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Anuran forelimb muscle tendinous structures and their relationship with

locomotor modes and habitat use

Article in Current Zoology · November 2018

DOI: 10.1093/cz/zoy086

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 Current Zoology, 2019, 65(5), 599–608
doi: 10.1093/cz/zoy086
Advance Access Publication Date: 30 November 2018
Article

Article

Anuran forelimb muscle tendinous structures

and their relationship with locomotor
modes and habitat use

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^ a, Félix B. CRUZB,*, Débora L. Moreno AZOCAR
Silvia DE OLIVEIRA-LAGOA  b
,
Esteban O. LAVILLAc, and Virginia ABDALAD,*
a
Facultad de Ciencias Exactas y Naturales - Universidad Nacional de Asunción, San Lorenzo, Paraguay, bInstituto
de Investigaciones en Biodiversidad y Medioambiente INIBIOMA (CONICET-UNCOMA) Quintral Bariloche, Rio
Negro, Argentina, cInstituto de Herpetologı́a, UEL (Fundación Miguel Lillo - CONICET), Tucumán, Argentina, and
d
Instituto de Biodiversidad Neotropical (UNT-CONICET) Horco Molle s/n Yerba Buena, Tucumán. Cátedra de
Biologı́a General, Facultad de Ciencias Naturales, UNT, Tucumán, Argentina
*Address correspondence to Félix B Cruz and Virginia Abdala. E-mail: [email protected];
[email protected].

Handing Editor: Rudiger Riesch

Received on 30 June 2018; accepted on 11 November 2018

Abstract
The interaction between organisms and their environment is central in functional morphology.
Differences in habitat usage may imply divergent morphology of locomotor systems; thus,
detecting which morphological traits are conservative across lineages and which ones vary under
environmental pressure is important in evolutionary studies. We studied internal and external
morphology in 28 species of Neotropical anurans. Our aim was to determine if internal morphology
(muscle and tendons) shows lower phylogenetic signal than external morphology. In addition, we
wanted to know if morphology varies in relation to the habitat use and if there are different functional
groups. We found differences in the degree of phylogenetic signal on the groups of traits.
Interestingly, postaxial regions of the forelimb are evolutionarily more labile than the preaxial
regions. Phylomorphospace plots show that arboreal (jumpers and graspers) and swimmer frogs
cluster based on length of fingers and the lack of sesamoid, also reflected by the use of habitat.
These functional clusters are also related to phylogeny. Sesamoid and flexor plate dimensions to-
gether with digit tendons showed to be important to discriminate functional groups as well as use of
habitat classification. Our results allow us to identify a “grasping syndrome” in the hand of these
frogs, where palmar sesamoid and flexor plate are absent and a third metacarpal with a bony knob
are typical. Thus, a lighter skeleton, long fingers and a prensile hand may be key for arboreality.

Key words: comparative analyses, ecomorphology, neotropical frogs, function, habits, phylogeny

How an organism interacts with its environments has important for natural selection to act upon (Arnold 1983; Kingsolver and
implications for the selective forces shaping the phenotypes of the Huey 2003). In this sense, the relationship between morphology,
species. The potential association between morphology and func- locomotor performance and habitat use is one of the most studied
tional performance at different levels (individual, population and aspects of evolutionary phenotypic variation (Losos and Sinervo
species) may yield differences in fitness providing the raw material 1989; Losos 1990a, 1990b; Bonine and Garland 1999; Van Damme

C The Author(s) (2018). Published by Oxford University Press.

V 599
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600 Current Zoology, 2019, Vol. 65, No. 5

and Vanhooydonck 2002; Goodman et al. 2008; Irschick et al. Fontanarrosa and Abdala 2014, 2016), we also included this struc-
2008). It was observed that differences in habitat occupation under- ture in our study. We test whether the external and muscle-
lie divergent evolution of the morphology of locomotor systems in tendinous morphologies of anuran forelimbs differ among taxa that
numerous taxa (Irschick et al. 2005; Calsbeek and Irschick 2007). exhibit different locomotor modes or habitat use. We also test
Among the studies on this issue, research on reptiles certainly out- whether such patterns can be explained solely by the phylogenetic
number those in other groups; for example, many studies have inves- relationships between the species examined or by another underly-
tigated the relationship between limb morphology and habitat use in ing factor. It should be noted that the muscle-tendinous structures
Anolis, liolaemids and tropidurine lizards (Losos 1990a, 1990b, have been seldom considered in ecomorphological studies of verte-
1990c; Kohlsdorf et al. 2001; Irschick et al. 2005; Calsbeek and brates (Abdala et al. 2008, 2014; Tulli et al. 2012b; Fabrezi et al.
Irschick 2007; Grizante et al. 2010; Tulli et al. 2009, 2011, 2012a, 2014; Carrizo et al. 2014; Fratani et al. 2018). We hypothesize that:
2012b). However, these associations are not always clear (Tulli a) internal morphology (muscle and tendons) will show a higher
et al. 2012b, 2016). In a broad evolutionary context, convergent phylogenetic signal pattern than external morphology as was shown
evolution of traits in species from different regions can lead to simi- in previous studies on other tetrapod taxa (Tulli et al. 2012a;
lar body shape among them, although they could be phylogenetical- Carrizo et al. 2014); b) morphological traits of terrestrial species

