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Adult—Juvenile interactions and temporal niche partitioning between life-stages in a tropical amphibian

  • Diana Székely,

    Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Resources, Validation, Visualization, Writing – original draft, Writing – review & editing

    Affiliations Laboratorio de Ecología Tropical y Servicios Ecosistémicos - EcoSs Lab, Departamento de Ciencias Biológicas, Universidad Técnica Particular de Loja, Loja, Ecuador, Faculty of Natural and Agricultural Sciences, Ovidius University Constanța, Constanța, Romania, Laboratory of Ecology and Conservation of Amphibians (LECA), Freshwater and OCeanic science Unit of reSearch (FOCUS), University of Liège, Liège, Belgium

  • Dan Cogălniceanu,

    Roles Conceptualization, Investigation, Methodology, Validation, Writing – review & editing

    Affiliations Faculty of Natural and Agricultural Sciences, Ovidius University Constanța, Constanța, Romania, Asociation Chelonia, București, Romania

  • Paul Székely ,

    Roles Conceptualization, Funding acquisition, Investigation, Methodology, Resources, Supervision, Writing – review & editing

    Affiliations Laboratorio de Ecología Tropical y Servicios Ecosistémicos - EcoSs Lab, Departamento de Ciencias Biológicas, Universidad Técnica Particular de Loja, Loja, Ecuador, Asociation Chelonia, București, Romania

  • Mathieu Denoël

    Roles Formal analysis, Investigation, Methodology, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing

    Affiliation Laboratory of Ecology and Conservation of Amphibians (LECA), Freshwater and OCeanic science Unit of reSearch (FOCUS), University of Liège, Liège, Belgium

Adult—Juvenile interactions and temporal niche partitioning between life-stages in a tropical amphibian

  • Diana Székely, 
  • Dan Cogălniceanu, 
  • Paul Székely, 
  • Mathieu Denoël


Divergence in ecological niche offers organisms the opportunity of exploiting different food and habitat resources, scaling down competition and predation both among species, and within different age or size-classes of the same species. In harsh environments, where abiotic factors determine a clustering of resources during short timespans, competition and predation between organisms is likely to be enhanced. This is the case in tropical dry forests, where amphibians have limited opportunities to feed, their activity being restricted to the short rainy season. One way to maximize resource exploitation while avoiding predation risk is by adopting different diel activity patterns. We tested this hypothesis by comparing activity patterns in adults and recently metamorphosed juveniles of Pacific horned frogs (Ceratophrys stolzmanni) during field surveys and in an experimental study. Field surveys showed that the adults are strictly nocturnal, whereas freshly metamorphosed juveniles can be found active above ground at all hours, with a peak activity during daytime. The average body condition index of juveniles found active during the night was higher than that of juveniles found active during the day, suggesting that the weaker individuals may be constrained to being active during the day. On the other hand, in a laboratory experiment, juveniles that were visually exposed to adults moved less than those in the absence of adults. Both field and experimental observations indicate a temporal niche divergence between life stages. The results of the experiment offer support to the hypothesis that the juveniles in this species display an inverse activity pattern compared to adults, which can reduce competitive interactions and predation pressure from the larger conspecifics.


The niche concept is essential to our understanding of community ecology [1]. Divergence in resource use as a result of interspecific interaction has been extensively documented in many taxa [24], but to a lesser extent for intraspecific interactions [5, 6]. The preferred ecological niche is predicted to offer optimal physiological conditions, maximizing the encounter rate with appropriate prey, while minimizing interactions with both predators and competitors [7]. Individual body size affects many life-history aspects, such as diet, physiology, behaviour, and predation [811], so it is expected that different body-size classes will differ in their ecological niche [1214].

In the case of animals with complex life cycles, many of which have aquatic larvae and terrestrial adults (such as many amphibians), the changes in ecological niche at metamorphosis are obvious [1517], while changes that take place during the terrestrial stage are largely disregarded. Overall, the best studied ontogenetic niche shifts refer to changes in habitat use [1820] and diet [21, 22]. The temporal axis of the ecological niche is another dimension of the ecological niche along which species can separate [23]. Temporal partitioning reduces competition for resources [24, 25], and can decrease exposure to predation risks [26]. However, major shifts in diel activity are much less ubiquitous than microhabitat or diet partitioning, especially amongst closely related taxa, and even less so amongst conspecifics, because activity patterns are evolutionarily constrained [27]. In the case of anurans, the vast majority of species avoid diurnal activity in terrestrial stages [28, 29], since nighttime offers protection from desiccation, higher temperatures [30], and some predators [31]. Because of their permeable wet skin used for respiration, amphibians are prone to desiccation, and, since the ratio between surface and volume is higher in smaller animals, juveniles are theoretically more susceptible to dehydration compared to adults [3234]. As a result, it is expected that juveniles would be more likely to be active during nighttime [35, 36]. Nevertheless, in a small number of species, empirical observations show that the opposite phenomenon takes place, with adults being predominantly nocturnal and juveniles exhibiting diurnal activity [35, 37]. In bufonid species, this is considered an adaptation that allows small juveniles to benefit from warmer conditions, which in turn promotes faster growth [38, 39]. However, at least in some cases, an alternative hypothesis is that the temporal shift in activity allows juveniles to reduce predation risk from larger conspecifics [40], and to avoid competition over the trophic resource [41].

