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Experimental evidence that toe-tapping behavior in the green-and-black poison frog (Dendrobates auratus) is related to prey detection

Experimental evidence that toe-tapping behavior in the green-and-black poison frog (Dendrobates... Toe-tapping, the quick movement of the middle toes of the hind legs, has been observed in many frogs and toads, and is usu- ally associated with feeding, calling, or courtship behaviors. While plenty of observations of toe-tapping exist for different species, experimental evidence regarding the stimuli triggering this behavior is almost non-existent. Here, we systematically tested the influence of different stimuli on the toe-tapping behavior in the green-and-black poison frog ( Dendrobates auratus, Dendrobatidae) from a captive colony in the Zoo Frankfurt. We found that, compared to a control, both big and small prey animals (crickets and fruit flies) elicited much more toe-tapping behavior, and that toe-tapping was positively correlated to feeding events. Playback advertisement calls in contrast did not trigger toe-tapping. We further showed that also juvenile frogs already toe-tap, but less frequently than adults. Our results support the observation-based data that toe-tapping is associated with hunting behaviors. While the auditory part of courtship does not seem to trigger toe-tapping, experimental evidence regarding visual and/or tactile courtship stimuli is still lacking. Keywords Advertisement calls · Amphibia · Dendrobatidae · Predation · Vibrational communication Introduction Claessens et al. 2020). While pedal luring (in horned frogs, Ceratophrys; Murphy 1976) and toe-waving (in cane toads, Many animal species use multimodal communication to Rhinella marina; Hagman and Shine 2008) have been shown interact with con- and heterospecifics (Higham and Hebets to function as visual lure for specific prey items (particu- 2013). In some cases, single behavioral components may larly other anurans), the function of toe-tapping, the fast serve as multimodal stimuli, such as specific movements, up- and down-movement of the middle toes of the hind which can be detected in the visual, tactile, and/or auditory legs (Fig. 1), is still less clear. Sloggett and Zeilstra (2008) domain (Sloggett and Zeilstra 2008). Such specific move - suggest that the substrate vibration caused by toe-tapping ments can be found, for example, in many spiders (e.g., Elias might not attract, but agitate prey (i.e., trigger movement), et al. 2012), insects (for review, see Virant-Doberlet et al. making the prey animals easier to detect for the frogs. This 2022), and amphibians. The latter move their limbs or dig- was further underlined by a multi-species analysis based on its during hunting and/or courtship, potentially to influence online-video material: toe-tapping behavior was observed the behavior of prey or mates. These so-called pedal luring, more frequently when prey animals were inactive than when toe-waving, and toe-tapping/twitching behaviors have been they were moving (Claessens et al. 2020). Contrary to this, observed in a large variety of anuran species and families Erdmann (2017) showed that toe-tapping vibrations in Gulf (for overview see Sloggett and Zeilstra 2008; Erdmann 2017; Coast toads (Incilius nebulifer) caused prey to move less, but change movement directions toward the predator. This supports another hypothesis made by Sloggett and Zeilstra (2008), stating that toe-tapping behavior might serve as a * Lisa M. Schulte Schulte@bio.uni-frankfurt.de prey-mimicking vibrational lure. However, tapping behaviors have not only been observed Wildlife-/Zoo-Animal-Biology and Systematics, in relation to hunting and feeding. Starnberger et al. (2018) Faculty of Biological Sciences, Goethe University, observed male spotted reed frogs (Hyperolius puncticulatus) Frankfurt, Frankfurt/Main, Germany Vol.:(0123456789) 1 3 acta ethologica respectively). For this, we systematically tested which of the three stimuli—small prey animals, big prey animals, and conspecific calls—triggered the toe-tapping behavior in green-and-black poison frogs kept in a colony in the Zoo Frankfurt, Germany. Based on previous observations in this species (see above), we hypothesized that all three stimuli would result in increased toe-tapping behavior. Methods Study animals We tested a group of 21 adults and 7 juvenile D. auratus between February and March 2022. The animals were kept together in a 4.2 m (2 m × 1.5 m × 1.4 m) large enclosure in Fig. 1 Adult D. auratus from the Zoo Frankfurt. The middle toes on the Zoo Frankfurt. Depending on the age of the frogs, they the hind legs, which are used for toe-tapping behavior, are marked shared the enclosure with their conspecifics already since with white arrows many years (i.e., the frogs knew each other). The enclo- sure contained a ca. 0.14 m large water body in the front, tapping their feet in response to male playback calls. Toe- several large branches reaching diagonally throughout the tapping during courtship and/or in association with calling tank, plants like blushing bromeliad (Neoregelia carolinae), behaviors was also reported for several dendrobatid species cornstalk dracaena (Dracaena fragrans), ferns (Microlepia (Claessens et al. 2020) as well as in female whipping frogs hookeriana) and spider lily (Crinum asiaticum), and leaf lit- (Polypedates; Narins 1995). In the green-and-black poi- ter on the ground. The animals were kept together with ser- son frog (Dendrobates auratus, Fig. 1), where toe-tapping rated basilisks (Laemanctus serratus), large-headed anoles behavior has first been observed in association with feeding (Anolis cybotes), Smith’s tropical night lizards (Lepido- (Murphy 1976), a recent field observation reports toe-tapping phyma smithii), and Cuvier’s foam froglets (Physalaemus