Skip to main content
Log in

Can Anyone Climb? The Skills of a Non-specialized Toad and its Bearing on the Evolution of New Niches

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Several studies of arboreal anuran species show morphological specializations for clinging onto narrow substrates. However, little is known about these capacities in non-specialized anurans, which is crucial to understand the initial phases of adaptation to a new niche. To assess the functional requirements related to the evolution of arboreality in anurans we analyzed climbing performance, and correlated anatomical traits, in the terrestrial toad Rhinella arenarum, a species choose as a proxy for the ancestral condition regarding the evolution of this specialized niche. We studied the impact of a substrate of wooden rods with different diameters, arrangements, and slopes on locomotion, grasping, and climbing with a comparative framework. Animals were confronted with climbing tests, video recording their behaviors. Preserved specimens were dissected to assess limb myology, osteology, and tendons’ characteristics. Our results show that how terrestrial toad R. arenarum climbs is different from those displayed by specialized tree frogs. Animals flexed their fingers and toes, grasping the substrate displaying hookings and partial graspings. The palm was scarcely involved in the grip, as in specialized anurans. These actions were performed although flexor and extensor muscles of the digits are highly conserved and generalized. Further, we formally assess the evolutionary history of ecological and anatomical traits related to climbing among Rhinella species to improving the comprehension of the relation between morphofunctional patterns and behavioral climbing skills. Our experiments revealed that this terrestrial toad possesses unexpected climbing capacities, suggesting a way in which evolution of new niches could have developed in the evolution of anurans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Abdala, V., Manzano, A. S., Tulli, M. J., & Herrel, A. (2009). The tendinous patterns in the palmar surface of the lizard manus: Tests of functional consequences for grasping ability. The Anatomical Record, 292, 842–853.

    Article  PubMed  Google Scholar 

  • Almendáriz, A., Cisneros-Heredia, D., Jungfer, K.-H., Coloma, L. A., & Ron, S. (2004). Rhinella festae. The IUCN Red List of THreatened Species, 2004, e.T54876A11205881.

    Google Scholar 

  • Angulo, A., Reichle, S., Köhler, J., & Córdova-Santa Gadea, J. (2004). Rhinella veraguensis. The IUCN Red List of Threatened Species, 2004, e.T54792A11192672.

    Google Scholar 

  • Anzeraey, A., Aumont, M., Decamps, T., Herrel, A., & Pouydebat, E. (2017). The effect of food properties on grasping and manipulation in the aquatic frog Xenopus laevis. The Journal of Experimental Biology, 220, 4486–4491.

    PubMed  Google Scholar 

  • Aubret, F., Bonnet, X., & Shine, R. (2007). The role of adaptive plasticity in a major evolutionary transition: Early aquatic experience affects locomotor performance of terrestrial snakes. Functional Ecology, 21, 1154–1161.

    Article  Google Scholar 

  • Azevedo-Ramos, C., Hoogmoed, M., Coloma, L. A., Ron, S., Castro, F., Rueda, J. V., Cisneros-Heredia, D., Icochea, J., & Angulo, A. (2004). Rhinella dapsilis. The IUCN Red List of Threatened Species, 2004, e.T54625A11177070.

    Google Scholar 

  • Bastos, R., Pavan, D., & Silvano, D. (2004). Rhinella ocellata. The IUCN Red List of Threatened Species, 2004, e.T54720A11192773.

    Google Scholar 

  • Bateson, P. (2017). Adaptability and evolution. Interface Focus, 7, 20160126. https://doi.org/10.1098/rsfs.2016.0126

    Article  PubMed  PubMed Central  Google Scholar 

  • Beltman, J. B., Haccou, P., & Ten Cate, C. (2004). Learning and colonization of new niches: A first step toward speciation. Evolution, 58(1), 35–46.

    PubMed  Google Scholar 

  • Blotto, B., Pereyra, M. O., Grant, T., & Faivovich, J. (2020). Hand and foot musculature of Anura: Structure, homology, terminology, and synapomorphies for major clades. Bulletin of the American Museum of Natural History, 443, 155. https://doi.org/10.1206/0003-0090.443.1.1

    Article  Google Scholar 

  • Burton, T. C. (1998). Are the distal extensor muscles of the fingers of Anurans an adaptation to arboreality? Journal of Herpetology, 32, 611–617.

