Were early pterosaurs inept terrestrial locomotors?

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Introduction

  1. Did the large uropatagium of non-pterodactyloids restrict hindlimb function during terrestrial locomotion?

  2. Is the absence of non-pterodactyloids trackways related to their terrestrial capabilities?

  3. Were the limbs of non-pterodactyloids sprawled during terrestrial locomotion?

Materials and Methods

Systematic declaration

Material

Results

  1. Did the large uropatagium of non-pterodactyloids restrict hindlimb function during terrestrial locomotion?

    The inference that relatively large uropatagia impeded early pterosaur terrestrial habits has received no detailed evaluation, despite its confident presentation in some literature. (“There can be no doubt that this shackling of the limbs must have hindered pterosaurs as they sought to move around on the ground”—Unwin, 2005, p. 204.) It might be presumed that attributes of fossil pterosaur soft-tissues or observations on modern animals with similar membrane structures support this assertion, but it is only the relatively large size of early pterosaur uropatagia which is cited in favour of this idea (e.g., Unwin & Bakhurina, 1994; Unwin, 2005). While it is difficult to evaluate the effects of soft-tissues on non-pterodactyloid hindlimb kinematics in the absence of footprints, evidence from pterosaur body fossils, and the anatomy and behaviour of modern animals, conflict with proposals that expansive uropatagia impeded early pterosaur terrestriality.

    Many gliding and flying mammals possess large, hindlimb-spanning uropatagia comparable in size to those of non-pterodactyloids (Fig. 2). A number of these species are terrestrially proficient (e.g., Sollberger, 1940; Nowak, 1994; Stafford, Thorington Jr & Kawamichi, 2003; Riskin et al., 2006; Meijaard, Kitchener & Smeenk, 2006), some spending considerable amounts of time on the ground in pursuit of food or refuge using fast, complex and sometimes strenuous behaviours (Sollberger, 1940; Daniel, 1976; Nowak, 1994; Pyare & Longland, 2002; Riskin et al., 2006). These animals are not confined to barren habitats, predator-free environments or the result of reduced competition from other terrestrial creatures. Rather, they inhabit complex, predator-filled habitats and have persisted for many millions of years in some regions (Hand et al., 2009). Examples include the New Zealand lesser short-tailed bat, Mystacina tuberculata, which is reported as having “rodent-like agility on the ground and on trunks, branches, and kiekie vines” by Daniel (1976; p. 397). Common vampires, Desmodus rotundus, rely on their terrestrial skills to stealthily stalk hosts or quickly evade danger using forelimb-propelled galloping (Nowak, 1994; Riskin & Hermanson, 2005; Riskin et al., 2006). Flying squirrels, such as Glaucomys species, forage on the ground, are capable of running, and have membranes resilient to frequent digging for fungal food sources (Sollberger, 1940). Similarly, membranes of Mystacina bats withstand crevice-crawling, as well as digging (Daniel, 1979). Clearly, the grounded activities of these animals are not impeded by their patagia, nor do their membranes snag on obstacles or become easily damaged. Presumably, membrane elasticity plays a role in reducing impedance to terrestrial activity, both allowing the limbs to move freely as well as drawing the membranes close to the body to prevent interference with the environment. The extent of such membrane shrinkage can be extreme, rendering them almost indiscernible in some circumstances (Meijaard, Kitchener & Smeenk, 2006). Critically, while some membrane-bound extant animals are poor terrestrial locomotors, this has not been linked to membrane size or distribution, but instead to aspects of skeletal morphology, limb strength or myology (Riskin, Bertram & Hermanson, 2005).

