Lateralized Turning Biases in Two Neotropical Tadpoles

Abstract

Lateralized turning behavior in startle responses and upon descent after surfacing for a breath of air has been documented for tadpoles in several anuran species. A left-handed preference is most common and was previously thought to be linked to the asymmetry in spiracle location. Here, we investigate the presence of behavioral asymmetries in tadpoles of Agalychnis callidryas and Leptodactylus melanonotus in explosive turns after air-breathing. Data were also collected on lateralized posture in the orientation of tails of embryonic A. callidryas within the egg case, as well as the startle response of free-swimming tadpoles exposed to mechanical stimulation. A left-curled tail bias was found among several clutches from Costa Rica, but this was not the case among clutches examined from Panama. Free-living tadpoles of L. melanonotus displayed a distinct right-handed preference during explosive turns. While some tadpoles of A. callidryas were at stages too early to detect any explosive turns when breathing, later-staged individuals did display a left-handed bias in startle response to mechanical stimulation. Additionally, it appears that the expression of behavioral lateralization of larvae (but not embryos) may predict whether or not the adults exhibit similar lateralization. Findings herein provide insight into the ontogeny and evolutionary origins of lateralized behavior in anurans.

Full text

RESEARCH PAPER
Lateralized Turning Biases in Two Neotropical Tadpoles
Venetia S. Briggs-Gonzalez*†& Sergio C. Gonzalez†
* Department of Biology, University of Miami, Coral Gables, FL, USA
†Department of Wildlife Ecology and Conservation, Fort Lauderdale Research and Education Center, University of Florida, Davie, FL, USA
Correspondence
Sergio C. Gonzalez, Department of Wildlife
Ecology and Conservation, Fort Lauderdale
Research and Education Center, University of
Florida, Davie, FL 33314, USA.
E-mail: sceliog@yahoo.com
Received: February 14, 2016
Initial acceptance: March 22, 2016
Final acceptance: April 21, 2016
(S. Foster)
doi: 10.1111/eth.12503
Keywords: laterality, tadpole, turning bias,
behavioral lateralization, anuran, ontogeny
Abstract
Lateralized turning behavior in startle responses and upon descent after sur-
facing for a breath of air has been documented for tadpoles in several anuran
species. A left-handed preference is most common and was previously
thought to be linked to the asymmetry in spiracle location. Here, we investi-
gate the presence of behavioral asymmetries in tadpoles of Agalychnis
callidryas and Leptodactylus melanonotus in explosive turns after air-breathing.
Data were also collected on lateralized posture in the orientation of tails of
embryonic A. callidryas within the egg case, as well as the startle response of
free-swimming tadpoles exposed to mechanical stimulation. A left-curled
tail bias was found among several clutches from Costa Rica, but this was not
the case among clutches examined from Panama. Free-living tadpoles of
L. melanonotus displayed a distinct right-handed preference during explosive
turns. While some tadpoles of A. callidryas were at stages too early to detect
any explosive turns when breathing, later-staged individuals did display a
left-handed bias in startle response to mechanical stimulation. Additionally,
it appears that the expression of behavioral lateralization of larvae (but not
embryos) may predict whether or not the adults exhibit similar lateraliza-
tion. Findings herein provide insight into the ontogeny and evolutionary
origins of lateralized behavior in anurans.
Introduction
Left–right behavioral asymmetries in bilateral mam-
malian organisms, particularly humans, have long
been established (LeMay 1976). Within the past
30 yr, evidence has accumulated to support hypothe-
ses on the presence of ‘handedness’ as well in fish,
amphibians, reptiles, and birds (Rogers 1980; Brad-
shaw & Rogers 1993; Bisazza et al. 1998; Vallortigara
et al. 1999; Dadda 2005; Robins 2005; Malashichev
2006). The ontogeny of lateralized behavior in larval
forms has received some attention in amphibians
(Bisazza et al. 1998; Malashichev & Wassersug 2004)
and is particularly interesting given the metamorphic
period that involves gross changes in both the mor-
phology and ecology of individuals. Studies of anuran
laterality during tadpole development present an
interesting opportunity to investigate the dominance
shift in the use of axial to appendicular musculature
throughout metamorphosis (Wassersug & Yamashita
2002). In some tadpoles, lateralized behavior patterns
are apparent in the direction of whole body turns that
individuals exhibit upon descent after taking a breath
of air, and during startle response behavior (Wasser-
sug et al. 1999; Yamashita et al. 2000; Goree &
Wassersug 2001; Rogers 2002; Wassersug & Yama-
shita 2002). These explosive turns, referred to as ‘C-
turns’ or ‘C-start’ responses, can occur within
<100 ms and are likely to be Mauthner cell-mediated
and ‘hard-wired’ in tadpoles (Bisazza et al. 1998;
Rogers 2002; Wassersug & Yamashita 2002). Such fast
reflex loops are adaptively significant as fast turns are
necessary for predator avoidance, and lateralized per-
ception centers (as opposed to redundant and compet-
ing bilateral centers) may reduce stimulus processing
and response times (Vallortigara et al. 1999; Rogers
2000; Wassersug & Yamashita 2002; Robins 2005).
