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Strange parental decisions: Fathers of the dyeing poison frog deposit their tadpoles in pools occupied by large cannibals

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Parents may increase the probability of offspring survival by choosing suitable rearing sites where risks are as low as possible. Predation and competition are major selective pressures influencing the evolution of rearing site selection. Poison frogs look after their clutches and deposit the newly hatched tadpoles in bodies of water where they remain until metamorphosis. In some species, cannibalism occurs, so parents deposit their tadpoles singly in very small pools. However, cannibalism also occurs in species that deposit tadpoles in larger pools already occupied by heterospecific or conspecific larvae that could be either potential predators or competitors. Here, I test the hypothesis that, given the choice, males of Dendrobates tinctorius would deposit their newly hatched tadpoles in low-risk sites for their offspring. I characterised the pools used by D. tinctorius for tadpole deposition, conducted experiments to determine the larval traits that predict the occurrence of and latency to cannibalism, and tested whether parents deposit their tadpoles in low-risk pools. I found that (1) neither pool capacity nor the presence of other larvae predict the presence/absence or number of tadpoles; (2) cannibalism occurs often, and how quickly it occurs depends on the difference in size between the tadpoles involved; and (3) the likelihood of males depositing their tadpoles in occupied pools increases with the size of the resident tadpole. I suggest that predation/cannibalism is not the only factor that parents assess when choosing deposition sites, and that the presence of larger conspecifics may instead provide information about pool quality and stability.
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ORIGINAL PAPER
Strange parental decisions: fathers of the dyeing poison frog
deposit their tadpoles in pools occupied by large cannibals
Bibiana Rojas
Received: 25 April 2013 /Revised: 9 December 2013 /Accepted: 10 December 2013
#Springer-Verlag Berlin Heidelberg 2014
Abstract Parents may increase the probability of offspring
survival by choosing suitable rearing sites where risks are as
low as possible. Predation and competition are major selective
pressures influencing the evolution of rearing site selection.
Poison frogs look after their clutches and deposit the newly
hatched tadpoles in bodies of water where they remain until
metamorphosis. In some species, cannibalism occurs, so par-
ents deposit their tadpoles singly in very small pools. How-
ever, cannibalism also occurs in species that deposit tadpoles
in larger pools already occupied by heterospecific or conspe-
cific larvae that could be either potential predators or compet-
itors. Here, I test the hypothesis that, given the choice, males
of Dendrobates tinctorius would deposit their newly hatched
tadpoles in low-risk sites for their offspring. I characterised the
pools used by D. tinctorius for tadpole deposition, conducted
experiments to determine the larval traits that predict the
occurrence of and latency to cannibalism, and tested whether
parents deposit their tadpoles in low-risk pools. I found that
(1) neither pool capacity nor the presence of other larvae
predict the presence/absence or number of tadpoles; (2) can-
nibalism occurs often, and how quickly it occurs depends on
the difference in size between the tadpoles involved; and (3)
the likelihood of males depositing their tadpoles in occupied
pools increases with the size of the resident tadpole. I suggest
that predation/cannibalism is not the only factor that parents
assess when choosing deposition sites, and that the presence
of larger conspecifics may instead provide information about
pool quality and stability.
Keywords Parental care .Rearing sites .Phytotelmata .
Cannibalism .Competition .Poison frog
Introduction
Decisions made by parents about where to raise their offspring
may have great fitness consequences. Selection, therefore, is
expected to favour mechanisms that enable parents to assess
the quality of such sites and select those that seem to maximise
offspring growth and survival (Thompson and Pellmyr 1991).
Predation, competition, and habitat desiccation, the main risks
faced by the offspring of species that breed in temporary
aquatic environments, have been identified as major selective
pressures shaping the evolution of rearing-site selection by
parents (Resetarits and Wilbur 1989;Fincke1992a;Katsand
Sih 1992; Blaustein and Kotler 1993;Murphy2003; Blaustein
et al. 2004;Riegeretal.2004). Oviposition site selection may
involve similar consideration of risks as selection of tadpole
deposition sites. Patterns of selection of oviposition sites in
relation to predator avoidance have been shown for mosqui-
toes (Mokany and Shine 2002; Blaustein et al. 2004;
Silberbush and Blaustein 2011; Kershenbaum et al. 2012),
frogs (Resetarits and Wilbur 1989; Rieger et al. 2004), and
salamanders (Sadeh et al. 2009). Similarly, some frog species
avoid intraspecific competitors of their offspring (Resetarits
and Wilbur 1989; Crump 1991). Choices can be made too on
the basis of environmental cues that are relevant for offspring
development, such as temperature (Robertson 2009b), mois-
ture (Brown and Shine 2005), or water presence (Rudolf and
Rödel 2005), as it is necessary to prevent offspring death by
desiccation of the rearing site. Likewise, choices can be
Communicated by K. Warkentin
B. Rojas
Centre for Integrative Ecology, School of Life and Environmental
Sciences, Deakin University, 75 Pigdons Road, Waurn Ponds,
VIC 3216, Australia
B. Rojas (*)
Centre of Excellence in Biological Interactions, Department of
Biological and Environmental Science, University of Jyväskylä, PO
Box 35, 40014 Jyväskylä, Finland
e-mail: bibiana.rojas@jyu.fi
Behav Ecol Sociobiol
DOI 10.1007/s00265-013-1670-y
influenced by food availability (Blaustein and Kotler 1993;
Robertson 2009a) or previous successful experiences, for
example by choosing places where there was a high hatching
success in a previous reproductive event (Brown and Shine
2004).