additionally in association with courtship behavior (Barquero cuvieri). Unlike D. auratus, P. cuvieri are night active and and Arguedas 2022). They suggest that toe-tapping might were not visible during the experiments. The reptiles only function as an intraspecific vibratory signal. stayed in the upper part of the enclosure and did not get Unlike for the more specific pedal luring and toe waving in contact with the frogs during the experiments. The day/ behaviors (Murphy 1976; Grafe 2008; Hagman and Shine night cycle was dependent on the natural light, with addi- 2008), most reports on toe-tapping are based on (single) tional artificial light from 10:00 to 17:00. The enclosure was observations from the wild or from pet frogs (e.g., Gagliardo sprayed with an automated sprinkler-system twice per day et  al. 2010; Turner 2011; Barquero and Arguedas 2022). (9:00 and 15:00). Under non-experimental conditions the Apart from a systematic analysis of online video-recordings animals were fed every other day. The main food source for of the latter (Claessens et al. 2020), the only experimental the animals were crickets (Acheata domesticus), regularly data on toe-tapping were, to the best of our knowledge, con- complemented with flight-deprived fruit flies (Drosophila ducted by Erdmann (2017). He tested toe-tapping behavior melanogaster). We could reliably recognize each animal in Gulf Coast toads (Incilius nebulifer) in relationship to based on its individual abdominal pattern, using picture prey animals (and vice versa). Due to the lack of experimen- cards made prior to the experiment when photographing tal evidence and the observation that toe-tapping may also each frog through the glass (i.e., without handling the ani- be related to intraspecific communication, with our study mals). However, we could not distinguish between males we had three goals: (1) we aimed to proof experimentally and females. Due to the very regular mating outcome in the that poison frogs react to prey with toe-tapping behavior, communal enclosure, we assumed a relatively even sex ratio. (2) we tried to find out if different size prey animals trigger toe-tapping behavior in the same manner, or if this behavior Experimental design and data collection is only directed at small or large prey animals, and (3) we aimed to get first experimental data on toe-tapping in rela- Our experiments included four different treatments in the fol- tion to intraspecific communication, focusing here merely lowing order: (i) non-fed control (“control-treatment”), (ii) on vocal communication (i.e., conspecific calls, triggering fed with fruit-flies (“fly-treatment”), (iii) fed with crickets territorial and reproductive behavior in males and females, (“cricket-treatment”), and (iv) confronted with conspecific 1 3 acta ethologica calls (“calls-treatment”). For the control-treatment, frogs 2017) in R 4.2.0 (R-Core-Team 2022). We entered the ID of received their last regular meal the day before and they each frog as well as the daytime of measurement (morning: were not fed during the recordings. The fly treatment as 9:00–11:00, midday: 11:00–13:00, afternoon: 13:00–15:00) well as the cricket-treatment both took place after 2 days of as random effects into the model. Because our data were last feeding, so frogs were most likely hungry. The flies (or overdispersed, observation-level random effects (OLRE) crickets) were presented to the frogs by directly dropping were fitted to the model (Browne et al. 2005). p-values were them ad libitum at the openable front of the enclosure. The obtained by likelihood ratio tests of the full models with the calls-treatment took place at a day when frogs were not fed effect in question (i.e., the different treatments) against the (i.e., 1 day after feeding). A small bluetooth-operated loud model without the effect in question (i.e., without the differ - speaker (JPB® Harman, CLIP2 Portable Bluetooth Speaker) ent treatments; Winter 2013). In order to find which of the was hung on a branch at 30 cm above the ground. Adver- treatments had an influence on the toe-tapping behavior, a tisement calls of D. auratus (recorded at 26 °C in captivity Tukey-corrected post-hoc test (multicomp-package; Hothorn by T. Ostrowski) were played to the frogs at roughly natu- et al. 2008) was conducted. ral volume in a loop. Even though we cannot exclude other To see if feeding events (or attempts) were correlated to potential intraspecific interactions, the intraspecific stimuli toe-tapping behavior, we calculated a Spearman’s rank cor- tested here (i.e., the calls) did not occur during any of the relation in R (after showing with a Shapiro–Wilk normality other treatments, because none of the frogs called at any test that our data were not normally distributed). We did not time of the experiments. During the control- and the calls- observe any calling behaviors during any of the trials, so no treatment, frogs were purposely not fed to be minimally analysis was conducted regarding this behavior. distracted by prey. Although it is possible that subjects have found small insects crawling through the leaf litter of the tank, these food items were very scarce compared to the Results fly- and cricket-treatments. During the treatments, frogs were filmed between 9:00 Toe‑tapping behavior during the different trials and 15:00 with a hand-held camera (Panasonic HC-V380) in a randomized order. Our goal was to record each frog Adult frogs tapped their toes during our recordings for up for 5 min during each trial in order to measure the duration to 56 s per minute, with an average of 16.30 s per minute. of toe-tapping behavior during this time. However, frogs Juveniles also showed toe-tapping behavior, but with an often did not stay in sight for long enough, or their toes average of 5.98 s per minute less than the adults (leading to were not