    Certain bats and flying squirrels show that large uropatagia do not rule out terrestrial potential in volant mammals, but are they suitable models for pterosaurs? Fossils of pterosaur wing membranes suggest some similarities to those of modern volant mammals in that they were likely elastic in their proximal regions. Pterosaur brachiopatagia were stiffened by structural fibres distally, but other membrane components—including the uropatagium—lack rigid structural fibres and are widely considered to have been compliant (e.g., Padian & Rayner, 1993; Unwin & Bakhurina, 1994; Bennett, 2000; Frey et al., 2003). Unwin & Bakhurina (1994), describing the uropatagium of Sordes pilosus, comment specifically on this, stating “…adjacent to the body the [structural] fibres are shorter, more sinuous and loosely packed, indicating that the propatagium, uropatagium and proximal regions of the cheiropatagium were somewhat softer and more elastic” (p. 64). From this, it can be expected that all pterosaur membranes would contract significantly when the limbs were not extended to flight position, as occurs in many volant mammals, clearing them of obstacles and permitting stretching of the membranes during walking or running. Some evidence for this contraction may be seen in pterosaur fossils with preserved membranes (Elgin, Hone & Frey, 2011). Trackways made by running pterodactyloids indirectly demonstrate how elastic their proximal membranes must have been, allowing track makers to take strides of considerable magnitude (Mazin et al., 2003) despite membranes stretching from the distal hindlimb to their hands (Elgin, Hone & Frey, 2011). The expansion and contraction of brachiopatagia in running pterodactyloids was probably no greater than that experienced by non-pterodactyloid uropatagia during terrestrial activity.

    Even if the hindlimb strides of non-pterodactyloids were restricted by membranes, they were likely capable of circumventing this issue by using asymmetrical, bounding gaits (Witton & Habib, 2010; Witton, 2013; Hyder, Witton & Martill, 2014). Indeed, both the fore- and hindlimbs of pterosaurs have been noted for their strength and leaping potential (Padian, 1983a; Bennett, 1997b; Habib, 2008; Witton & Habib, 2010), and there are obvious parallels between forelimb-dominated Desmodus galloping and recent, compelling hypotheses concerning forelimb use in pterosaur launch (Habib, 2008). Pterosaurian bounding locomotion may be countered by exclusive trackway evidence for symmetrical gaits in pterodactyloids (e.g., Stokes, 1957; Mazin et al., 1995; Mazin et al., 2003; Lockley & Wright, 2003; Hwang et al., 2002), but it remains unclear if these gaits were employed by all pterosaurs, all the time, nor is it clear if interpretations of these tracks are applicable to non-pterodactyloids. Bounding gaits are at least tenable from a functional and biomechanical perspective.

    In light of these observations, the proposal that early pterosaurs were terrestrially hindered by their membranes is peculiar. It relies on the uncertain assumption that the uropatagium was especially restrictive compared to other pterosaur wing membranes and behavioural restrictions—membranes snagging on obstacles and limiting stride length—which have no precedent among modern pterosaur analogues. Clear evidence demonstrating broad uropatagia were barriers to early pterosaur terrestriality has yet to be presented, whereas what we know of pterosaur soft-tissues and modern animals with similar anatomy indicates that their membranes likely had little, if any, impact on terrestrial potential.

  2. Is the absence of non-pterodactyloids trackways related to terrestrial capabilities?

    The view that a lack of early pterosaur trackways must equate to their terrestrial ineptitude (e.g., Unwin, 2005; Butler, Benson & Barrett, 2013) relies on a very literal interpretation of the pterosaur fossil record and an assumption that we can distinguish genuine absences of fossil phenomena from biases affecting fossil datasets. There are reasons to consider both these assertions uncertain.

    The non-pterodactyloid body fossil record is not only poorer than that of pterodactyloids, but also many contemporary terrestrial tetrapod groups (e.g., Benton & Spencer, 1995; Kielan-Jaworowska et al., 2004). It is particularly impoverished in terrestrial basins (Butler, Benson & Barrett, 2013). This is thought to reflect the general lack of inland or near-shore pterosaur-bearing Lagerstätten before the Late Jurassic; the small body sizes and low preservation potential of early pterosaurs; a possibly restricted distribution of the group in its early history; or perhaps existence of the first pterosaurs in habitats unconducive to fossilisation and sediment accumulation—inland forests or upland environments (Bennett, 1997b; Unwin, 2005; Witton, 2013; Butler, Benson & Barrett, 2013). Regardless of the cause, recent studies have concluded that recorded patterns of Triassic and Jurassic pterosaur diversity—the interval dominated by non-pterodactyloids—have little statistical significance (e.g., Butler, Benson & Barrett, 2013; Upchurch et al., 2014), and that our understanding of early pterosaur history remains generally poor. This is difficult to reconcile with suggestions that the lack of early pterosaur fossils—specifically their track record—is somehow significant. If understanding of the early pterosaur record is demonstrably limited, how can any apparent trends or patterns in that data be confidently interpreted, and especially those reliant on an absence of data?