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ly unrelated (Donley et al. 2004; Moen et al. 2013). Alternatively, will differ from arboreal ones because climbing ability is associated
despite the dispersal of lineages, relevant ecological traits may be with the position of the center of gravity; thus, arboreal species need
conserved during and after separation (Losos, 1990a, 1990b, 1990c; different morphological arrangements to compensate the potential
Stephens and Wiens 2004; Moen et al. 2013). For these reasons, problem of a displaced center of gravity (Cartmill 1985; Tulli et al.
detecting which morphological traits are conserved across lineages 2009) and c) arboreal graspers and jumpers will show different
and which ones vary under environmental pressure is an important morphology compared with walker jumpers and swimmer frogs that
aspect of evolutionary studies. tend to exhibit a morphological continuum (Soliz et al. 2017).
Several studies made interesting observations on the variation of Specifically, we predict that the grasping anurans will exhibit a
muscles across different taxonomic groups of amphibians (Dunlap “grasping syndrome” as described by Fontanarrosa and Abdala (2016).
1960; Davies and Burton 1982; Burton 1983, 1996a, 1996b, 1998,
2001, 2004; Liem 1970; Manzano and Lavilla 1995; Manzano 2000;
Faivovich 2002; Manzano et al. 2008; Salgar et al. 2009; Hoyos et al.
Material and Methods
2014; Hoyos and Salgar 2016; Blotto et al. 2017). In addition, it has We dissected the forearm and manus of 156 adult specimens belong-
been observed that in the palmar surface of the hand of some lizard ing to 28 species of 7 anuran families: Bufonidae, Leptodactylidae,
and anuran taxa, the flexor tendon connecting the forearm muscles Hylidae, Phyllomedusidae, Telmatobiidae, Odontophrynidae, and
with the digits present an embedded palmar sesamoid (Abdala et al. Microhylidae (Figure 1, Supplementary Material) that occur in
2009; Ponssa et al. 2010) that prevents the palmar flexion of the hand Northwestern Argentina, Paraguay, South of Bolivia and Brazil. The
and consequently restricts its movement (Abdala et al. 2009; Sustaita choice of the species aimed to maximize representation of habitat
et al. 2013; Fontanarrosa and Abdala 2014, 2016). Some studies on use and locomotor modes in the sample of species occurring in simi-
the palmar sesamoid and myotendinous structures in Squamata lar habitats, such as Chaco (arid, semiarid and wet) and Monte
(Haines 1950; Moro and Abdala 2004; Abdala et al. 2009; Tulli et al. (Cabrera and Willink 1980). In addition, we aimed for a balanced
2012b; Fontanarrosa and Abdala 2014, 2016), marsupials (Abdala phylogenetic representation of different clades within each studied
et al. 2006) and placental mammals (Carrizo et al. 2014) showed that family, with the exception of one Telmatobius species. Sample sizes
these structures can be associated with ecological aspects of the for each species ranged from 3 to 9 specimens according to availabil-
studied animals, such as habitat use or locomotor modes (Abdala ity (Supplementary Material). Because sample size might be small
et al. 2006; Tulli et al. 2012b; Carrizo et al. 2014). and variable, we measured the variation coefficient (VC, given in
Anuran morphology has been studied in association with loco- percentage) for snout-vent length within each species (as this is the
motor mode in several cases (Rand 1952; Zug 1972, 1978; Emerson most variable trait) obtaining variation coefficients from 3% to
1978, 1988; Gomes et al. 2009; Jorgensen and Reilly 2013; Vidal- 11% (mean VC for the entire sample was 6.17% and set point
Garcı́a et al. 2014). The remarkable abilities of frogs to swim, hop, 4.24–8.87%). A broad intraspecific variation may be an important
walk, climb, dig and even glide allow them to occur in almost all avail- source of uncertainty that can influence our results and may lead to
able environments and make them an interesting group to highlight misinformed conclusions (Garamszegi and Møller 2010); however,
relationships between morphology and ecology (Soliz and Ponssa our data did not show a broad dispersion. For each individual we
2016; Soliz et al. 2017). In the past, hind limb morphology has been made dissections of the palmar sesamoid and myological and tendin-
studied in relation to the mentioned locomotor modes, because of the ous traits related to the forelimb and manus under a binocular
biomechanical role of the limbs as the propulsive agent (Zug 1972). microscope (Nikon SMZ645), for details see Abdala et al. (2006,
As such, strong jumpers are known to exhibit proportionately longer 2008). Muscle-tendinous variables were measured with a digital
hind limbs and longer tibio-fibulae (Zug 1972; Emerson 1978, 1985). caliper (Mitutoyo CD-15B; 6 0.01 mm, Japan). Species means and
Comparatively, variations in the forelimb anatomy of frogs has the number of individuals per species used are included as support-
received less attention (but see Gillis et al. 2014). ing information (Supplementary Material).
Here, we studied the comparative anatomy of the forelimb in Following the protocol of Abdala et al. (2006), Tulli et al.
28 species of Neotropical anurans focusing on the muscle-tendinous (2012b), and Carrizo et al. (2014), we studied the variability be-
system. We postulate that muscle-tendinous structures can also tween muscle and tendon dimensions of the structures directly impli-
reflect the evolutionary history of a group, acting as anatomical cated in manual burrowing, grasping, walking, jumping, and
descriptors and showing adaptive changes to lifestyle (Burton 1998). swimming. External characters are shown in Figure 2A, B; muscles
Considering the relevance of the palmar sesamoid in the manual and tendons measured are shown in Figure 2C, D. All of the muscles
abilities of tetrapods (Abdala et al. 2009; Sustaita et al. 2013; analyzed exhibit a parallel-fibered arrangement. In addition to
De Oliveira-Lagôa et al.  Muscle tendinous structure, locomotor modes and habitat use 601

