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How to recover from a bad start: size at metamorphosis affects growth and survival in a tropical amphibian

How to recover from a bad start: size at metamorphosis affects growth and survival in a tropical... Background: In species with complex life cycles, size at metamorphosis is a key life‑history trait which reflects the complex interactions between costs and benefits of life in the aquatic and terrestrial environments. Whereas the effects of a deteriorating larval habitat (e.g. pond desiccation) on triggering an early metamorphosis have been extensively investigated in amphibians, the consequences of the resulting reduced size at metamorphosis on fitness in the post‑metamorphic terrestrial stage remain poorly understood. We tested the hypothesis that a smaller size at metamorphosis negatively affects performance and survival in the ensuing terrestrial stage. Using as model a tropical amphibian (Ceratophrys stolzmanni) showing a large phenotypic plasticity in metamorphosing traits, we evaluated the effects of size at metamorphosis on fitness‑related trophic and locomotor performance traits, as well as on growth and survival rates. Results: Our results support the hypothesis that a larger size at metamorphosis is correlated with better survival and performance. The survival rate of large metamorphosing individuals was 95%, compared to 60% for those completing metamorphosis at a small size. Locomotor performance and gape size were positively correlated with body size, larger animals being more mobile and capable to ingest larger prey. However, smaller individuals achieved higher growth rates, thus reducing the size gap. Conclusions: Overall, size at metamorphosis affected profoundly the chances of survival in the short term, but smaller surviving individuals partly compensated their initial disadvantages by increasing growth rates. Keywords: Adaptive plasticity, Growth compensation, Life cycles, Life‑history, Metamorphosis Background accompanied by a complete change of the ecological Species with complex life cycles, such as biphasic niche [3, 4]. Pond-breeding amphibians, which in their amphibians and insects, are able to exploit different eco - post-larval stages become terrestrial, represent ideal logical niches and optimize their life-history in discrete models to investigate the independence of pre- and post- developmental stages [1, 2]. The transition occurring at metamorphic life-stages and the presence of carry-over metamorphosis usually requires dramatic and irrevers- effects from one stage to the other, affecting the over - ible morphological transformations, and is frequently all fitness of individuals [5]. The most evident trade-off between the aquatic and terrestrial stages is reflected in body size at metamorphosis. When the aquatic lar- *Correspondence: dcogalniceanu@univ‑ovidius.ro vae are confronted with unfavourable conditions, such Faculty of Natural and Agricultural Sciences, Ovidius University Constanța, Constanța, Romania as food shortage [6, 7], high density [8], desiccation risk Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Székely et al. BMC Ecol (2020) 20:24 Page 2 of 8 [9] or predation [10, 11], they can leave the aquatic envi- population. From the encountered spectrum of sizes, ronment by undergoing metamorphosis. However, this we assigned the 20 largest and 20 smallest individuals to is usually done at a smaller size, which allows them to their respective size-categories (see “Methods” section). escape the immediate aquatic threats faster, but in turn We tested if smaller froglets can amend the detrimental exposes them to different selective pressures on land [1]. survival effects induced by metamorphosing at a reduced Larger size in freshly metamorphosed individuals is size through (i) allometric changes in morphology or per- correlated with improved traits, like locomotor abilities formance (wider heads, longer limbs, or better jumping and metabolic rates [12], endurance [13], resistance to skills) and/or (ii) more intense growth rates. desiccation [14], feeding success [15], and dispersal suc- cess [16]. Although the paradigm model [17] assumes Results that body size at metamorphosis is a good predictor of Morphology and locomotor performance subsequent fitness, there are authors [e.g. 3, 18] who At the completion of metamorphosis, individual body assert that this is not always the case. Since in amphib- mass (BM) and snout-vent length (SVL) showed a strong ians a substantial percent of the adult body size is gained correlation (Pearson’s r = 0.923, n = 40, P < 0.001), but after metamorphosis, and because age of sexual maturity there was no significant difference in body condition is variable, the relationship between body size at meta- between the two categories of froglets (i.e. small vs. large: morphosis and fitness is more complex, especially in t = 0.175, P = 0.862; Additional file 1). unpredictable environments [19]. For example, if smaller Since absolute head width was strongly correlated individuals have compensating mechanisms, such as to SVL at metamorphosis (r = 0.982, n = 40, P < 0.001), more intense growth rates, metamorphic size may not larger froglets had significantly wider heads compared have a significant effect on adult traits like mortality, age to the smaller ones (t = 17.123, P < 0.001; Fig. 1a). Rela- and size at first reproduction, or fecundity [20, 21]. The tive head width did not differ significantly between the detrimental consequences of a small size at metamorpho- two size categories of froglets (t = − 0.902, P = 0.373), sis can also be compensated by changes in the morphol- and was correlated with individual initial BCI (r = 0.479, ogy of juveniles [22, 23]. For example, the small froglets n = 40, P = 0.002), with froglets in better body condition can have, proportionally to their body size, larger heads having larger heads regardless of their SVL (Additional or longer legs than the bigger individuals. Such modifi - file 1). cations would be beneficial because leg length influences There was a strong positive correlation between locomotor (i.e. jumping) performance [23, 24], which in hindlimb length and SVL (r = 0.988, n = 40, P < 0.001). turn has been shown to positively affect food acquisition Compared to the large juveniles, small froglets had signif- [25], predator avoidance [26] and dispersal [27]. In a sim- icantly shorter hindlimbs both in terms of absolute size ilar manner, a large head width favours the swallowing (t = − 17.001, P < 0.001), and relative size (t = − 6.309, 38 38 ability, which is a limiting factor in prey selection [28, 29]. P < 0.001). We found no relationship between the body In this context, we were interested to understand the condition of juveniles and their relative hindlimb lengths influence of size at metamorphosis on post-metamorphic (r = 0.114, n = 40, P = 0.485). traits such as survival, morphology and performance, Absolute jumping ability was predicted by SVL and to investigate the existence of compensating mecha- (F = 102.364, P < 0.001), with no significant effect 1,36 nisms. Hypothesizing that the difference would be most of either relative hindlimb length (F = 