    Article  Google Scholar 

  • CalPhotos Photo Database. (2020). Rhinella castaneotica. BNHM Berkeley Natural History Museums, University of California, Berkeley. https://calphotos.berkeley.edu/cgi/img_query?enlarge=0000+0000+1009+1826. Accessed 3 June 2020.

  • CalPhotos Photo Database. (2020). Rhinella manu. BNHM Berkeley Natural History Museums, University of California, Berkeley. https://calphotos.berkeley.edu/cgi/img_query?enlarge=0000+0000+1009+1823. Accessed 3 June 2020.

  • CalPhotos Photo Database. (2020). Rhinella veraguensis. BNHM Berkeley Natural History Museums,University of California, Berkeley. https://calphotos.berkeley.edu/cgi/img_query?enlarge=1111+1111+1111+1354. Accessed 11 June 2020.

  • CalPhotos Photo Database. (2020). Rhinella ocellata. BNHM Berkeley Natural History Museums, University of California, Berkeley. https://calphotos.berkeley.edu/cgi/img_query?enlarge=1111+1111+1111+6041. Accessed 11 June 2020.

  • CalPhotos Photo Database. (2020). Rhinella granulosa. BNHM Berkeley Natural History Museums, University of California, Berkeley. https://calphotos.berkeley.edu/cgi/img_query?enlarge=1111+1111+1111+2971. Accessed 3 June 2020.

  • CalPhotos Photo Database. (2020). Rhinella arequipensis. BNHM Berkeley Natural History Museums, University of California, Berkeley. https://calphotos.berkeley.edu/cgi/img_query?seq_num=86671&one=T. Accessed 14 June 2020.

  • Chaparro, J. C., Pramuk, J. B., & Gluesenkamp, A. G. (2007). A new species of arboreal Rhinella (Anura: Bufonidae) from cloud forest of southeastern Peru. Herpetologica, 63(2), 203–212.

    Article  Google Scholar 

  • Chuliver Pereyra, M. (2018). Ontogenia del aparato locomotor de Physalaemus biligonigerus (Anura: Leptodactylidae): Bases para comprender la función locomotora y su origen en los anuros [Ontogeny of the locomotor apparatus of Physalaemus biligonigerus (Anura: Leptodactylidae): Basis for understanding locomotor function and its origin in anurans]. PhD Thesis. Universidad Nacional de Córdoba, Argentina.

  • Coloma, L. A., Páez-Rosales, N., Ortiz, D. A., Frenkel, C., Ron, S. R., & Pazmiño-Armijos, G. (2018). Rhinella marina. In S. R. Ron, A. Merino-Viteri, & D. A. Ortiz (Eds.), Anfibios del Ecuador. Version 2019.0. Museo de Zoología.Pontificia Universidad Católica del Ecuador.

    Google Scholar 

  • Correa, C., Sallaberry, M., Jara-Arancio, P., Lobos, G., Soto, E., & Méndez, M. A. (2008). Amphibia, Anura, Bufonidae, Rhinella atacamensis: Altitudinal distribution extension, new records and geographic distribution map. Check List, 4(4), 478–484.

    Article  Google Scholar 

  • Cusi, J. C., Moravec, J., Lehr, E., & Gvoždík, V. (2017). A new species of semiarboreal toad of the Rhinella festae group (Anura, Bufonidae) from the Cordillera Azul National Park, Peru. ZooKeys, 673, 21–47. https://doi.org/10.3897/zookeys.673.13050

    Article  Google Scholar 

  • Dagg, A. I., & Windsor, D. E. (1972). Swimming in northern terrestrial mammals. Canadian Journal of Zoology, 50, 117–130.

