Acta Herpetologica 17(1): 13-20, 2022

ISSN 1827-9635 (print) © Firenze University Press 
ISSN 1827-9643 (online) www.fupress.com/ah

DOI: 10.36253/a_h-11453

Influence of tail injury on the development of Neotropical elegant 
treefrog tadpoles

Ana Glaucia da Silva Martins1,#, Raoni Rebouças2,3,*,#, Isaias Santos1, Adão Henrique Rosa Domingos1, Luís 
Felipe Toledo2

1 IPBio – Instituto de Pesquisas da Biodiversidade, Reserva Betary, Iporanga, São Paulo, Brazil 
2 Laboratório de História Natural de Anfíbios Brasileiros (LaHNAB), Departamento de Biologia Animal, Instituto de Biologia, Universi-
dade Estadual de Campinas, Cidade Universitária Zeferino Vaz, 13083-970, Campinas, São Paulo, Brazil
3 Programa de Pós-Graduação em Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, Cidade Universitária 
Zeferino Vaz, 13083-970, Campinas, São Paulo, Brazil
*Corresponding author. E-mail: raonisreboucas@gmail.com
# These authors contributed equally to this work

Submitted on: 2021, 5th July; revised on: 2021, 1st November; accepted on: 2021, 8th November
Editor: Simon Baeckens 

Abstract. Anuran larvae in aquatic environments are important prey items for several vertebrate and invertebrate spe-
cies. Besides avoiding predation, there are some strategies that may reduce the physical damage in those tadpoles that 
survive the predation attempt. For example, the injured tadpole tail can regrow after a predator bite, but few studies 
have examined the consequences of such injury. We examined the consequences of three levels of injury to the tail 
and how this influenced development and feeding behavior of tadpoles of the Neotropical elegant treefrog, Dendrop-
sophus elegans. We collected spawns and kept them in the laboratory until tadpoles reached Gosner’s stages 28 to 35. 
Then, they were separated in four experimental groups: individuals with tail trimmed in 30, 50 or 70 % of its length, 
and a control group, with no tail removing. We counted the days until metamorphosis, calculated the Scaled Mass 
Index (SMI) through weight and length of newly-metamorphosed, and evaluated the feeding frequency to evaluate the 
influence of tail amputation on them. We found that the time until metamorphosis was positively related to the extent 
of the amputation, but SMI and feeding behavior were not influenced. As the time to metamorphose is related to 
the survivorship chances of individuals: i.e., if the aquatic environment is with high density of predators, it would be 
advantageous to rapidly metamorphose out of the water. However, tail injury delays the metamorphose process, which 
could influence the survival of the individual.

Keywords. Anuran larvae, Dendropsophus elegans, Atlantic rainforest, tail loss, development, feeding.

INTRODUCTION

Most anurans present aquatic larval stages and terres-
trial post-metamorphic (adult) life stages, and are suscep-
tible to predators of both environments. In this context, 
several defensive strategies were already reported for tad-
poles in face of predators’ attack. For example, tadpoles of 
Pelophylax lessonae can alter their behavior in the pres-

ence of dragonfly larvae (van Buskirk and Arioli, 2002), 
and tadpoles of Dryophites crysoscelis can change the 
morphology of their tails in order to increase swimming 
speed, which consequently promotes a higher probability 
of escaping in a possible attack of predators (McCollum 
and Leimberger, 1997). Also, Other species rely on visu-
al aspects to avoid predation, such as tadpoles of Scinax 
machadoi, which select background colors to improve 



14 Ana Glaucia da Silva Martins et alii

their camouflage (Eterovick et al., 2018; Gontijo et al., 
2018), Pseudacris regilla, which alter their tail color to 
avoid predator attacks (Benard, 2006), and Boana semi-
lineata, which uses aposematic coloration to avoid pre-
dation (D’Heursel and Haddad, 1999). Hence, other spe-
cies, such as Bufo bufo, rely on chemical defenses to avoid 
attacks of predators (Üveges et al., 2019).