always visible in the recordings. So, recording time an exclusion from the statistical analyses). ranged from 1 min (only in two cases) to 10 min, with an average recording time of 4:52 min per frog per trial. Each frog was only filmed once per trial. The continuous record- ings were analyzed via behavior sampling, with a focus on toe-tapping behavior. The accumulated time (in seconds) was counted for toe-tapping in each frog. To account for the variation in recording time, the average duration per minute was calculated. In addition to the toe-tapping behavior we also recorded all events (or attempts) of feeding for each frog per trial. The juveniles were recorded and analyzed in the same manner as the adults in order to compare the average duration of their toe-tapping behavior with that of the adults. How- ever, because their toe-tapping behavior varied from that of the adults, they were excluded from the statistical analyses. Statistical analysis We performed a generalized linear mixed-effect model of the Fig. 2 Duration of toe-tapping behavior per minute during the differ - relationship between the duration of toe-tapping behavior as ent treatments (control, calls, crickets, fruit flies). The horizontal lines response variable and the treatments (i–iv) as explanatory represent the median, the boxes delimitate the 25th and 75th percen- variable, with a poisson error distribution, using the Tem- tile of the data, and the whiskers the minimum and maximum values plate Model Builder package glmmTMB (Magnusson et al. (excluding the outliers presented by the circles). ***p < 0.001 1 3 acta ethologica Fig. 3 Relationship between feeding events and toe-tapping behavior (pooled from all four treatments). The plot was made in the R-package ggplot 2 (Wickham et al. 2016). Dots represent the data points. The dark line indicates the regres- sion line, with the grey shade marking the 95% confidence interval Our comparison of the null versus the full model showed (Hyperoliidae), for D. auratus, we could not find a relation- that the duration of toe-tapping behavior in the adults ship between playback advertisement calls and toe-tapping. was significantly influenced by the different treatments This contradicts our hypothesis that advertisement calls (χ (2) = 60.77, p < 0.001). When we compared the effects would have the same effect as food. We can, however, not of the trials individually, we found that the effect of the exclude the possibility at this point that the frogs, due to calls-treatment did not differ from the control-treatment their communal enclosure, are generally less interested in (z = 2.08, p = 0.153). The two treatments including food conspecic fi interactions. In addition, we were not able to dif - (i.e., fly-treatment and cricket-treatment), were, however, ferentiate between sexes and cannot rule out if only one and significantly different from both, the control-treatment (flies not both sexes react with toe-tapping to the calls. However, vs. control: z = 6.20, p < 0.001; crickets vs. control: z = 6.15, the generally low amount of toe-tapping observations dur- p < 0.001), as well as the calls-treatment (flies vs. calls: ing this trial rather suggests that neither males nor females z = 5.78, p < 0.001; crickets vs. calls: z = 5.71, p < 0.001). reacted to the calls. But our results do not exclude the possi- Both food-treatments elicited much more toe-tapping behav- bility that toe-tapping behavior is displayed during the physi- ior (Fig. 2). There was no difference in effect between the cal part of courtship, as reported from field observations different types of food offered (z = 0.11, p = 1.0). (Barquero and Arguedas 2022). However, the question to what extent we are dealing with multimodal communica- Toe‑tapping behavior in relation to feeding tion evolved to communicate visually and vibrationally with conspecifics still awaits further testing. As expected, we could count more feeding events (and Regarding the relationship between toe-tapping and feed- attempts) during the fly- and cricket-treatments (on aver - ing, the size (or species) of prey presented to the frogs dur- age 1.78 and 1.96 per minute) than during the control- and ing the food treatments (flies vs. crickets) did not affect the calls-treatments (0.15 and 0.08 per minute). The Spearman’s predators’ response, leading to the conclusion that prey in rank correlation revealed that there was a significant posi- general triggers toe-tapping. However, this behavior seems tive relationship between toe-tapping behavior and feeding to be less pronounced in juveniles, possibly because, due to events (r = 0.62, p < 0.001; Fig. 3). their smaller size, toe-tapping has a weaker effect on the prey animals. What effect this exactly is and if it differs between prey species still needs further investigation, since predic- Discussion tions here diverge (attraction vs. movement stimulation; Erdmann 2017; Sloggett and Zeilstra 2008). All in all, our In this study, we show for the first time experimental evi- experimental results support the online-video analysis based dence for the relationship between toe-tapping behavior and on observational reports from different poison frog species feeding in dendrobatids, supporting part of our hypothesis. (Claessens et al. 2020). Being visual hunters, it is most likely However, unlike Starnberger et al. (2018), who showed that that the frogs’ reaction to prey is based on visual cues (i.e., different types of playback calls (advertisement and aggres- prey movement; Eibl-Eibesfeldt 1951). However, it remains sion) triggered foot-tapping behavior in H. puncticulatus unknown if for example also the smell or 2D-visual stimuli 1 3 acta ethologica Browne WJ, Subramanian SV, Jones K, Goldstein H (2005) Variance (i.e., video recordings) of prey can trigger toe-tapping in partitioning in multilevel logistic