    Article  Google Scholar 

  • Daneri, F., Papini, M. R., & Muzio, R. N. (2007). Common toads (Bufo arenarum) learn to anticipate and avoid hypertonic saline solutions. Journal of Comparative Psychology, 121(4), 419–427. https://doi.org/10.1037/0735-7036.121.4.419

    Article  PubMed  Google Scholar 

  • Daneri, M. F., Casanave, E., & Muzio, R. N. (2011). Control of spatial orientation in terrestrial toads (Rhinella arenarum). Journal of Comparative Psychology, 125(3), 296–307. https://doi.org/10.1037/a0024242

    Article  PubMed  Google Scholar 

  • de Freitas, M. A., Santos, E. M., de Amorim, F. O., & Lima de Almeida, G. V. (2018). First record of Rhinella ocellata (Günther, 1858) for the state of Bahia, northeastern Brazil (Anura: Bufonidae). Herpetology Notes, 11, 17–18.

    Google Scholar 

  • De la Riva, I. (2002). Taxonomy and distribution of the South American toads, Bufo poeppigii Tschudi, 1845 (Amphibia, Anura, Bufonidae). Graellsia, 58(1), 49–57.

    Article  Google Scholar 

  • de Noronha, J. C., Barros, A. B., Da Paixao, E. C., Almeida, E. J., Miranda, R. M., & Rodrigues, D. J. (2013). Climbing behaviour of terrestrial bufonids in the genus Rhinella. Herpetological Bulletin, 124, 22–23.

    Google Scholar 

  • Díaz-Páez, H., & Ortiz, J. C. (2003). Evaluación del estado de conservación de los anfibios en Chile. Revista Chilena De Historia Natural, 76(3), 509–525.

    Article  Google Scholar 

  • Diogo, R. (2017). Evolution driven by organismal behavior. A unifying view of life, function, form, mismatches and trends (1st ed.). . Springer.

    Book  Google Scholar 

  • Dunlap, D. G. (1960). The comparative myology of the pelvic appendage in the salientia. Journal of Morphology, 106, 1–76.

    Article  CAS  PubMed  Google Scholar 

  • Frenkel, C. (2019). Rhinella festae. In S. R. Ron, A. Merino-Viteri, & D. A. Ortiz (Eds.), Anfibios del Ecuador. Version 2019.0. Museo de Zoología.Pontificia Universidad Católica del Ecuador.

    Google Scholar 

  • FLICKR Photo Database (2020). Rhinella humboldti. FLICKR. https://www.flickr.com/photos/125903191@N07/15329580297. Accessed 3 June 2020.

  • FLICKR Photo Database (2020). Rhinella schneideri. FLICKR. https://www.flickr.com/photos/cdtimm/8075491625. Accessed 3 June 2020.

  • Gaupp, E. (1896). Anatomie des Frosches. Braunschweig: Friedrich Vieweg und Sohn.

    Google Scholar 

  • GBIF Global Biodiversity Information Facility, Secretariat (2020). Rhinella limensis. GBIF Backbone Taxonomy. Checklist dataset. Accessed via GBIF.org on 3 June 2020. https://doi.org/10.15468/39omei

  • Gomes, F. R., Rezende, E. L., Grizante, M. B., & Navas, C. A. (2009). The evolution of jumping performance in anurans: Morphological correlates and ecological implications. Journal of Evolutionary Biology, 22, 1088–1097.

    Article  CAS  PubMed  Google Scholar 

  • Gosá, A. (2008). Explotación del sustrato vertical por los anuros (Amphibia) del bosque atlántico. Naturzale, Cuadernos De Ciencias Naturales, 19, 131–148.

    Google Scholar 

  • Gould, S. J., & Vrba, E. S. (1982). Exaptation-A missing term in the science of form. Paleobiology, 8, 4–15.

    Article  Google Scholar 

  • Granda-Rodríguez, H. D., Portillo-Mozo, A. D., & Renjifo, J. M. (2008). Uso de hábitat en Atelopus laetissimus (Anura: Bufonidae) en una localidad de la Sierra Nevada de Santa Marta, Colombia. Herpetotrópicos, 4, 87–93.

    Google Scholar 

  • Grant, T., & Bolívar, G. W. (2014). A new species of semiarboreal toad with a salamander-like ear (Anura: Bufonidae: Rhinella). Herpetologica, 70, 198–210.

    Article  Google Scholar 

  • Herrel, A., Perrenoud, M., Decamps, T., Abdala, V., Manzano, A., & Pouydebat, E. (2013). The effect of substrate diameter and incline on locomotion in an arboreal frog. The Journal of Experimental Biology, 216, 3599–3605.