Anurans are well known to be centralized in trophic 
webs (Blanco-Torres et al., 2020) since they are both prey 
and predators (Rebouças et al., 2013; Rebouças and Solé, 
2015). In this way, they evolved several strategies to avoid 
predation (e.g., Lourenço-de-Moraes et al., 2016; Toledo 
et al., 2007). In larvae, one of the possible sublethal con-
sequences of a predation attempt is the partial tail loss or 
injury (Morin, 1985; Touchon and Wojdak, 2014; Wilbur 
and Semlitsch, 1990), but the consequences of it to indi-
vidual survival are very variable. For some species, past 
evidence suggest that it incurs little cost for tadpoles, 
since they, after escaping the predation, can regenerate 
the tail completely (Wilbur and Semlitsch, 1990). For 
example, van Buskirk et al. (2003) observed that tails 
may play a role as a lure, in which larger tail fins reduced 
predations in 16 % of the observations. Indeed, although 
firstly reported that enlarged tail fins enables predator 
escaping by enabling faster swimming (Smith and van 
Buskirk, 1995), posterior studies showed that tadpoles 
with injured tails did not lost speed in relation to those 
with an intact tails (van Buskirk and McCollum, 2000a). 
The effect on speed was significant only if large portions 
of the tails were removed (Hoff and Wassersug, 2000; van 
Buskirk and McCollum, 2000b). However, for some spe-
cies tail injuries result in less swimming performance, 
and consequently a higher predation risk. In Dryophytes 
chrysoscelis, for example, tadpoles with no tail injury pre-
sented a survival almost twice as high as those with 75 
% of tail loss (Semlitsch, 1990). Also, in Bombina orienta-
lis tadpoles presented less survivorship and longer larval 
period (Parichy and Kaplan, 1992).

Beyond the ecological consequences, tail loss in 
tadpoles can also present feeding activity modification. 
Theoretically, if individuals need no regenerate tails after 
a predation attempt, they should acquire more energy 
through feeding to reach the maximum of tail length 
as less time as possible, and consequently reach the full 
swim performance, which is related to tail shape (van 
Buskirk and McCollum, 2000b). However, although 
modification of feeding behavior is already observed  in 
presence of predators (e.g., Feminella and Hawkins, 1994; 
Pueta et al., 2016), the effects of tail loss on it, which is 
the most common consequence of predation attempt, still 
were not observed. Hence, while regenerating the tail, 
tadpoles are in continuous growth, which per se requires 

a constant food intake until reach the metamorphosis 
stage. Thus, the tail injury, and an extra acquisition of 
nutrients during its regeneration, must affect the feeding-
growth-time until metamorphosis balance. It is relevant 
because tail injuries may impact on the population sur-
vivorship coupled with the fact that this species occurs in 
Atlantic rainforest, one of the most diverse and vulner-
able environments of the world, where pandemic diseases 
(Carvalho et al., 2017) climatic changes (Moura-Campos 
et al., 2021; Rebouças et al., 2021), habitat fragmentation 
(Becker et al., 2010; Dixo et al., 2009), and introduced 
predators (da Silva et al., 2009; de Oliveira et al., 2016; 
Forti et al., 2017) are threatening endemic anurans.

Therefore, this study evaluates the consequences of 
tadpole’s tail injuries in a Neotropical anuran species, 
Dendropsophus elegans (Anura; Hylidae), testing the fol-
lowing hypotheses: i) different levels of tail injury result 
in less healthy newly-metamophosed; ii) different levels 
of tail injury increase the time to complete metamorpho-
sis; and iii) tail injury reduces foraging activity of tad-
poles.

MATERIALS AND METHODS

Tadpoles of Dendropsophus elegans (Fig. 1) were 
obtained through the maintenance of egg masses collect-
ed at Reserva Betary, Iporanga, São Paulo, Brazil. After 
hatching, each tadpole was kept in an individual aquar-
ium (40 x 45 x 30 cm), to avoid pseudo-replicates and 
the influence of one individual in another, maintained 
at room temperature (25 ºC), and half of the water was 
replaced twice a week after tadpoles reach the stage 28. 
We used tadpoles between Gosner’s (1960) stages 28 and 
36 for the experiments. These stages were chosen because 
they comprehend most of growth and development of 
anuran larvae (Pfab et al., 2020). Environmental condi-
tions of laboratory were constantly monitored and indi-
viduals were observed until metamorphosis. Thus, our 
experiment began before hatching and finished after met-
amorphosis. After the experiment, all individuals were 
released in the original sampling locality. 