Poison frogs (Grant et al. 2006) display a diversity of parental
care modes, including no care (for example those species with
endotrophic tadpoles), clutch attendance (one of the parents
either stays constantly near the eggs or checks them a few times
a day), tadpole transport, and, in some species, tadpole feeding
(Grant et al. 2006; Lötters et al. 2007). Tadpoles are transported
to bodies of water of varying size (Summers 1990;Brust1993;
Crump 1996; Poelman and Dicke 2007) where, in most cases,
they remain unattended until metamorphosis. Some species
deposit their tadpoles in large bodies of water, such as streams
or permanent ponds, places at which anuran larvae seem to be
under great predation risk by invertebrate larvae (Alford 1999);
some others deposit their tadpoles individually in bromeliad
axils and other small phytotelmata as a strategy to avoid larval
cannibalism (Summers 1999; Summers and McKeon 2004).
Individual deposition seems to be related to further parental care
such as trophic egg provisioning (Brust 1993; Poelman and
Dicke 2007; Brown et al. 2009), and the assessment of pool
suitability prior to tadpole deposition (Schulte et al. 2011).
The intermediate situation, in which males carry tadpoles
to large phytotelmata, such as tree holes, either previously or
subsequently occupied by conspecific or heterospecific (an-
uran or insect) larvae, has received less attention. Food variety
and availability in these pools are very low, and the predation
risk is posed mainly by other tadpoles and invertebrate larvae,
such as odonate naiads (Summers and McKeon 2004). Field
studies on Dendrobates auratus (Summers 1990),
Dendrobates castaneouticus (Caldwell and De Araújo
1998), and Dendrobates truncatus (BR, J. Gómez and A.
Amézquita, unpublished data) indicate that larval cannibalism
is common in large phytotelmata, and suggest that it could be
the result of indiscriminate predatory behaviour of tadpoles as
a way to eliminate potential predators and competitors (Cald-
well and De Araújo 1998; Summers and McKeon 2004).
These species, therefore, constitute a great study system to
assess the implications of parental decision-making.
The cost of choosing the wrong sites to deposit tadpoles
can be very high in terms of increased offspring mortality, and
in turn decreased fitness for the parent. Given that larvae are
unable to leave the sites where their parents deposit them
(Rudolf and Rödel 2005), selection should favour mecha-
nisms by which parents can assess the danger in their young's
rearing environment prior to depositing their tadpoles and
choose the sites that minimize risks, such as predation and
desiccation and maximise survival. Here, I test the hypothesis
that parents choose rearing sites without potential predators/
competitors that threaten offspring's survival. This was done
in a population of the poison frog Dendrobates tinctorius in
French Guiana by (1) characterising the sites where tadpoles
are deposited, (2) assessing whether cannibalism occurs and
determining the intrinsic traits of tadpoles that predict its
occurrence, and (3) testing whether, given the choice, parents
deposit their tadpoles in sites without large conspecifics.
Materials and methods
Study site and species
D. tinctorius is a diurnal, large (3753 mm at the study site
(Rojas and Endler 2013)) frog of the Neotropical family
Dendrobatidae. It occurs around canopy gaps in primary
forests in the Eastern Guiana Shield, at elevations from 0 to
600 m (Noonan and Gaucher 2006;Bornetal.2010). In the
field, pairs lay clutches of four to five eggs that hatch after
approximately 2 weeks (BR, personal observation). Tadpoles
are then carried by the male, one or two at a time (Fig. 1), to
tree holes either in standing trunks or fallen trees, or to palm
bracts (hereon referred to as pools) at variable heights (P.
Gaucher, personal communication; this study). Such pools
may contain nonpredaceous larvae of other frog species such
as Ameerega hahneli,Rhinella castaneotica,Allobates
femoralis,Trachycephalus resinifictrix and Trachycephalus
hadroceps (P. Gaucher, personal communication; this study).
Once at their rearing site, tadpoles remain unattended until
metamorphosis, which occurs after approximately 2 months
(BR, unpublished data). At present, not much about the be-
havioural ecology of the species is known, although there is
preliminary evidence (BR, unpublished data) that males may
move up to a few hundreds of metres from the area where they
live (as per mark-capture-recapture data) during tadpole trans-
port. More than one male can be seen depositing tadpoles in a
given pool (BR, personal observation), which indicates that
tadpoles found in the same pool could be unrelated or only
partially related (for example if they were offspring of differ-
ent males but the same female). Males carrying two tadpoles
Fig. 1 A male Dendrobates tinctorius transporting two tadpoles on his
back
Behav Ecol Sociobiol
can deposit one tadpole at a given pool and leave with the
second one still attached to their back until another suitable
deposition site is chosen, or deposit both tadpoles in the same
pool, at the same time (BR, personal observation).
This study was done at Camp Pararé, Les Nouragues
Reserve, French Guiana (3°59N, 52°35W) in a low-land
forest where there is a large population of D. tinctorius
(Courtois et al. 2013). The average annual temperature and
precipitation at the study site are 26 °C and 2,990 mm, re-
spectively (Grimaldi and Riéra 2001).
Characterisation of tadpole deposition sites
In order to identify the kind of pools that D. tinctorius uses for
tadpole deposition, I did an extensive search for available
water-filled pools on both fallen logs and standing trees along
a 1.5 km transect. Every pool found was measured in its
length, width, depth, and height above the ground. A stable
indicator of pool water-holding capacity was calculated using
the formula for the volume of an ellipse (4/3 π×length/
width/2× depth) divided by two; actual water volume of a
given pool varied visibly with changes in precipitation and
temperature (BR, personal observation). For every pool, I
recorded the presence or absence, and number of D. tinctorius
tadpoles. The occurrence of eggs or larvae of other frog
species, as well as the presence/absence of odonate naiads
were also recorded as binary variables in both cases. In order
to estimate the characteristics of preferred sites for tadpole
deposition, I compared the characteristics of available pools
with no tadpoles of D. tinctoriusto those of pools occupied by
the species by means of a logistic regression. The measured
characteristics were used as predictor variables and the pres-
ence (1) and absence (0) of D. tinctorius tadpoles was entered
as a binary variable. The characteristics of the subset of pools
where D. tinctorius tadpoles were found were tested as pre-
dictors of the number of tadpoles found at a given time by
means of a regression analysis. A pool was considered unused
only if tadpoles were never seen there during the regular
surveys done throughout the nearly 5 months of the duration
of the study. I tested for the effect of the presence of larvae of
odonates and of other frog species on the presence of
D. tinctorius larvae by means of Chi-square analyses. The
characterisation of deposition sites was done throughout the
whole field season in 2011.