Turning biases do not occur in all anuran species,
but there is typically a left-sided bias during explosive
turns that was originally thought to be obligatorily
linked to the common asymmetry of a left-sided spira-
cle (Wassersug et al. 1999). However, subsequent
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Ethology

data show that some species that are morphologically
symmetrical nonetheless exhibit behavioral asymme-
tries during turning (reviewed in Malashichev &
Wassersug 2004). These turning biases are apparent
shortly after hatching, decrease throughout tadpole
development, and disappear before metamorphosis,
coinciding with the shift from axial musculature
dependent movement in the larvae to post-meta-
morphic appendicular locomotion (Yamashita et al.
2000; Dadda 2005; Malashichev 2006).
Usually this laterality exists on the order of 60–90%
of turns per individual (Wassersug & Yamashita
2002). Other forms of lateralized behavior may be
apparent in anurans prior to the free-living larval
stage. These include the side to which an embryo coils
its tail within the egg case (Thibaudeau & Altig 1999)
and the side to which a new hatchling leans when
lying on a substrate (Wassersug & Yamashita 2002).
Published studies on tadpole laterality are restricted
to the last two decades and include a small number of
species, many of which occur in temperate zones, and
none of which record handedness of tadpoles in the
field. Here, we test the hypothesis that lateralized
behavior, such as those used in descending after a
breath of air and in startle responses to mechanical
stimulation, is found in two distantly related species
of New World tropical frogs. We provide data on
embryonic tail orientation and turning bias as indica-
tors of laterality in tadpoles of Agalychnis callidryas
(Hylidae) and Leptodactylus melanonotus (Leptodactyli-
dae) by implementing two previously developed pro-
tocols (Wassersug et al. 1999; Yamashita et al. 2000).
Whether behavioral lateralization in anurans is an
evolutionarily conserved trait that is reflective of phy-
logeny (with more basal archaeobatrachian clades lack-
ing behavioral lateralization) has been questioned by
Malashichev (2006). As all chordates exhibit neural lat-
eralization, Xenopus (Archaeobatrachia) larvae have
been shown to exhibit visual perception laterality
(Gouchie et al. 2008), and not all neobatrachians exhi-
bit similar behavioral lateralization (Bisazza et al. 1997;
Malashichev 2002; Malashichev 2006); we are inclined
to agree with the idea that variation in type and degree
of lateralization is more related to functional traits than
phylogenetic relatedness. We also bring our results on
previously unstudied species into this context to pro-
vide more resolution to the matter.
Methods
We collected 10 egg masses for a total of 523 eggs of
A. callidryas during June 27, 2002, to June 29, 2002,
from the Research Swamp at the La Selva Biological
Station, Heredia Province, Costa Rica. In the labora-
tory, we staged egg development (Gosner 1960),
counted number of eggs in each clutch, and assessed
the tail orientation of the developing embryo in as
subset of seven of the clutches. To supplement our
data on embryonic tail orientation, we also examined
photographs of 23 egg clutches of A. callidryas col-
lected from a population at a man-made experimental
pond at Smithsonian Tropical Research Institute facili-
ties, adjacent to el Parque Nacional Soberania, Gam-
boa, Panama in 2005. Egg masses, attached to host
leaves, were suspended above a cup of pond water
(250 ml) until hatching, after which tadpoles were
counted and relocated as a sibship to a larger con-
tainer with 2000 ml of pond water. Tadpoles were
kept in a laboratory that was open to ambient light
and temperature fluctuations and were fed powdered
fish food daily and water was changed regularly.