    Article  PubMed  Google Scholar 

  • Hildebrand, M., & Goslow, G. (2001). Analysis of vertebrate structure. John Wiley.

    Google Scholar 

  • Hudson, C. M., Gregory, P. B., & Shine, R. (2016). Athletic anurans: The impact of morphology, ecology and evolution on climbing ability in invasive cane toads. Biological Journal of the Linnean Society, 119(4), 992–999.

    Article  Google Scholar 

  • Hyams, S. E., Jayne, B. C., & Cameron, G. N. (2012). Arboreal habitat structure affects locomotor speed and perch choice of whitefooted mice (Peromyscus leucopus). Journal of Experimental Zoology, 317A, 540–551.

    Article  Google Scholar 

  • IUCN. (2014). International Union for Conservation of Nature and Natural Resources Red List of threatened species. Version 2014.3. IUCN.

    Google Scholar 

  • IUCN SSC Amphibian Specialist Group. (2014). Rhinella limensis. The IUCN Red List of Threatened Species, 2014, e.T54691A43476884.

    Google Scholar 

  • IUCN SSC Amphibian Specialist Group. (2015). Rhinella castaneotica. The IUCN Red List of Threatened Species, 2015, e.T54603A61393360.

    Google Scholar 

  • IUCN SSC Amphibian Specialist Group. (2015). Rhinella arunco. The IUCN Red List of Threatened Species, 2015, e.T54577A79810607.

    Google Scholar 

  • IUCN SSC Amphibian Specialist Group. (2018). Rhinella vellardi. The IUCN Red List of Threatened Species, 2018, e.T54791A89197536.

    Google Scholar 

  • IUCN SSC Amphibian Specialist Group. (2018). Rhinella nesiotes. The IUCN Red List of Threatened Species, 2018, e.T54715A89197422.

    Google Scholar 

  • IUCN SSC Amphibian Specialist Group. (2020). Rhinella poeppigii. The IUCN Red List of Threatened Species, 2020, e.T54735A61394155.

    Google Scholar 

  • IUCN SSC Amphibian Specialist Group. (2020). Rhinella arequipensis. The IUCN Red List of Threatened Species, 2020, e.T88991897A89226267. https://doi.org/10.2305/IUCN.UK.2020-1.RLTS.T88991897A89226267.en

    Article  Google Scholar 

  • Jetz, W., & Pyron, R. A. (2018). The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nature Ecology and Evolution, 2(5), 850–858. https://doi.org/10.1038/s41559-018-0515-5

    Article  PubMed  Google Scholar 

  • Karantanis, N.-E., Rychlik, L., Herrel, A., & Youlatos, D. (2017). Arboreal gaits in three sympatric rodents Apodemus agrarius, Apodemus flavicollis (Rodentia, Muridae) and Myodes glareolus (Rodentia, Cricetidae). Mammalian Biology—Zeitschrift Für Säugetierkunde, 83, 51–63. https://doi.org/10.1016/j.mambio.2016.12.004

    Article  Google Scholar 

  • Lauder, G. V. (1996). The argument from design. In M. R. Rose & G. V. Lauder (Eds.), Adaptation (pp. 55–91). Academic Press.

    Google Scholar 

  • Lavilla, E. O., Ponssa, M. L., Baldo, D., Basso, N., Bosso, A., Cespedez, J., Chebez, J. C., Faivovich, J., Ferrari, L., Lajmanovich, R., Langone, J. A., Peltzer, P., Úbeda, C., Vaira, M., & Vera Candioti, F. (2000). Categorización de los Anfibios de Argentina. In E. O. Lavilla, E. Richard, & G. J. Scrocchi (Eds.), Categorización de los Anfibios y Reptiles de la República Argentina (pp. 11–34). Asociación Herpetológica Argentina.

    Google Scholar 

  • Lehr, E., Kohler, G., Aguilar, C., & Ponce, E. (2001). New Species of Bufo (Anura: Bufonidae) from Central Peru. Copeia, 2001, 216–223.