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Figure 1. Composite tree of the species studied here. Colored circles on the right show the functional groups (left) and habits categories (right) these species
have.

length, maximum width of muscles was also recorded to obtain an Mean values of all morphological variables (Supporting
estimate of the morphometric variation of each muscle as a whole to Information Supplementary Material) were log10 transformed for
allow testing if there exists correlation between aponeurosis and ten- further analyses. We then tested the data for phylogenetic signal
don dimensions that are associated with these muscles. (i.e., the consistency in trait values with the phylogeny); for this pur-
The different categories of habitat use and locomotor modes pose, we used the Pagel’s k value estimator for each variable (Pagel
were considered after Cei (1980), Wells (2007), Jorgensen and 1999) that varies between 0 and 1, where 0 means no phylogenetic
Reilly (2013) and personal observations. Therefore, we obtained 4 signal and 1 means that a variable is highly dependent of the phylo-
habitat use categories (fossorial, terrestrial, arboreal and aquatic), genetic structure. In addition, a randomization analysis was per-
and 6 locomotor mode categories (terrestrial walker, terrestrial formed for each variable to determine the probability of the
jumper, terrestrial burrower, arboreal jumper, arboreal grasper- estimator.
walker and swimmer; Figure 1). As the morphological variables studied here showed to be highly
Because species have a shared history (Figure 1), data of traits correlated with body size (r2 > 0.8), and to consider the phylogenet-
corresponding to these species cannot be considered as independent ic context of this study, we proceeded with phylogenetic size correc-
data-points (Harvey and Pagel 1991) and phylogenetically informed tion (Revell 2009). Through this, we obtained the residuals of each
statistical analyses are required. For this purpose, we used a compos- target morphological trait (least squares regression analysis trait vs.
ite tree of the phylogenetic relationship based on Pyron and Wiens body size - snout-vent length, SVL) while simultaneously controlling
(2011) tree and because branch lengths (BL) were not available, we for phylogenetic independence. Then, we used the residuals in subse-
used arbitrary branch lengths (e.g., all BL equal to one, BL trans- quent analyses as size-corrected morphological measurements.
formed with Grafen method and BL transformed with Pagel We studied 23 different morphological variables (Supplementary
method). We tested the adequacy of each one of these 3 arbitrary Material, Table S2). Since this amount of information is difficult to
branch lengths following Garland et al. (1992), by plotting the abso- analyze, we reduced the number of variables by running a phylogen-
lute value of each standardized independent contrast versus its etically based principal component analysis (phyl.pca). We collected
standard deviation. We used Mesquite v2.74 (Maddison and the scores of each principal component from the phylogenetically
Maddison 2015) and the PDAP PDTREE v1.15 modules (Midford informed PCA. We considered the first 4 principal components that
et al. 2009) and searched for significant differences. After plotting attained for 84% of the accumulated variance of the total analyses.
trees and BL for all traits, we found that the tree with BL equal to We also plotted the phylomorphospace and the contribution of all
one was the more adequate arrangement (BL ¼ 1 showed 4 out of morphological variables; for this descriptive purpose, we used the
26 significant plots, while Pagel BL transformation showed 8/26 and command phylomorphospace from the program Phytools (Revell
Grafen 11/26 significant relationships). 2012).
602 Current Zoology, 2019, Vol. 65, No. 5