    It seems unwise to link the absence of a track record to a very specific cause, such as functional anatomy when there are a number of reasons why non-pterodactyloids may not have an ichnological record. If non-pterodactyloids were genuinely rare in terrestrial basins—as their record currently indicates—their likelihood of creating traces must also be low. Likewise, it seems most early pterosaurs were small, with wingspans of 1–2 m (O’Sullivan, Martill & Groocock, 2013) and corresponding masses of 0.55–3.26 kg (using data from Witton, 2008). Their footprints would thus be small and shallow, without substantial underprinting, and require exceptional conditions for impression, fossilisation and discovery. In contrast, pterodactyloids are generally larger bodied than early pterosaurs (Hone & Benton, 2007; Benson et al., 2014), which may constitute creation of deeper, longer-lasting tracks which are better suited to fossilisation and detection. A related problem concerns our ability to distinguish the footprints of pterodactyloids from those expected of non-pterodactyloids (Lockley, Harris & Mitchell, 2008): all pterosaurs have the same basic manus and pes structure, the only exception being the longer fifth toe in non-pterodactyloids. Given the role of this structure in supporting the uropatagium, it may have been held aloft when walking (Lockley, Harris & Mitchell, 2008). If so, the tracks of all pterosaurs might look similar, and some alleged Jurassic pterodactyloid ichnites may be misidentified.

    It should also not be assumed that early pterosaurs and pterodactyloids occupied ecologies with similar track-making potential. The start of the pterosaur footprint record in the Middle Jurassic roughly corresponds with the emergence of pterodactyloid clades predicted to be waders, suspension-feeders and molluscivores (ctenochasmatoids and dsungaripterids—Unwin, 2005; Witton, 2013). Such animals are expected to routinely patrol lake margins and other habitats suitable to footprint preservation in search of food. Lockley & Wright (2003) and Lockley, Harris & Mitchell (2008) note that pterodactyloid tracks are frequently associated with invertebrate traces and occasional feeding marks, which may indicate foraging was a common factor in pterosaur ichnite creation, inferring ecological influences on the delayed start of the pterosaur ichnological record. By contrast, non-pterodactyloids are largely perceived as pelagic piscivores or insectivores (Wellnhofer, 1975; Wild, 1978; Chatterjee & Templin, 2004; Ősi, 2011; Witton, 2008; Witton, 2013), neither of which are habits lending themselves to sustained terrestrial activity on mudflats, water margins or other settings liable to preserving footprints.

    Perhaps most importantly, early pterosaurs are not alone in having a very sparse track record. The tracks and traces of many fully terrestrial Mesozoic clades are surprisingly poorly known—examples include geographically widespread, long-lived lineages with good body fossil records, such as Mesozoic Mammaliaformes, tyrannosaurids and ceratopsids (Lockley & Hunt, 1995; Kielan-Jaworowska et al., 2004; McCrea et al., 2014). Not only are the ichnological records of these groups poor—restricted to single localities in some cases—but many ichnites referred to them are controversially identified (Kielan-Jaworowska et al., 2004; McCrea et al., 2014). This occurs despite these animals seemingly being abundant (as evidenced by their good body fossil records) and fully terrestrial in their habits, thus potentially creating tracks in virtually all of their activities (unlike pterosaurs, which, in being volant, avoided track creation much of the time). In contrast to perceptions of the pterosaur track record however, the sparse trackways of Mesozoic Mammaliaformes or certain dinosaur clades are not interpreted as signs terrestrial ineptitude, but as biases of behaviour, ecology, preservation, sampling or interpretation.

    Ultimately, while the absence of early pterosaur footprints is an intriguing phenomenon of the pterosaur record, and one with possible implications for the development of terrestriality in Pterosauria, its significance cannot be divorced from a number of factors unrelated to functional morphology. As with any case supported by negative evidence, data deficits can only be interpreted so far, especially when related datasets are demonstrably poor. Considering the absence of early pterosaur tracks as significant requires ignorance of not only statistics on the quality of the pterosaur fossil record, but also data concerning early pterosaur palaeobiology and the broader ichnological record. Other sources of evidence should be pursued for more reliable insights into the development of pterosaur terrestriality.