0.539, 1,36 evident between individuals at the opposite ends of the P = 0.468), or BCI (F = 0.056, P = 0.815). Larger 1,36 size range, we evaluated the impact of extreme size phe- individuals were able to jump over greater distances notypes. We selected as a model a species capable of (mean ± SE = 100.4 ± 3.6  mm) than the smaller ones high plasticity in metamorphosing size [30], the Pacific (59.4 ± 2.3 mm; t = − 9.501, P < 0.001; Fig. 1b). horned frog (Ceratophrys stolzmanni). This fossorial frog inhabits tropical dry forests, a highly seasonal eco- Growth system characterized by a short rainy season that lasts At the end of the study period (i.e. 2 months after meta- less than 4  months annually. The tadpoles have some of morphosis), the two categories of froglets did not differ in the most intense growth rates reported for anurans and terms of their body condition indices (BCI; t = − 0.289, can leave the water in as little as 2 weeks after egg-laying P = 0.774). Individual BCI after 2  months of terrestrial [30]. Because several environmental parameters can have growth was not correlated with the froglet’s SVL at meta- interacting effects in the natural habitat [31], we used morphosis (r = 0.107, n = 31, P = 0.566), nor with initial freshly metamorphosed froglets resulting from tadpoles BCI (r = 0.191, n = 31, P = 0.302). that grew in field conditions (natural ponds) in order to There was a significant effect of size at metamorphosis cover the entire range of size at metamorphosis in the on post-metamorphic growth rates, with individuals that Sz ékely et al. BMC Ecol (2020) 20:24 Page 3 of 8 Fig. 1 Differences in performance between froglets of the Pacific horned frogs Ceratophrys stolzmanni which metamorphosed at small versus large body size (developmental stage Gosner 46; mean ± SE): a head width (gape size) and b jump distance metamorphosed at a smaller size having a higher increase study (t = − 13.089, P < 0.001), although the magnitude in SVL, both in absolute values (r = 0.31, F = 13.054, decreased (the difference between average SVL in the 1,29 P = 0.001), and in percentage gained by the end of the two groups decreasing from 39% at the start of the study study (r = 0.566, F = 37.782, P < 0.001, Fig.  2a). This to 27% at the end). 1,29 means that individuals metamorphosing at a small size grew at a significantly higher rate than those metamor - Mortality phosing at a large size (0.08  mm/day versus 0.06  mm/ Survivorship over the 2-month study was significantly day on average, respectively; t = 2.29, P =0.03). In spite different between the two categories of froglets: 95% of this, the differences in SVL between the two catego - (19 out of 20) of the large individuals survived until the ries of froglets remained significant until the end of the end of the study (i.e. 62  days), compared to 60% (12 out Fig. 2 a Growth (mean ± SE increase in SVL) of juveniles of Pacific horned frogs Ceratophrys stolzmanni that metamorphosed at a small versus a large body size over the study period following metamorphosis (62 days); b Kaplan–Meier survival curves for the two groups of juveniles after metamorphosis. Dotted line: small metamorphosing juveniles; full line: large metamorphosing juveniles Székely et al. BMC Ecol (2020) 20:24 Page 4 of 8 to predators and competitors because of prolonged for- of 20) of the small individuals (log-rank test, χ = 7.318, aging [38], several other components can contribute P = 0.007; Fig.  2b). The BCI at metamorphosis was not to the lower fitness associated with accelerated growth a predictor of mortality (Cox regression, χ = 0.154, rates, amongst which a lower resistance to starvation d.f. = 1, P = 0.695). because of intense metabolism and low lipid reserves [40], delayed ossification [41], depressed immunological Discussion function [42], or cellular oxidative stress [43]. Some of Life-history switch-points such as metamorphosis, that the intrinsic costs mentioned above might have contrib- require major and irreversible changes in morphology, uted to the observed higher mortality in the froglets that anatomy, physiology, and habitat and resource use, have had metamorphosed at a small size in our study. a profound effect on individual fitness and involve trade- Pacific horned frogs showed one of the widest range offs [17, 32, 33]. Our study reveals that individuals mak- of sizes at metamorphosis reported for any amphibian ing the transition from aquatic larvae to the terrestrial in their natural population, individuals differing by up to stage at a large size experience higher survival rates dur- 100% in body size and 890% in body mass. This range is ing the first activity season. Even under favourable exper - broader than previously reported intrapopulation vari- imental conditions, with no predation or competition, ation in the literature [31, 43]. Pond permanence [30], and ad  libitum food resources, the juveniles that meta- food availability [44], temperature [45] and presence morphosed at a small size had a higher mortality rate. of predators or competitors [46, 47] are known to have It is expected that in the natural environment, smaller a profound effect on individual metamorphosing size size would result in a further increase in mortality due in anurans, and the interaction between various selec- to exposure to predators [34] and desiccation [14]. Our tive pressures can determine a large spectrum of sizes. results imply that, although developmental plasticity can Additionally, in the case of anuran species reproduc- allow tadpoles to escape an unfavourable aquatic envi- ing in ephemeral ponds, individuals are less capable to ronment (e.g. drying pond, high density, reduced food delay their metamorphosis or further increase their larval availability) before reaching an optimal size, thus avoid- growth rates, which are already close to the physiologi- ing mortality in the larval stage, it has a direct cost on cal limit [48]. This implies that differences in larval envi - survival in the terrestrial stage. The lower survival rate of ronment will produce a large variation in metamorphic smaller juveniles in terrestrial habitat is consistent with body sizes, such as the one we report here. In the natural observations made by some authors [6, 15], although in habitat, a high diversity of sizes is likely to reduce food other cases no significant long-term benefits for larger competition amongst froglets and allow for a more rapid size at metamorphosis in terms of survival was found [21, growth for both large and small individuals [49]. 