Abstract
Aposematism is an anti-predator strategy where predators learn to associate the warning signal on prey with an unpleasant experience, and consequently, avoid attacking similar prey in the future. Conspicuous coloration in poison frogs (Dendrobatidae) is considered a warning signal. During parental care, parents transport their tadpoles on the dorsum, which could alter the detectability and recognition of such warning coloration by visually oriented predators. We tested this hypothesis using domestic chicks trained to avoid and discriminate between printed frog models with and without conspicuous-warning coloration. We tested whether the chicks recognized the warning coloration on printed frog models that varied in the quantity of tadpoles on the dorsum. Chicks first attacked frog models without warning coloration, whether they had tadpoles on the dorsum or not. In contrast, frog models with warning coloration were attacked last by chicks. Moreover, the frog models with warning coloration and without tadpoles experienced a lower risk of attack by chicks than similar frog models with tadpoles. However, aposematic frog models maintained the warning function of conspicuous coloration if it was located on parts of the parent's body that are not covered by the tadpoles when transported. Our results suggest that tadpoles on the dorsum of parents might compromise the effectiveness of the warning signal display in poison frogs increasing the risk of attack by visually oriented predators.
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Script used in this study is available at the FigShare data repository https://figshare.com/s/0855586b4a985625214e
References
Aichinger M (1991) Tadpole transport in relation to rainfall, fecundity, and body size in five species of poison frogs from Amazonian Peru. Amphibia-Reptilia 12:49–55
Amézquita A, Flechas SV, Lima AP et al (2011) Acoustic interference and recognition space within a complex assemblage of dendrobatid frogs. PNAS 108:17058–17063
Amézquita A, Castro L, Arias M et al (2013) Field but not lab paradigms support generalisation by predators of aposematic polymorphic prey: the Oophaga histrionica complex. Evol Ecol 27:769–782
Aronsson M, Gamberale-Stille G (2008) Domestic chicks primarily attend to colour, not pattern, when learning an aposematic coloration. Anim Behav 75:417–423
Aronsson M, Gamberale-Stille G (2009) Importance of internal pattern contrast and contrast against the background in aposematic signals. Behav Ecol 20:1356–1362
Aronsson M, Gamberale-Stille G (2012) Evidence of signaling benefits to contrasting internal color boundaries in warning coloration. Behav Ecol 24:349–354
Bajger, J (1980) Diversity of defensive responses in populations of fire toads (Bombina bombina and Bombina variegata). Herpetologica 133–137
Banci KR, Eterovic A, Marinho PS, Marques OA (2020) Being a bright snake: Testing aposematism and mimicry in a neotropical forest. Biotropica 52:1229–1241
Barbour T (1905) The Vertebrata of Gorgona Island, Colombia: Reptilia; Amphibia. Bull Museum Comp Zool Camb Mass 46:98–102
Barnett JB, Scott-Samuel NE, Cuthill IC (2016) Aposematism: balancing salience and camouflage. Biol Lett 12(8):20160335
Barnett JB, Redfern AS, Bhattacharyya-Dickson R et al (2017) Stripes for warning and stripes for hiding: spatial frequency and detection distance. Behav Ecol Sociobiol 28:373–381
Barnett JB, Michalis C, Scott-Samuel NE, Cuthill IC (2018) Distance-dependent defensive coloration in the poison frog Dendrobates tinctorius, Dendrobatidae. PNAS 115(25):6416–6421
Barnett JB, Varela BJ, Jennings BJ et al (2021) Habitat disturbance alters color contrast and the detectability of cryptic and aposematic frogs. Behav Ecol 32(5):814–825