The Pacific horned frog (Ceratophrys stolzmanni) is a fossorial amphibian inhabiting the Neotropical seasonally dry forests of coastal Ecuador and Peru [42]. These frogs are active during the rainy season (January–May), reproduce in February–March and juveniles metamorphose after a short larval period, that lasts two–three weeks [43]. Juveniles metamorphose at a relatively large size (approx. 55% of the adult size; [44]), and both juveniles and adults are easy to spot when not buried underground, both during the day and at night. Like other members of the family Ceratophryidae, the Pacific horned frog is anurophagous, being able to swallow large vertebrate prey species [45]. The extremely seasonal environment concentrates the activity of these frogs to a short time period each year, making competition for resources and the agonistic interactions between conspecific individuals likely. We hypothesized that a temporal partitioning between adult and juvenile life-stages occurs in the population, which would be adaptive by reducing competition and predation risk (i.e. cannibalism). The avoidance of adults by juveniles because of predation risk (the cannibalistic hypothesis) was specifically tested in a laboratory experiment, in which we tested if adult presence impacts juvenile activity, expecting that visual exposure to a large frog should reduce movement in juveniles. Additionally, we expected differences in body condition between juveniles foraging during nighttime compared to those active during daytime, under the hypothesis that juveniles with a lower body mass are constrained to activity under less favourable conditions (dryness and higher temperatures) to avoid interaction with adults.

Materials and methods

Research permit for the study was issued by Ministerio del Ambiente del Ecuador (MAE-DNB-CM-2015-0016, granted to Universidad Técnica Particular de Loja). All applicable institutional and/or national guidelines for the care and use of animals were followed. The study was approved by the Universidad Técnica Particular de Loja Ethics Committee (UTPL-CBEA-2016-001).

Field sampling

The study was carried out in Arenillas Ecological Reserve, southern Ecuador (03°34'S; 80°08'E, 30 m a.s.l.), during the rainy season (21 January–18 March, 2016), along a 2.5 km transect, consisting of narrow forest trails in the centre of the reserve (Fig 1), with low human impact and a relatively homogenous vegetation [46]. Where the path was travelled twice (going and returning), animals were counted only during the first pass. At this location and for the duration of the study, sunrise time varied between 06:22 and 06:24, while sunset was between 18:31 and 18:40. As a result, we assigned surveys carried out between 9:00 and 18:59 as diurnal, and between 19:00 and 7:00 as nocturnal. Field observations started at various hours (17:00, 19:00, 21:00, 23:00, 01:00, 03:00, 05:00), with one transect lasting 2h during the whole study interval. For a week after the onset of metamorphosis of horned frogs (11–18 March), each night transect was doubled by another transect during the day, starting at either 09:00, 11:00, 13:00, 15:00, or 17:00 (S1 Table). Only individuals at Gosner stage 46 (tail completely resorbed; [47]) or older were counted. Frogs were considered adults if having snout-vent length (SVL) over 50 mm, and juveniles if under 45 mm [44]. Measured juveniles had a mean SVL ± S.E. of 29.9 ± 0.2 (range: 23.2–42.9 mm, n = 286), while adult SVL varied between 50.3 and 77.8 mm (61.5 ± 0.17, n = 564). Air temperature and relative humidity were measured on location, using an EL-21CFR-2-LCD-UK data logger (Lascar Electronics, Wiltshire, UK) positioned 2 m above ground, in the shade, set to record the parameters each minute.

Fig 1. Forest trail at the study site (Arenillas Ecological reserve, Ecuador).

Of the encountered juveniles, 20 randomly-chosen individuals were measured during each transect whenever available (SVL with a Dial-Max calliper of 0.1 mm precision, body mass—BM with a My Weigh 300Z portable scale of 0.1 g precision). Measurements were taken in situ, and the individuals were immediately released at the capture point. These values served to calculate the body condition index (BCI) of individuals as the residuals of the regression of lnBM (body mass) on lnSVL [48], which is a good estimate of energy storage in amphibians [49].