Experiment 1. Determinants of tadpole cannibalism
Twenty pairs of tadpoles were formed in order to test for
the occurrence of cannibalism. Pairs were formed ran-
domly from tadpoles coming from different natural pools
placed simultaneously in an opaque plastic container with
approximately 200 ml of rainwater and crushed leaf litter.
Both tadpoles of each pair were photographed prior to
beginning the experiment in order to measure their body
length(fromthetipofthesnouttothebaseofthetail)
with the software ImageJ. The containers were left in the
field, covered in order to avoid additional tadpole depo-
sitions, and checked twice a day until cannibalism oc-
curred in order to record the latency to cannibalism.I
tested for the effect of the absolute difference in size
between the tadpoles in each pair (length of the largest
length of the smallest) on the probability of cannibalism
within the first 24 h, and on the latency to cannibalism, by
means of logistic regression and logarithmic regression,
respectively.
Experiment 2. Tadpole deposition site choice
Because cannibalism seems to occur often (this study), it
would be expected that fathers choose to deposit their
tadpoles in pools without larger conspecifics if given the
choice. To test this, I ran a second experiment by setting
up 35 pairs of opaque plastic containers scattered in the
forest in places were D. tinctorius adults had been seen.
Five tadpoles were held individually in the containers for a
week prior to the beginning of the experiments in order to
detect negative effects of the plastic on the survival of
larvae, if any, but no effects were noted. All tadpoles
survived, behaved normally and looked healthy, and were
not included in the subsequent experiment. Each experi-
mental pair consisted of two containers with approximate-
ly 200 ml of rainwater and crushed leaf litter in the
bottom. One of the containers had a tadpole of
D. tinctorius (resident) whereas the other one was unoc-
cupied. Resident tadpoles were collected from pools lo-
cated at least 400 m away from the experimental setup
where they were used. Paired containers were 1530 cm
apart. Each pair of containers was checked twice a day for
the presence of newly deposited tadpoles. The father's
choice was recorded as a binary variable: 1 for tadpoles
deposited in the occupied container and 0 for depositions
in the unoccupied container. When a newly deposited
tadpole was found in either container (newcomer), both
the resident tadpole and the newcomer were photographed
in order to measure their body length and calculate the
difference in size between them. Additionally, residence
time (the number of days since each pair of containers was
set up until a tadpole was deposited in either container)
was recorded. The difference in size between the two
tadpoles (length of the residentlength of the newcomer)
was tested as a predictor variable of the father's choice
with a logistic regression (Rudolf and Rödel 2005), with
residence time as a covariate, using a stepwise procedure
(backward: LR (Menard 2001)). These and all statistic
analyses were done with the software SPSS 20.0 for
Behav Ecol Sociobiol
Mac. Both experiments were carried out between March
22 and May 31, 2011.
Results
Characterisation of tadpole deposition sites
Among the 30 pools found and surveyed regularly during the
study, neither pool capacity nor height were good predictors of
the presence of D. tinctorius larvae, which were found in only
16 of them (logistic regression; heightWa ld Χ
2
=0.565, P=
0.452; capacityWa ld Χ
2
=0.814, P=0.367; N=30). In vari-
ous cases, more than one pool that seemed suitable for
D. tinctorius tadpole deposition was found on the same
treefall, but not all pools were used. On a few occasions, I
observed males without tadpoles visiting used pools, and
coming back a few days later with tadpoles attached to their
back; other times, I saw also tadpole-carrying males visiting
used pools, and leaving with the tadpoles still attached to their
back. Interestingly, on at least three occasions, tadpole-
carrying males arrived to never-used pools, stayed there for
longer than 15 min, and left without depositing any tadpoles.
Odonate larvae were found in 10 (33 %) of the pools and
tadpoles of other frog species (namely R. castaneotica,
A. femoralis and A. hahneli) were found at some point in 29
(97 %) of the pools. Neither the presence of naiads (Χ
2
=0.068,
df=1, P=0.794, N=30,) nor the presence of eggs or larvae of
other frog species (Χ
2
=0.851, df=1, P=0.356, N=30) were
related to the presence of D. tinctorius tadpoles in the pools
examined. D. tinctorius deposit their tadpoles in pools of small
to medium capacity (median=254.78 ml; min =11.8 ml;
max= 1684.7 ml; Fig. 2) at observed heights between 0 and
65 cm (mean±SD= 29.44± 17.90 cm; median =30.50 cm), al-
though there are anecdotal reports of tadpoles of this species in
tree holes over 20 m above the ground (P. Gaucher, personal
communication). I found between 1 and 10 tadpoles (mean±
SD= 3.29± 2.33; median=3.00) of D. tinctorius at once in 16
pools, 14 water-filled cavities found in fallen trees (tree holes)
and two fallen palm bracts. Pool capacity was not found to be
a good predictor of the maximum number of tadpoles found in
each pool at once (linear regression (on Log
10
-transformed
variables): R
2
=0.126, F
1,15
=2.025, P=0.177). Tadpoles of
D. tinctorius were often deposited in pools already occupied
by both conspecifics and heterospecifics. The larvae of other
anuran or insect species ended up, in most cases, being eaten
by the predaceous larvae of D. tinctorius. Likewise, tadpoles
of D. tinctorius could precede tadpole deposition or egg laying
by other species of frogs or odonates. Those tadpoles and eggs
(or embryos) also ended up, invariably, being eaten by
D. tinctorius larvae. Interestingly, some of the pools that were
never found to have tadpoles of D. tinctorius had a high
number of tadpoles of A. femoralis or A. hahneli, sometimes
more than 20.