Bateman P, Fleming P, Wolfe A (2017) A different kind of ecological modelling: the use of clay model organisms to explore predator–prey interactions in vertebrates. J Zool 301:251–262
Beck KB, Loretto MC, Ringler M et al (2017) Relying on known or exploring for new? Movement patterns and reproductive resource use in a tadpole-transporting frog. PeerJ 5:e3745
Bell WJ (1991) Searching behaviour: the behavioural ecology of finding resources. Springer, Southport
Bernal-Bautista MH, Luna-Mora VF, Gallego O, Quevedo-Gil A (2007) A new species of poison frog (Amphibia: Dendrobatidae) from the Andean mountains of Tolima, Colombia. Zootaxa 1638:59–68
Bordignon D, Caorsi Z, Colombo P et al (2018) Are the unken reflex and the aposematic colouration of Red-Bellied Toads efficient against bird predation? PLoS ONE 13:e0193551
Boulenger GA (1882) Catalogue of the Batrachia Salientia s Ecaudata in the Collection of the British Museum, 2nd edn. Taylor and Francis, London
Boulenger GA (1883) On a collection of frogs from Yurimaguas, Huallaga River, Northern Peru Proc. Zool Soc Lond 1883:635–638
Boulenger GA (1899) Descriptions of new reptiles and batrachians collected by Mr P O Simons in the Andes of Ecuador. Ann Mag Nat Hist Ser 7(4):454–457
Brandley N, Johnson M, Johnsen S (2016) Aposematic signals in North American black widows are more conspicuous to predators than to prey. Behav Ecol 27:1104–1112
Braun PC, Braun CAS (1979) Nova espécie de Melanophryniscus Gallardo, 1961 do Estado do Rio Grande do Sul, Brasil (Anura, Bufonidae) Iheringia. Série Zoologia 54:7–17
Briolat ES, Burdfield-Steel ER, Paul SC et al (2019) Diversity in warning coloration: selective paradox or the norm? Biol Rev 94:388–414
Brown JL (2013) The evolution of parental care, aposematism, and color diversity in Neotropical poison frogs. Evol Ecol 27:825–829
Brown JL, Twomey EM (2009) Complicated histories: three new species of poison frogs of the genus Ameerega (Anura: Dendrobatidae) from north-central Peru. Zootaxa 2049:1–38
Brown JL, Twomey EM, Pepper M, Sanchez-Rodriguez M (2008a) Revision of the Ranitomeya fantastica species complex with description of two new species from central Peru (Anura: Dendrobatidae). Zootaxa 1823:1–24
Brown JL, Twomey E, Morales V, Summers K (2008b) Phytotelm size in relation to parental care and mating strategies in two species of Peruvian poison frogs. Behaviour 145:1139–1165
Caldwell JP (1996) The evolution of myrmecophagy and its correlates in poison frogs (Family Dendrobatidae). J Zool 240:75–101
Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, London
Carvajal-Castro JD, Vargas-Salinas F, Casas-Cardona S et al (2021) Aposematism facilitates the diversification of parental care strategies in poison frogs. Sci Rep 11:1–15
Casas-Cardona S, Márquez R, Vargas-Salinas F (2018) Different colour morphs of the poison frog Andinobates bombetes (Dendrobatidae) are similarly effective visual predator deterrents. Ethology 124:245–255
Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton
Cope ED (1868) An examination of the Reptilia and Batrachia obtained by the Orton Expedition to Ecuador and the Upper Amazon, with notes on other species Proc. Acad Nat Sci 20:96–140
Cope ED (1871) Ninth contribution to the herpetology of tropical America. Proc Acad Nat Sci 23:200–224
Cott HB (1940) Adaptive coloration in animals. Methuen, London
Crothers L, Gering E, Cummings M (2011) Aposematic signal variation predicts male-male interactions in a polymorphic poison frog. Evolution 65:599–605
Cuthill IC, Stevens M, Sheppard J et al (2005) Disruptive coloration and background pattern matching. Nature 434:72–74
Cuvier G (1797) "An VI" Tableau Élémentaire de l'Histoire Naturelle des Animaux Paris: Baudoin
Daly J (1982) Alkaloids of neotropical poison frogs (Dendrobatidae). Fortschr Der Chem Organ Nat/progress in the Chem Org Nat Prod 41:205–340