Laboratory experiments

On 15–17 March 2016, we conducted an experiment, testing for behavioural interaction between adults and juveniles. We collected 15 adults and 30 freshly metamorphosed juveniles (Gosner stage 46) from the reserve (about 500 m from the location of the transect). All individuals were kept individually in plastic enclosures (50 x 37 cm, 30 cm height for adults; 21 x 15cm, 12 cm height for juveniles), with a layer of 6 cm humid soil (same as in their capture site) to acclimate for approximately 24 h previously to being used in the experiments. The laboratory was situated on site, with natural conditions (daylight duration, temperature, humidity). Experimental enclosures consisted of 50 x 37 cm, 30 cm height, plastic boxes, split into two arenas of equal surface by a transparent glass, and monitored from above with a Logitech HD Pro C920 webcam (resolution: 1920 x 1080 pixels), situated 150 cm above the enclosures, connected to a laptop. To improve visibility during the experiments, lighting was supplemented by ExoTerra Infrared light bulbs (50W, 800 nm) that do not affect the activity of frogs [50]. Using Chronolapse 1.0.7 software (Green 2008,, time-lapse photos were taken every 5 sec, for 1 h duration, starting 10 min after the introduction of experimental individuals.

Juveniles were assigned randomly to one of two treatments (absence vs. presence of an adult; n = 15 juveniles for each treatment), with no difference between them in SVL (Student's t-test, t28 = -0.524, p = 0.605) or BCI (t28 = -1.289, p = 0.208). Two open-top experimental enclosures (randomized position), lined with moist tissue paper, separated by an opaque wall, were monitored at the same time: (1) one with a juvenile in one arena and an adult on the other side of the glass, in the other arena (Fig 2a, right enclosure), and (2) the second identical to the first, but without the adult (Fig 2a, left enclosure). The enclosures were thoroughly washed and sun-dried between trials, in an attempt to remove any possible chemical cues from previous individuals. Each individual was used only once and released after the experiment at the capture site.

Fig 2.

Influence of adult presence on juvenile activity: (a) examples of tracks (i.e. individual movements) of the juveniles in the experimental design. The left and right enclosures correspond to the single (i.e. no adult) and the exposed (i.e. adult visible) treatments, respectively. Each enclosure consisted of two arenas separated by transparent glass. The coloured paths indicate the distance travelled by individuals during 1 h recording (red and yellow: juveniles; green: adult); (b) distance travelled (mean ± S.E.) in the experimental enclosure during 1 h by juveniles, without and with the presence of an adult.

Images (720 per replicate, i.e. 10,800 in total) were processed using ImageJ 1.46r software (U.S. National Institute of Health) along with the MTrackJ 1.5.0 plugin [51], that allows tracking movement of study animal, through manual input of position in the enclosure on each individual image [52]. We used the total distance travelled, in cm, during 1h, as a measure of individual activity.

Statistical analysis

All analyses were carried out with SPSS software, version 21.0 (IBM Corp., Armonk, NY), with a significance level of 0.05 and two-tailed tests. Parameters that after QQ-plot inspection were considered not normally distributed (i.e. the number of individuals encountered during surveys and distance travelled in experimental trials) were ln-transformed prior to analysis. To determine the temporal niche partitioning between adults and juveniles, we used the Czekanowski index of overlap [53]: , where is the proportion of adults active during the 2-h interval i, and pi.juv is the proportion of juveniles active during the same interval i. The values of the index range between 0 (i.e. full partitioning between time intervals used), and 1 (i.e. full overlap in temporal niche use). We used Student's t-tests to determine significant differences in the number of juveniles counted during transects, their body condition, and the meteorological conditions (temperature and humidity, recorded at the middle time of the survey) during diurnal vs. nocturnal surveys. We used linear regressions to test for the effect of SVL and BCI on the distance travelled by juveniles in the laboratory experiment. The distances travelled by juveniles in absence versus presence of an adult during the experimental tests were compared with a Student’s t-test. Additionally, we tested through linear regressions the predictive value of two traits of the adults on exposed juvenile distance travelled: adult activity (also measured as distance travelled), and size (measured as SVL). We included both parameters in the model since adult activity and SVL were not correlated (r = 0.14, F1,13 = 0.275, p = 0.609).


Field survey

A total of 621 adults and 2,356 juveniles were encountered during the study period. We found a strong difference in the time of day when the two life-stages were active above ground, with a value of the Czekanowski index of temporal overlap of 0.074. Adults were exclusively nocturnal, with toads coming out of the ground not sooner than 19:04 and hiding in their burrows before 06:15, and variable numbers being active throughout the night, particularly between 23:00 and 5:00 (Fig 3a). Juveniles could be encountered at all hours, but the occurrence rate differed according to the time of day, with a peak of activity between 9:00 and 11:00 (Fig 3b).

Fig 3. Effect of the time of day on number of encountered horned frogs, according to life-stage: (a) adults (dark brown); (b) juveniles (light brown).

Surveys between 7:00–19:00 considered diurnal, and those between 19:00–7:00 nocturnal. Bars: mean; whiskers: S.E.