We tested if internal or external variables showed variability in modes; these analyses were conducted through a phylogenetically
relation to the 6 functional groups considered here (fossorial informed ANOVA too. All these analyses were performed including
walkers, terrestrial walkers, terrestrial jumpers, arboreal jumpers, phylogenetic information through the following functions; phylosig,
arboreal walker or graspers and aquatic swimmers) as well as for phyl.resid, phyl.pca, phylomorphospace, phylANOVA of the
the type of habitats these frogs use (e.g., burrows, terrestrial, arbor- Phytools package version 6.0 (Revell 2012) in the open access envir-
eal and aquatic). In this case we used phylogenetic MANOVA by onment R (Version 3.4.0, R Core team 2017).
running Geiger program (Harmon et al. 2008), we concatenated the
internal or external variables in relation to the different factors
(functional groups or habitat types) as a formula to compute the Results
analyses. Finally, for testing if there were differences in each one of In all dissected specimens the m. flexor digitorum communis origi-
the different morphological traits (in total 23 external and internal nates from the humerus distal condyle, through a wide and short
traits) among species as a function of their habitat use (aquatic, ter- tendon from the aponeurosis covering the elbow. The m. flexor
restrial, arboreal or fossorial) a phylogenetically based analysis of carpi ulnaris originates on the medial epicondylus of the humerus,
variance was performed (phylANOVA of Phytools, Revell 2012) with some fibers connected to the m. flexor digitorum communis.

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with 1000 iterations. Similarly, we used the same 23 traits to deter- All specimens present a superficial and a deep fascia that can be col-
mine whether there were differences due to the species locomotor ored (Figure 2C, D). Bufonidae, Leptodactylidae, Telmatobiidae,

Figure 2. External characters. (A) body and arm external measurements, (B) manus external measurements (C) muscle and tendons showing sesamoid and flex-
or plate, (D) tendons and muscles where no flexor plate or sesamoid are present (drawings courtesy S. De Oliveira Lagôa).
De Oliveira-Lagôa et al.  Muscle tendinous structure, locomotor modes and habitat use 603

Odontophrynidae, and most of Microhylidae present a flexor plate showed high values of phylogenetic signal estimators (0.999,
with an embedded palmar sesamoid, over which a palmar aponeur- Table 1).
osis is distinguishable (Figure 2C); conversely, hylids, Phylogenetic PCA showed that the following variables contrib-
Phyllomedusidae and some microhylids lack a palmar sesamoid uted most (based on higher absolute eigenvalues) to the principal
(Figure 2D). From the flexor plate originate the flexor tendons of components functions (Table 2): sesamoid length, sesamoid width,
digits III, IV, and V that insert onto the basal portion of the distal digit IV and V tendon length and width (respectively), flexor carpi
phalanx of each digit (Figure 2D). ulnaris tendon length and width (internal morphology variables;
In the case of bufonids, a tendinous sheet between the mm. flex- Table 2); similarly, forearm width and hand length show high load-
or digitorum longus and mm. opponens of digit II are distinguish- ings in the PCA (Table 2). In addition, phylomorphospace plots con-
able. In leptodactylids, telmatobiids, and odontophrynids, there is sidering external and internal morphology characters show that all
an aponeurosis between the flexor plate and the muscles of digit II. arboreal (jumpers and graspers) and one swimmer species cluster
In Leptodactylus fuscus, the flexor tendon of digit II is visible and according to the length of finger tendons and sesamoid (Figure 3A),
originates from the flexor plate inserting into the basal portion of which is reflected by the use of habitat where aquatic (partially) and
the distal phalanx. The tendon is covered by fascias and the mm. arboreal species clearly differ from terrestrial and burrower species