Tadpole development. To evaluate the influence of tail 
loss in the size and growth of individuals, we selected 
tadpoles that measured 25 mm of total length. Individu-
als were measured with a digital caliper (to the nearest 
0.01 mm) and weighted with a digital scale (to the near-
est 0.01 g). We then arranged these tadpoles into four 
groups, following Semlitsch (1990) and Figiel Jr and Sem-
litsch (1991), representing each of the treatments: i) tad-
poles with 30 % of the tail clipped; ii) tadpoles with 50 
% of tail clipped; iii) tadpoles with 70 % of tail clipped; 



15Influence of tail injury on the development of Neotropical elegant treefrog tadpoles

and iv) tadpoles with intact tails, which was the control 
group (Fig 1). Each group contained between 8 and 10 
individuals (Table 1), which were isolated in each aquar-
ium. Tail modifications were performed using a sterilized 
scalpel blade. Individuals in all treatments were equally 
fed with a standard fish food (extruded AquaLine), with 
0.1 g every day. Individuals were observed until the meta-
morphosis was completed (complete tail absorption), and 
snout-vent length (SVL) of newly-metamorphosed indi-
viduals was measured with the digital caliper and body 
mass was weighted with the digital scale. Body mass 
and weight were used to calculated the Scale Mass Index 
(SMI), which is and index that can be used as a proxy of 
animals’ health and fitness (Peig and Green, 2009).

Foraging. In order to evaluate the influence of par-
tial tail loss in tadpoles foraging, we performed a second 
experiment also using 10 individuals measuring 25 mm 
in total length and between Gosner’s (1960) stages 28 and 
36. These individuals were separated in two treatments: 
i) individuals with 70 % of tail amputated; and ii) indi-
viduals with intact tails, treated as the control. Tadpoles 
were kept individually in glass jars measuring 6.5 cm in 
diameter and 6 cm height, with 120 ml of water and 0.1 g 

of fish food. After two min of acclimation, tadpoles were 
observed for 12 min. During this time, the feeding fre-
quency was observed in intervals of 20 s, and during each 
observation we evaluated if were feeding or not. 

Statistical analyses. Firstly, we used an Analysis of 
Variance (ANOVA) and a Student’s t test to evaluate of 
SMI present difference between treatments (tail amputa-
tions of 30 %, 50 % and 70 %; and tail amputation per 
se, respectively). To evaluate the influence of tail injury 
on SMI and on time until metamorphosis, we ran two 
Generalized Linear Models analyses (GLM), both using 
treatment (30 %, 50 % and 70 % of tail amputations and 
control, coded as 1, 2, 3 and 0, respectively) as predic-
tive variable, the first one with SMI of newly metamor-
phosed individual as response, and the second with days 
until metamorphosis as response. Both analyses were 
performed using gaussian family and identity link. Addi-
tionally, we ran other two GLM’s, with the same param-
eters, to evaluate if SMI or days until metamorphosis 
were influenced by amputation per se (all treatments 
were classified as “amputated”, for treatments which the 
tail was clipped, coded as 1, and “intact” for the control 
treatment, coded as 0). Finally, in order to evaluate the 

Fig. 1. An adult individual of Dendropsophus elegans (A), tadpoles of control (B) and 50 % of the tail clipped treatments (C), and with 
regenerated tail (D).



16 Ana Glaucia da Silva Martins et alii

influence of tail loss in foraging we also used a GLM, 
but with quasipoisson family and logit link, considering 
“treatment” as predictive variable (control, coded as 0, 
or amputation, coded as 1), and the feeding frequency as 
response variable. 