    Article  Google Scholar 

  • Lindquist, E. D., Sapoznick, S. A., Griffith-Rodriguez, E. J., Johantgen, P. B., & Criswell, J. M. (2007). Nocturnal position in the Panamanian golden frog Atelopus zeteki (Anura, Bufonidae), with notes on fluorescent pigment tracking. Phyllomedusa, 6, 37–44.

    Article  Google Scholar 

  • Losos, J. B., Schoener, T. W., & Spiller, D. A. (2004). Predator-induced behaviour shifts and natural selection in field-experimental lizard populations. Nature, 432, 505–508.

    Article  CAS  PubMed  Google Scholar 

  • Maddison, W. P., & Maddison, D. R. (2019). Mesquite: A modular system for evolutionary analysis. Version 3.61. Retrieved from http://www.mesquiteproject.org

  • Manzano, A. S., Abdala, V., & Herrel, A. (2008). Morphology and function of the forelimb in arboreal frogs: Specializations for grasping ability? Journal of Anatomy, 213, 296–307.

    Article  PubMed  PubMed Central  Google Scholar 

  • Manzano, A. S., Fabrezi, M., & Vences, M. (2007). Intercalary elements, treefrogs, and the early differentiation of a complex system in the Neobatrachia. Anatomical Record, 290, 1551–1567.

    Article  Google Scholar 

  • Manzano, A. S., Fontanarrosa, G., & Abdala, V. (2018). Manual and pedal grasping among anurans: A review of relevant concepts with empirical approaches. Biological Journal of the Linnean Society, 127, 598–610.

    Article  Google Scholar 

  • Manzano, A. S., Fontanarrosa, G., Prieto, Y., & Abdala, V. (2017). La prensilidad en anfibios y reptiles: Perspectivas evolutivas basadas en la anatomía y la función. In V. Abdala, A. Manzano, & A. I. Vassallo (Eds.), Morfología de Vertebrados: Hacia una integración de conceptos, metodologías y grupos de investigación del país (pp. 59–81). EUDEM Editorial Universitaria de Mar del Plata.

    Google Scholar 

  • Manzano, A. S., Herrel, A., Fabre, A. C., & Abdala, V. (2017). Variation in brain anatomy in frogs and its possible bearing on their locomotor ecology. Journal of Anatomy, 231, 38–58.

    Article  PubMed  PubMed Central  Google Scholar 

  • Müller, G. B., & Wagner, G. P. (1991). Novelty in evolution: Restructuring the concept. Annual Review of Ecology and Systematics, 22, 229–256.

    Article  Google Scholar 

  • Muzio, R. N., Pistone Creydt, V., Iurman, M., Rinaldi, M., Sirani, B., & Papini, M. R. (2011). Incentive or habit learning in amphibians? PLoS ONE, 6(11), e25798. https://doi.org/10.1371/journal.pone.0025798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muzio, R. N., Segura, E. T., & Papini, M. R. (1992). Effect of schedule and magnitude of reinforcement on instrumental acquisition and extinction in the toad, Bufo arenarum. Learning and Motivation, 23, 406–429.

    Article  Google Scholar 

  • Napier, J. R. (1993). Hands. Princeton University Press.

    Book  Google Scholar 

  • Odling-Smee, J., Laland, K., & Feldman, M. (2003). Niche construction: The neglected process in evolution. Princeton University Press.

    Google Scholar 

  • Ortiz, D. A., & Coloma, L. A. (2018). Rhinella dapsilis. In S. R. Ron, A. Merino-Viteri, & D. A. Ortiz (Eds.), Anfibios del Ecuador. Version 2019.0. Museo de Zoología.Pontificia Universidad Católica del Ecuador.

    Google Scholar 

  • Ortiz, D. A., Ron, S. R., Coloma, L. A., & Páez-Rosales, N. (2018). Rhinella margaritifera. In S. R. Ron, A. Merino-Viteri, & D. A. Ortiz (Eds.), Anfibios del Ecuador. Version 2019.0. Museo de Zoología.Pontificia Universidad Católica del Ecuador.

    Google Scholar 

  • Padial, J. M., Chaparro, J. C., Köhler, J., & De la Riva, I. (2009). Rediscovery, resurrection and redescription of Rhinella leptoscelis (Boulenger, 1912) (Anura: Bufonidae). Zootaxa, 2115, 56–64.