During the week following the metamorphosis of juveniles (11–18 March), climatic conditions differed between the nocturnal transects and diurnal transects (Student's t-test, temperature: t8.3 = 5.404, p = 0.001; relative humidity: t7.58 = - 4.218, p = 0.003): average temperature was higher (mean ± S.E. = 31.3 ± 0.8 °C) and relative humidity lower (mean ± S.E. = 73.1 ± 3.2%) during the day compared to during the night (temperature 26.5 ± 0.3 °C; relative humidity 86.7 ± 0.6%; S1 Fig).

The number of encountered juveniles was larger during diurnal surveys (mean ± S.E. = 272 ± 96 / survey) than at night (26 ± 6 / survey; Student's t-test, t13 = 2.749, p = 0.017). Juvenile individuals that were found active during the night were in significantly better body condition than those found active during the day (average BCI ± S.E.: night = 0.03 ± 0.01, day = -0.019 ± 0.01; Student's t-test, nday = 176, nnight = 108, t282 = 2.793, p = 0.006; Fig 4).

Fig 4. Differences in body condition (mean ± S.E.) between juvenile Pacific horned frogs active during the day (n = 176) compared to those active during the night (n = 108).

Behavioural experiment

Juveniles that were visually exposed to the presence of an adult moved less during the 1h monitored interval (mean ± S.E. = 155.1 ± 111.7 cm) than in the absence of adults (740.8 ± 197.2 cm; Student's t-test, t28 = -3.99, p < 0.001 (Fig 2b). The distance travelled by the juveniles exposed to the sight of an adult was not influenced by the size of the adult (r2 = 0.015, F1,13 = 0.195, p = 0.666), nor by the activity of the adult (r2 = 0.061, F1,13 = 0.841, p = 0.376). Overall, neither the size of the juvenile (r2 = 0, F1,28 = 0.003, p = 0.954), nor its body condition (r2 = 0.02, F1,28 = 0.558, p = 0.461) affected its mobility (S2 Fig). However, the distance travelled was positively correlated with juvenile BCI in the absence of an adult (r2 = 0.268, F1,13 = 4.753, p = 0.048).


The study shows that, in their post-metamorphic, terrestrial stages, Pacific horned frogs display an ontogenetic change in the temporal niche used, with adults being strictly nocturnal, while juveniles are mainly active during daytime. Our results emphasize the fact that important changes in the ecological niche are not limited to the metamorphic event, and shed new insights on intraspecific temporal resource partitioning, one of the least studied aspects of community structuring [27]. The results contrast with most previous research that showed amphibians to be conservative in terms of preferred diel activity throughout their terrestrial lives [28, 54] because of the strong dependence of their activity on climatic factors [34]. Indeed, in the majority of studied fossorial amphibians both juveniles and adults are nocturnal [35, 5557]; alternatively, in a few species, juvenile dispersal can occur during the crepuscular hours, juveniles moving either early in the morning or shortly after sunset, and only after heavy rains [58]. However, since the observations here presented are limited to only one activity season, a better understanding of the impact of climatic factors might result from repeated observations spanning several years.

In some systems, biological interactions are more important than environmental pressures in determining activity patterns [40, 59, 60]. We interpreted the lower activity levels of juveniles in the presence of adults as an antipredator mechanism [61, 62], which can efficiently mitigate predation risks associated with morphology, in this case small size [63]. The fact that Ceratophrys juveniles modified their behaviour in response to the presence of conspecifics supports the hypothesis that juveniles might avoid intraspecific interactions by diverging from adult typical activity time-frame in their most vulnerable stage. These results extend the observations made by Schalk and Fitzgerald [64] regarding a related species, Ceratophrys cranwelli, that inhabits similar seasonally dry environments and is frequently anurophagous [65]. In this species there was a strong divergence in micro-habitat use, with juveniles hunting in drier areas and avoiding the optimal humid habitats close to ephemeral ponds that were dominated by large individuals [64]. In our study, we did not analyse the spatial distribution of life-stages; however, we found both juveniles and adults on the same portions of the monitored transect. Altogether, our results and those of Schalk & Fitzgerald [64] suggest that juveniles can employ both spatial and temporal strategies to avoid adults.

Being gape-limited predators, the maximum size of ingested prey increases along with individual size [66], and large individuals have a more diverse diet through access to larger prey items [67]. However, large individuals do not disregard small prey organisms [45], a typical behaviour found in other amphibians [65, 68]. As such, we could expect a significant dietary overlap between age-classes. Consequently, in addition to lowering predation risk, the observed partitioning along the temporal niche axis should be effective in relaxing competition between juveniles and adults, reducing the overlap in resource use and the agonistic interactions between age-classes [27].

Our field observations showed that the nighttime niche is dominated by adults, along with a non-random subset of juveniles with higher body condition. In this context, it seems plausible that the less fit juveniles might be constrained to diurnal activity in order to improve their foraging efficiency by taking advantage of food sources that are less exploited during the day [69, 70], thus avoiding competition and predation risks from both adults and the better fit juveniles. The lower body condition found in diurnal juveniles as compared to nocturnal juveniles suggests a lower payoff of the diurnal behaviour. This situation may be considered as a best of a bad lot tactic [71]. Therefore, part of the juveniles might “choose” nocturnal activity, which is more energetically profitable and involves a lower hydric stress, but also implies more risks; their success depending on the density of adults.