Experiment 1. Determinants of tadpole cannibalism
Cannibalism occurred in 100 % of the experiments within
2 weeks, with the larger tadpole always eating the smaller
one. Difference in length between the two tadpoles had a
significant effect on the latency to cannibalism (logarithmic
regression: R
2
=0.23, F
1,20
=5.35, P=0.033; Fig. 3). Pairs of
tadpoles with similar sizes showed the greatest variation in
latency to cannibalism (Fig. 3). In 50 % of the cases, canni-
balism occurred within the first 24 h. Cannibalism was ob-
served in natural circumstances (i.e., in the natural pools
chosen by the species for tadpole deposition) on 12 occasions
in 5 out of 16 used pools.
Experiment 2. Tadpole deposition site choice
Twenty-four out of 35 pairs of experimental containers
(68.6 %) were used by adults to deposit their tadpoles. The
size of the resident tadpoles at the time when the choice was
made varied from 5.41 to 10.90 mm (mean±SD=7.46±1.25),
whereas the newcomers' size ranged from 4.60 to 6.06 mm
(mean±SD =5.29± 0.42; the resident was always larger).
None of the tadpoles used as residents showed hind limbs or
other signs of being near metamorphosis, which is reached at
11.0615.26 mm (mean±SD=13.330±1.09) in this species
(BR, unpublished data). Thus, resident tadpoles represented a
real threat of cannibalism for newcomers.
Fig. 2 Distribution of capacity among the pools where tadpoles of
Dendrobates tinctorius were found
Behav Ecol Sociobiol
Tadpole deposition seemed to occur at similar rates in
occupied and unoccupied containers (11 unoccupied
(45.9 %), 13 occupied (54.1 %); binomial test statistic =
13.00, P=0.838, N= 24). However, the difference in size be-
tween resident and newcomer was found to be a good predictor
of parental choice: the larger the size difference between the
two, the more likely it was for fathers to deposit their tadpoles
in the occupied container (logistic regression; residence time:
B=0.085, Wald Χ
2
=1.813, P=0.178; difference in size: B=
1.709, Wald Χ
2
=5.515, P=0.019; N=21; Fig. 4). Residence
time had no influence on the parental decision. Three pairs of
tadpoles could not be photographed because of extreme rain, so
are not included in the logistic regression; in two cases, the
father chose the unoccupied container, and in the third case, he
chose the occupied one. The difference in size between one pair
of tadpoles was an outlier; removing that data point did not
change the conclusion.
Discussion
Males of D. tinctorius make what seem to be strange decisions
regarding where to deposit their tadpoles. In a choice exper-
iment between an unoccupied pool and a pool already occu-
pied by a conspecific, fathers preferred to deposit their newly
hatched tadpole with a large conspecific, but in an unoccupied
pool if the conspecific in the alternative site was similar in size
to its own tadpole. These results are interestingly counterintu-
itive given how often larval cannibalism takes place in natural
pools. Cannibalism may be favoured in situations where re-
sources are scarce and competition is high, as seems to be the
case in phytotelmata (Lehtinen et al. 2004). During the course
of this study, cannibalism occurred in all of the experimental
setups (experiment 1) and was seen on numerous occasions in
natural pools, which is an indication of its prevalence in
natural conditions. In all cases, cannibalism involved a large
tadpole eating a smaller one. Surveys of the natural pools used
by D. tinctorius males for tadpole deposition (i.e., tree holes
and palm bracts) revealed that the probability of finding
tadpoles of D. tinctorius in a given pool does not depend on
its capacity or height, or on the presence of potential
heterospecific predators (odonate naiads) or prey (small na-
iads or larvae of other frog species). The number of tadpoles in
a pool is also not related to its overall capacity.
Parents can lessen the risk of mortality to their larvae by
avoiding competitors and potential predators. Some species of
dendrobatids seem to inspect pools prior to depositing tad-
poles, and use visual and/or chemical, and possibly
mechanosensory, cues to avoid depositing in pools that are
already occupied by conspecifics (Summers 1990;Caldwell
and de Oliveira 1999; Poelman and Dicke 2007; Brown et al.
2008b; Schulte et al. 2011). This does not seem to be the case
for D. tinctorius: the present study provides experimental
evidence that, regardless of the high risk of cannibalism,
fathers do not avoid depositing newly hatched tadpoles in
pools already occupied by conspecific larvae. If only the
occupancy of the pool is taken into account, there is a slight
tendency towards preferring occupied pools. Some deposition
events may have been missed due to cannibalism by the
resident tadpole, which was free in the container rather than
isolated as in other studies (Schulte et al. 2011; Schulte and
Lötters 2013). However, this would produce a bias favouring
the detection of deposition events in unoccupied containers,
Fig. 3 Relationship between difference in size (body length; from the tip
of the snout to the base of the tail) between two tadpoles and the latency to
cannibalism. Line shows predicted values from a logarithmic regression
Fig. 4 Effect of the difference in size between a resident tadpole and a
newcomer, on the probability that the fatherdeposits his tadpole in a pool
already occupied by a conspecific. Circles denote observed data; the line
shows predicted probabilities from a binomial logistic regression
Behav Ecol Sociobiol
counter to the trend. Selection would be expected to favour
parental choices that maximise offspring survival. Therefore,
given that cannibalism is common and heavily dependent on
size differences between the tadpoles involved, male
D. tinctorius should avoid depositing newly hatched tadpoles
in pools already occupied by conspecifics, especially if they
are large. This study shows the opposite and is, to my knowl-
edge, the first to consider not only the presence but also the
size of conspecifics, as a factor influencing parental decision-
making in the context of offspring rearing site selection.