Darst CR, Cummings ME, Cannatella DC (2006) A mechanism for diversity in warning signals: conspicuousness versus toxicity in poison frogs. PNAS 103:5852–5857
David GK, Mitchel K (2012) Survival analysis: a self-learning text. Springer, Berlin
Dessai S, Patil V (2019) Testing and interpreting assumptions of COX regression analysis. Cancer Res Stat Treat 2:108
Dixon LM, Brocklehurst S, Sandilands V et al (2014) Measuring motivation for appetitive behaviour: food-restricted broiler breeder chickens cross a water barrier to forage in an area of wood shavings without food. PLoS ONE 9:e102322
Downie JR, Robinson E, Linklater-McLennan RJ et al (2005) Are there costs to extended larval transport in the Trinidadian stream frog, Mannophryne trinitatis (Dendrobatidae)? J Nat Hist 39:2023–2034
Dreher CE, Cummings ME, Prohl H (2015) An Analysis of predator selection to affect aposematic coloration in a poison frog species. PLoS ONE 10:e0130571
Dumbacher JP, Beehler BM, Spande TF (1992) Homobatrachotoxin in the genus Pitohui: chemical defense in birds? Science 258:799–801
Endler JA (1991) Interactions between predators and prey. In: Krebs JR, Davies NB (eds) Behavioral ecology, 3d edn. Blackwell Scientific, Oxford, pp 169–196
Endler JA, Mappes J (2004) Predator mixes and the conspicuousness of aposematic signals. Am Nat 163:532–547
Exnerová A, Svádová K, Štys P et al (2006) Importance of colour in the reaction of passerine predators to aposematic prey: experiments with mutants of Pyrrhocoris apterus (Heteroptera). Biol J Linn Soc 88:143–153
Exnerová A, Ježová D, Štys P et al (2015) Different reactions to aposematic prey in 2 geographically distant populations of great tits. Behav Ecol 26:1361–1370
Fox J, Weisberg S (2018) An R companion to applied regression. Sage Publications, Thousand Oaks
Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/ audio coding and live observations. Methods Ecol Evol 7:1325–1330
Frost DR (2022) Amphibian species of the world: an online reference. Version 6.1 electronic database. In: https://amphibiansoftheworld.amnh.org/index.php. American Museum of Natural History, New York, USA. Accessed April 2022
Gamberale-Stille G, Guilford T (2003) Contrast versus colour in aposematic signals. Anim Behav 65:1021–1026
Gamberale-Stille G, Tullberg BS (1999) Experienced chicks show biased avoidance of stronger signals: an experiment with natural colour variation in live aposematic prey. Evol Ecol 13:579–589
Gamberale-Stille G, Tullberg BS (2001) Fruit or aposematic insect? Context-dependent colour preferences in domestic chicks. Proc Biol Sci 268:2525–2529
Gottsberger B, Gruber E (2004) Temporal partitioning of reproductive activity in a neotropical anuran community. J Trop Ecol 20(3):271–280
Guilford T (1986) How do" warning colours" work? Conspicuousness may reduce recognition errors in experienced predators. Anim Behav 4:286–288
Halpin CG, Penacchio O, Lovell PG et al (2020) Pattern contrast influences wariness in naive predators towards aposematic patterns. Sci Rep 10:9246
Ham AD, Osorio D (2007) Colour preferences and colour vision in poultry chicks. Proc Biol Sci 274:1941–1948
Ham AD, Ihalainen E, Lindström L, Mappes J (2006) Does colour matter? The importance of colour in avoidance learning, memorability, and generalisation. Behav Ecol Sociobiol 60:482–491
Hämäläinen L, Thorogood R (2020) The signal detection problem of aposematic prey revisited: integrating prior social and personal experience. Philos Trans R Soc Lond B Biol Sci 375:20190473
Hatle JD, Salazar BA (2001) Aposematic coloration of gregarious insects can delay predation by an ambush predator. Environ Entomol 30:51–54
Hauglund K, Hagen SB, Lampe HM (2006) Responses of domestic chicks (Gallus gallus domesticus) to multimodal aposematic signals. Behav Ecol 17:392–398