models that exhibit overdisper- these animals. Corresponding results would be especially sion. J R Stat Soc 168:599–613 interesting with regard to enrichment of captive (zoo) ani- Claessens LSA, Ganchev NO, Kukk MM, Schutte CJ, Sloggett JJ mals without the involvement of food—a subject that is still (2020) An investigation of toe-tapping behaviour in anurans by analysis of online video resources. J Zool 312:158–162 largely ignored in amphibians (Michaels et al. 2014). Eibl-Eibesfeldt I (1951) Nahrungserwerb und Beuteschema der Erdkröte (Bufo bufo L.). Behaviour 4:1–34 Acknowledgements We are very grateful to the Zoo Frankfurt for their Elias DO, Maddison WP, Peckmezian C, Girard MB, Mason AC financial support and for providing the facilities for this study. We want (2012) Orchestrating the score: complex multimodal courtship in to especially thank Johannes Köhler, Gerrit Wehrenberger, Thomas the Habronattus coecatus group of Habronattus jumping spiders Tikatsch, and the rest of the animal care taker team of the Exotarium (Araneae: Salticidae). Biol J Linn Soc 105:522–547 for their organizational help. We further thank Thomas Ostrowski for Erdmann JA (2017) The function of toe movement in feeding by the providing us with a recording of the natural call of the study species. gulf coast toad (Incilius nebulifer). Master’s thesis. Southeastern Louisiana University, Hammond, Louisiana Author contribution Study conception and methodology: LMS; per- Gagliardo R, Griffith E, Hill R, Ross H, JR MI, Timpe E, Wilson B, formance of the experiments: YK; data analysis: YK, LMS; writing/ (2010) Observations on the captive reproduction of the horned manuscript preparation: LMS, YK. marsupial frog Gastrotheca cornuta (Boulenger 1898). Herpetol Rev 41:52–58 Funding Open Access funding enabled and organized by Projekt Grafe TU (2008) Toe waving in the brown marsh frog Rana baramica: DEAL. Financial support of the Lab by the Zoo Frankfurt. pedal luring to attract prey? Sci Bruneiana 9:3–5 Hagman M, Shine R (2008) Deceptive digits: the functional signifi- Availability of data and materials The datasets generated during and/ cance of toe waving by cannibalistic cane toads, Chaunus mari- or analyzed during the current study are available from the authors on nus. Anim Behav 75:123–131 reasonable request. Higham JP, Hebets EA (2013) An introduction to multimodal com- munication. Behav Ecol Sociobiol 67:1381–1388 Code availability Not applicable. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in gen- eral parametric models. Biometrical J 50:346–363 Declarations Magnusson A, Skaug H, Nielsen A, Berg C, Kristensen K, Maechler M, van Bentham K, Bolker B, Brooks M, Brooks MM (2017) Ethics approval Not applicable. Package ‘glmmtmb.’ R Packag Version 02 0 Michaels CJ, Downie JR, Campbell-Palmer R (2014) The importance Consent to participate Not applicable. of enrichment for advancing amphibian welfare and conservation goals. Amphib Reptil Conserv 8:7–23 Consent for publication All authors gave their consent for the publica- Murphy JB (1976) Pedal luring in the leptodactylid frog, Ceratophrys tion of the manuscript. calcarata Boulenger. Herpetologica 339–341 Narins PM (1995) Comparative aspects of interactive communica- Competing interests The authors declare no competing interests. tion. In: Flock A, Ottoson D, Ulfendahl M (eds) Active hearing. Elvesier Science, London, pp 363–372 Additional declarations for articles in life science journals that report R-Core-Team (2022) R: a language and environment for statistical the results of studies involving humans and/or animals Data collection computing. In: Found. Stat. Comput. https:// www.r- proje ct. org/ conducted with the approval of the Zoo Frankfurt. Sloggett JJ, Zeilstra I (2008) Waving or tapping? Vibrational stim- uli and the general function of toe twitching in frogs and toads Open Access This article is licensed under a Creative Commons Attri- (Amphibia: Anura). Anim Behav 76:e1–e4 bution 4.0 International License, which permits use, sharing, adapta- Starnberger I, Maier PM, Hödl W, Preininger D (2018) Multimodal tion, distribution and reproduction in any medium or format, as long signal testing reveals gestural tapping behavior in spotted reed as you give appropriate credit to the original author(s) and the source, frogs. Herpetologica 74:127–134 provide a link to the Creative Commons licence, and indicate if changes Turner GS (2011) Toe-twitching in juvenile Sudell’s frog ‘Neobatra- were made. The images or other third party material in this article are chus sudelli’. Vic Nat 128:147–149 included in the article's Creative Commons licence, unless indicated Virant-Doberlet M, Stritih-Peljhan N, Žunič-Kosi A, Polajnar J (2022) otherwise in a credit line to the material. If material is not included in Functional diversity of vibrational signaling systems in insects. the article's Creative Commons licence and your intended use is not Annu Rev Entomol 68:191–210 permitted by statutory regulation or exceeds the permitted use, you will Wickham H, Chang W, Wickham MH (2016) Package ‘ggplot2’. Cre- need to obtain permission directly from the copyright holder. To view a ate elegant data visualisations using the grammar of graphics. copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . Version 2:1–189 Winter B (2013) Linear models and linear mixed effects models in R with linguistic applications. arXiv 1308:5499 References Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Barquero MD, Arguedas V (2022) Mass movement and potential vibratory toe signalling in the green and black poison-dart frog, Dendrobates auratus (Amphibia: Dendrobatidae). Herpetol Notes 15:79–82 1 3 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png acta ethologica Springer Journals

Experimental evidence that toe-tapping behavior in the green-and-black poison frog (Dendrobates auratus) is related to prey detection

