Eye size and investment in frogs and toads correlate with adult habitat, activity pattern and breeding ecology

Abstract

Frogs and toads (Amphibia: Anura) display diverse ecologies and behaviours, which are often correlated with visual capacity in other vertebrates. Additionally, anurans exhibit a broad range of relative eye sizes, which have not previously been linked to ecological factors in this group. We measured relative investment in eye size and corneal size for 220 species of anurans representing all 55 currently recognized families and tested whether they were correlated with six natural history traits hypothesized to be associated with the evolution of eye size. Anuran eye size was significantly correlated with habitat, with notable decreases in eye investment among fossorial, subfossorial and aquatic species. Relative eye size was also associated with mating habitat and activity pattern. Compared to other vertebrates, anurans have relatively large eyes for their body size, indicating that vision is probably of high importance. Our study reveals the role that ecology and behaviour may have played in the evolution of anuran visual systems and highlights the usefulness of museum specimens, and importance of broad taxonomic sampling, for interpreting macroecological patterns.

Keywords: allometry; amphibians; anurans; morphological evolution; sensory evolution; visual ecology.

Figure 1.

Examples of variation in anuran relative eye size across different species and ecologies. (a) Xenopus laevis (Pipidae; aquatic); (b) Bufo bufo (Bufonidae; ground-dwelling); (c) Ascaphus truei (Ascaphidae; semiaquatic); (d) Rhinophrynus dorsalis (Rhinophrynidae; fossorial); (e) Boana punctata (Hylidae: scansorial) with measurements of eye diameter (solid) and cornea diameter (dashed); (f) Lepidobatrachus laevis (Ceratophryidae; aquatic); (g) Boophis luteus (Mantellidae; scansorial); (h) Nanorana liebigii (Dicroglossidae; semiaquatic); (i) Hemisus marmoratus (Hemisotidae; fossorial). Photographs by S. Mahony, J. Streicher, D. Gower, C. Cox and M. Fujita. (Online version in colour.)

Figure 2.

Allometric scaling of anuran eyes across 220 species. Transverse eye diameter scales hypoallometrically with both (a) the cube root of mass and (b) snout–vent length, exhibiting extreme negative outliers for species with small relative eye sizes. (c) Cornea diameter scales slightly hypoallometrically with eye diameter. Species means are coloured by adult habitat; lines show fits for PGLS (solid), SMA (dashed) and OLS (dotted) regressions. (Online version in colour.)

Figure 3.

Eye size and investment vary significantly across adult habitats in anurans. (a) Phylogeny adapted from [36] shows species means for absolute eye diameter (ED) and relative eye investment. Eye investment represents the species residuals from the PGLS fit for log-transformed ED versus the cube root of body mass (RM), exponentiated so that species that fall precisely along the allometric fit have an eye investment of 1× the value predicted by fit, those that fall below have eye investments of less than 1× (small relative eye sizes), and those that fall above the fit have eye investments of greater than 1× (large relative eye sizes). Bars are coloured by adult habitat. Meg. = Megophryidae, Brev. = Brevicepitidae, Arthro. = Arthroleptidae, Pyx. = Pyxicephalidae, Dicro. = Dicroglossidae, Myo. = Myobatrachidae, Hem. = Hemiphractidae, Ele. = Eleutherodactylidae, Lep. = Leptodactylidae. (b) Absolute EDs and (c) relative eye investments differ significantly across adult habitats. Black diamonds indicate the mean and black bars the median for each state. (d) Silhouettes of four species (coloured by adult habitat) that exhibit differences in eye investment relative to body mass. (Online version in colour.)

Figure 4.

Eye investment differs significantly in phylogenetic ANCOVAs among anurans (a) utilizing different mating habitats and (b) active during different periods. Points are coloured by adult habitat, which showed the largest differences among states. Black diamonds indicate the mean and black bars the median for each state. (Online version in colour.)

Figure 5.

Anurans show large relative eye sizes and steep allometric slopes for eye–body scaling among vertebrate groups with published data for (a) axial length (AL) versus the cube root of mass (RM), (b) AL versus snout–vent length (SVL), (c) eye diameter (ED) versus RM, and (d) ED versus SVL. Data from ¹this study, ²[51], ³[15], ⁴[22], ⁵[20], ⁶[52], ⁷[54], ⁸[53], ⁹[21], ¹⁰[19]. (Online version in colour.)