Hegna RH, Saporito RA, Gerow KG, Donnelly MA (2011) Contrasting colors of an aposematic poison frog do not affect predation. Ann Zool Fenn 48(1):29–38
Honma A, Mappes J, Valkonen JK (2015) Warning coloration can be disruptive: aposematic marginal wing patterning in the wood tiger moth. Ecol Evol 5:4863–4874
Jöels M, Pu Z, Wiegert O et al (2006) Learning under stress: how does it work? Trends Cog. Sci 10:152–158
Jungfer KH (1989) Pfeilgiftfrösche der Gattung Epipedobates mit rot granuliertem Rücken aus dem Oriente von Ecuador and Peru. Salamandra 25:81–98
Kaefer IL, Montanarin A, Da Costa RS, Lima AP (2012) Temporal patterns of reproductive activity and site attachment of the brilliant-thighed frog Allobates femoralis from central Amazonia. J Herpetol 46(4):549–554
Kahn TR, La Marca E, Lötters S (2016) Aposematic Poison Frogs (Dendrobatidae) of the Andean Countries: Bolivia, Colombia, Ecuador, Peru. Arlington
Kazemi B, Gamberale-Stille G, Tullberg BS, Leimar O (2014) Stimulus salience as an explanation for imperfect mimicry. Curr Biol 24:965–969
Killius AM, Dugas MB (2014) Tadpole transport by male Oophaga pumilio (Anura: Dendrobatidae): an observation and brief review. Herpetol Notes 7:747–749
Kneller M, Henle K (1985) Ein neuer Blattsteiger-Frosch (Salientia: Dendrobatidae: Phyllobates) aus Peru. Salamandra 21:62–69
Lawrence JP, Noonan BP (2018) Avian learning favors colorful, not bright, signals. PLoS ONE 13(3):e0194279
Lawrence JP, Rojas B, Fouquet A et al (2019) Weak warning signals can persist in the absence of gene flow. PNAS 116:19037–19045
Lehtinen R, Lannoo MJ, Wassersug RJ (2004) Phytotelm-breeding anurans: past, present, and future research. Misc Publ Mus Zool Univ Mich 193:1–9
Lev-Yadun S (2003) Weapon (thorn) automimicry and mimicry of aposematic colorful thorns in plants. J Theor Biol 224:183–188
Lindström L, Alatalo RV, Mappes J et al (1999) Can aposematic signals evolve by gradual change? Nature 397:249–251
Linnaeus C (1761) Fauna Svecica sisten Animalia Sveciae Regni Mammalia, Aves, Amphibia, Pisces, Insecta, Vermes Distributa per Classes & Ordines, Genera & Species, cum Differentiis Specierum, Synonymis Auctorum, Nominibus Incolarum, Locis Natalium Descriptionibus Insectorum. Editio altera Stockholm: Laurentius Salvius
Loeffler-Henry K, Kang C, Yip Y et al (2018) Flash behavior increases prey survival. Behav Ecol 29:528–533
Lötters S, Mutschmann F, Schimidt W (2007) Poison frogs: biology, species, and captive care. Edition Chimaira
Lynn SK (2005) Learning to avoid aposematic prey. Anim Behav 70:1221–1226
Mappes J, Marples N, Endler JA (2005) The complex business of survival by aposematism. Trends Ecol Evol 20(11):598–603
Márquez R, Mejía-Vargas D, Palacios-Rodríguez P et al (2017) A new species of Andinobates (Anura: Dendrobatidae) from the Urabá region of Colombia. Zootaxa 4290:531–546
Mastrota NF, Mench JA (1995) Colour avoidance in northern bobwhites: effects of age, sex, and previous experience. Anim Behav 50:519–526
Matsushima T, Izawa EI, Aoki N, Yanagihara S (2003) The mind through chick eyes: memory, cognition, and anticipation. Zool Sci 20:395–409
McDiarmid R, Altig R (1999) Tadpoles: the biology of anuran larvae. University of Chicago Press, London
Moore, DF (2016) Applied survival analysis using R. Springer Chams
Myers CW, Daly JW (1980) Taxonomy and ecology of Dendrobates bombetes, a new Andean poison frog with new skin toxins. Am Mus Novit 2692:1–23
Myers CW, Daly JW, Malkin B (1978) A dangerously toxic new frog (Phyllobates) used by Emberá Indians of western Colombia, with discussion of blowgun fabrication and dart poisoning. Bull Am Mus Nat Hist 161:307–366
Navas CA (1996) Metabolic physiology, locomotor performance, and thermal niche breadth in neotropical anurans. Physiol Zool 69:1481–1501