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opponens and flexor digitorum II longus. Some microhylids, such as (Figure 3B). These clusters are probably due to phylogeny, since
Dermatonotus muelleri present a flexor tendon of digit II. In Figure 3C shows the same pattern and also because of the high
Hylidae and Phyllomedusidae, the m. flexor digitorum communis is phylogenetic signal observed in the most informative traits of PC1
where the flexor tendons of digits III, IV and V originate, then they (see Table 2). With respect to the habitat use groups, both arboreal
insert in the basal portion of the distal phalanx of each digit. The jumpers and walkers (Hylidae and Phyllomedusidae) are different
pennation angle is lower than 45 in all analyzed species. from other functional groups in their flexor plates (Figure 3A).
Depending on the source of the data (external or internal morph- However, it must be taken into account that there is an important
ology), we found different degrees of phylogenetic signal on the component of phylogeny in these results as the phylogenetic signal
group of traits. Snout-vent length (SVL) showed no significant and phylomorphospace analyses show (see Table 1 and Figure 3C).
phylogenetic signal, whereas among the external morphology traits, The phylogenetic MANOVAs with locomotor modes as factor
only arm length showed a significant phylogenetic signal (Table 1). revealed that, according to the Wilks’ statistic, only internal traits
For the internal morphology traits (muscles and tendinous systems), differed in response to habitat use (Table 3). However, phylogenetic
8 out of 16 traits showed significant phylogenetic signal based on MANOVA of external traits showed significant differences when
the values of the k estimate (Table 1). Finally, the distribution of spe- considering functional groups only (Table 3). The detailed phylo-
cies in different types of habitats and their locomotor modes also genetic ANOVA revealed that external traits do not show significant
variation in any of the cases (functional groups or habitat types).

Table 1. Phylogenetic signal using Pagel’s lambda estimate

Table 2. Phylogenetic PCA analysis on external and internal morph-
k P ology variables
External Measures Variable PC1 PC2 PC3 PC4
Snout-vent length 0.152 0.653
Arm length 0.587 0.047 External measures
Forearm length 0.126 0.697 Arm length 0.078 0.122 0.465 0.799
Forearm width <0.001 1 Forearm length 0.206 0.246 0.466 0.515
Palm length 0.171 0.584 Forearm width 0.047 0.275 0.342 0.424
Palm width 0.272 0.375 Palm length 0.315 0.196 0.112 0.049
Hand length 0.335 0.301 Palm width 0.045 0.116 0.003 0.219
Internal Measures Hand length 0.095 0.235 0.663 0.112
Sesamoid length 0.958 <0.001 Internal Measures
Sesamoid width 0.931 <0.001 Sesamoid length 0.880 0.365 0.101 0.040
Flexor plate length 0.999 <0.001 Sesamoid width 0.946 0.091 0.149 0.001
Flexor plate width 0.999 <0.001 Flexor plate length 0.954 0.202 0.072 0.022
Finger III tendon length 0.682 0.042 Flexor plate width 0.975 0.014 0.011 0.044
Finger IV tendon length 0.694 0.026 Finger III tendon length 0.200 0.338 0.804 0.185
Finger V tendon length 0.999 <0.002 Finger IV tendon length 0.243 0.057 0.767 0.216
Finger III tendon width 0.446 0.045 Finger V tendon length 0.433 0.199 0.780 0.043
Finger IV tendon width 0.120 0.613 Finger III tendon width 0.405 0.194 0.428 0.087
Finger V tendon width 0.291 0.663 Finger IV tendon width 0.172 0.346 0.122 0.137
Flexor carpi ulnaris muscle length 0.484 0.145 Finger V tendon width 0.070 0.171 0.545 0.010
Flexor carpi ulnaris muscle width 0.335 0.149 Flexor carpi ulnaris muscle length 0.042 0.026 0.854 0.186
Flexor digitorum communis muscle length 0.275 0.367 Flexor carpi ulnaris muscle width 0.028 0.301 0.641 0.575
Flexor digitorum communis muscle width <0.001 1 Flexor digitorum communis m. length 0.001 0.053 0.787 0.291
Flexor carpi ulnaris tendon length 0.317 0.105 Flexor digitorum communis m. width 0.543 0.077 0.303 0.096
Flexor carpi ulnaris tendon width 0.314 0.123 Flexor carpi ulnaris tendon length 0.238 20.958 0.049 0.034
Ecology Flexor carpi ulnaris tendon width 0.252 20.957 0.008 0.103
Function 0.999 <0.001 Cumulative contribution to variance 35.6 63.6 78.31 84.42
Habitat 0.999 <0.001
Boldface denotes most informative variables in the morphospace after abso-
Boldface denotes the presence of phylogenetic signal in the variable. lute values of eigenvalues.
604 Current Zoology, 2019, Vol. 65, No. 5