    Article  Google Scholar 

  • Pereyra, M. O., Baldo, D., Blotto, B. L., Iglesias, P. P., Thomé, M. T. C., Haddad, C. F. B., Barrio-Amorós, C., Ibáñez, R., & Faivovich, J. (2015). Phylogenetic relationships of toads of the Rhinella granulosa group (Anura: Bufonidae): A molecular perspective with comments on hybridization and introgression. Cladistics, 32(1), 36–53. https://doi.org/10.1111/cla.12110

    Article  Google Scholar 

  • Pizzatto, L., Both, C., Brown, G., & Shine, R. (2017). The accelerating invasion: Dispersal rates of cane toads at an invasion front compared to an already-colonized location. Evolutionary Ecology, 31, 533–545. https://doi.org/10.1007/s10682-017-9896-1

    Article  Google Scholar 

  • Pramuk, J. B., Robertson, T., Sites, J. W., Jr., & Noonan, B. P. (2008). Around the world in 10 million years: Biogeography of the nearly cosmopolitan true toads (Anura: Bufonidae). Global Ecology and Biogeography, 17, 72–83.

    Google Scholar 

  • Puddington, M. M., Papini, M. R., & Muzio, R. N. (2018). Duration of extinction trials as a determinant of instrumental extinction in terrestrial toads (Rhinella arenarum). Animal Cognition, 21, 165–174. https://doi.org/10.1007/s10071-017-1149-8

    Article  PubMed  Google Scholar 

  • Rezende Oliveira, S., Fachi, M. B., Silva, D. A., & Morais, A. R. (2017). Predation on Rhinella mirandaribeiroi (Gallardo, 1965) (Anura; Bufonidae) by a Neotropical snake, including a list with predation events for species of the genus Rhinella. Herpetological Notes, 10, 151–155.

    Google Scholar 

  • Rodríguez, L. O., Cordova, J. H., & Icochea, J. (1993). Lista preliminar de los anfibios del Peru. Publicaciones Del Museo De Historia Natural U.n.m.s.m., 45, 1–22.

    Google Scholar 

  • SIB Sistema de Información de Biodiversidad (2020). Rhinella spinulosa. Administración de Parques Nacionales, Argentina. Checklist database. Accessed 3 June 2020. https://sib.gob.ar/especies/rhinella-spinulosa

  • Silvano, D., Azevedo-Ramos, C., La Marca, E., Narvaes, P., di Tada, I., Baldo, D., Solís, F., Ibáñez, R., Jaramillo, C., Fuenmayor, Q., & Hardy, J. (2010). Rhinella granulosa (errata version published in 2016). The IUCN Red List of Threatened Species, 2010, e.T54655A86595684.

    Google Scholar 

  • Sotelo, M. I., Bingman, V. P., & Muzio, R. N. (2015). Goal orientation by geometric and feature cues: Spatial learning in the terrestrial toad Rhinella arenarum. Animal Cognition, 18(1), 315–323. https://doi.org/10.1007/s10071-014-0802-8

    Article  PubMed  Google Scholar 

  • Sotelo, M. I., Bingman, V. P., & Muzio, R. N. (2017). Slope-based and geometric encoding of a goal location by the terrestrial toad (Rhinella arenarum). Journal of Comparative Psychology, 131, 362–369. https://doi.org/10.1037/com0000084

    Article  PubMed  Google Scholar 

  • Sotelo, M. I., Bingman, V. P., & Muzio, R. N. (2019). Mating call as a spatial signal and its brain representation in the terrestrial toad Rhinella arenarum. Brain, Behavior and Evolution, 94, 7–17. https://doi.org/10.1159/000504122

    Article  PubMed  Google Scholar 

  • Sustaita, D., Pouydebat, E., Manzano, A., Abdala, V., Hertel, F., & Herrel, A. (2013). Getting a grip on tetrapod grasping: Form, function, and evolution. Biological Reviews of the Cambridge Philosophical Society, 88, 380–405.

    Article  PubMed  Google Scholar 

  • Thomas, D., Hiscox, J., & Dixon, B. J. (2016). 3D scanning and printing skeletal tissues for anatomy education. Journal of Anatomy, 229(3), 473–481.