No data regarding diel variation in prey availability is available for the study site. However, in other seasonally dry tropical environments, the ground-level insect availability changes little between daytime and nighttime, both in terms of species composition and abundance [72, 73]. Further studies on differential distribution and availability of prey and energy acquisition according to diel patterns, as well as preferred prey types in relation to developmental stage, might test if variations in prey availability make diurnal activity beneficial for early-stages terrestrial horned frogs.

Along with competition and predation risk from conspecific adults, there are several other, non-exclusive, determinants that could explain the observed dichotomic pattern of activity between the life-stages, such as differences in physiological tolerance between life stages, mainly to desiccation risk, or susceptibility to predation (other than cannibalism), compared to adults. Since in juveniles the ratio between surface and volume is smaller than in adults, resulting in a higher desiccation risk, theory predicts that the preference for nocturnal activity should be accentuated in juveniles, especially in hot climates [32]. However, amongst anurans, some bufonid species can be described as heliophilic in their early post-metamorphic stages, benefiting from the increased temperatures, as they intensify growth rates [74]. In such species, juveniles are active during daytime and have a higher tolerance for critically high temperatures compared to the nocturnal adults [37]. To mitigate the risk of dehydration and overheating, they can remain clustered in humid habitats in close vicinity to their emergence ponds [39, 75], and have thinner, less cornified skin, allowing them to rehydrate more quickly [37]. Additionally, most diurnally active amphibian species benefit from protection from predators through toxic skin secretions. It is for instance typically the case of bufonids [76], dendrobatids [77], and salamandrids [31, 78].

In comparison to some other anurans, horned frogs (genus Ceratophrys) are poorly equipped for cutaneous chemical defence [79], and rely mostly on camouflage [80] and behavioural strategies [81] to avoid predation. Further testing of other hypotheses will improve our understanding of the mechanisms that structure the activity patterns within populations in extremely seasonal environments, such as size-dependent susceptibility to predation or specific physiological or morphological adaptations that allow Pacific horned frog juveniles to be active during daytime, as well as individual variations (behavioural types).

Supporting information

S1 Fig. (a) Active Pacific horned frog in its habitat; (b) climate conditions during surveys on 10–18 March 2016, according to the time of day (red line—temperature, blue line—relative humidity) and the number of juveniles encountered during the surveys (during the day—white bars, during the night—full bars).


S2 Fig. Distance travelled by Pacific horned frog juveniles (n = 30), in relation to their Snout-Vent Length (a) and body condition (b).

Red dots—single (i.e. no adult), and yellow dots—exposed (i.e. adult visible) treatments, respectively.


S1 Table. Schedule of transects and number of encountered Pacific horned frogs, according to their life-stage.



Fieldwork in the reserve was possible thanks to the help of the Arenillas Ecological Reserve administration. We are especially grateful to the REA “guardaparques” for their friendship and support during the fieldwork.