Nokelainen O, Stevens M (2016) Camouflage. Curr Biol 26:R654-656
Nokelainen O, Moraes Rezende F, Valkonen JK, Mappes J (2022) Context-dependent coloration of prey and predator decision making in contrasting light environments. Behav Ecol 33(1):77–86
Osorio D, Miklósi A, Gonda Z (1999) Visual ecology and perception of coloration patterns by domestic chicks. Evol Ecol 13:673–689
Palacios-Rodríguez P, González-Santoro M, Amézquita A, Brunetti AE (2022) Sexual dichromatism in a cryptic poison frog is correlated with female tadpole transport. Evol Ecol 36:153–162
Pašukonis A, Loretto MC (2020) Predation on the Three–striped poison frog, Ameerega trivitatta (Boulenger 1884; Anura: Dendrobatidae), by Erythrolamprus reginae (Linnaeus 1758; Squamata: Collubridae). Herpetol Notes 13:557–559
Pašukonis A, Beck KB, Fischer MT et al (2017) Induced parental care in a poison frog: a tadpole cross–fostering experiment. J Exp Biol 220:3949–3954
Pašukonis A, Loretto MC, Rojas B (2019) How far do tadpoles travel in the rainforest? Parent–assisted dispersal in poison frogs. Evol Ecol 33:613–623
Pough FH, Taigen TL (1990) Metabolic correlates of the foraging and social behaviour of dart-poison frogs. Anim Behav 39:145–155
Poulton EB (1890) The colours of animals: their meaning and use, especially considered in the case of insects. D Appleton
Preißler K, Pröhl H (2017) The effects of background coloration and dark spots on the risk of predation in poison frog models. Evol Ecol 31:683–694
Pröhl H (2005) Territorial behavior in dendrobatid frogs. J Herpetol 39:354–365
Pröhl H, Hödl W (1999) Parental investment, potential reproductive rates, and mating system in the strawberry dart-poison frog Dendrobates Pumilio. Behav Ecol Sociobiol 46(4):215–220
Qvarnström A, Rudh A, Edstrom T, Odeen A et al (2014) Coarse dark patterning functionally constrains adaptive shifts from aposematism to crypsis in strawberry poison frogs. Evolution 68:2793–2803
Ramos-Torres DI, Caicedo-Moncada JF (2019) Predation event on the poison frog Ameerega trivittata (Spix, 1824) by the giant fishing spider Ancylometes rufus (Walckenaer, 1837). Herpetol Notes 12:1167–1168
Ringler E, Pašukonis A, Hödl W, Ringler M (2013) Tadpole transport logistics in a Neotropical poison frog: indications for strategic planning and adaptive plasticity in anuran parental care. Front Zool 10:67
Ringler E, Pasukonis A, Ringler M, Huber L (2016) Sex-specific offspring discrimination reflects respective risks and costs of misdirected care in a poison frog. Anim Behav 114:173–179
Rivero JA, Serna MA (1986) Dos nuevas especies de Colostethus (Amphibia, Dendrobatidae). Caldasia Bogotá 15:525–531
Rojas B (2016) Behavioural, ecological, and evolutionary aspects of diversity in frog colour patterns. Biol Rev 92:1059–1080
Rojas B, Devillechabrolle J, Endler JA (2014) Paradox lost: variable colour–pattern geometry is associated with differences in movement in aposematic frogs. Biol Lett 10(6):20140193
Rojas B, Burdfield-Steel E, De Pasqual C et al (2018) Multimodal aposematic signals and their emerging role in mate attraction. Front Ecol Evol 6:93
Roper T (1990) Responses of domestic chicks to artificially coloured insect prey: effects of previous experience and background colour. Anim Behav 39:466–473
Roper T, Cook S (1989) Responses of chicks to aposematic prey: effects of prey colour and early experience. Behaviour 100:276–293
Roper T, Wistow R (1986) Aposematic colouration and avoidance learning in chicks. Q J Ex Psychol Sect B 38:141–149
Rößler DC, Lötters S, Mappes J, Valkonen JK et al (2019) Sole coloration as an unusual aposematic signal in a Neotropical toad. Sci Rep 9:1–11
Rößler DC, Lötters S, Veith M et al (2020) An amplicon sequencing protocol for attacker identification from DNA traces left on artificial prey Methods. Ecol Evol 11:1338–1347