35]. Differences in shape at metamorphosis (i.e. size of dif - Although size at metamorphosis is predicted to have ferent structures in relation to total individual size) are a large impact on size at maturity [32], in some species attributed to environmental conditions that promote it was shown that, if environmental conditions are opti- variations in larval growth rates [23, 50]. Studies carried mal for growth, smaller juveniles can compensate by out on various species give contrasting results, especially growing faster and the differences in size eventually fade in the case of the relationship between hind-limb size (or away [7, 36]. Indeed, our study showed that individuals segments of it) and the individual size [22]. For example, metamorphosing at a small size are able to increase their temperature-induced intensification of larval growth growth rate compared to larger individuals, and thus rates can generate individuals with relatively shorter legs diminish the size gap over time. However, long-term cap- [22, 24] or longer legs [51]; desiccation-triggered acceler- ture-mark-recapture surveys are needed to confirm this ation of growth can determine relatively shorter legs [23], pattern in natural conditions. while presence of predators and lack of food can deter- The existence of compensatory growth (i.e. an increase mine slower growth correlated with relatively shorter legs in growth rates once the conditions are favourable in [11]. In our case, metamorphosing at a smaller size was order to compensate partly or completely the depriva- associated with shorter hindlimbs, not only in absolute, tions experienced in younger stages) has been reported but even in relative terms, indicating a departure from in various taxa [37] and can be the result of behavioural isometric size of limbs in this species. Such shorter legs modifications, such as prolonged foraging activity and have also been shown to be a result of accelerated devel- higher ingestion rates [6, 38, 39], or morphological adap- opment in other species [11, 52]. tations that allow digestion of larger quantities of food However, we found that the differences in relative size [40]. However, a higher than optimal growth rate comes of hindlimbs did not affect jumping ability in the case at a fitness cost, reflected in decreased survival [37]. of horned frogs; the main factor determining locomotor Along with ecological factors, such as increased exposure Sz ékely et al. BMC Ecol (2020) 20:24 Page 5 of 8 performance was the body size of juveniles. In fossorial they are able to compensate for smaller size at metamor- frogs, the leg length in relation to the body size is prob- phosis with an increased growth rate. However, there is a ably less flexible compared to non-fossorial species of trade-off, as the benefits of leaving water early in life are frogs [24, 53], as a result of managing the contrasting offset by a lower survival. selective pressures of avoiding predation or desiccation and efficient burrowing [54]. Alternatively, the variation Methods of leg length might have been too small to determine a Study site and sampling. On the 16–17 April 2015, we measurable difference in jumping distance [55]. We collected 92 freshly metamorphosed C. stolzmanni, all found locomotor performance to be strictly size-depend- in developmental stage Gosner 45 [mouth angle at level ent, larger individuals having longer legs and jumping of posterior margin of the eye, tail reduced to a stub, 60] over larger distances in response to a simulated predator in Arenillas Ecological Reserve (03° 34′ S; 80° 08′ E, 30 m attack. In anurans, jumping ability is directly related to a.s.l.), southern Ecuador. This stage was chosen because individual fitness, allowing predator avoidance [26, 34], it allows to select individuals that just exited water at prey acquisition [25] and dispersal [27]. metamorphosis. Because mating is generally synchro- For gape-limited predators such as amphibians, the nized to one night in the studied population [61], we width of the head is another morphological trait that can considered that all froglets had approximately the same improve fitness, by permitting individuals with wider age. The froglets (n = 92) were found in terrestrial habi- gape access to larger food items [56]. Since tadpoles of tats, in an area within a 50-m radius from ponds used for Ceratophryidae are macrophagous, and because their reproduction. The average snout-vent length (SVL ± SD) mouth parts go through relatively little restructura- of froglets was 34.5 ± 4.9  mm (range: 23.8–47.9  mm), tion at metamorphosis [57], it can be assumed that the and average body mass (BM  ±  SD) was 4.1 ± 1.9  g larger relative head width can be an explanation for the (range: 1.2–11.9  g). From this spectrum of sizes (Addi- improved individual body condition at metamorpho- tional file  2), we selected the extreme phenotypes, i.e. sis, regardless of the body size. Overall, head width after the smallest 20 individuals (SVL = 28.21 ± 1.9  mm, range metamorphosis was proportional to individual SVL. In 23.8–30.3  mm; BM = 2.1 ± 0.6  g, range 1.2–3.6) and the the case of strong intra- and inter-specific competition or largest 20 individuals (SVL = 41.1 ± 2.7 mm, range 38.3– food shortage, the larger individuals may thus be better 47.9 mm; BM = 6.7 ± 1.6 g, range 5.1–11.9 g). equipped for prey ingestion compared to smaller individ- uals by having access to a wider range of prey sizes. Addi- Animal care tionally, since Ceratophrys species are known to prey on We raised the froglets in an outdoor laboratory for a other amphibians [58], small individuals would also be period of 62  days (until 24 June 2015), mimicking the more at risk of being victims of cannibalistic events. In duration of an activity season in the natural environment, the cane toad (Rhinella marina), the victims of canni- until the aestivation period (during the dry season), balistic events were a non-random subset of the juvenile which begins approximately at the end of June (pers. population, represented by the smallest and weakest indi- obs.). The froglets were kept individually, in mesh-cov - viduals [59]. The lack of beneficial modifications in the ered (to prevent escape) plastic tanks (21 × 15  cm, 12  cm proportions of investigated anatomical features, together high), with a 5-cm layer of moist soil that allowed natural with the effect of size are likely to act synergistically in burrowing behaviour [54]. Temperature, relative humid- nature, decreasing the chances of survival of small meta- ity and light regime were similar to the ones in natural morphosing individuals, especially in areas with a high habitat, except for a roof that provided protection from density of individuals that increase the probability of can- direct sun heating. All tanks were kept in similar condi- nibalistic encounters. tions, and their relative position was randomly changed after each feeding. The animals were fed an ad  libitum, Conclusions appropriately sized, diet of crickets (similar mixed sizes Our study links two stages (i.e. aquatic and terrestrial) in items for both frog size groups at any time, overall size amphibian life-history, helping to understand how size of crickets slightly larger as the froglets grew). Uneaten at metamorphosis, which is determined by conditions insects were removed and fresh food was added every in the aquatic environment, affects the subsequent ter - day for the first month, and afterwards every other day restrial stage, impacting the success and survival of indi- until the end of the study. The tanks were checked daily viduals and potentially influencing population dynamics. for potential occurrence of death of individuals and When aquatic conditions deteriorate, faster metamor- sprayed with water to maintain soil humidity. After the phosis is the best survival option for tadpoles, allowing