Landing in basal frogs: evidence of saltational patterns in the evolution of anuran locomotion
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- Essner, R.L., Suffian, D.J., Bishop, P.J. et al. Naturwissenschaften (2010) 97: 935. doi:10.1007/s00114-010-0697-4
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All frogs are assumed to jump in a similar manner by rapidly extending hindlimbs during the propulsive phase and rotating the limbs forward during flight in order to land forelimbs first. However, studies of jumping behavior are lacking in the most primitive living frogs of the family Leiopelmatidae. These semi-aquatic or terrestrial anurans retain a suite of plesiomorphic morphological features and are unique in using an asynchronous (trot-like) rather than synchronous “frog-kick” swimming gait of other frogs. We compared jumping behavior in leiopelmatids to more derived frogs and found that leiopelmatids maintain extended hindlimbs throughout flight and landing phases and do not land on adducted forelimbs. These “belly-flop” landings limit the ability for repeated jumps and are consistent with a riparian origin of jumping in frogs. The unique behavior of leiopelmatids shows that frogs evolved jumping before they perfected landing. Moreover, an inability to rapidly cycle the limbs may provide a functional explanation for the absence of synchronous swimming in leiopelmatids.
Frogs have experienced a remarkable adaptive radiation since diverging from a common ancestor prior to the Triassic (Anderson et al. 2008; Marjanović and Laurin 2007) and saltation appears to be a key element in their evolutionary success. It is generally assumed that all anurans jump in a similar manner, and morphological evidence has been used to argue that terrestrial jumping was the primitive locomotor mode from which all other locomotor modes evolved (Jenkins and Shubin 1998; Shubin and Jenkins 1995; Přikryl et al. 2009). The propulsive phase of jumping involves rapid hindlimb extension accompanied by loss of forelimb contact. The aerial phase is characterized by midair body and limb rotations in preparation for landing (Duellman and Trueb 1994; Nauwelaerts and Aerts 2006; O’Reilly et al. 2000). Limb recovery begins near mid-flight and involves protraction and flexion of the hindlimbs and protraction, adduction, and extension of the forelimbs, placing them in position to absorb impact forces (Duellman and Trueb 1994; Emerson and De Jongh 1980; Peters et al. 1996). The extended forelimbs also serve as a pivot during landing, allowing the flexed hindlimbs to rotate into position beneath the body, enabling the rapid initiation of another takeoff (Duellman and Trueb 1994; Emerson and De Jongh 1980; Peters et al. 1996). These generalizations are based on observations of landing behavior in a few crown group anurans (Bufonidae, Microhylidae, and Ranidae; Emerson and De Jongh 1980; Gillis et al. 2010; Gillis and Biewener 2000; Kamel et al. 1996; Nauwelaerts and Aerts 2006; Peters et al. 1996). It is unclear if such generalizations are applicable to basal anurans. Indeed, there is reason to suspect that the basal-most anuran family Leiopelmatidae, represents an exception as evidenced by their plesiomorphic swimming behavior. Leiopelmatids use an asynchronous (trotting) swimming gait, in which the hindlimbs move out-of-phase with one another (Abourachid and Green 1999). In contrast, the primary swimming stroke of their sister group, Lalagobatrachia (Frost et al. 2006), is the “frog-kick,” in which the hindlimbs are extended and flexed together (Nauwelaerts and Aerts 2002) with hindlimb flexion beginning near mid-flight as it does when they jump (Peters et al. 1996).
The goal of this study was to test the generality of anuran jumping by comparing a member of the basal-most living frog family Leiopelmatidae, Ascaphus montanus with a basal lalagobatrachian, Bombina orientalis, and a derived lalagobatrachian, Lithobates pipiens (Frost et al. 2006). In addition to quantitative comparisons among these three semi-aquatic species, we examined representative video footage from two other leiopelmatids from New Zealand, the terrestrial Leiopelma pakeka and the semi-aquatic Leiopelma hochstetteri.
Materials and methods
A. montanus (n = 6 males), B. orientalis (n = 6 unknown sex), and L. pipiens (n = 6 unknown sex) were filmed jumping in a 155 × 60-cm arena with an AOS X-PRI high-speed video camera at 500 fps and a 45° mirror on an anti-slip surface (3 M Safety Walk tape). B. orientalis and L. pipiens were filmed at ecologically relevant temperatures of 25 ± 2°C (Blomquist and Hunter 2009; Choi and Park 1996). Because the primary streams (<15°C) and nocturnal temperatures (≤10°C) inhabited by adult A. montanus are cold (Metter 1964), we kept them at 15 ± 2°C during trials. Temperature is known to affect jumping performance in frogs (Hirano and Rome 1984; James et al. 2007). In order to ensure that general features of jumping behavior were not attributable to temperature differences, two A. montanus were filmed jumping five times each (ten trials) at 25°C; whereas, two B. orientalis and two L. pipiens were filmed jumping five times each at 15°C. Qualitative comparisons of all three species at both 15°C and 25°C revealed no general behavioral differences attributable to temperature.