Rowland HM, Fulford AJ, Ruxton GD (2017) Predator learning differences affect the survival of chemically defended prey. Anim Behav 124:65–74
Royle NJ, Smiseth PT, Kölliker M (2012) The evolution of parental care. Oxford University Press, Oxford
Rueda-Almonacid JV, Rada M, Sánchez-Pacheco SJ et al (2006) Two new and exceptional poison dart frogs of the genus Dendrobates (Anura: Dendrobatidae) from the northeastern flank of the cordillera Central of Colombia. Zootaxa 1259:39–54
Ruxton G, Sherratt T, Speed M (2018) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford
Santos JC (2012) Fast molecular evolution associated with high active metabolic rates in poison frogs. Mol Biol 29:2001–2018
Santos JC, Cannatella DC (2011) Phenotypic integration emerges from aposematism and scale in poison frogs. PNAS 108:6175–6180
Santos JC, Coloma LA, Cannatella DC (2003) Multiple, recurring origins of aposematism and diet specialization in poison frogs. PNAS 100:12792–12797
Santos JC, Baquero M, Barrio-Amoros C et al (2014) Aposematism increases acoustic diversification and speciation in poison frogs. Proc Biol Sci 281:20141761
Saporito RA, Zuercher R, Roberts M et al (2007) Experimental evidence for aposematism in the dendrobatid poison frog Oophaga pumilio. Copeia 4:1006–1011
Schmidt O (1857) Diagnosen neuer Frösche des zoologischen Cabinets zu Krakau Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften, Mathematisch-Naturwissenschaftliche Classe 24:10–15
Schuler W, Hesse E (1985) On the function of warning coloration: a black and yellow pattern inhibits prey–attack by naive domestic chicks. Behav Ecol 16:249–255
Schuler W, Roper TJ (1992) Responses to warning coloration in avian predators. Adv Study Behav 12:111–146
Segami Marzal JC, Rudh A, Rogell B et al (2017) Cryptic female Strawberry poison frogs experience elevated predation risk when associating with an aposematic partner. Ecol Evol 7:744–750
Seshadri KS, Thaker M (2022) Correlated evolution of parental care with dichromatism, colours, and patterns in anurans. Evolution 76(4):737–748
Seymoure BM, Raymundo A, McGraw KJ et al (2018) Environment-dependent attack rates of cryptic and aposematic butterflies. Curr Zool 64:663–669
Sherratt TN (2011) The optimal sampling strategy for unfamiliar prey. Evolution 65:2014–2025
Sherratt TN, Beatty CD (2003) The evolution of warning signals as reliable indicators of prey defense. Am Nat 162:377–389
Siegel S (1956) Nonparametric statistics for the behavioral sciences. J Nerv Ment Dis 125(3):497
Skelhorn J, Halpin CG, Rowe C (2016) Learning about aposematic prey. Behav Ecol 27:955–964
von Spix JB (1824) Animalia nova sive Species novae Testudinum et Ranarum quas in itinere per Brasiliam annis MDCCCXVII–MDCCCXX jussu et auspiciis Maximiliani Josephi I Bavariae Regis München:F S Hübschmann
Stevens M, Cuthill IC (2006) Disruptive coloration, crypsis and edge detection in early visual processing. Proc Biol Sci 273:2141–2147
Stevens M, Merilaita S (2011) Animal camouflage: mechanisms and function. Cambridge University Press, Cambridge
Stevens M, Ruxton GD (2012) Linking the evolution and form of warning coloration in nature. Proc Biol Sci 279:417–426
Summers K, Tumulty J (2014) Parental care, sexual selection, and mating systems in neotropical poison frogs. In: Sexual Selection. Elsevier, pp 289–320
Summers K, McKeon CS (2004) The evolutionary ecology of phytotelmata use in Neotropical poison frogs. Misc Publ Mus Zool Univ Mich 193:55–73
Svádová K, Exnerová A, Štys P et al (2009) Role of different colours of aposematic insects in learning, memory, and generalization of naïve bird predators. Anim Behav 77:327–336
Tarvin RD, Powell EA, Santos JC et al (2017) The birth of aposematism: High phenotypic divergence and low genetic diversity in a young clade of poison frogs. Mol Phylogenet Evol 109:283–295