completion of the study, on 25 June 2015, all froglets were them to take advantage of the terrestrial habitat, where released at the capture site. Székely et al. BMC Ecol (2020) 20:24 Page 6 of 8 Morphological traits normality (QQ-plot inspection) and homogeneity of The morphometric parameters used in the analyses were variance (Levene test, P > 0.05); some variables (SVL, SVL (snout-vent length, from the tip of the snout to the BM, head width and hindlimb length) were square- cloaca), BM (body mass), head width (at the corners of transformed to fit the normality assumption. The cor - the mouth), hindlimb length [total hindlimb length, relations between various morphological variables measured as the sum of the right femur, tibia, metatar- were assessed with Pearson’s r correlation tests. Linear sus, and the length between the end of the metatarsus to regression (F test) was used to test the effect of size at the end of digit IV, 62]. Total hindlimb length in amphib- metamorphosis on growth rates (absolute, percentual) ians and its size relative to the total size of the animal is of the froglets. Body condition indexes (BCI) were com- a morphometric trait influencing locomotor ability [63]. puted as residuals of lnBM against lnSVL [65]; BCI is Measurements were taken at the beginning (on the 23 considered a good estimate of lipid storage in amphib- April 2015, in G46 developmental stage, i.e. after the ians [66]. We calculated a relative hindlimb length as complete resorption of the tail so that it does not inter- the ratio between hindlimb length and SVL, as this was fere with movement) and at the end of the study (62 days shown to be related to jumping ability [67], and the rel- after the start of the experiment - SVL and BM only), ative head width as the ratio between head width and using a Dial-Max calliper (0.1  mm precision) and a My SVL. Comparisons of various relevant traits (BCI, head Weigh 300Z portable scale (0.1 g precision). Daily growth width, hindlimb length, growth rates) between the two rates were calculated as (final SVL − initial SVL)/62. Indi- size-categories of froglets were investigated using Stu- viduals that died during the study (n = 9) were excluded dent’s t-tests. To assess if size-free changes in leg size from the growth rate analysis. can influence jumping ability, general linear models were built using SVL and size independent traits (rela- tive hindlimb length and BCI) as explanatory variables, Locomotor performance and jumping ability as the dependent variable. Jumping performance tests were taken on 23 April 2015, Survival rates were calculated as the percentage of when individuals had reached developmental stage G46. individuals that survived until the end of the study in During the 2  days prior to these trials, the juveniles did each size-group. The log-rank (Mantel-Cox) test based not receive any food, so that the presence of food in the on Kaplan–Meier survival curves was used to detect digestive system would not influence the results [53]. The differences in survivorship among the two groups, lack of feeding during metamorphosis is normal in anu- while the influence of body condition on survival prob - rans, due to changes in their digestive system [64]. Jump- ability was tested through a Cox proportional-hazards ing performance trials were carried out at a mean ± SE of regression model. 22 ± 1 °C, at night-time (21:00–24:00, local time, i.e. dur- ing the normal activity hours for the species). Each tested Supplementary information individual (n = 40) was placed in the centre of a plastic Supplementary information accompanies this paper at https ://doi. arena (75 × 45  cm, 33  cm high), lined with a 5  cm layer org/10.1186/s1289 8‑020‑00291 ‑w. of moist soil, to provide natural adherence and favour movement [36]; the soil layer being replaced between Additional file 1. Morphometry, locomotor performance traits and each trial. Movement (i.e. jumping) was elicited by a growth rates for individuals from the two “metamorphosis” size groups gentle touching of the urostyle with a long probe (50 cm (SVL: snout‑ vent length). Initial measurement of morphometric traits, as well as jumping trials, were performed in Gosner 46 developmental stage, long, 1  mm diameter metal stick, with rounded tip), at while final ones were taken 62 days after metamorphosis. three times, with a 1-min break between two succes- Additional file 2. Difference in size at metamorphosis in Pacific horned sive trials. The juvenile was replaced in the centre of the frogs Ceratophrys stolzmanni (developmental stage Gosner 45), n = 92. arena before each trial. In the rare occasions when touch- The 20 smallest (white circles) and 20 largest individuals (black dots) were selected to be used in the experiment. The small insert shows a large and ing elicited a series of multiple movements, only the first a small froglet (photos Diana Székely). jump was measured. The final jumping distance for each Additional file 3. Raw data. individual was the maximum value of the three trials. Abbreviations Statistical analysis SVL: Snout‑ vent length; BM: Body mass; BCI: Body condition index. Data analysis was carried out with SPSS 21.0 (IBM Acknowledgements Corp., Armonk, NY), with a significance level set at Fieldwork in the reserve was possible thanks to the help of the Arenillas 0.05 (dataset available in Additional file  3). Values are Ecological Reserve administration. We are especially grateful to the REA “guar‑ daparques” for their friendship and support during the fieldwork. given as mean ± SE. All data were first assessed for Sz ékely et al. BMC Ecol (2020) 20:24 Page 7 of 8 Authors’ contributions 9. Székely P, Tudor M, Cogălniceanu D. Eec ff t of habitat drying on the DS and PS designed the study. DS, PS, DAO and VEM conducted fieldwork and development of the Eastern spadefoot toad (Pelobates syriacus) tadpoles. performed the experiments. DS analyzed the data. DS, DC, PS, DAO and MD Amphibia‑Reptilia. 2010;31:425–34. https ://doi.org/10.1163/15685 38107 wrote the manuscript. All authors read and approved the final manuscript.91769 536. 10. Skelly DK, Werner EE. Behavioral and life‑historical responses of larval Funding American toads to an odonate predator. Ecology. 1990;71:2313–22. https DSz benefited from a research Grant from Universidad Técnica Particular de ://doi.org/10.2307/19386 42. Loja (Convocatoria Estancias Cortas de Investigacion 2019). The collaboration 11. Van Buskirk J, Saxer G. Delayed costs of an induced defense in tadpoles? between Ovidius University Constanța and University of Liège was supported Morphology, hopping, and development rate at metamorphosis. 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How to recover from a bad start: size at metamorphosis affects growth and survival in a tropical amphibian

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Abstract