Schulte, Lisa M.; König, Yannis
acta ethologica , Volume 26 (2) – Jun 1, 2023
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10.1007/s10211-023-00422-8
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Abstract

Toe-tapping, the quick movement of the middle toes of the hind legs, has been observed in many frogs and toads, and is usu- ally associated with feeding, calling, or courtship behaviors. While plenty of observations of toe-tapping exist for different species, experimental evidence regarding the stimuli triggering this behavior is almost non-existent. Here, we systematically tested the influence of different stimuli on the toe-tapping behavior in the green-and-black poison frog ( Dendrobates auratus, Dendrobatidae) from a captive colony in the Zoo Frankfurt. We found that, compared to a control, both big and small prey animals (crickets and fruit flies) elicited much more toe-tapping behavior, and that toe-tapping was positively correlated to feeding events. Playback advertisement calls in contrast did not trigger toe-tapping. We further showed that also juvenile frogs already toe-tap, but less frequently than adults. Our results support the observation-based data that toe-tapping is associated with hunting behaviors. While the auditory part of courtship does not seem to trigger toe-tapping, experimental evidence regarding visual and/or tactile courtship stimuli is still lacking. Keywords Advertisement calls · Amphibia · Dendrobatidae · Predation · Vibrational communication Introduction Claessens et al. 2020). While pedal luring (in horned frogs, Ceratophrys; Murphy 1976) and toe-waving (in cane toads, Many animal species use multimodal communication to Rhinella marina; Hagman and Shine 2008) have been shown interact with con- and heterospecifics (Higham and Hebets to function as visual lure for specific prey items (particu- 2013). In some cases, single behavioral components may larly other anurans), the function of toe-tapping, the fast serve as multimodal stimuli, such as specific movements, up- and down-movement of the middle toes of the hind which can be detected in the visual, tactile, and/or auditory legs (Fig. 1), is still less clear. Sloggett and Zeilstra (2008) domain (Sloggett and Zeilstra 2008). Such specific move - suggest that the substrate vibration caused by toe-tapping ments can be found, for example, in many spiders (e.g., Elias might not attract, but agitate prey (i.e., trigger movement), et al. 2012), insects (for review, see Virant-Doberlet et al. making the prey animals easier to detect for the frogs. This 2022), and amphibians. The latter move their limbs or dig- was further underlined by a multi-species analysis based on its during hunting and/or courtship, potentially to influence online-video material: toe-tapping behavior was observed the behavior of prey or mates. These so-called pedal luring, more frequently when prey animals were inactive than when toe-waving, and toe-tapping/twitching behaviors have been they were moving (Claessens et al. 2020). Contrary to this, observed in a large variety of anuran species and families Erdmann (2017) showed that toe-tapping vibrations in Gulf (for overview see Sloggett and Zeilstra 2008; Erdmann 2017; Coast toads (Incilius nebulifer) caused prey to move less, but change movement directions toward the predator. This supports another hypothesis made by Sloggett and Zeilstra (2008), stating that toe-tapping behavior might serve as a * Lisa M. Schulte Schulte@bio.uni-frankfurt.de prey-mimicking vibrational lure. However, tapping behaviors have not only been observed Wildlife-/Zoo-Animal-Biology and Systematics, in relation to hunting and feeding. Starnberger et al. (2018) Faculty of Biological Sciences, Goethe University, observed male spotted reed frogs (Hyperolius puncticulatus) Frankfurt, Frankfurt/Main, Germany Vol.:(0123456789) 1 3 acta ethologica respectively). For this, we systematically tested which of the three stimuli—small prey animals, big prey animals, and conspecific calls—triggered the toe-tapping behavior in green-and-black poison frogs kept in a colony in the Zoo Frankfurt, Germany. Based on previous observations in this species (see above), we hypothesized that all three stimuli would result in increased toe-tapping behavior. Methods Study animals We tested a group of 21 adults and 7 juvenile D. auratus between February and March 2022. The animals were kept together in a 4.2 m (2 m × 1.5 m × 1.4 m) large enclosure in Fig. 1 Adult D. auratus from the Zoo Frankfurt. The middle toes on the Zoo Frankfurt. Depending on the age of the frogs, they the hind legs, which are used for toe-tapping behavior, are marked shared the enclosure with their conspecifics already since with white arrows many years (i.e., the frogs knew each other). The enclo- sure contained a ca. 0.14 m large water body in the front, tapping their feet in response to male playback calls. Toe- several large branches reaching diagonally throughout the tapping during courtship and/or in association with calling tank, plants like blushing bromeliad (Neoregelia carolinae), behaviors was also reported for several dendrobatid species cornstalk dracaena (Dracaena fragrans), ferns (Microlepia (Claessens et al. 2020) as well as in female whipping frogs hookeriana) and spider lily (Crinum asiaticum), and leaf lit- (Polypedates; Narins 1995). In the green-and-black poi- ter on the ground. The animals were kept together with ser- son frog (Dendrobates auratus, Fig. 1), where toe-tapping rated basilisks (Laemanctus serratus), large-headed anoles behavior has first been observed in association with feeding (Anolis cybotes), Smith’s tropical night lizards (Lepido- (Murphy 1976), a recent field observation reports toe-tapping phyma smithii), and Cuvier’s foam froglets (Physalaemus additionally in association