Table 3. Phylogenetic MANOVA of external and internal variables

grouped as a function of locomotor mode (terrestrial walker, ter-
restrial jumper, fossorial walker, arboreal jumper, arboreal grasper
or walker, and aquatic swimmer) and habitat use (fossorial, terres-
trial, arboreal, aquatic)

Locomotor mode

df Wilk’s F P

External 5 22 0.111 1.707 0.034

Internal 5 22 <0.001 3.926 <0.001

Habitat use

df Wilk’s F P

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External 3 24 0.405 1.132 0.349
Internal 3 24 0.005 2.692 0.003

Boldface denotes significant differences.

When examining internal traits, sesamoid width and length showed

significant differences, as well as flexor plate dimensions. Terrestrial
and burrowing species formed a homologous group, separated from
the aquatic and arboreal species after Holm post hoc test (Table 4).
The results for functional groups after the phylogenetic ANOVA of ses-
amoid and flexor plate dimensions show that terrestrial (jumpers and
walkers), burrowers and swimmers species form a homogeneous group
different from the arboreal species (walker and jumpers, see Table 4)
that exploit vertical habitats. Tendon width also shows significant dif-
ferences in the functional groups: swimmers, arboreal jumpers, and ar-
boreal walkers or graspers form a group separated from terrestrial
(burrowers, jumpers, and walkers) species (Table 4). When considering
habitat use, phylogenetic ANOVA showed that for sesamoid and flex-
or plate, tendon width of finger V and tendon length of finger VI, ter-
restrial and burrower species form a group and arboreal and aquatic
species were segregated (Table 4). Noticeably, Hylidae and
Phyllomedusidae species mostly belong to the arboreal habitat use cat-
egory (except for Pseudis platensis) segregated by Holm post hoc test
(Figure 3B, C, Table 4). Finally, the flexor digitorum communis muscle
width showed significant differences in habitat type used, although no
homogeneous group was formed (Table 4). These results highlight the
importance of the palmar sesamoid and the flexor plate in the exploit-
ation of vertical dimensions of the habitat.

Discussion
Our data show an important pattern of phylogenetic signal: half of the
internal morphology traits show high phylogenetic signal estimator val-
ues (Table 1). The effect of the phylogeny on the internal morphology
was also verified in other tetrapod groups, such as lizards and anurans
(Tulli et al. 2012a; Abdala et al. 2014; Fratani et al. 2018). Interestingly,
digit tendons length was additionally an important trait that segregated
Figure 3. Phylomorphospace plots of (a) functional groups (terrestrial walker, arboreal and swimming species showing that this morphology–lifestyle
jumper, and burrower; swimmer and arboreal walker and jumper); (b) habitat relationship probably arose from features clustered in phylogenetic
use (terrestrial; fossorial, swimmer, and arboreal) and (c) family level groups with the same habitat use (Vanhooydonck and Van Damme
(Microhylidae, Hylidae, Leptodactylidae, Odontophynidae, Bufonidae, 1999). This niche conservatism (Wiens and Graham 2005) was also ap-
Telmatobiidae) among the 28 anuran species. Axes correspond to PC1 35.6%
parent among microhylids that exhibit a strong conservatism in ecology,
of variance (increase of finger tendon [III, IV, and V] length, decrease of ses-
morphology and performance (although, not in body size). This is espe-
amoid and flexor plate size) and PC2 28.0% of variance (increase of flexor
carpi ulnaris—FCU muscle and sesamoid length and decrease of FCU tendon cially remarkable, given that these species have been separated for more
size). than 65 million years (Moen et al. 2013). Taken together these data
De Oliveira-Lagôa et al.  Muscle tendinous structure, locomotor modes and habitat use 605

Table 4. Phylogenetic ANOVA of external and internal variables as a function of locomotor mode (Tw ¼ terrestrial walker, Tj ¼ terrestrial
jumper, Bw ¼ fossorial walker, Aj ¼ arboreal jumper, Aw ¼ arboreal grasper or walker, and S ¼ aquatic swimmer) and habitat use (F ¼ fos-
sorial, T ¼ terrestrial, Ar ¼ arboreal, Aq ¼ aquatic)