Background: In species with complex life cycles, size at metamorphosis is a key life‑history trait which reflects the complex interactions between costs and benefits of life in the aquatic and terrestrial environments. Whereas the effects of a deteriorating larval habitat (e.g. pond desiccation) on triggering an early metamorphosis have been extensively investigated in amphibians, the consequences of the resulting reduced size at metamorphosis on fitness in the post‑metamorphic terrestrial stage remain poorly understood. We tested the hypothesis that a smaller size at metamorphosis negatively affects performance and survival in the ensuing terrestrial stage. Using as model a tropical amphibian (Ceratophrys stolzmanni) showing a large phenotypic plasticity in metamorphosing traits, we evaluated the effects of size at metamorphosis on fitness‑related trophic and locomotor performance traits, as well as on growth and survival rates. Results: Our results support the hypothesis that a larger size at metamorphosis is correlated with better survival and performance. The survival rate of large metamorphosing individuals was 95%, compared to 60% for those completing metamorphosis at a small size. Locomotor performance and gape size were positively correlated with body size, larger animals being more mobile and capable to ingest larger prey. However, smaller individuals achieved higher growth rates, thus reducing the size gap. Conclusions: Overall, size at metamorphosis affected profoundly the chances of survival in the short term, but smaller surviving individuals partly compensated their initial disadvantages by increasing growth rates. Keywords: Adaptive plasticity, Growth compensation, Life cycles, Life‑history, Metamorphosis Background accompanied by a complete change of the ecological Species with complex life cycles, such as biphasic niche [3, 4]. Pond-breeding amphibians, which in their amphibians and insects, are able to exploit different eco - post-larval stages become terrestrial, represent ideal logical niches and optimize their life-history in discrete models to investigate the independence of pre- and post- developmental stages [1, 2]. The transition occurring at metamorphic life-stages and the presence of carry-over metamorphosis usually requires dramatic and irrevers- effects from one stage to the other, affecting the over - ible morphological transformations, and is frequently all fitness of individuals [5]. The most evident trade-off between the aquatic and terrestrial stages is reflected in body size at metamorphosis. When the aquatic lar- *Correspondence: dcogalniceanu@univ‑ovidius.ro vae are confronted with unfavourable conditions, such Faculty of Natural and Agricultural Sciences, Ovidius University Constanța, Constanța, Romania as food shortage [6, 7], high density [8], desiccation risk Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Székely et al. BMC Ecol (2020) 20:24 Page 2 of 8 [9] or predation [10, 11], they can leave the aquatic envi- population. From the encountered spectrum of sizes, ronment by undergoing metamorphosis. However, this we assigned the 20 largest and 20 smallest individuals to is usually done at a smaller size, which allows them to their respective size-categories (see “Methods” section). escape the immediate aquatic threats faster, but in turn We tested if smaller froglets can amend the detrimental exposes them to different selective pressures on land [1]. survival effects induced by metamorphosing at a reduced Larger size in freshly metamorphosed individuals is size through (i) allometric changes in morphology or per- correlated with improved traits, like locomotor abilities formance (wider heads, longer limbs, or better jumping and metabolic rates [12], endurance [13], resistance to skills) and/or (ii) more intense growth rates. desiccation [14], feeding success [15], and dispersal suc- cess [16]. Although the paradigm model [17] assumes Results that body size at metamorphosis is a good predictor of Morphology and locomotor performance subsequent fitness, there are authors [e.g. 3, 18] who At the completion of metamorphosis, individual body assert that this is not always the case. Since in amphib- mass (BM) and snout-vent length (SVL) showed a strong ians a substantial percent of the adult body size is gained correlation (Pearson’s r = 0.923, n = 40, P < 0.001), but after metamorphosis, and because age of sexual maturity there was no significant difference in body condition is variable, the relationship between body size at meta- between the two categories of froglets (i.e. small vs. large: morphosis and fitness is more complex, especially in t = 0.175, P = 0.862; Additional file 1). unpredictable environments [19]. For example, if smaller Since absolute head width was strongly correlated individuals have compensating mechanisms, such as to SVL at metamorphosis (r = 0.982, n = 40, P < 0.001), more intense growth rates, metamorphic size may not larger froglets had significantly wider heads compared have a significant effect on adult traits like mortality, age to the smaller ones (t = 17.123, P < 0.001; Fig. 1a). Rela- and size at first reproduction, or fecundity [20, 21]. The tive head width did not differ significantly between the detrimental consequences of a small size at metamorpho- two size categories of froglets (t = − 0.902, P = 0.373), sis can also be compensated by changes in the morphol- and was correlated with individual initial BCI (r = 0.479, ogy of juveniles [22, 23]. For example, the small froglets n = 40, P = 0.002), with froglets in better body condition can have, proportionally to their body size, larger heads having larger heads regardless of their SVL (Additional or longer legs than the bigger individuals. Such modifi - file 1). cations would be beneficial because leg length influences There was a strong positive correlation between locomotor (i.e. jumping) performance [23, 24], which in hindlimb length and SVL (r = 0.988, n = 40, P < 0.001). turn has been shown to positively affect food acquisition Compared to the large juveniles, small froglets had signif- [25], predator avoidance [26] and dispersal [27]. In a sim- icantly shorter hindlimbs both in terms of absolute size ilar manner, a large head width favours the swallowing (t = − 17.001, P < 0.001), and relative size (t = − 6.309, 38 38 ability, which is a limiting factor in prey selection [28, 29]. P < 0.001). We found no relationship between the body In this context, we were interested to understand the condition of juveniles and their relative hindlimb lengths influence of size at metamorphosis on post-metamorphic (r = 0.114, n = 40, P = 0.485). traits such as survival, morphology and performance, Absolute jumping ability was predicted by SVL and to investigate the existence of compensating mecha- (F = 102.364, P < 0.001), with no significant effect 1,36 nisms. Hypothesizing that the difference would be most of either relative hindlimb length (F = 0.539, 1,36 evident between individuals at the opposite ends of the P = 0.468), or BCI (F = 0.056, P = 0.815). Larger 1,36 size range, we evaluated the impact of extreme size phe- individuals were able to jump over greater distances notypes. We selected as a model a species capable of (mean ± SE = 100.4 ± 3.6  mm) than the smaller ones high plasticity in metamorphosing size [30], the Pacific (59.4 ± 2.3 mm; t = − 9.501, P < 0.001; Fig. 1b). horned frog (Ceratophrys stolzmanni). This fossorial frog inhabits tropical dry forests, a highly seasonal eco- Growth system characterized by a short