with courtship behavior (Barquero cuvieri). Unlike D. auratus, P. cuvieri are night active and and Arguedas 2022). They suggest that toe-tapping might were not visible during the experiments. The reptiles only function as an intraspecific vibratory signal. stayed in the upper part of the enclosure and did not get Unlike for the more specific pedal luring and toe waving in contact with the frogs during the experiments. The day/ behaviors (Murphy 1976; Grafe 2008; Hagman and Shine night cycle was dependent on the natural light, with addi- 2008), most reports on toe-tapping are based on (single) tional artificial light from 10:00 to 17:00. The enclosure was observations from the wild or from pet frogs (e.g., Gagliardo sprayed with an automated sprinkler-system twice per day et  al. 2010; Turner 2011; Barquero and Arguedas 2022). (9:00 and 15:00). Under non-experimental conditions the Apart from a systematic analysis of online video-recordings animals were fed every other day. The main food source for of the latter (Claessens et al. 2020), the only experimental the animals were crickets (Acheata domesticus), regularly data on toe-tapping were, to the best of our knowledge, con- complemented with flight-deprived fruit flies (Drosophila ducted by Erdmann (2017). He tested toe-tapping behavior melanogaster). We could reliably recognize each animal in Gulf Coast toads (Incilius nebulifer) in relationship to based on its individual abdominal pattern, using picture prey animals (and vice versa). Due to the lack of experimen- cards made prior to the experiment when photographing tal evidence and the observation that toe-tapping may also each frog through the glass (i.e., without handling the ani- be related to intraspecific communication, with our study mals). However, we could not distinguish between males we had three goals: (1) we aimed to proof experimentally and females. Due to the very regular mating outcome in the that poison frogs react to prey with toe-tapping behavior, communal enclosure, we assumed a relatively even sex ratio. (2) we tried to find out if different size prey animals trigger toe-tapping behavior in the same manner, or if this behavior Experimental design and data collection is only directed at small or large prey animals, and (3) we aimed to get first experimental data on toe-tapping in rela- Our experiments included four different treatments in the fol- tion to intraspecific communication, focusing here merely lowing order: (i) non-fed control (“control-treatment”), (ii) on vocal communication (i.e., conspecific calls, triggering fed with fruit-flies (“fly-treatment”), (iii) fed with crickets territorial and reproductive behavior in males and females, (“cricket-treatment”), and (iv) confronted with conspecific 1 3 acta ethologica calls (“calls-treatment”). For the control-treatment, frogs 2017) in R 4.2.0 (R-Core-Team 2022). We entered the ID of received their last regular meal the day before and they each frog as well as the daytime of measurement (morning: were not fed during the recordings. The fly treatment as 9:00–11:00, midday: 11:00–13:00, afternoon: 13:00–15:00) well as the cricket-treatment both took place after 2 days of as random effects into the model. Because our data were last feeding, so frogs were most likely hungry. The flies (or overdispersed, observation-level random effects (OLRE) crickets) were presented to the frogs by directly dropping were fitted to the model (Browne et al. 2005). p-values were them ad libitum at the openable front of the enclosure. The obtained by likelihood ratio tests of the full models with the calls-treatment took place at a day when frogs were not fed effect in question (i.e., the different treatments) against the (i.e., 1 day after feeding). A small bluetooth-operated loud model without the effect in question (i.e., without the differ - speaker (JPB® Harman, CLIP2 Portable Bluetooth Speaker) ent treatments; Winter 2013). In order to find which of the was hung on a branch at 30 cm above the ground. Adver- treatments had an influence on the toe-tapping behavior, a tisement calls of D. auratus (recorded at 26 °C in captivity Tukey-corrected post-hoc test (multicomp-package; Hothorn by T. Ostrowski) were played to the frogs at roughly natu- et al. 2008) was conducted. ral volume in a loop. Even though we cannot exclude other To see if feeding events (or attempts) were correlated to potential intraspecific interactions, the intraspecific stimuli toe-tapping behavior, we calculated a Spearman’s rank cor- tested here (i.e., the calls) did not occur during any of the relation in R (after showing with a Shapiro–Wilk normality other treatments, because none of the frogs called at any test that our data were not normally distributed). We did not time of the experiments. During the control- and the calls- observe any calling behaviors during any of the trials, so no treatment, frogs were purposely not fed to be minimally analysis was conducted regarding this behavior. distracted by prey. Although it is possible that subjects have found small insects crawling through the leaf litter of the tank, these food items were very scarce compared to the Results fly- and cricket-treatments. During the treatments, frogs were filmed between 9:00 Toe‑tapping behavior during the different trials and 15:00 with a hand-held camera (Panasonic HC-V380) in a randomized order. Our goal was to record each frog Adult frogs tapped their toes during our recordings for up for 5 min during each trial in order to measure the duration to 56 s per minute, with an average of 16.30 s per minute. of toe-tapping behavior during this time. However, frogs Juveniles also showed toe-tapping behavior, but with an often did not stay in sight for long enough, or their toes average of 5.98 s per minute less than the adults (leading to were not always visible in the