  1. 1. Chase JM, Leibold MA. Ecological niches—linking classical and contemporary approaches. Chicago, Illinois, USA: University of Chicago Press; 2003.
  2. 2. van Leeuwen A, Huss M, Gårdmark A, Casini M, Vitale F, Hjelm J, et al. Predators with multiple ontogenetic niche shifts have limited potential for population growth and top-down control of their prey. Am Nat. 2013;182: 53–66.
  3. 3. Sánchez-Hernández J, Eloranta AP, Finstad AG, Amundsen PA. Community structure affects trophic ontogeny in a predatory fish. Ecol Evol. 2017;7: 358–367.
  4. 4. Lovette IJ, Hochachka WM. Simultaneous effects of phylogenetic niche conservatism and competition on avian community structure. Ecology. 2006;87: S14–S28.
  5. 5. Zandonà E, Dalton CM, El-Sabaawi RW, Howard JL, Marshall MC, Kilham SS, et al. Population variation in the trophic niche of the Trinidadian guppy from different predation regimes. Sci Rep. 2017;7: 5770.
  6. 6. Clegg T, Ali M, Beckerman AP. The impact of intraspecific variation on food web structure. Ecology. 2018;99: 2712–2720.
  7. 7. Holt RD. Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. PNAS. 2009;106: 19659–19665.
  8. 8. Downes SJ. Size-dependent predation by snakes: selective foraging or differential prey vulnerability? Behav Ecol. 2002;13: 551–560.
  9. 9. Hanson JO, Salisbury SW, Campbell HA, Dwyer RG, Jardine TD, Franklin CE. Feeding across the food web: the interaction between diet, movement and body size in estuarine crocodiles (Crocodylus porosus). Austral Ecol. 2015;40: 275–286.
  10. 10. Nielsen ME, Papaj DR. Effects of developmental change in body size on ectotherm body temperature and behavioral thermoregulation: caterpillars in a heat-stressed environment. Oecologia. 2015;177: 171–179.
  11. 11. Titon BJ, Gomes FR. Relation between water balance and climatic variables associated with the geographical distribution of anurans. PLoS ONE. 2015;10: e0140761.
  12. 12. Werner EE, Gilliam JF. The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst. 1984;15: 393–425.
  13. 13. Rudolf VHW. A multivariate approach reveals diversity of ontogenetic niche shifts across taxonomic and functional groups. Freshwater Biology. 2020;65: 745–756.
  14. 14. Denoël M. Size-related predation reduces intramorph competition in paedomorphic Alpine newts. Can J Zool. 2001;79: 943–948.
  15. 15. Denoël M. Terrestrial versus aquatic foraging in juvenile Alpine newts (Triturus alpestris). Ecoscience. 2004;11: 404–409.
  16. 16. Nakazawa T. Ontogenetic niche shifts matter in community ecology: a review and future perspectives. Popul Ecol. 2015;57: 347–354.
  17. 17. Rowe L, Ludwig D. Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology. 1991;72: 413–427.
  18. 18. Werner EE, Hall DJ. Ontogenetic habitat shifts in bluegill: the foraging rate-predation risk trade-off. Ecology. 1988;69: 1352–1366.
  19. 19. Eskew EA, Willson JD, Winne CT. Ambush site selection and ontogenetic shifts in foraging strategy in a semi-aquatic pit viper, the Eastern cottonmouth. J Zool, Lond. 2009;277: 179–186.
  20. 20. Matich P, Heithaus MR. Individual variation in ontogenetic niche shifts in habitat use and movement patterns of a large estuarine predator (Carcharhinus leucas). Oecologia. 2015;178: 347–359.
  21. 21. Lima P, Magnusson A, Ernest W. Partitioning seasonal time: interactions among size, foraging activity and diet in leaf-litter frogs. Oecologia. 1998;116: 259–266.
  22. 22. Hertz E, Trudel M, El-Sabaawi R, Tucker S, Dower JF, Beacham TD, et al. Hitting the moving target: modelling ontogenetic shifts with stable isotopes reveals the importance of isotopic turnover. J Anim Ecol. 2016;85: 681–691.
  23. 23. Lima AP, Magnusson WE. Does foraging activity change with ontogeny? An assessment for six sympatric species of postmetamorphic litter anurans in central Amazonia. J Herpetol. 2000;34: 192–200.
  24. 24. Huey RB, Pianka ER. Temporal separation of activity and interspecific dietary overlap. In: Huey R, Pianka E, Schoener T, editors. Lizard Ecology. Cambridge, UK: Harvard University Press; 1983. pp. 281–290.
  25. 25. Monterroso P, Alves PC, Ferreras P. Plasticity in circadian activity patterns of mesocarnivores in Southwestern Europe: implications for species coexistence. Behav Ecol Sociobiol. 2014;68: 1403–1417.
  26. 26. Orr MR. Parasitic flies (Diptera: Phoridae) influence foraging rhythms and caste division of labor in the leaf-cutter ant, Atta cephalotes (Hymenoptera: Formicidae). Behav Ecol Sociobiol. 1992;30: 395–402.
  27. 27. Kronfeld-Schor N, Dayan T. Partitioning of time as an ecological resource. Annu Rev Ecol Evol S. 2003;34: 153–181.