We placed two individuals in a translucent cup with
250 ml pond water providing sufficient room for
swimming without contacting each other, nor the
confines of the container nor be exposed to air. In this
way, we could observe two tadpoles simultaneously
in the laboratory. Following the protocol of Wassersug
et al. (1999), we recorded whether turns made by
each tadpole upon descent after taking a breath of air
were toward the right or left. In addition to these tri-
als, we also observed the combined turns of individu-
als found as an aggregate in the field to determine
cohort-level handedness. We observed the group
housed in the laboratory and recorded turns. Data on
direction of explosive turns were recorded for each
tadpole housed in pairs and tadpoles housed in a
group as a representative of population handedness.
To investigate potential handedness in a wild popu-
lation, we observed tadpole behavior of L. melanonotus
in a small temporary pond (approximate area
190.5 90.2 m) at the Selva Tica Research Station,
10 km from La Selva in the corridor connecting La
Selva to Parque Nacional Braulio Carrillo. We
recorded turning direction of each individual that sur-
faced for air in the group (Wassersug et al. 1999).
Individual turns were obvious because of water clarity
and the time in between turns, both ensured that sev-
eral different tadpoles were surfacing to breathe. Tad-
poles were temporarily collected for staging and were
found to be between Gosner stages 26–27 (Gosner
1960).
To investigate individual lateralized behavior in
startle response among A. callidryas to mechanical
stimulation (Wassersug et al. 1999), tadpoles were
grouped in pairs for individual observation and a fine-
point probe attached to an extendable handle was
Ethology 122 (2016) 1–6 ©2016 Blackwell Verlag GmbH2
Laterality in Tropical Tadpoles V. S. Briggs-Gonzalez & S. C. Gonzalez

directed toward the top of the tadpole’s body on the
midline. Tadpoles were stimulated only when in a
resting position in the water column. Tadpoles that
were actively swimming were not mechanically stim-
ulated. The directional response (left or right) of each
tadpole was recorded. To assess a response to mechan-
ical stimulation when in a group setting, we examined
natal cohorts in separate tanks by directing a probe
toward the center of the container creating a small
ripple in the water column that elicited a startle
response.
We used a nonparametric chi-square test (IBM
SPSS ver. 20) to test for significant differences in the
direction of tail orientation of embryos and to investi-
gate the direction of explosive turns (1) after tadpoles
of A. callidryas and L. melanonotus surfaced for a breath
of air and (2) after mechanically stimulating A. cal-
lidryas tadpoles in pairs and groups. All tadpoles at La
Selva were returned to the Research Swamp, and no
tadpoles of L. melanonotus were removed from Selva
Tica. Eggs and embryos from the Panamanian popula-
tion were used for other experiments, after which tad-
poles and metamorphs of various stages were released
at the collection site.
Results
Costa Rican egg clutch size ranged from 14 to 94 eggs
(
x=51.7 8.83 SD), and each of the ten clutches
represented a cohort to determine handedness at the
group level in the larval experiments. Seven egg
masses were suitable for surveying embryonic orien-
tation and contained 306 embryos of A. callidryas of
which 162 embryos had curled tails toward the left
representing 53% of the population and 144 had
right-handed curled tails at 47%, but these were not
significantly different (v
2
=1.059, df =1, p =0.303).
However, when clutches were surveyed separately,
five of the seven clutches showed a left-handed ten-
dency in tail orientation of the developing embryos,
and the two that did not reflect this tendency com-
prised larger egg masses (n =94, and n =55). This
may infer a genetic component, or the possibility of
multiple clutches from different females, but could
easily be an effect of a lower sample size at the clutch
level.
Clutch size of 23 Panamanian egg clutches ranged
from 31 to 71 eggs (
x=44.4 10.64 SD), totaling
1022 eggs. We similarly used each clutch to represent
group handedness. Just over half of the eggs were vis-
ible in photographs to determine whether embryos
had tails curled in either direction (n =625). Of the
observable embryos, 300 had tails curled to the left
representing 48% of the population, while 325, 52%,
had tails curled to the right. These were not signifi-
cantly different (v
2
=0.50, df =1, p =0.48).