There are at least four possible explanations for this
strange parental choice, whereby males deposit their tad-
poles in pools occupied by large cannibals. First, despite
the high risk of cannibalism, males might choose to de-
posit a newly hatched tadpole in an occupied pool because
the presence of a larger conspecific tadpole indicates that
other important requirements for larval development are
met in that pool. Considering the ephemeral nature of
most phytotelmata the presence of a large conspecific
might, for example, give fathers an indication of habitat
permanence (i.e., water-holding ability of a pool (Edgerly
et al. 1998)). Cues of habitat permanence have been
shown to influence oviposition site choice by some insects
(Edgerly et al. 1998;MokanyandShine2003)andother
frog species, which are capable of timing oviposition in a
given site according to its water-holding capacity and
water presence in the future (Rudolf and Rödel 2005).
Habitat desiccation is a major cause of mortality among
species that develop in ephemeral habitats (Aspbury and
Juliano 1998; Altermatt et al. 2009). A recent study, in
which chemical cues were used to simulate the presence of
conspecific tadpoles, showed that males of Ranitomeya
variabilis deposit their tadpoles in occupied pools during
the dry season, when the risk of pool desiccation is very
high (Schulte and Lötters 2013). Poelman and Dicke
(2007)alsoreportedovipositioninoccupiedpoolsby
Ranitomeya ventrimaculata towards the dry season,
whereas Rudolf and Rödel (2005) demonstrated that in
the tree hole-breeding frog Phrynobatrachus guineensis
the presence of conspecifics in a tree hole could be used
by parents as a cue of habitat permanence. Females of
Oophaga pumilio, which deposit their tadpoles in
phytotelmata of very small capacity, consistently chose
among the available deposition sites those with the greatest
water volume. This choice would give their offspring a
better chance to reach metamorphosis before the pools dry
(Maple 2002), and highlights how different strategies could
be employed by parents to prevent offspring death by
dehydration. During the course of this study, water volume
varied greatly over time, with both used and unused pools
being totally full 1 day and less than a half full a few days
later. In fact, at least seven pools were completely dry after
a couple of days with temperatures over 30 °C and virtually
no rain (BR, personal observation). A few tadpoles, usually
the largest ones, managed to survive in these conditions by
remainingburiedinthemudatthebottomofthepool,but
many of them died (BR, personal observation).
Second, tadpole deposition in pools occupied already by
conspecifics, despite the occurrence of cannibalism, can be a
consequence of suitable sites being a limited resource. Par-
ents, therefore, may have no alternative. Previous studies
where the density of adult Oophaga pumilio increased con-
siderably after the addition of tadpole deposition sites
(bromeliads), suggest that these are indeed a limited resource
(Donnelly 1989). Additionally, although mothers of
Oophaga pumilio prevent larval cannibalism by depositing
their tadpoles individually, multiple depositions in a single
axil can occur when the availability of sites for tadpole depo-
sition is limited (Brust 1990). D. tinctorius males readily
utilise newly available natural and artificial deposition sites
(BR, unpublished data), which could indicate that for this
species the resource is limited, as is the case for A. femoralis
(Ringler et al. 2013), R. ventrimaculata (Poelman and Dicke
2007) and some species of odonates (Fincke 1992b). Howev-
er, of the 30 pools that were measured and checked for
tadpoles throughout the study, only 16 ever had D. tinctorius
larvae and neither the pool capacity nor the presence of larvae
of odonates or other frogs was a good predictor of D. tinctorius
presence. It thus seems that pool traits not considered in this
study might influence fathers' choices, and that not every
water-holding hole may be suitable for tadpole deposition.
Abiotic factors such as temperature and chemical properties
of the water (pH, conductivity, etc.) should be included in
further attempts to elucidate those pool traits that determine
their use by parents as tadpole-rearing sites. However, the
abundance of unused pools does not support the idea that
the strange parental choiceof D. tinctorius is due to limita-
tion in rearing-site availability.
Third, tadpole deposition in occupied pools might be a
feeding strategy that speeds growth rates of residents. Carniv-
orous diets are known to increase growth rate (Wildy et al.
1998; Summers 1999; Alvarez and Nicieza 2002), which
could in turn shorten the time until metamorphosis allowing
individuals to leave desiccation-prone pools sooner (Alford
1999). Furthermore, increasing growth rates could also im-
prove fitness because rapid growth allows tadpoles to more
quickly reach a size at which they are safer from particular
predators, and to attain a larger size at metamorphosis, which
might enhance terrestrial survival and fecundity (Alford 1999;
Harris 1999). This could make sense if, for example, the new
tadpole were related to the resident, because the probability of
survival of the latter would be increased with the consumption
of the newcomer. Such is the case of species, such as
R. ventrimaculata, which lay egg clutches in phytotelmata
already occupied by a related conspecific tadpole, presumably
as a feeding strategy; this occurs especially during the dry
Behav Ecol Sociobiol
season, when speeding up growth might reduce the risk of
death by desiccation (Poelman and Dicke 2007). However,
this scenario is unlikely in D. tinctorius. Several times more
than one male was seen depositing tadpoles in the same pool,
and residenttadpoles for the choice experiment were col-
lected more than 400 m away from where they were used,
making it highly unlikely that they were related to the males
making the choice. To my knowledge, there is no evidence of
parents deliberately feeding young tadpoles to older ones.