  28. 28. Anderson SR, Wiens JJ. Out of the dark: 350 million years of conservatism and evolution in diel activity patterns in vertebrates. Evolution. 2017;71: 1944–1959.
  29. 29. Duellman WE. Tropical herpetofaunal communities: patterns of community structure in neotropical rainforests. In: Harmelin-Vivien ML, Bourlière F, editors. Vertebrates in complex tropical systems. New York, NY: Springer New York; 1989. pp. 61–88.
  30. 30. Tracy CR, Christian KA, Burnip N, Austin BJ, Cornall A, Iglesias S, et al. Thermal and hydric implications of diurnal activity by a small tropical frog during the dry season. Austral Ecol. 2013;38: 476–483.
  31. 31. Semlitsch RD, Pechmann JHK. Diel pattern of migratory activity for several species of pond-breeding salamanders. Copeia. 1985;1985: 86–91.
  32. 32. Tracy CR, Christian KA, Tracy CR. Not just small, wet, and cold: effects of body size and skin resistance on thermoregulation and arboreality of frogs. Ecology. 2010;91:1477–1484.
  33. 33. Jørgensen CB. 200 years of amphibian water economy: from Robert Townson to the present. Biol Rev. 1997;72: 153–237.
  34. 34. Gouveia SF, Bovo RP, Rubalcaba JG, Da Silva FR, Maciel NM, Andrade DV, et al. Biophysical modeling of water economy can explain geographic gradient of body size in anurans. Am Nat. 2019; 193: 51–58.
  35. 35. Todd BD, Winne CT. Ontogenetic and interspecific variation in timing of movement and responses to climatic factors during migrations by pond-breeding amphibians. Can J Zool. 2006;84: 715–722.
  36. 36. Bovo RP, Navas CA, Tejedo M, Valença SE, Gouveia SF. Ecophysiology of amphibians: Information for best mechanistic models. Diversity. 2018;10: 118.
  37. 37. Navas CA, Antoniazzi MM, Carvalho JE, Suzuki H, Jared C. Physiological basis for diurnal activity in dispersing juvenile Bufo granulosus in the Caatinga, a Brazilian semi-arid environment. Comp Biochem Phys A. 2007;147: 647–657.
  38. 38. Lillywhite HB, Licht P, Chelgren P. The role of behavioral thermoregulation in the growth energetics of the toad, Bufo boreas. Ecology. 1973;54:375–383.
  39. 39. Taigen TL, Pough FH. Activity metabolism of the toad (Bufo americanus): ecological consequences of ontogenetic change. J Comp Physiol. 1981;144: 247–52.
  40. 40. Pizzatto L, Child T, Shine R. Why be diurnal? Shifts in activity time enable young cane toads to evade cannibalistic conspecifics. Behav Ecol. 2008;19:990–997.
  41. 41. Cunningham CX, Scoleri V, Johnson CN, Barmuta LA, Jones ME. Temporal partitioning of activity: rising and falling top-predator abundance triggers community-wide shifts in diel activity. Ecography. 2019;42: 2157–2168.
  42. 42. Székely D, Cogălniceanu D, Székely P, Denoël M. Dryness affects burrowing depth in a semi-fossorial amphibian. J Arid Environ. 2018;155: 79–81.
  43. 43. Székely D, Denoël M, Székely P, Cogălniceanu D. Pond drying cues and their effects on growth and metamorphosis in a fast developing amphibian. J Zool, Lond. 2017;303: 129–135.
  44. 44. Székely D, Székely P, Stănescu F, Cogălniceanu D, Sinsch U. Breed fast, die young—demography of a poorly known fossorial frog from the xeric Neotropics. Salamandra. 2018;54: 37–44.
  45. 45. Székely D, Gaona FP, Székely P, Cogălniceanu D. What does a Pacman eat? Macrophagy and necrophagy in a generalist predator (Ceratophrys stolzmanni). PeerJ. 2019;7: e6406.
  46. 46. Espinosa CI, de la Cruz M, Jara-Guerrero A, Gusmán E, Escudero A. The effects of individual tree species on species diversity in a tropical dry forest change throughout ontogeny. Ecography. 2016;39: 329–337.
  47. 47. Gosner KL. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica. 1960;16: 183–190.
  48. 48. Băncilă RI, Hartel T, Plăiaşu R, Smets J, Cogălniceanu D. Comparing three body condition indices in amphibians: a case study of yellow-bellied toad Bombina variegata. Amphibia-Reptilia. 2010;31: 558–562.
  49. 49. Denoël M, Hervant F, Schabetsberger R, Joly P. Short- and long-term advantages of an alternative ontogenetic pathway. Biol J Linn Soc. 2002;77: 105–112.
  50. 50. Buchanan BW. Effects of enhanced lighting on the behaviour of nocturnal frogs. Anim Behav. 1993;45: 893–899.
  51. 51. Meijering E, Dzyubachyk O, Smal I. Methods for cell and particle tracking. Methods Enzymol. 2012;504: 183–200.
  52. 52. Manenti R, Denoël M, Ficetola GF. Foraging plasticity favours adaptation to new habitats in fire salamanders. Anim Behav. 2013;86: 375–382.
  53. 53. Feinsinger P, Spears EE, Poole RW. A simple measure of niche breadth. Ecology. 1981;62: 27–32.
  54. 54. Hut RA, Kronfeld-Schor N, van der Vinne V, De la Iglesia H. In search of a temporal niche: environmental factors. In: Kalsbeek A, Merrow M, Roenneberg T, Foster RG, editors. Progress in Brain Research. Vol. 199. Oxford, UK: Elsevier; 2012. pp. 281–304.