Upon hatching, we attempted to observe the turn-
ing bias of Gosner stage 23 tadpoles (Gosner 1960) of
A. callidryas (n =134); however, tadpoles did not
exhibit explosive turns after breathing and instead
drifted toward the bottom of the container after sur-
facing. More developed tadpoles (Gosner stages 26–
27) of a small population of L. melanonotus (n =72) in
the wild showed a preference toward the right
(n
right
=58 vs. n
left
=14) when descending after a
breath of air (v
2
=26.889, df =1, p <0.001).
To test startle responses to mechanical stimulation
in A. callidryas, we recorded the turn of each tadpole
(Gosner stage 26) that were housed (1) in pairs
(n =54 tadpoles) and (2) in natal cohorts (n =134
tadpoles). Tadpoles in pairs originated from three sep-
arate clutches, and more tadpoles displayed a left-
handed tendency than a right-handed tendency (30
left vs. 24 right). However, this small difference was
not significant (v
2
=1.852, df =1, p =0.174). When
tadpoles of five separate clutches were observed in
their natal cohort as an aggregated group, tadpoles
displayed a significant left-handed turning preference
at 59% vs. 41% right-handedness (n
left
=79 vs.
n
right
=55) in their explosive turns (v
2
=4.299,
df =1, p =0.038).
Discussion
Embryos at Gosner stage 21 have well-developed tails
and a coiled orientation within the egg that may be a
precursor to lateralized movements post-hatching
(Wassersug & Yamashita 2002). A previous study with
Eleutherodactylus coqui suggested a left-sided coiling
preference but no supporting data were presented
(Thibaudeau & Altig 1999). In this study, we provide
data on embryonic tail orientation as a precursor to
tadpole lateralized behavior in A. callidryas. Results
from the Costa Rican population may hint toward a
left-handed clutch level bias, if a ‘population’ (in this
case ‘clutch’) is said to be lateralized when more than
50% of the individuals are lateralized in the same
direction (Bisazza et al. 1998). However, this observa-
tion was no longer apparent at the population level
(all clutches), nor did the Panamanian population
show any biases within clutches or when all embryos
were grouped together.
Recently hatched pond tadpoles remain mostly sta-
tionary before they take up active swimming and are
thought not to be capable of making explosive turns
prior to Gosner stage 25 (Wassersug & Yamashita
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V. S. Briggs-Gonzalez & S. C. Gonzalez Laterality in Tropical Tadpoles

2002; Wassersug & Yamashita 2002), and we confirm
this with all 134 A. callidryas tadpoles that were at
Gosner stage 23. Results of the startle response of
A. callidryas tadpoles at Gosner stage 26 to mechanical
stimulation illustrate that the observed left-handed
bias was more apparent in larger groups. The amplifi-
cation of apparent lateralization in behavioral
responses has been linked to intraspecific aggregations
(Bisazza et al. 2002; Dadda 2005; Gouchie et al. 2008;
Karenina et al. 2013). Evidence also exists for lateral-
ization of visual perception among certain larval anu-
rans and fish, and this is believed to assist in both
schooling with conspecifics as well as predator detec-
tion (Rogers 2000; Dadda 2005; Gouchie et al. 2008).
Agalychnis callidryas tadpoles exhibit multiple preda-
tor-mediated phenotypically plastic traits (including
timing of hatching and metamorphosis) and experi-
ence associated trade-offs with shifts in growth,
behavior, and ontogeny (Warkentin 1995; Vonesh &
Warkentin 2006; Gonzalez et al. 2010). Perhaps the
direction of the C-turning bias in populations of larval
anurans may be a consequence of exposure to certain
predators.
Field observations of wild tadpoles of L. melanonotus
in a small ephemeral pond revealed that these tad-
poles exhibit immediate explosive turns upon descent
after surfacing for a breath. We found an 81% right-
handed bias. Leptodactylid tadpoles are externally
asymmetrical with a single, lateral, and sinistral spira-
cle (Savage 2002). These findings taken alone support
the early hypothesis that morphological asymmetry
may be causal to behavioral asymmetries (Wassersug
et al. 1999). However, in addition to successive find-
ings in the literature (Malashichev 2002; Malashichev
& Nikitina 2002; Malashichev & Wassersug 2004), we
note inconsistencies with this hypothesis. Previously
studied populations of Rana catesbiana, similarly exter-
nally asymmetric, exhibit a left-turning bias in the
direction of spiracle location (Wassersug et al. 1999),
whereas the turning behavior in this population of
L. melanonotus was biased away from the spiracle. This
difference between L. melanonotus and R. catesbiana
may reflect phylogenetic distance and may be linked
to possible asymmetry in the number of Mauthner
neurons located in the brain of these two externally
similar species (Wassersug & Yamashita 2002). How-
ever, our own results on A. callydrias also refute the
hypothesis that larval symmetry is causal to behav-
ioral laterality altogether.