Cases of what has been called reproductive parasitismare
known, in which tadpoles are deposited in places where there
are conspecific eggs or embryos (Brown et al. 2008b), so that
the newly deposited tadpole has a size advantage over the
residents.InanEcuadorianpopulationofR. ventrimaculata,
for example, embryos may slip down the axil where they were
laid as eggs. Males (either related or unrelated to the embryos)
can use those same axils to deposit new tadpoles, which have
a size advantage over the embryos and will feed on them
(Summers and Amos 1997). Because the new tadpoles are
not necessarily related to those already occupying the axil, this
behaviour does not entail a feeding strategy either. These cases
do not resemble what happens in D. tinctorius, in which
resident tadpoles are larger than the newly deposited ones.
Therefore, the feeding strategyhypothesis is the least plau-
sible explanation for the choice made by male D. tinctorius of
depositing newly hatched tadpoles in pools with large canni-
bals. Nonetheless, it should not be entirely discarded until
more is known about the abilities of fathers to identify a
tadpole in a pool within their spatial range as their own.
Fourth, these strange decisionscould be a mistake made
by fathers, which might be unable to detect the presence of a
conspecific tadpole during their visit to potential deposition
sites, or the product of a random choice. This, however, is
highly unlikely given the growing body of evidence regarding
site assessment prior to tadpole deposition (Brust 1993;
Summers 1999; Brown et al. 2008a,b; Stynoski 2009;
Schulte et al. 2011). Furthermore, recent findings indicate that
even poison frogs with a low level of parental care are capable
of deciding strategically, rather than randomly, where to de-
posit their tadpoles (Ringler et al. 2013).
Besides cannibalistic conspecifics, tadpoles also face
heterospecific predators and both conspecific and heterospecific
competitors (Alford and Wilbur 1985;Twomeyetal.2008).
Males of D. tinctorius do not seem to avoid either predators or
competitors for their offspring when choosing sites for tadpole
deposition, as they can be deposited either before or after other
species bring tadpoles to or lay eggs in the same pool. Rather,
D. tinctorius tadpoles seem to be a good example of intraguild
predators (Polis et al. 1989;vonMayetal.2009) partially
governed by priority effects (Fincke 1999). Early arrivals may
have access to more abundant resources and not only become
better competitors but also become predators rather than prey.
Thus, the order of arrival may affect not only the outcome but
also the nature of interspecific interactions (Blaustein and
Margalit 1996), determining who will be a better competitor
(Alford and Wilbur 1985;LawlerandMorin1993; Knight et al.
2009; Hernandez and Chalcraft 2012) and whether the interac-
tion will be competition or predation (Fincke 1999; Eitam et al.
2005).
Odonate naiads are major predators of anuran tadpoles
(Alford 1999). Naiads were found simultaneously with tad-
poles of D. tinctorius in 33 % of the pools examined in this
study, but naiads large enough to kill a co-occurring large
D. tinctorius tadpole were found only in one pool (two naiads
at once). In a subsequent visit, that tadpole had disappeared
but the naiads were still alive, which strongly suggests that
one of them ate the tadpole. On several occasions, adult
odonates were seen ovipositing in pools containing
D. tinctorius tadpoles and the tadpoles subsequently seen
preying on the hatching odonate larvae. Thus, if the odonate
naiads arrive early enough they can prey on D. tinctorius
tadpoles and vice versa.
The presence of larvae of other frog species (potential
heterospecific competitors) did not seem to prevent
D. tinctorius tadpole deposition, and either eggs or tadpoles
of other species were found at some point in 97 % of the pools
surveyed during this study. On the contrary, if heterospecifics
do not represent strong competitors, pools with heterospecific
eggs or tadpoles could be even preferred by fathers. In most
cases, given favourable differences in size, both eggs and
tadpoles of other frogs are quickly consumed by the voracious
tadpoles of D. tinctorius, providing very nutritious meals. For
example, tadpoles of D. tinctorius have been seen in tree holes
where the hylid frogs T. res inifi ct rix and T. hadroceps breed (P.
Gaucher, personal communication). Eggs, embryos and larvae
of these two species are readily consumed by D. tinctorius
larvae (P. Gaucher, personal communication), which in turn
experience considerably higher growth rates than when fed
only with detritus (BR, P. Gaucher and T. Legagne, unpub-
lished data). Similarly, tadpoles of A. femoralis deposited in a
pool already occupied by D. tinctorius do not survive for long
(BR, personal observation). This is also the case of the closely
related D. auratus, which preys on tadpoles of Oophaga
granulifera whenever the two co-occur (Ryan and Barry
2011).
Future work combining behavioural ecology and molecu-
lar techniques may elucidate the reasons why frogs in the
D. tinctorius group (Grant et al. 2006) did not evolve the
strategy of single tadpole deposition despite their high levels
of cannibalism. So far, however, it seems that D. tinctorius
larvae have the ability to successfully outcompete both con-
specifics (provided a minimum difference in size) and
heterospecifics co-occurring in their pools via predation. Fur-
ther research is needed in order to assess the effect of large
noncarnivorous larvae on the growth of newly deposited
tadpoles of D. tinctorius.
Behav Ecol Sociobiol
Choosing good places for tadpole deposition has direct
effects on fitness because the conditions experienced by larvae
affect their survival as well as other important life history traits
such as time to and size at metamorphosis (BR, J. Gómez and
A. Amézquita, unpublished data), and size at maturity
(Mokany and Shine 2003). Apparently, strange parental deci-
sions, such as depositing offspring with large cannibals, may
ultimately not be that strange if they entail the consideration of
factors that influence the survival of offspring not only imme-
diately (i.e., predation) but also over the longer term (e.g.,
competition, habitat desiccation, and food availability). The
results presented here raise questions regarding those benefits
that would compensate for the loss of offspring to cannibal-
ism, and those abiotic traits that ultimately make a pool
suitable for tadpole deposition. The answers to these questions
would represent an important step forward in our current
understanding of parental decision making. Finally, this study
emphasises the importance of rearing site selection and prior-
ity effects in shaping the dynamics of temporary pool
communities.
