1449-1456 doi: 10.1007/s00265-013-1489-6 http://link.springer.com/article/10.1007/s00265-013-1489-6
J. Stangel, D. Preininger, M. Sztatecsny & W. Hödl. 2015. Ontogenetic change of signal brightness in the foot-flagging frog species Staurois parvus and S. guttatus. Herpetologica 71(1): 1–7.
http://dx.doi.org/10.1655/HERPETOLOGICA-D-14-00014
Preininger, D., S. Handschuh, M. Boeckle, M. Sztatecsny & W. Hödl. 2016. Comparison of female and male vocalisation and larynx morphology in the size dimorphic foot-flagging frog species Staurois guttatus. Herpetological Journal 26/3:187-197 http://www.ingentaconnect.com/content/bhs/thj/2016/00000026/00000003/art00001
Mangiamele L.A., M.J. Fuxjager, E. Schuppe, R.S. Taylor, W. Hödl & D. Preininger. 2016. Increased androgenic sensitivity in the hind limb neuromuscular system marks the evolution of a derived gestural display. PNAS 113:5464-69. doi: 10.1073/pnas.1603329113
http://www.pnas.org/content/113/20/5664.full