All models were checked through residuals deviance, 
and models with more than one predictive variable and 
collinearity was checked through Variance Inflation Factor 
(VIF) through the “vif ” function of “car” package (Fox & 
Weisberg, 2019). We considered levels higher than 4 as an 
indicator of multicollinearity (Hair et al., 2010). Hence, as 
pos hoc tests, we used estimated marginal means to com-
pare groups of tail-trimmed individuals with the control 
group through the “emmeans” package (Lenth, 2020). All 
analyses were carried out in R 4.1.0 (R Core Team, 2021) 
considering a significance level of 5 %.

RESULTS

During the experiment about tadpole development, 
we recorded the death of four individuals: one from the 
control group, one from the 50 % amputation group, 
and two from the 70 % amputation group. All individu-
als from the treatment groups presented the tail totally 
regenerated within 12 days after the beginning of the 
experiment (Table 1). We observed tail regeneration in all 
individuals that had their tail clipped (Fig. 2).

The average time until metamorphosis (from eggs 
until newly-metamorphosed) was 87.5 days for the con-
trol group (room mean temperature of 26.5 ºC; Table 1). 
We observed no difference between treatment groups (F 
= 0.91, P = 0.44) or between individuals with tail ampu-
tation or not (t = -0.06, P = 0.95). Newly metamorphosed 
individuals presented an average SMI of 0.148 ± 0.012, 
with control group presenting 0.148 ± 0.011, 30 % group 
presenting 0.143 ± 0.013, 50 % group presenting 0.153 ± 
0.012, and 70 % group presenting 0.149 ± 0.014. During 
foraging experiment, individuals with injured tail were 

observed feeding in an average of 36.6 ± 25.9 times, while 
individuals with no tail injuring were observed feeding in 
an average of 55.1 ± 22.9 times.

In our analysis, none of the variables presented VIF 
higher than 4 (SVL = 3.02, weight = 3.35, days until met-
amorphosis = 1.2). We observed no influence of treat-
ment on SMI or in weight, but treatment presented a sig-
nificant influence on time until metamorphosis. Amputa-
tion per se showed no influence in any of our variables. 
Regarding to foraging, we observed no influence of tail 
injury on feeding frequency. All model outputs are in 
Table 2 and estimated marginal means in Table 3.

Table 1. Time until metamorphosis, snout-vent length (SVL) and body mass of newly metamorphosed individuals during experimentation. 
Values presented as mean ± standard deviation (minimum – maximum; number of individuals tested; standard error).

Treatment Time until metamorphosis (days) SVL (mm) Weight (g)

Control
29.8 ± 11.5

(18.3 – 41.3; 9; 3.83)
12.06 ± 0.44

(11.62 – 12.49; 9; 0.14)
0.15 ± 0.02

(0.13 – 0.17; 9; 0.007)

30 %
35 ± 10.8 

(24.2 – 45.8; 10; 2.98)
11.86 ± 0.46

(11.40 – 12.32; 10; 0.14)
0.14 ± 0.02  

(0.12 – 0.16; 10; 0.006)

50 %
32.8 ± 7.1

(25.7 – 39.9; 9; 2.36)
12.13 ± 0.24

(11.90 – 12.37; 9; 0.08)
0.16 ± 0.02

(0.14 – 0.18; 9; 0.007)

70 %
42.0 ± 15.1 

(26.9 – 57.1; 8; 5.34)
12.01 ± 0.44

(11.57 – 12.46; 8; 0.14)
0.15 ± 0.02

(0.13 – 0.17; 10; 0.006)

Fig. 2. Days until metamorphosis of Dendropsophus elegans tad-
poles subjected to four treatments: control (intact tail), and 30, 50 
and 70% of tail removal. The top and bottom of the boxes repre-
sent the first and last quartiles, the horizontal line within the box 
represents the median, the whiskers represent the tenth and 90th 
percentiles. Asterisks represent the category of tail amputation that 
showed significant reduction of time until metamorphosis.