recordings. So, recording time an exclusion from the statistical analyses). ranged from 1 min (only in two cases) to 10 min, with an average recording time of 4:52 min per frog per trial. Each frog was only filmed once per trial. The continuous record- ings were analyzed via behavior sampling, with a focus on toe-tapping behavior. The accumulated time (in seconds) was counted for toe-tapping in each frog. To account for the variation in recording time, the average duration per minute was calculated. In addition to the toe-tapping behavior we also recorded all events (or attempts) of feeding for each frog per trial. The juveniles were recorded and analyzed in the same manner as the adults in order to compare the average duration of their toe-tapping behavior with that of the adults. How- ever, because their toe-tapping behavior varied from that of the adults, they were excluded from the statistical analyses. Statistical analysis We performed a generalized linear mixed-effect model of the Fig. 2 Duration of toe-tapping behavior per minute during the differ - relationship between the duration of toe-tapping behavior as ent treatments (control, calls, crickets, fruit flies). The horizontal lines response variable and the treatments (i–iv) as explanatory represent the median, the boxes delimitate the 25th and 75th percen- variable, with a poisson error distribution, using the Tem- tile of the data, and the whiskers the minimum and maximum values plate Model Builder package glmmTMB (Magnusson et al. (excluding the outliers presented by the circles). ***p < 0.001 1 3 acta ethologica Fig. 3 Relationship between feeding events and toe-tapping behavior (pooled from all four treatments). The plot was made in the R-package ggplot 2 (Wickham et al. 2016). Dots represent the data points. The dark line indicates the regres- sion line, with the grey shade marking the 95% confidence interval Our comparison of the null versus the full model showed (Hyperoliidae), for D. auratus, we could not find a relation- that the duration of toe-tapping behavior in the adults ship between playback advertisement calls and toe-tapping. was significantly influenced by the different treatments This contradicts our hypothesis that advertisement calls (χ (2) = 60.77, p < 0.001). When we compared the effects would have the same effect as food. We can, however, not of the trials individually, we found that the effect of the exclude the possibility at this point that the frogs, due to calls-treatment did not differ from the control-treatment their communal enclosure, are generally less interested in (z = 2.08, p = 0.153). The two treatments including food conspecic fi interactions. In addition, we were not able to dif - (i.e., fly-treatment and cricket-treatment), were, however, ferentiate between sexes and cannot rule out if only one and significantly different from both, the control-treatment (flies not both sexes react with toe-tapping to the calls. However, vs. control: z = 6.20, p < 0.001; crickets vs. control: z = 6.15, the generally low amount of toe-tapping observations dur- p < 0.001), as well as the calls-treatment (flies vs. calls: ing this trial rather suggests that neither males nor females z = 5.78, p < 0.001; crickets vs. calls: z = 5.71, p < 0.001). reacted to the calls. But our results do not exclude the possi- Both food-treatments elicited much more toe-tapping behav- bility that toe-tapping behavior is displayed during the physi- ior (Fig. 2). There was no difference in effect between the cal part of courtship, as reported from field observations different types of food offered (z = 0.11, p = 1.0). (Barquero and Arguedas 2022). However, the question to what extent we are dealing with multimodal communica- Toe‑tapping behavior in relation to feeding tion evolved to communicate visually and vibrationally with conspecifics still awaits further testing. As expected, we could count more feeding events (and Regarding the relationship between toe-tapping and feed- attempts) during the fly- and cricket-treatments (on aver - ing, the size (or species) of prey presented to the frogs dur- age 1.78 and 1.96 per minute) than during the control- and ing the food treatments (flies vs. crickets) did not affect the calls-treatments (0.15 and 0.08 per minute). The Spearman’s predators’ response, leading to the conclusion that prey in rank correlation revealed that there was a significant posi- general triggers toe-tapping. However, this behavior seems tive relationship between toe-tapping behavior and feeding to be less pronounced in juveniles, possibly because, due to events (r = 0.62, p < 0.001; Fig. 3). their smaller size, toe-tapping has a weaker effect on the prey animals. What effect this exactly is and if it differs between prey species still needs further investigation, since predic- Discussion tions here diverge (attraction vs. movement stimulation; Erdmann 2017; Sloggett and Zeilstra 2008). All in all, our In this study, we show for the first time experimental evi- experimental results support the online-video analysis based dence for the relationship between toe-tapping behavior and on observational reports from different poison frog species feeding in dendrobatids, supporting part of our hypothesis. (Claessens et al. 2020). Being visual hunters, it is most likely However, unlike Starnberger et al. (2018), who showed that that the frogs’ reaction to prey is based on visual cues (i.e., different types of playback calls (advertisement and aggres- prey movement; Eibl-Eibesfeldt 1951). However, it remains sion) triggered foot-tapping behavior in H. puncticulatus unknown if for example also the smell or 2D-visual stimuli 1 3 acta ethologica Browne WJ, Subramanian SV, Jones K, Goldstein H (2005) Variance (i.e., video recordings) of prey can trigger toe-tapping in partitioning in multilevel logistic models that exhibit