Functional group Habitat type

F P posthoc F P posthoc

External Measures
Arm length 1.138 0.429 1.244 0.768
Forearm length 4.081 0.549 0.192 0.98
Palm length 4.084 0.545 0.974 0.808
Palm width 0.874 0.941 0.735 0.868
Hand length 1.631 0.848 2.851 0.549
Internal Measures
Sesamoid length 21.012 0.009 TwTjBwS AjAw 31.285 0.005 BT Aq Ar

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Sesamoid width 19.37 0.022 TwTjBwS AjAw 29.282 0.008 BT Aq Ar
Flexor plate length 28.184 0.007 TwTjBwS AjAw 47.078 0.001 BT Aq Ar
Flexor plate width 26.408 0.007 TwTjBwS AjAw 46.606 0.001 BT Aq Ar
Finger III tendon length 8.664 0.211 14.114 0.061
Finger IV tendon length 5.193 0.451 9.168 0.16
Finger V tendon length 13.318 0.071 23.448 0.019 BT Aq Ar
Finger III tendon width 19.914 0.021 TwTjBw SAjAw 30.836 0.007 BT Aq Ar
Finger IV tendon width 4.898 0.454 5.878 0.262
Finger V tendon width 3.173 0.651 1.675 0.712
Flexor carpi ulnaris muscle length 1.561 0.866 0.864 0.828
Flexor carpi ulnaris muscle width 3.774 0.587 1.424 0.707
Flexor digitorum communis m. length 0.327 0.995 0.186 0.975
Flexor digitorum communis m. width 10.579 0.14 18.326 0.036 BT Aq Ar
Flexor carpi ulnaris tendon length 2.982 0.67 2.064 0.613
Flexor carpi ulnaris tendon width 2.835 0.701 1.833 0.647

Boldface denotes significant differences and post hoc (Holm method) shows the homogeneous groups formed between groups (when underlined together).

support our first hypothesis, since internal morphology traits tended to may play in locomotion (Wang et al. 2014). Previous studies have
have higher phylogenetic signal than external ones. shown that toads use their forelimbs almost exclusively to decelerate
Among external morphology traits, only arm length exhibited a and control the body at the moment of impact (Gillis et al. 2014),
phylogenetic pattern indicating that this trait is somehow more our results suggest that the postaxial region of the forelimbs could
unique to each lineage among the species studied here. Traits exhib- exert a differential role in landing deserving special consideration,
iting strong phylogenetic signal suggest gradual changes over time particularly in jumping species (all leptodactylid frogs and some
(e.g., Brownian Motion model of evolution), and traits with no hylids).
phylogenetic signal may be highly labile on the time scale of phyl- Our phylogenetic informed MANOVA and ANOVA show that
ogeny, or may not change at all (Revell 2008). some of the selected morphological variables are clearly related to
Other traits that showed low phylogenetic signal were the width the arboreal locomotion mode and may be characterized by the mor-
and length of the tendon of the flexor carpi ulnaris that also played phological pattern of the forelimb, such as lack of sesamoid bone
an important role in our phylomorphospace figures. These traits and flexor plate. Forearm structures in arboreal anurans show that
may segregate the jumper species from the rest (particularly among they present in their manus the same pervasive trend exhibited for
the terrestrial species), but we need more detailed information to all lineages of grasping tetrapods (Sustaita et al. 2013; Manzano
corroborate this assumption. The low phylogenetic signal in the et al. in press). A vertical position in terrestrial environments
flexor tendons width of digits IV and V, and flexor carpi ulnaris requires that the animals stay in balance by pulling their fore-feet to-
muscle suggests that the postaxial regions of the forelimb are evolu- ward the substrate, while their hind feet push on the substrate (Tulli
tionarily more prompted to vary than the preaxial regions. These et al. 2011). This ability allows organisms to balance over a vertical
results are interesting as the postaxial region corresponds to the pri- substrate and requires that the organisms maintain their center-of-
mary axis that passes through digit IV in early limb development mass aligned with their support. This can be achieved by developing
(Fabrezi et al. 2007) and it would be expected a more stable config- an adhesive or suction force between their body and the contact sur-
uration to this crucial limb zone. However, it should be considered face (Cartmill 1985) or grabbing a narrow stem of the surface, as
that those variables related to length of the postaxial (ulnar) struc- most arboreal anurans and other grasping tetrapods do (Sustaita
tures show a strong phylogenetic pattern, decoupled thus of their et al. 2013; Manzano et al. in press). These morphological descrip-
width, which exhibit a lower phylogenetic signal, contrasting with tors of the arboreal habitat use in the studied frogs allow us to up-
the observations of Herrel et al. (2014) for hind limb kinematics of hold our second and third predictions. Previous studies across many
Xenopus tropicalis. These authors found that hind limb length in organisms have shown a strong relationship between ecology (e.g.,
females were good descriptors of the peak resultant jumping force, microhabitat use and diet) and morphology (see reviews in
compared with longer iliums and the length of the longest toe in Wainwright 2007). Far fewer have considered performance (e.g.,
males. This probably indicates the different roles fore and hind limb Losos 1990a, 1990b, 1990c; Herrel et al. 2014; Tulli et al. 2011,
606 Current Zoology, 2019, Vol. 65, No. 5