rainy season that lasts At the end of the study period (i.e. 2 months after meta- less than 4  months annually. The tadpoles have some of morphosis), the two categories of froglets did not differ in the most intense growth rates reported for anurans and terms of their body condition indices (BCI; t = − 0.289, can leave the water in as little as 2 weeks after egg-laying P = 0.774). Individual BCI after 2  months of terrestrial [30]. Because several environmental parameters can have growth was not correlated with the froglet’s SVL at meta- interacting effects in the natural habitat [31], we used morphosis (r = 0.107, n = 31, P = 0.566), nor with initial freshly metamorphosed froglets resulting from tadpoles BCI (r = 0.191, n = 31, P = 0.302). that grew in field conditions (natural ponds) in order to There was a significant effect of size at metamorphosis cover the entire range of size at metamorphosis in the on post-metamorphic growth rates, with individuals that Sz ékely et al. BMC Ecol (2020) 20:24 Page 3 of 8 Fig. 1 Differences in performance between froglets of the Pacific horned frogs Ceratophrys stolzmanni which metamorphosed at small versus large body size (developmental stage Gosner 46; mean ± SE): a head width (gape size) and b jump distance metamorphosed at a smaller size having a higher increase study (t = − 13.089, P < 0.001), although the magnitude in SVL, both in absolute values (r = 0.31, F = 13.054, decreased (the difference between average SVL in the 1,29 P = 0.001), and in percentage gained by the end of the two groups decreasing from 39% at the start of the study study (r = 0.566, F = 37.782, P < 0.001, Fig.  2a). This to 27% at the end). 1,29 means that individuals metamorphosing at a small size grew at a significantly higher rate than those metamor - Mortality phosing at a large size (0.08  mm/day versus 0.06  mm/ Survivorship over the 2-month study was significantly day on average, respectively; t = 2.29, P =0.03). In spite different between the two categories of froglets: 95% of this, the differences in SVL between the two catego - (19 out of 20) of the large individuals survived until the ries of froglets remained significant until the end of the end of the study (i.e. 62  days), compared to 60% (12 out Fig. 2 a Growth (mean ± SE increase in SVL) of juveniles of Pacific horned frogs Ceratophrys stolzmanni that metamorphosed at a small versus a large body size over the study period following metamorphosis (62 days); b Kaplan–Meier survival curves for the two groups of juveniles after metamorphosis. Dotted line: small metamorphosing juveniles; full line: large metamorphosing juveniles Székely et al. BMC Ecol (2020) 20:24 Page 4 of 8 to predators and competitors because of prolonged for- of 20) of the small individuals (log-rank test, χ = 7.318, aging [38], several other components can contribute P = 0.007; Fig.  2b). The BCI at metamorphosis was not to the lower fitness associated with accelerated growth a predictor of mortality (Cox regression, χ = 0.154, rates, amongst which a lower resistance to starvation d.f. = 1, P = 0.695). because of intense metabolism and low lipid reserves [40], delayed ossification [41], depressed immunological Discussion function [42], or cellular oxidative stress [43]. Some of Life-history switch-points such as metamorphosis, that the intrinsic costs mentioned above might have contrib- require major and irreversible changes in morphology, uted to the observed higher mortality in the froglets that anatomy, physiology, and habitat and resource use, have had metamorphosed at a small size in our study. a profound effect on individual fitness and involve trade- Pacific horned frogs showed one of the widest range offs [17, 32, 33]. Our study reveals that individuals mak- of sizes at metamorphosis reported for any amphibian ing the transition from aquatic larvae to the terrestrial in their natural population, individuals differing by up to stage at a large size experience higher survival rates dur- 100% in body size and 890% in body mass. This range is ing the first activity season. Even under favourable exper - broader than previously reported intrapopulation vari- imental conditions, with no predation or competition, ation in the literature [31, 43]. Pond permanence [30], and ad  libitum food resources, the juveniles that meta- food availability [44], temperature [45] and presence morphosed at a small size had a higher mortality rate. of predators or competitors [46, 47] are known to have It is expected that in the natural environment, smaller a profound effect on individual metamorphosing size size would result in a further increase in mortality due in anurans, and the interaction between various selec- to exposure to predators [34] and desiccation [14]. Our tive pressures can determine a large spectrum of sizes. results imply that, although developmental plasticity can Additionally, in the case of anuran species reproduc- allow tadpoles to escape an unfavourable aquatic envi- ing in ephemeral ponds, individuals are less capable to ronment (e.g. drying pond, high density, reduced food delay their metamorphosis or further increase their larval availability) before reaching an optimal size, thus avoid- growth rates, which are already close to the physiologi- ing mortality in the larval stage, it has a direct cost on cal limit [48]. This implies that differences in larval envi - survival in the terrestrial stage. The lower survival rate of ronment will produce a large variation in metamorphic smaller juveniles in terrestrial habitat is consistent with body sizes, such as the one we report here. In the natural observations made by some authors [6, 15], although in habitat, a high diversity of sizes is likely to reduce food other cases no significant long-term benefits for larger competition amongst froglets and allow for a more rapid size at metamorphosis in terms of survival was found [21, growth for both large and small individuals [49]. 35]. Differences in shape at metamorphosis (i.e. size of dif - Although size at metamorphosis is predicted to have ferent structures in relation to total individual size) are a large impact on size at maturity [32], in some species attributed to environmental conditions that promote it was shown that, if environmental conditions are opti- variations in larval growth rates [23, 50]. Studies carried mal for growth, smaller juveniles can compensate by out on various species give contrasting results, especially growing faster and the differences in size eventually fade in the case of the relationship between hind-limb size (or away [7, 36]. Indeed, our study showed that individuals segments of it) and the individual size [22]. For example, metamorphosing at a small size are able to increase their temperature-induced intensification of larval growth growth rate compared to larger individuals, and thus rates can generate individuals with relatively shorter legs diminish the size gap over time. However, long-term cap- [22, 24] or longer legs [51]; desiccation-triggered acceler- ture-mark-recapture surveys are needed to confirm this ation of growth can determine relatively shorter legs [23], pattern in natural conditions. while presence of predators and