Therneau TM (2015) coxme: Mixed effects cox models (R Package Version: 2–2, 2015). https://cranr-projectorg/web/packages/coxme/vignettes/coxmepdf. Accessed March 2021
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed), Sexual Selection, and the descent of the Man: 1871–1971. Aldine de Gruyter, Chicago pp 136–179
Tullberg BS, Merilaita S, Wiklund C (2005) Aposematism and crypsis combined as a result of distance dependence: functional versatility of the colour pattern in the swallowtail butterfly larva. Proc Biol Sci 272:1315–1321
Veech JA (2012) Significance testing in ecological null models. Thyroid Res 5:611–616
Wang IJ, Shaffer HB (2008) Rapid color evolution in an aposematic species: A phylogenetic analysis of color variation in the strikingly polymorphic strawberry poison-dart frog. Evolution 62:2742–2759
Wells KD (1980) Evidence for growth of tadpoles during parental transport in Colostethus inguinalis. J Herpetol 14:428–430
Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chicago
Wells KD, Taigen TL (1992) The energetics of reproductive behavior. In: Feder ME, Burggren WW (eds) Environmental physiology of the amphibians. University of Chicago Press Chicago, pp 410–426
Weygoldt P (1987) Evolution of parental care in dart poison frogs (Amphibia: Anura: Dendrobatidae). J Zool Syst Evol Res 25:51–67
Whitlock M, Schluter D (2015) The analysis of biological data. Roberts Publishers, New York
Acknowledgements
We are grateful to Emmanuel Valencia, Edward Toro, Yamileth Gómez, Valentina Toro, Gustavo Lupaco and Rubiel Londoño, for their valuable help during experiments in the middle of a pandemic. To Finca Agroecológica "El Recuerdo" for hosting chicks. Also, thanks to Bibiana Rojas, Víctor Hugo García-Merchán, Marco Gonzalez-Santoro, Roberto Márquez, and members of the research group EECO for invaluable comments on previous versions of this manuscript. Two anonymous reviewers and the editor help to greatly improve previous versions of this manuscript with their suggestions. To Genrietta Yagudayeva and María Isabel Mejía for improving the English of the manuscript. Finally, thanks to Universidad del Quindío (Colombia) for logistical support and research permits.
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All authors contributed to the study conception and design. J.D.C.C., S.C.C, and F.V.S developed the research concept. Experiments, data collection and analysis were performed by M.P.T.G. All authors planned the research, interpreted the data, read, edited, and approved the final manuscript.
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Survival curves used to test the proportional hazard assumption for the survival analysis performed in phase III. Note that the curves do not cross each other and are constant over time. Supplementary file2 (JPG 303 KB)
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Results of the Nemenyi post hoc analysis. P values > 0.05 in pairwise comparison indicate differences in chick attack order between frog model types. Supplementary file3 (TIF 9835 KB)
Experimental arena used for Phases I, II, and III (see methodology in the text for details). Supplementary file4 (MOV 6642 KB)
Chick performance during Phases I, II, and III (see methodology in the text for details). Supplementary file5 (MOV 130886 KB)
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Toro-Gómez, M.P., Carvajal-Castro, J.D., Casas-Cardona, S. et al. Experimental evidence in a poison frog model suggests that tadpole transport on the dorsum may affects warning signal effectiveness in poison frogs. Evol Ecol 37, 267–289 (2023). https://doi.org/10.1007/s10682-022-10219-z
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DOI: https://doi.org/10.1007/s10682-022-10219-z