Frogs were enticed to jump by tapping behind the animal. Each frog was filmed ten times and the five longest distance trials for each individual were used for key performance, timing, and angular variables (30 trials/species). Images were captured using AOS Imaging Studio V22.214.171.124 and imported into APAS motion-analysis software (Ariel Dynamics) for kinematic analysis. Landmarks were digitized and a series of angular variables was taken from each sequence to describe and compare statistically the three-dimensional movements of the body and limbs (see appendix for details). Timing variables were obtained by marking the appearance of key kinematic events while reviewing video. Statistical comparisons were made using repeated measures ANOVA and post hoc tests for species differences (Scheffe’s multiple comparison). Both Leiopelma species were filmed at 250 fps with a Fastek Troubleshooter digital video camera under similar conditions.
Knee and ankle angles at landing contact were higher in A. montanus (Table 1) reflecting delayed hindlimb recovery. On average, landing body attack angle did not differ among species. However, as shown above, attack angles (and landing postures) in A. montanus were highly variable (ranging from +62° to −71°) compared to the consistently negative angles (and consistent landing postures) exhibited by L. pipiens (mean = −24.5 ± 1.2°; Table 1). Elbow angles did not differ among species; however, forelimb protraction angles were significantly different, with A. montanus protracting to a lesser degree than the other species (Table 1). In all cases, A. montanus did not use forelimbs first landings, contributing to their greater forward translation (Fig. 1a), while the others consistently landed on their forelimbs (Fig. 1b, c).
Video footage from the terrestrial L. pakeka (Online Resource 6) and the semi-aquatic L. hochstetteri (Online Resource 7) indicates that delayed hindlimb recovery is a shared feature of leiopelmatids. Leiopelma spp. protract their forelimbs to a greater extent than does A. montanus. However, unlike the lalagobatrachians in this study, Leiopelma spp. abduct their forelimbs such that they do not land on them; although, their protracted position may serve to minimize skidding since there was less forward translation at landing.
Leiopelmatid frogs provide insight into the evolution of anuran jumping. It has been hypothesized that jumping evolved in a riparian context as a means of rapidly escaping (diving) into water (Gans and Parsons 1966). Our results are consistent with this hypothesis because late limb recovery and variable landing postures pose few problems for escape diving into water, but seem less suited to terrestrial environments. Nevertheless, as shown here, leiopelmatids do jump during terrestrial escapes, but not like other frogs. Landing forces are not directed through forelimbs as in lalagobatrachians studied to date, but are distributed across a range of ventral elements.
The unusual landing behavior of leiopelmatids may provide a functional explanation for some enigmatic morphological features. Their small body size limits the risk of exceeding safety factors of skeletal elements during landing. However, soft tissues (e.g., viscera or ova) could be damaged by uncontrolled landings, which may explain the presence (retention) of large, shield-shaped epipubic cartilages in leiopelmatids, as well as the novel inscriptional ribs of Leiopelma (Green and Cannatella 1993).
Our finding of a temporal separation of jumping and limb recovery in leiopelmatids suggests that the evolution of jumping in frogs was a two-step process with symmetrical hindlimb extension jumping appearing first and mid-flight hindlimb recovery and landing on adducted forelimbs appearing in the ancestor of lalagobatrachians. Studies of basal frogs have shown that swimming behavior has also evolved in a step-wise fashion at the same place on the phylogeny (Abourachid and Green 1999). We propose that an inability to rapidly cycle the hindlimbs provides a functional explanation for the absence of synchronous swimming in leiopelmatids.
The switch to lalagobatrachian landing and swimming behavior appears to have involved a simple evolutionary change in the timing of limb muscle motor patterns, shifting the onset of hindlimb flexors to an earlier point in the stride cycle. All else being equal, if A. montanus shifted the onset of recovery so that flexion began at mid-flight it would land on its limbs like other frogs. Thus, the simple shift to early hindlimb recovery may have been a key feature in the evolutionary history of frogs, facilitating controlled terrestrial landings and enabling rapid repetition of jumping and swimming cycles. These changes may have offered advantages for longer distance locomotion, better landing postures, and improved predator avoidance and foraging.
We thank Paul Brunkow, Mike Jorgensen, Sandra Nauwelaerts, Mike Paulin, James Robins, and John Scheibe for their comments and assistance. The Idaho Department of Fish and Game and United States Forest Service provided collecting permits. This work was supported by a Summer Research Fellowship and a Funded University Research grant from Southern Illinois University Edwardsville to RLE and an Ohio University Research Challenge grant to SMR.