Acknowledgments This study was funded by the CIE at Deakin Uni-
versity (Australia). J. Devillechabrolle provided invaluable field assis-
tance, the staff at Nouragues station helped with logistics and P. Gaucher
shared his knowledge on the species. I am grateful to John Endler, Karen
Warkentin, Jason Brown and anonymous reviewers for helpful comments
that improved the manuscript. Many thanks to Andrés López-Sepulcre
and Janne Valkonen for statistical advice, and to the Darwingroup at
the University of Jyväskylä for a fruitful discussion on this work.
Ethical standards This study was done in compliance with local
regulations. Research permits were issued by the CNRS-Guyane.
Conflict of interest There is no conflict of interest with the institution
that funded this study.
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... Empirically, many studies have found that winners of cannibalistic interactions are larger than losers (Claessen et al. 2004;Ibáñez and Keyl 2010;Barkae et al. 2014;Rojas 2014), although exceptions exist when larger individuals are weakened (Richardson et al. 2010) or when individuals compensate for their size with increased aggressiveness (Issa et al. 1999). Kinship between individuals can also explain aggression. ...
... Dendrobates tinctorius is a Neotropical poison frog with parental care whose larvae are facultative cannibals (Rojas 2014). Tadpoles are often deposited by their fathers in ephemeral pools of water, where they are confined until metamorphosis (Rojas and Pašukonis 2019). ...
... While tadpoles are most often transported singly, the ephemeral pools in which they are deposited can have multiple tadpoles of various developmental stages (Rojas and Pašukonis 2019) and degrees of relatedness (Rojas B, and Ringler E, unpublished data). In these environments, cannibalism is common (Rojas 2014(Rojas , 2015, but not necessary for the successful development and metamorphosis of an individual tadpole. In closely related poison frogs, cannibalism is usually an outcome of sequentially intensified attacks (Summers and Symula 2001;Gray et al. 2009), although exceptions where tadpole aggression does not include cannibalism exist (i.e., obligate egg-feeders with parental care, Dugas et al. 2016a). ...
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In juveniles extreme intraspecies aggression can seem counter-intuitive, as it might endanger their developmental goal of surviving until reproductive stage. Ultimately, aggression can be vital for survival, although the factors (e.g., genetic or environmental) leading to the expression and intensity of this behavior vary across taxa. Attacking (and sometimes killing) related individuals may reduce inclusive fitness; as a solution to this problem, some species exhibit kin discrimination and preferentially attack unrelated individuals. Here, we used both experimental and modeling approaches to consider how physical traits (e.g., size in relation to opponent) and genetic relatedness mediate aggression in dyads of cannibalistic Dendrobates tinctorius tadpoles. We paired full-sibling, half-sibling, and non-sibling tadpoles of different sizes together in an arena and recorded their aggression and activity. We found that the interaction between relative size and relatedness predicts aggressive behavior: large individuals in non-sibling dyads are significantly more aggressive than large individuals in sibling dyads. Unexpectedly, although siblings tended to attack less overall, in size-mismatched pairs they attacked faster than in non-sibling treatments. Using a theoretical model to complement these empirical findings, we propose that larval aggression reflects a balance between relatedness and size where individuals trade-off their own fitness with that of their relatives. Lay Summary Before you eat someone, you have to attack them first. Here, we investigated the factors that shape aggression in the cannibalistic tadpoles of the dyeing poison frog. We find that aggression depends on both size and relatedness: when set in pairs, large tadpoles are half as aggressive towards their smaller siblings than to nonsibs. It looks like belonging to the same family provides some protection against aggression, though no one is ever truly safe.
... However, some species deposit tadpoles in sites occupied by conspecifics (Poelman & Dicke, 2007;Rojas, 2015). This can depend on the size of the tadpole already deposited (Rojas, 2014), the presence of heterospecific tadpoles (Schulte & Lötters, 2014), or the influence of climatic seasonality (Schulte & Lötters, 2013). As tadpole survivorship may be affected during this decision-making, parents may face a trade-off between current and future offspring, and between site features and quantity (Alonso-Alvarez & Velando, 2012;Ringler et al., 2018). ...
... Consequently, the usage of large pools with high nutrient availability may substantially reduce the risk of cannibalism or competition between conspecific tadpoles (Brown et al., 2008b;McKeon & Summers, 2013;Poelman et al., 2013). In some species, the presence of large tadpoles might provide information about the quality of the site and availability of nutrients (Rojas, 2014). Alternatively, A. claudiae males exhibit extensive searching during tadpole transportation. ...
... Alternatively, A. claudiae males exhibit extensive searching during tadpole transportation. Therefore, the limited number of unoccupied phytotelmata may be used by conspecific tadpoles, forcing A. claudiae males to use pools containing other tadpoles (Poelman & Dicke, 2007;Rojas, 2014). ...
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The selection of habitats with potential reproductive resources may maximize individual reproductive success and overall fitness. Dendrobatid frogs display remarkable parental care which is associated with water bodies (phytotelmata) contained in plants with characteristics that are important to offspring survival. It has been shown that the size of phytotelmata is a key factor that drove the divergence in parental care patterns in poison frogs and that the distribution of reproductive resources can influence space use in these species. Here, we investigated parental care strategies and the influence of reproductive resource distribution on space use patterns in a wild population of Andinobates claudiae in Bocas del Toro, Panama. We identified the phytotelmata characteristics that predict tadpole deposition and analysed the association between the spatial distribution of phytotelmata and spatial use of males and females. Our observations showed that this species mates polygamously and exhibits male parental care. We found that male frogs have smaller kernel density home ranges and core areas compared to females, and that space use is related to the density of Heliconia plants whose axil cavities are used for tadpole rearing. Furthermore, we found that tadpoles were more frequently found in phytotelmata that were at lower heights and contained larger water volumes. Fathers invested time inspecting multiple cavities and travelled further than predicted from their territories to find suitable deposition sites. Our observations suggest a selective choice of phytotelmata regarding tadpole deposition, where distribution and quality of cavities might influence parental care decisions.