    Article  PubMed  PubMed Central  Google Scholar 

  • Toledo, L. F., Ribeiro, R. S., & Haddad, C. F. B. (2007). Anurans as prey: An exploratory analysis and size relationships between predators and their prey. Journal of Zoology, 271, 170–177.

    Article  Google Scholar 

  • Torres-Suárez, O. L., & Vargas-Salina, F. (2014). Rhinella humboldti (Gallardo 1965). Catálogo De Anfibios y Reptiles De Colombia, 2(2), 19–23.

    Google Scholar 

  • Tulli, M. J., Abdala, V., & Cruz, F. B. (2012). Effects of different substrates on the sprint performance of lizards. The Journal of Experimental Biology, 215, 774–784.

    Article  PubMed  Google Scholar 

  • Urra, F. A. (2013). Síntesis del conocimiento actual sobre los sapos Rhinella atacamensis, R. arunco y R. spinulosa. La Chiricoca, 16, 4–15.

    Google Scholar 

  • Varela-Jaramillo, A., & Ron, S. R. (2018). Rhinella poeppigii. In S. R. Ron, A. Merino-Viteri, & D. A. Ortiz (Eds.), Anfibios del Ecuador. Version 2019.0. Museo de Zoología.Pontificia Universidad Católica del Ecuador.

    Google Scholar 

  • Vassallo, A. I., Becerra, F., Echeverría, A. I., Díaz, A. O., Longo, M. V., Cohen, M., & Buezas, G. N. (2019). Analysis of the form-function relationship: Digging behavior as a case study. Journal of Mammalian Evolution. https://doi.org/10.1007/s10914-019-09492-7

    Article  Google Scholar 

  • Wagley, R. (2019). Species Account Citation: AmphibiaWeb Rhinella schneideri: Cururu Toad, Rococo Toad. University of California.

    Google Scholar 

  • Wassersug, R. J. (1976). A procedure for differential staining of cartilage and bone in whole formalin-fixed vertebrates. Staining Techniques, 51, 131–134.

    Article  CAS  Google Scholar 

  • West-Eberhard, M. J. (2005). Developmental plasticity and the origin of species differences. Proceedings of the National Academy of Sciences (USA), 102, 6543–6549.

    Article  CAS  Google Scholar 

  • Williams León de Castro, M. W., & Rey Sánchez, D. R. (2014). Primer registro de la presencia y reproducción del anuro Rhinella poeppigii (Tschudi, 1845) en un área antrópica del Departamento de Lima, Perú. Ecología Aplicada, 13(2), 109–115.

  • Wyles, J. S., Kunkel, J. G., & Wilson, A. C. (1983). Birds, behavior, and anatomical evolution. Proceedings of the National Academy of Sciences USA, 80(14), 4394–4397.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

María Florencia Daneri helped in the early design of the experimental device and Marcelo Ibarzabal helped to build it. Federico Becerra helped capturing specimens in the field. Martina Vassallo helped during photograph of behavioral recording. Silvia Etcheverry helped with the specimens of the herpetological collection of CICyTTP-CONICET (Diamante). Martín Pereyra (IBS CONICET, Argentina) and Julián Faivovich (MACN CONICET, Argentina) suggested useful literature. We are also grateful to Mariana Chuliver Pereyra and Miriam C. Vera for contributing with photos used in this study.

Funding

This research was funded in part by Grants PICT 4300-2016 (FONCYT) and UBACYT 20020160100068BA (University of Buenos Aires), Argentina, to RNM; by Grants PIP 2014-2016 (CONICET) No. 11220130100375 and EXA918/18 (University of Mar del Plata) to AIV; and by Grants PICT 2772-2016, PICT 0832-2018 (FONCYT) and PIP 0389 (CONICET) to VA.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rubén N. Muzio.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vassallo, A.I., Manzano, A., Abdala, V. et al. Can Anyone Climb? The Skills of a Non-specialized Toad and its Bearing on the Evolution of New Niches. Evol Biol 48, 293–311 (2021). https://doi.org/10.1007/s11692-021-09539-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-021-09539-9

Keywords

Navigation