17Influence of tail injury on the development of Neotropical elegant treefrog tadpoles

DISCUSSION

We showed that although tadpoles reach metamor-
phosis with the same weight and size in all classes, the 
time spent until the end of the metamorphosis tends to 
increase, and it was significantly longer when 70 % of tail 
is removed. It means that individuals with a severe dam-
age in tail tend to spend more time under larval stage, 
which can submit individuals that were already threat-
ened by a predator under aquatic predation pressure for 
a longer time. Also, it delays the development of adult life 
stage, and consequently reproduction can be retarded. 
Therefore, a high predation pressure can influence other 
life stages of individuals, and in a larger scale, can impair 
the permanence of a population. 

We also observed that the feeding frequency was 
not significantly higher in the group with tail trimmed. 
Some similar results were observed in other experiments 
involving artificial tail removing in tadpoles of Aquarana 
catesbeiana, where individuals also had a delay in growth 
and development (Wilbur and Semlitsch, 1990). A possi-
ble explanation for these observed results is that a preda-
tion attempt does not result in increasing of uptake but in 
reallocation of energy, since feeding presented no increas-
ing, and it consequently could cause a delay in develop-
ment. Additional studies are necessary to further eluci-
date the physiology of this possible energy reallocation 
and verify this hypothesis.

We did not observe influence of tail removal on the 
SMI of newly-metamorphosed individuals, similarly to 
what was reported for size in Osteopilus septentrionalis 
(Koch and Wilcoxen, 2019) and Hoplobatrachus rugulo-
sus (Ding et al., 2014). However, opposing results were 
found for other species. For example, in Bombina ori-
entalis, for which the time until metamorphosis was the 
same independently of the tail injury extent, newly meta-
morphosed individuals were smaller than those without 
tail injury (Parichy and Kaplan, 1992). Likewise, tadpoles 
with 55 % of the tail removed resulted in smaller newly-
metamorphosed individuals in Pelobates cultripes (Zamo-
ra-Camacho et al., 2019). Besides, such effect lead to a 
reduction in the jumping performance of post-metamor-
phic individuals (Zamora-Camacho and Aragón, 2019), 
which could expose them to higher risk of predation on 
land. So, these cases highlight a trade-off: tadpoles will 
either stay longer in the water, exposed for a longer time 
to aquatic predators but with newly metamorphosed with 
an ‘ideal’ size, with less exposure to terrestrial preda-
tors (Semlitsch, 1990; Wilbur and Semlitsch, 1990), or 
they could leave the water smaller and with some mobil-
ity handicaps, which could limit the exposure to aquatic 
predators but exposing them more to terrestrial predation 

Table 2. Coefficients of Generalized Linear Model analysis, which 
considers the percentage of tail injury as a predictor of (1) Scaled 
Mass Index (SMI) and (2) days until metamorphosis; tail injury per 
se as a predictor of (3) SMI and (4) days until metamorphosis; and 
(5) tail injury as a predictor of feeding frequency. All models pre-
sent degrees of freedom = 35 and significant values are in bold.

Estimate Std Error t value P

(1) SMI ~ % tail injury
Intercept 0.15 0.004 34.42 <0.001
30% -0.005 0.006 0.79 0.44
50% 0.005 0.006 -0.81 0.42
70% 0.001 0.006 0.25 0.81

(2) Days until metamorphosis ~ % tail injury
Intercept 29.78 2.99 9.95 <0.001
30% 5.22 4.13 1.27 0.21
50% 3 4.23 0.71 0.48
70% 12.22 4.36 2.8 0.008

(3) SMI ~ tail injury
Intercept 0.15 0.004 34.05 <0.001
tail loss 0.0003 0.005 0.05 0.96

(4) Days until metamorphosis ~ tail injury
Intercept 29.79 3.15 9.56 <0.001
tail loss 6.56 3.6 1.82 0.08

(5) Feeding frequency ~ tail injury
Intercept 4.01 0.18 22.56 <0.001
tail loss -0.41 0.28 -1.45 0.17

Table 3. Summary contrasts of Estimated Marginal Means, used 
as a pos hoc test to compare groups of different levels of tail injury 
with the control group. Significant value is in bold.