overdisper- these animals. Corresponding results would be especially sion. J R Stat Soc 168:599–613 interesting with regard to enrichment of captive (zoo) ani- Claessens LSA, Ganchev NO, Kukk MM, Schutte CJ, Sloggett JJ mals without the involvement of food—a subject that is still (2020) An investigation of toe-tapping behaviour in anurans by analysis of online video resources. J Zool 312:158–162 largely ignored in amphibians (Michaels et al. 2014). Eibl-Eibesfeldt I (1951) Nahrungserwerb und Beuteschema der Erdkröte (Bufo bufo L.). Behaviour 4:1–34 Acknowledgements We are very grateful to the Zoo Frankfurt for their Elias DO, Maddison WP, Peckmezian C, Girard MB, Mason AC financial support and for providing the facilities for this study. We want (2012) Orchestrating the score: complex multimodal courtship in to especially thank Johannes Köhler, Gerrit Wehrenberger, Thomas the Habronattus coecatus group of Habronattus jumping spiders Tikatsch, and the rest of the animal care taker team of the Exotarium (Araneae: Salticidae). Biol J Linn Soc 105:522–547 for their organizational help. We further thank Thomas Ostrowski for Erdmann JA (2017) The function of toe movement in feeding by the providing us with a recording of the natural call of the study species. gulf coast toad (Incilius nebulifer). Master’s thesis. Southeastern Louisiana University, Hammond, Louisiana Author contribution Study conception and methodology: LMS; per- Gagliardo R, Griffith E, Hill R, Ross H, JR MI, Timpe E, Wilson B, formance of the experiments: YK; data analysis: YK, LMS; writing/ (2010) Observations on the captive reproduction of the horned manuscript preparation: LMS, YK. marsupial frog Gastrotheca cornuta (Boulenger 1898). Herpetol Rev 41:52–58 Funding Open Access funding enabled and organized by Projekt Grafe TU (2008) Toe waving in the brown marsh frog Rana baramica: DEAL. Financial support of the Lab by the Zoo Frankfurt. pedal luring to attract prey? Sci Bruneiana 9:3–5 Hagman M, Shine R (2008) Deceptive digits: the functional signifi- Availability of data and materials The datasets generated during and/ cance of toe waving by cannibalistic cane toads, Chaunus mari- or analyzed during the current study are available from the authors on nus. Anim Behav 75:123–131 reasonable request. Higham JP, Hebets EA (2013) An introduction to multimodal com- munication. Behav Ecol Sociobiol 67:1381–1388 Code availability Not applicable. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in gen- eral parametric models. Biometrical J 50:346–363 Declarations Magnusson A, Skaug H, Nielsen A, Berg C, Kristensen K, Maechler M, van Bentham K, Bolker B, Brooks M, Brooks MM (2017) Ethics approval Not applicable. Package ‘glmmtmb.’ R Packag Version 02 0 Michaels CJ, Downie JR, Campbell-Palmer R (2014) The importance Consent to participate Not applicable. of enrichment for advancing amphibian welfare and conservation goals. Amphib Reptil Conserv 8:7–23 Consent for publication All authors gave their consent for the publica- Murphy JB (1976) Pedal luring in the leptodactylid frog, Ceratophrys tion of the manuscript. calcarata Boulenger. Herpetologica 339–341 Narins PM (1995) Comparative aspects of interactive communica- Competing interests The authors declare no competing interests. tion. In: Flock A, Ottoson D, Ulfendahl M (eds) Active hearing. Elvesier Science, London, pp 363–372 Additional declarations for articles in life science journals that report R-Core-Team (2022) R: a language and environment for statistical the results of studies involving humans and/or animals Data collection computing. In: Found. Stat. Comput. https:// www.r- proje ct. org/ conducted with the approval of the Zoo Frankfurt. Sloggett JJ, Zeilstra I (2008) Waving or tapping? Vibrational stim- uli and the general function of toe twitching in frogs and toads Open Access This article is licensed under a Creative Commons Attri- (Amphibia: Anura). Anim Behav 76:e1–e4 bution 4.0 International License, which permits use, sharing, adapta- Starnberger I, Maier PM, Hödl W, Preininger D (2018) Multimodal tion, distribution and reproduction in any medium or format, as long signal testing reveals gestural tapping behavior in spotted reed as you give appropriate credit to the original author(s) and the source, frogs. Herpetologica 74:127–134 provide a link to the Creative Commons licence, and indicate if changes Turner GS (2011) Toe-twitching in juvenile Sudell’s frog ‘Neobatra- were made. The images or other third party material in this article are chus sudelli’. Vic Nat 128:147–149 included in the article's Creative Commons licence, unless indicated Virant-Doberlet M, Stritih-Peljhan N, Žunič-Kosi A, Polajnar J (2022) otherwise in a credit line to the material. If material is not included in Functional diversity of vibrational signaling systems in insects. the article's Creative Commons licence and your intended use is not Annu Rev Entomol 68:191–210 permitted by statutory regulation or exceeds the permitted use, you will Wickham H, Chang W, Wickham MH (2016) Package ‘ggplot2’. Cre- need to obtain permission directly from the copyright holder. To view a ate elegant data visualisations using the grammar of graphics. copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . Version 2:1–189 Winter B (2013) Linear models and linear mixed effects models in R with linguistic applications. arXiv 1308:5499 References Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Barquero MD, Arguedas V (2022) Mass movement and potential vibratory toe signalling in the green and black poison-dart frog, Dendrobates auratus (Amphibia: Dendrobatidae). Herpetol Notes 15:79–82 1 3

Journal

acta ethologica – Springer Journals

Published: Jun 1, 2023

Keywords: Advertisement calls; Amphibia; Dendrobatidae; Predation; Vibrational communication

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