2012a), which forms the link between ecology and morphology narrow branches or twigs (Manzano et al. in press). Aquatic frogs
(Wainwright 1991). In addition, Moen et al. (2013) found that frog such as Xenopus with a large palmar sesamoid suggest that their
species using the same microhabitat had both similar morphology presence is owed more to phylogeny than to ecological reasons.
and performance, regardless of geographical location. However, recent studies suggest that Xenopus, a genus lacking
A recent study on morphology and habitat use also found that grasping syndrome, exhibits also considerable manual abilities,
frogs that live in the bush and swim and jump, exhibit modifications including an intermediate or scissor grip (Anzeraey et al. 2017). This
in the postcranial skeleton such as broad proximal sacral diapophy- report defied the pervasive link between arboreality and manual
ses, broad vertebral bodies, and longer urostyles that relate their grasping and requires a new perspective to explain the genesis of
morphology and habits (Soliz and Ponssa 2016). These authors also grasping among anurans (Manzano et al. in press). In addition, it
suggest that a slender body would be better adjusted to face any has to be noted that the palmar sesamoid may be ambiguously pre-
challenging locomotor modes, which is typical of hylid frogs that sent or absent (Ponssa et al. 2010); consequently, our results should
possess slender hands too. In addition, arboreal and walker species be taken with caution because of a possible taxon sampling prob-
have smaller and shorter vertebral bodies in their column, weaker lem, probably as a consequence of choosing species that may coexist
coracoids and clavicles compared with jumper and swimmer species as they occur in Chaco and Monte biogeographic provinces

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(Soliz and Ponssa 2016). Likewise, some features found in (Cabrera and Willink 1980).
Odontophoridae frogs suggest a functional relationship of some
morphological features, as they present a typical configuration of
burrowing frogs (Reilly and Jorgensen 2011). However, our data are
Supplementary Material
not strong and clear enough to support a specific hypothesis related to Supplementary material can be found at https://academic.oup.com/cz.
this burrowing group of frogs (Blotto et al. 2017), despite the fact that
we the studied 5 species belonging to 2 different families.
A nested clade (Hylidae and Phyllomedusidae) showed a particu- Acknowledgments
lar and different composition of limb anatomy, which caused them We thank Instituto de Investigación Biológica del Paraguay (IIBP), Museo
to be clustered together in a separate group from the rest of the spe- Nacional de Historia Natural del Paraguay (MNHNP), Fundación Miguel
cies in our phylomorphospace figure. Our results also showed that Lillo and Colección Zoológica de FaCEN, for providing access to specimens.
the traits that differentiate these anuran species exhibiting an arbor-
eal locomotor mode are the palmar sesamoid and the flexor plate
Funding
(Table 3). These traits allow us to identify a “grasping syndrome”
(Fontanarrosa and Abdala 2016) in the hand skeleton of these frogs, Funding for this study was provided by Consejo Nacional de Investigaciones
characterized by no palmar sesamoid, no flexor plate and the third Cientı́ficas y Técnicas de Argentina (Grant PIP-CONICET 389 to VA),
Agencia Nacional de Promoción Cientı́fica y Tecnológica, Argentina (Grant
metacarpal bone with a bony knob (Dang et al. 2018); supporting
PICT 2015-2471 to FBC, PICT 2016-2772 to VA).
our third hypothesis. Previous studies have shown that a large pal-
mar sesamoid embedded in a large flexor plate is a clear impairment
for flexing the hand and, consequently, prevents the acquisition of References
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