... However, their small size provides protection from large predators and overall reduced interspecific competition (Kitching, 2001;Summers & Tumulty, 2014). Various species have evolved different strategies for their offspring to succeed in these pools (substrate specialization: von May et al., 2009;Pettitt et al., 2018; trophic egg feeding: Brown et al., 2010;Weygoldt, 1980; larval aggression/cannibalism: Gray et al., 2009;Poelman & Dicke, 2007;Rojas, 2014; pool choice based on specific physical or chemical cues: Lin et al., 2008;Schulte et al., 2011). Despite the widespread use of phytotelmata (Lehtinen, 2021), and the nonrandom site selection shown by many frog parents, few studies go beyond quantifying basic pool dimensions and pool occupation to understand tadpole deposition decisions. ...
... Osteocephalus oophagus (Hylidae)) that were most frequently detected in phytotelmata throughout field surveys at our study site in French Guiana. Following broad species-wide comparisons, we focus on a more detailed analysis of pool choice in D. tinctorius, a phytotelm specialist with predatory and cannibalistic tadpoles which are deposited in a range of phytotelm types (e.g., palm bracts, tree holes, fallen trees; Figures 1 and 2) that occur from the forest floor to more than 20 m in vertical height (Gaucher, 2002;Rojas, 2014Rojas, , 2015. The use of the high canopy pools is perplexing because D. ...
... tinctorius is commonly successful in terrestrial pools (Rojas, 2014). ...
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... The alteration of forest habitats for different human land-uses, as well as changes in climate 342 patterns can also affect poison frogs during larval and adult stages by modifying the 343 availability and quality of important resources and microhabitats. For example, by clearing 344 primary forest and reducing the canopy cover, the ground becomes more exposed to solar 345 radiation, which increases near-ground temperature and, in turn, phytotelmata desiccation presence as a cue for pool quality and persistence, as is the case in Dendrobates tinctorius 385 (Rojas 2014). This last idea is further supported by a study on Edalorhina perezi 386 (Leptodactylidae), which also loses their sensitivity to invertebrate predators late in the rainy 387 season (Murphy 2003b). ...
... We hypothesized that tadpoles may benefit from exhibiting limited movement when exposed to a predator but may show differential avoidance behavior depending on the predators foraging mode (i.e. ambush/sit-and-wait strategy seen in some odonate larvae or active foraging seen in some other odonate larvae and D. tinctorius tadpoles; Johansson, 1991;Fouilloux et al., 2020;Pritchard, 1965;Rojas, 2014). We also hypothesize that the use of multiple cues may improve predator recognition and avoidance. ...
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... Infanticide often occurs to destroy the young of a competitor, such as in male lions (Packer and Pusey, 1983) or poison frogs (Ringler et al., 2017). When environmental resources are scarce, parents may also choose to invest in specific offspring to the harm of others, like when poison frogs feed their younger tadpoles to older ones (Rojas, 2014). Neurogenetics experiments have shed light on the reciprocal interactions of care and infanticidal circuits, where circuit nodes highly active during parental care are often silent in infanticidal animals and vice versa, suggesting that the behavior circuits may be intertwined in order to tightly control the expression of behavior (Wu et al., 2014;Odaka et al., 2015). ...
... This inference implies that most species using phytotelmata as rearing sites should exhibit tadpole cannibalism, which appears not to be the case. Larval cannibalism has been studied in only a few species 37,95,[105][106][107][108][109] and, in some instances, it appears to be facultative or opportunistic. The fact that few instances of cannibalistic behavior have been documented might be the result of limited observations, and we thus propose that this behavior might be more widespread than currently thought. ...
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... Tadpoles of many species often show cannibalistic behaviors (usually larger tadpoles cannibalize smaller ones and/or eggs), which also affect female oviposition strategies (Crump, 1992;Sadeh et al., 2009;. Frogs often avoid laying eggs where conspecific cues exist (Dillon and Fiaño, 2000;von May et al., 2009;Schulte et al., 2011), but this behavior does not appear to be universal (Rudolf and Rödel, 2005;Rojas, 2014). There is also another strategy, shown by the wood frog, Rana sylvatica, which synchronizes the timing of egg-laying with that of conspecifics so that tadpoles vary only slightly in size, consequently reducing the risk of cannibalism (Petranka and Thomas, 1995). ...
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Introductions of Hyla (=Pseudacris) crucifer and Bufo woodhousii tadpoles at different times produced small differences in growth rates and larval periods when each anuran species occurred alone. In ponds containing both species, differences in the order and temporal separation of introductions had complex effects on the intensity of interspecific competition. When Bufo preceded Hyla, Hyla had prolonged larval periods and reduced mass and growth. When Hyla preceded Bufo, it was unaffected by Bufo. Hyla had no effects on Bufo, whether its introduction preceded or followed the introduction of Bufo. Early arrival increased the competitive impact of Bufo on Hyla, but failed to generate a competitive effect of Hyla on Bufo. Bufo tadpoles are more active than Hyla, and so may consume resources at higher rates that cannot be offset by a temporal advantage. Competition from Bufo was strongest when Hyla arrived 7 d later, suggesting that Hyla arriving 14 d after Bufo benefited from a longer period of reduced competition after Bufo metamorphosed from the ponds. The natural pattern, where Hyla breeds before or simultaneously with Bufo, permits Hyla to minimize competition from Bufo, while Bufo suffers no measurable cost from the size advantage obtained by competitively weaker Hyla tadpoles, Bufo may be prevented from breeding any earlier in the season by physiological constraints acting on eggs or breeding adults. -from Authors