lack of food can deter- The existence of compensatory growth (i.e. an increase mine slower growth correlated with relatively shorter legs in growth rates once the conditions are favourable in [11]. In our case, metamorphosing at a smaller size was order to compensate partly or completely the depriva- associated with shorter hindlimbs, not only in absolute, tions experienced in younger stages) has been reported but even in relative terms, indicating a departure from in various taxa [37] and can be the result of behavioural isometric size of limbs in this species. Such shorter legs modifications, such as prolonged foraging activity and have also been shown to be a result of accelerated devel- higher ingestion rates [6, 38, 39], or morphological adap- opment in other species [11, 52]. tations that allow digestion of larger quantities of food However, we found that the differences in relative size [40]. However, a higher than optimal growth rate comes of hindlimbs did not affect jumping ability in the case at a fitness cost, reflected in decreased survival [37]. of horned frogs; the main factor determining locomotor Along with ecological factors, such as increased exposure Sz ékely et al. BMC Ecol (2020) 20:24 Page 5 of 8 performance was the body size of juveniles. In fossorial they are able to compensate for smaller size at metamor- frogs, the leg length in relation to the body size is prob- phosis with an increased growth rate. However, there is a ably less flexible compared to non-fossorial species of trade-off, as the benefits of leaving water early in life are frogs [24, 53], as a result of managing the contrasting offset by a lower survival. selective pressures of avoiding predation or desiccation and efficient burrowing [54]. Alternatively, the variation Methods of leg length might have been too small to determine a Study site and sampling. On the 16–17 April 2015, we measurable difference in jumping distance [55]. We collected 92 freshly metamorphosed C. stolzmanni, all found locomotor performance to be strictly size-depend- in developmental stage Gosner 45 [mouth angle at level ent, larger individuals having longer legs and jumping of posterior margin of the eye, tail reduced to a stub, 60] over larger distances in response to a simulated predator in Arenillas Ecological Reserve (03° 34′ S; 80° 08′ E, 30 m attack. In anurans, jumping ability is directly related to a.s.l.), southern Ecuador. This stage was chosen because individual fitness, allowing predator avoidance [26, 34], it allows to select individuals that just exited water at prey acquisition [25] and dispersal [27]. metamorphosis. Because mating is generally synchro- For gape-limited predators such as amphibians, the nized to one night in the studied population [61], we width of the head is another morphological trait that can considered that all froglets had approximately the same improve fitness, by permitting individuals with wider age. The froglets (n = 92) were found in terrestrial habi- gape access to larger food items [56]. Since tadpoles of tats, in an area within a 50-m radius from ponds used for Ceratophryidae are macrophagous, and because their reproduction. The average snout-vent length (SVL ± SD) mouth parts go through relatively little restructura- of froglets was 34.5 ± 4.9  mm (range: 23.8–47.9  mm), tion at metamorphosis [57], it can be assumed that the and average body mass (BM  ±  SD) was 4.1 ± 1.9  g larger relative head width can be an explanation for the (range: 1.2–11.9  g). From this spectrum of sizes (Addi- improved individual body condition at metamorpho- tional file  2), we selected the extreme phenotypes, i.e. sis, regardless of the body size. Overall, head width after the smallest 20 individuals (SVL = 28.21 ± 1.9  mm, range metamorphosis was proportional to individual SVL. In 23.8–30.3  mm; BM = 2.1 ± 0.6  g, range 1.2–3.6) and the the case of strong intra- and inter-specific competition or largest 20 individuals (SVL = 41.1 ± 2.7 mm, range 38.3– food shortage, the larger individuals may thus be better 47.9 mm; BM = 6.7 ± 1.6 g, range 5.1–11.9 g). equipped for prey ingestion compared to smaller individ- uals by having access to a wider range of prey sizes. Addi- Animal care tionally, since Ceratophrys species are known to prey on We raised the froglets in an outdoor laboratory for a other amphibians [58], small individuals would also be period of 62  days (until 24 June 2015), mimicking the more at risk of being victims of cannibalistic events. In duration of an activity season in the natural environment, the cane toad (Rhinella marina), the victims of canni- until the aestivation period (during the dry season), balistic events were a non-random subset of the juvenile which begins approximately at the end of June (pers. population, represented by the smallest and weakest indi- obs.). The froglets were kept individually, in mesh-cov - viduals [59]. The lack of beneficial modifications in the ered (to prevent escape) plastic tanks (21 × 15  cm, 12  cm proportions of investigated anatomical features, together high), with a 5-cm layer of moist soil that allowed natural with the effect of size are likely to act synergistically in burrowing behaviour [54]. Temperature, relative humid- nature, decreasing the chances of survival of small meta- ity and light regime were similar to the ones in natural morphosing individuals, especially in areas with a high habitat, except for a roof that provided protection from density of individuals that increase the probability of can- direct sun heating. All tanks were kept in similar condi- nibalistic encounters. tions, and their relative position was randomly changed after each feeding. The animals were fed an ad  libitum, Conclusions appropriately sized, diet of crickets (similar mixed sizes Our study links two stages (i.e. aquatic and terrestrial) in items for both frog size groups at any time, overall size amphibian life-history, helping to understand how size of crickets slightly larger as the froglets grew). Uneaten at metamorphosis, which is determined by conditions insects were removed and fresh food was added every in the aquatic environment, affects the subsequent ter - day for the first month, and afterwards every other day restrial stage, impacting the success and survival of indi- until the end of the study. The tanks were checked daily viduals and potentially influencing population dynamics. for potential occurrence of death of individuals and When aquatic conditions deteriorate, faster metamor- sprayed with water to maintain soil humidity. After the phosis is the best survival option for tadpoles, allowing completion of the study, on 25 June 2015, all froglets were them to take advantage of the terrestrial habitat, where released at the capture site. Székely et al. BMC Ecol (2020) 20:24 Page 6 of 8 Morphological traits normality (QQ-plot inspection) and homogeneity of The morphometric parameters used in the analyses were variance (Levene test, P > 0.05); some variables (SVL, SVL (snout-vent length, from the tip of the snout to the BM, head width and hindlimb length) were square- cloaca), BM (body mass), head width (at the corners of transformed to fit the normality assumption. The cor - the mouth), hindlimb length [total hindlimb length, relations between various morphological variables measured as the sum of the right femur, tibia, metatar- were assessed with Pearson’s r correlation tests. Linear sus, and the length between the end of the metatarsus to regression (F test) was used to test the effect of size at the end of digit IV, 62]. Total hindlimb length in amphib- metamorphosis on growth rates (absolute, percentual) ians and its size relative to the total size of the animal is of the froglets. Body condition indexes (BCI) were com- a morphometric trait influencing locomotor ability [63]. puted as residuals of lnBM against lnSVL [65]; BCI is Measurements were taken at the beginning (on the 23 considered a good estimate of lipid storage in amphib- April 2015, in G46 developmental stage, i.e. after the ians [66]. We calculated a relative hindlimb length as complete resorption of the tail so that it does not inter- the ratio between hindlimb length and SVL, as this was fere with movement) and at the end of the study (62 days shown to be related to jumping ability [67], and the rel- after the start of the experiment - SVL and BM only), ative head width as the ratio between head width and using a Dial-Max calliper (0.1  mm precision) and a My SVL. Comparisons of various relevant traits (BCI, head Weigh 300Z portable scale (0.1 g precision). Daily growth width, hindlimb length, growth rates) between the two rates were calculated as (final SVL − initial SVL)/62. Indi- size-categories of froglets were investigated using Stu- viduals that died during the study (n = 9) were excluded dent’s t-tests. To assess if size-free changes in leg size from the growth rate analysis. can influence jumping ability, general linear models were built using SVL and size independent traits (rela- tive hindlimb length and BCI) as explanatory variables, Locomotor performance and jumping ability as the dependent variable. Jumping performance tests were taken on 23 April 2015, Survival rates were calculated as the percentage of when individuals had reached developmental stage G46. individuals that survived until the end of the study in During the 2  days prior to these trials, the juveniles did each size-group. The log-rank (Mantel-Cox) test based not receive any food, so that the presence of food in the on Kaplan–Meier survival curves was used to detect digestive system would not influence the results [53]. The differences in survivorship among the two groups, lack of feeding during metamorphosis is normal in anu- while the influence of body condition on survival prob - rans, due to changes in their digestive system [64]. Jump- ability was tested through a Cox proportional-hazards ing performance trials were carried out at a mean ± SE of regression model. 22 ± 1 °C, at night-time (21:00–24:00, local time, i.e. dur- ing the normal activity hours for the species). Each tested Supplementary information individual (n = 40) was placed in the centre of a plastic Supplementary information accompanies this paper at https ://doi. arena (75 × 45  cm, 33  cm high), lined with a 5  cm layer org/10.1186/s1289 8‑020‑00291 ‑w. of moist soil, to provide natural adherence and favour movement [36]; the soil layer being replaced between Additional file 1. Morphometry, locomotor performance traits and each trial. Movement (i.e. jumping) was elicited by a growth rates for individuals from the two “metamorphosis” size groups gentle touching of the urostyle with a long probe (50 cm (SVL: snout‑ vent length). Initial measurement of morphometric traits, as well as jumping trials, were performed in Gosner 46 developmental stage, long, 1  mm diameter metal stick, with rounded tip), at while final ones were taken 62 days after metamorphosis. three times, with a 1-min break between two succes- Additional file 2. Difference in size at metamorphosis in Pacific horned sive trials. The juvenile was replaced in the centre of the frogs Ceratophrys stolzmanni (developmental stage Gosner 45), n = 92. arena before each trial. In the rare occasions when touch- The 20 smallest (white circles) and 20 largest individuals (black dots) were selected to be used in the experiment. The small insert shows a large and ing elicited a series of multiple movements, only the first a small froglet (photos Diana Székely). jump was measured. The final jumping distance for each Additional file 3. Raw data. individual was the maximum value of the three trials. Abbreviations Statistical analysis SVL: Snout‑ vent length; BM: Body mass; BCI: Body condition index. Data analysis was carried out with SPSS 21.0 (IBM Acknowledgements Corp., Armonk, NY), with a significance level set at Fieldwork in the reserve was possible thanks to the help of the Arenillas 0.05 (dataset available in Additional file  3). Values are Ecological Reserve administration. We are especially grateful to the REA “guar‑ daparques” for their friendship and support during the fieldwork. given as mean ± SE. All data were first assessed for Sz ékely et al. BMC Ecol (2020) 20:24 Page 7 of 8 Authors’ contributions 9. Székely P, Tudor M, Cogălniceanu D. Eec ff t of habitat drying on the DS and PS designed the study. DS, PS, DAO and VEM conducted fieldwork and development of the Eastern spadefoot toad (Pelobates syriacus) tadpoles. performed the experiments. DS analyzed the data. DS, DC, PS, DAO and MD Amphibia‑Reptilia. 2010;31:425–34. https ://doi.org/10.1163/15685 38107 wrote the manuscript. All authors read and approved the final manuscript.91769 536. 10. Skelly DK, Werner EE. Behavioral and life‑historical responses of larval Funding American toads to an odonate predator. Ecology. 1990;71:2313–22. https DSz benefited from a research Grant from Universidad Técnica Particular de ://doi.org/10.2307/19386 42. Loja (Convocatoria Estancias Cortas de Investigacion 2019). The collaboration 11. Van Buskirk J, Saxer G. Delayed costs of an induced defense in tadpoles? between Ovidius University Constanța and University of Liège was supported Morphology, hopping, and development rate at metamorphosis. Evolu‑ by Wallonie‑Bruxelles International ( W.B.I.) and CCCDI‑UEFISCDI (A.N.C.S.: tion. 2001;55:821–9. https ://doi.org/10.1111/j.0014‑3820.2001.tb008 17.x. Autoritatea Nationala pentru Cercetare Stiintifica)–project no. 105 BM/2017. 12. Beck CW, Congdon JD. Eec ff ts of age and size at metamorphosis MD is a Research Director at Fonds de la Recherche Scientifique–FNRS on performance and metabolic rates of southern toad, Bufo ter- (Belgium). restris, metamorphs. Funct Ecol. 2000;14:32–8. https ://doi.org/10.104 6/j.1365‑2435.2000.00386 .x. Availability of data and materials 13. John‑Alder HB, Morin PJ. Eec ff ts of larval density on jumping ability All data generated or analysed during this study are included in this published and stamina in newly metamorphosed Bufo woodhousii fowleri. Copeia. article and its supplementary information files (Additional files 1, 2 and 3). 1990;1990:856–60. https ://www.jstor .org/stabl e/14464 53. 14. Child T, Phillips BL, Brown GP, Shine R. 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BMC Ecology – Springer Journals

Published: Apr 21, 2020

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