  55. 55. Linsdale JM. Environmental responses of vertebrates in the Great Basin. Am Midl Nat. 1938;19: 1–206.
  56. 56. Bragg AN. Breeding habits, eggs, and tadpoles of Scaphiopus hurterii. Copeia. 1944;1944: 230–241.
  57. 57. Stănescu F, Iosif R, Székely P, Székely D, Cogălniceanu D. Mass migration of Pelobates syriacus (Boettger, 1889) metamorphs. Herpetozoa. 2016;29: 87–89.
  58. 58. Neill WT. Notes on metamorphic and breeding aggregations of the eastern spadefoot, Scaphiopus holbrooki (Harlan). Herpetologica. 1957;13: 185–187.
  59. 59. Winandy L, Colin M, Denoël M. Temporal habitat shift of a polymorphic newt species under predation risk. Behav Ecol. 2016;27: 1025–1132.
  60. 60. Jones KA, Ratcliffe N, Votier SC, Newton J, Forcada J, Dickens J, et al. Intra-specific niche partitioning in Antarctic fur seals, Arctocephalus gazella. Scientific Reports. 2020;10: 3238.
  61. 61. Williams CR, Brodie ED, Tyler MJ, Walker SJ. Antipredator mechanisms of Australian frogs. J Herpetol. 2000;34: 431–443.
  62. 62. Heinen JT. Antipredator behavior of newly metamorphosed American toads (Bufo a. americanus), and mechanisms of hunting by eastern garter snakes (Thamnophis s. sirtalis). Herpetologica. 1994;50: 137–145.
  63. 63. Touchon JC, Jiménez RR, Abinette SH, Vonesh JR, Warkentin KM. Behavioral plasticity mitigates risk across environments and predators during anuran metamorphosis. Oecologia. 2013;173: 801–811.
  64. 64. Schalk CM, Fitzgerald LA. Ontogenetic shifts in ambush-site selection of a sit-and-wait predator, the Chacoan Horned Frog (Ceratophrys cranwelli). Can J Zool. 2015;93: 461–467.
  65. 65. Schalk CM, Montaña CG, Klemish JL, Wild ER. On the diet of the frogs of the Ceratophryidae: synopsis and new contributions. S Am J Herpetol. 2014;9: 90–105.
  66. 66. Emerson SB. Skull shape in frogs: correlations with diet. Herpetologica. 1985;41:177–188.
  67. 67. Maret TJ, Collins JP. Individual responses to population size structure: the role of size variation in controlling expression of a trophic polyphenism. Oecologia. 1994;100: 279–285.
  68. 68. Denoël M, Whiteman HH, Wissinger SA. Temporal shift of diet in alternative cannibalistic morphs of the tiger salamander. Biol J Linn Soc. 2006;89: 373–382.
  69. 69. Pettit L, Ducatez S, DeVore JL, Ward-Fear G, Shine R. Diurnal activity in cane toads (Rhinella marina) is geographically widespread. Sci Rep. 2020;10:5723.
  70. 70. Kronfeld-Schor N, Dayan T. The dietary basis for temporal partitioning: food habits of coexisting Acomys species. Oecologia. 1999;121: 123–128.
  71. 71. Whiteman HH, Wissinger SA, Denoël M, Mecklin CJ, Gerlanc NM, Gutrich JJ. Larval growth in polyphenic salamanders: making the best of a bad lot. Oecologia. 2012;168: 109–18.
  72. 72. Janzen DH. Sweep samples of tropical foliage insects: effects of seasons, vegetation types, elevation, time of day, and insularity. Ecology. 1973;54: 687–708.
  73. 73. Silva JO, Leal CRO, Espírito-Santo MM, Morais HC. Seasonal and diel variations in the activity of canopy insect herbivores differ between deciduous and evergreen plant species in a tropical dry forest. J Insect Conserv. 2017;21: 667–676.
  74. 74. Brattstrom BH. Amphibian temperature regulation studies in the field and laboratory. Am Zool. 1979;19: 345–356.
  75. 75. Freeland W, Kerin S. Ontogenteic alteration of activity and habitat selection by Bufo marinus. Wildl Res. 1991;18: 431–443.
  76. 76. Santos RR, Grant T. Diel pattern of migration in a poisonous toad from Brazil and the evolution of chemical defenses in diurnal amphibians. Evol Ecol. 2011;25: 249–258.
  77. 77. Darst Catherine R, Menéndez‐Guerrero PA, Coloma LA, Cannatella DC. Evolution of dietary specialization and chemical defense in poison frogs (Dendrobatidae): a comparative analysis. Am Nat. 2005;165: 56–69.
  78. 78. Brodie ED Jr, Ducey PK, Baness EA. Antipredator skin secretions of some tropical salamanders (Bolitoglossa) are toxic to snake predators. Biotropica. 1991;23: 58–62.
  79. 79. Arifulova I, Delfino G, Dujsebayeva T, Fedotovskikh G, Nosi D, Terreni A. Serous cutaneous glands in the South American horned frog Ceratophrys ornata (Leptodactyliformes, Chthonobatrachia, Ceratophrydae): ultrastructural expression of poison biosynthesis and maturation. J Morphol. 2007;268: 690–700.
  80. 80. Toledo LF, Haddad CFB. Colors and some morphological traits as defensive mechanisms in anurans. Int J Zool. 2009;2009: 1–12.
  81. 81. Toledo LF, Sazima I, Haddad CFB. Behavioural defences of anurans: an overview. Ethol Ecol Evol. 2011;23: 1–25.