Estimate Std. Error P

SMI ~ % tail injury
30% - control -0.005 0.006 0.73
50% - control 0.005 0.006 0.75
70% - control 0.001 0.006 0.98

Days until metamorphosis ~ % tail injury
30% - control 5.2 4.13 0.44
50% - control 3 4.23 0.79
70% - control 12.22 4.36 0.01

SMI ~ tail injury
injuried - control 0.0003 0.005 0.96

Days until metamorphosis ~ tail injury
injuried - control 6.56 3.6 0.07

Feeding frequency ~ tail injury
injuried - control -0.41 0.28 0.15



18 Ana Glaucia da Silva Martins et alii

in the developmental stage that they are most suscep-
tible to predation (Toledo et al. 2007). In D. elegans we 
observed that the strategy adopted is the first one. Tad-
poles threatened by a predator spend more time under 
larval stage, i.e., reduce the growth rhythm, but reach 
the same size after metamorphosis, and consequently the 
same SMI, than unharmed individuals.

We also did not observe change in feeding frequency 
as a result of tail injury. It probably implies that the tail 
regeneration was not provided by an extra acquisition of 
energy – expected by a more frequent feeding. Although 
these stages (stages 28 until 36) are those when generally 
tadpoles present the most significant growth and energy 
uptake (Pfab et al., 2020), we did not observe any differ-
ence when the tail was lost. Considering that for some spe-
cies locomotion is more important than feeding, such as in 
Pleurodema thaul (Pueta et al., 2016) and Pelophylax lesso-
nae (Steiner, 2007), and that tail fins enable fast swimming 
(Smith and van Buskirk, 1995), perhaps for D. elegans the 
regeneration of tail is energetically more important than 
time until metamorphosis. Consequently, there is not an 
increase in feeding to regenerate the tail, but a realloca-
tion of the energy that otherwise would be used to growth. 
Thus, such observation supports the hypothesis of a prob-
able reallocation of the energy from the regular develop-
ment/metamorphosis process directed to tail regeneration. 
However, different results were reported for other species. 
For example, in Ascaphus truei, a simple clue of preda-
tors’ presence was enough to modify the foraging in tad-
poles, which reduced up to six-folds its foraging activity 
(Feminella and Hawkins, 1994). Also, similar results were 
observed for Rana sylvatica (Fraker, 2010) and Rana clami-
tans (Fraker, 2008, 2009). It efforts that more studies are 
necessary to elucidate this process of energy reallocation 
during larval stage until metamorphosis.

Our experiments showed consequences of predatory 
events in D. elegans tadpoles. Tail injury caused by preda-
tors can result in several consequences for the individu-
als, decreasing their survivorship, affecting tadpole mor-
phology (Nunes et al., 2010), and swimming speed (Figiel 
Jr and Semlitsch, 1991). Besides, as tadpoles of D. elegans 
remained more time in the larval stage when the tail was 
injured, this fact may have several consequences, since 
evolutionary approach until conservation of native popu-
lations.

ACKNOWLEDGEMENTS

We thank to all volunteers and IPBio – Instituto de 
Pesquisas da Biodiversidade by its help during the experi-
mentation. The study was conducted with the sampling 

permits of ICMBio (SISBio #24013 and #29484), SisGen 
(#ADEA910), and the animal ethics committee approval 
(CEUA #2405-1). This study was supported by Coordina-
tion for the Improvement of Higher Education Personnel 
(CAPES - Finance Code 001), São Paulo Research Foun-
dation (FAPESP #2016/25358-3; #2019/18335-5), and the 
National Council for Scientific and Technological Devel-
opment (CNPq #300896/2016-6; #302834/2020-6).

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	XI International Symposium on the Mediterranean Lacertid Lizards
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	Influence of tail injury on the development of Neotropical elegant treefrog tadpoles
	Ana Glaucia da Silva Martins1,#, Raoni Rebouças2,3,*,#, Isaias Santos1, Adão Henrique Rosa Domingos1, Luís Felipe Toledo2
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