Turning biases of tadpoles of A. callidryas are of par-
ticular interest because they are a neobatrachian (Hyl-
idae) frog. They also exhibit near external symmetry
in their body plan; larvae have a ventral spiracle that
opens on or near the midline of the body (Duellman
2001). Previous work has shown that Xenopus laevis
and Bombina orientalis (both archaeobatrachians) that
maintain a similarly symmetrical morphological
arrangement show no turning bias (Wassersug et al.
1999; Goree & Wassersug 2001) while a left-handed
bias has been observed in the neobatrachian micro-
hylid, Microhyla ornata, which also has a symmetrical
external body plan (Yamashita et al. 2000). Work on
R. catesbeiana (Wassersug et al. 1999) and Rana sylvat-
ica (Oseen et al. 2001) also show consistency in the
patterns of lateralized behavior among neobatrachians
despite larval asymmetry. A rightward turning
response has also been documented in the Australian
neobatrachian, Litoria latopalmata (Rogers 2002). Con-
sidering that L. melanonotus is also a neobatrachian,
the findings presented here, thus, support the hypoth-
esis that lateralized behavior among tadpoles reflects
phylogenetic relationships and is not coupled with
morphological asymmetries (Malashichev 2002;
Malashichev & Wassersug 2004). Lateralized behavior
may be a highly conserved feature and may have
been acquired at the base of the neobatrachian group.
Thereafter, distinct evolutionary radiations may have
resulted in some genera exhibiting a left-handed bias
(e.g., Rana) and others a right-handed bias (e.g., Lepto-
dactylus).
Furthermore, these findings also support the
hypothesis of Malashichev (2006) that behavioral
asymmetry may be an artifact of alternating limb
locomotion. Thus, we propose that the potential for
behavioral lateralization is an evolutionarily con-
served trait that is mediated by ecological adaptations
of locomotion. Indeed, even archaeobatrachians have
been shown to possess strong lateralization of physio-
logical traits, such as vision –which affects behavior,
if not lateralization of a behavior itself (Bisazza et al.
2002; Gouchie et al. 2008). Because studies exploring
behavioral lateralization in tadpoles are limited to
movement, it seems logical that particular lateralized
behaviors examined in the larval stage may also be a
precursor to lateralization in locomotive strategy of
the adult stage.
Assuming that tadpole behavioral laterality may
be linked to laterality in the adults, our results fit
the model outlined by Malashichev (2006). An
arboreal Hylid (A. callydrias) that moves primarily by
alternating limb movements should be expected to
exhibit locomotive laterality, despite a symmetrical
body plan. Tadpoles of L. melanonotus also exhibited
behavioral laterality which has similar locomotive
strategies as Ceratophrys ornata, which was shown to
possess behavioral lateralization in Malashichev
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Laterality in Tropical Tadpoles V. S. Briggs-Gonzalez & S. C. Gonzalez

(2006). Our results support the idea that the expres-
sion of behavioral lateralization (within the scope of
these types of experiments) is inextricably linked to
movement and thus locomotive strategy. It appears
that the expression of behavioral lateralization of
larvae (but not embryos) can be predicted by
whether or not the adults exhibit similar lateraliza-
tion. Our results have strong implications, not only
for supporting the link between lateralization and
functional traits as opposed to viewing lateralization
as an independently inheritable trait, but also in
demonstrating new ways for how functional traits
of one life history stage can influence behavior ear-
lier in an organism’s ontogeny.
Acknowledgements
Research was supported by the Organization of
Tropical Studies and the University of Miami. We
thank R. J. Wassersug for intellectual stimulation and
assistance with manuscript production and J. Robert-
son, J. Hunt, and R. Rundell for field assistance. We
are grateful to Sam C. for the opportunity to work on
this project.
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