  3. Were the limbs of non-pterodactyloids sprawled during terrestrial locomotion?

    Postural sprawl and the use of rotatory limb mechanics has been proposed for grounded non-pterodactyloids from assessments of their limb joint arthrology (e.g., Wellnhofer, 1975; Unwin, 1988; Unwin, 1999; Unwin, 2005; Padian, 2008b). These suggestions have mostly applied to their forelimbs, but some have suggested that both limbsets were constrained to sprawling stances (Unwin, 1988; Unwin, 1999; Unwin, 2005). Unwin (1988) argued that the Dimorphodon femoral-pelvic joint projected the femur anterolaterally and somewhat dorsally when ‘naturally articulated’, while the tibiotarsus was capable of twisting medially at the knee, permitting the foot to face forwards. This is said to allow for semi-erect or sprawling stances, which are in accordance with suggested similarities between the pelves of Dimorphodon and the sprawling or semi-erect archosauriform Euparkeria capensis (Unwin, 1988). Computer modelling has also predicted entirely sprawling stances and rotatory gaits for non-pterodactyloids through a digital model of Rhamphorhynchus (Fig. 1B; Unwin, 2005). The methodology behind this has not been presented, but the resultant digital non-pterodactyloid model ‘Roborhamphus’ shows hindlimbs projecting entirely laterally from the body, similarly-sprawling forelimbs, low clearance from the ground and slow walking speeds (Unwin, 2005). The latter is seemingly a consequence of the limited reach afforded by the sprawling limbs.

    There are several reasons to think that the non-pterodactyloid hindlimb did not sprawl. Firstly, the assumption that a ‘natural articulation’ of the hindlimb can be determined from acetabulum and femoral head morphology (Unwin, 1988) is problematic. As evidenced by debates over ‘osteological neutral pose’ in fossil animal necks (e.g., Stevens & Parrish, 1999; Taylor, Wedel & Naish, 2009; Taylor & Wedel, 2013; Stevens, 2013), attempts to determine ‘neutral’ or ‘natural’ poses of animal joints rely on arbitrary assignments of optimal joint configurations which often have little or no significance to typical animal postures (Taylor, Wedel & Naish, 2009). It is probably unwise to suggest the hindlimb of Dimorphodon sprawled based on acetabulum and femoral head morphology alone.

    Secondly, the pelves of Dimorphodon and other early pterosaurs are clearly distinguished from those of Euparkeria and other sprawling animals in having a well-developed preacetabular process (Unwin, 1988; Hyder, Witton & Martill, 2014). In this respect, non-pterodactyloid pelves resemble those of other ornithodirans—including pterodactyloids—and mammals. These taxa are characterised by erect limbs, the preacetabular process anchoring large hip flexors for moving the hindlimb forward in the parasagittal plane (Hyder, Witton & Martill, 2014). Assessments of pterosaur hindlimb muscle mechanics seem to confirm that the pterosaur pelvic and femoral musculoskeletal system is optimally configured for an erect stance (Fastnacht, 2005; Costa, Rocha-Barbosa & Kellner, 2014). Furthermore, while arguments for bipedal, pronograde pterosaurs with parasagittal hindlimbs and digitigrade pedes (Padian, 1983a; Padian, 1985) have been largely criticised in recent years (e.g., Wellnhofer, 1988; Bennett, 1997a; Clark et al., 1998; Fastnacht, 2005—also see above), observations that their hip, knee and ankle articulations have hallmarks of upright limb functionality have been borne out by further study (Bennett, 1997b; Padian, 2008a; Padian, 2008b; Fastnacht, 2005; Costa, Rocha-Barbosa & Kellner, 2014).

    Thirdly, virtually all recent models of pterosaur evolution suggest taxa with erect hindlimbs bracket non-pterodactyloids, with Scleromochlus taylori and non-pterosaurian ornithodirans on one side, and pterodactyloids the other (Sereno, 1991; Benton, 1999; Hone & Benton, 2008; Nesbitt, 2011; but also see Bennett, 2013). This implicates erect hindlimb postures as probably ancestral for Pterosauria and, given the similarity of their pelvic and hindlimb osteology to their nearest probable relatives, there is little reason to assume non-pterodactyloids deviated from this ancestral state (Bennett, 1997b; Padian, 2008a; Hyder, Witton & Martill, 2014). It seems that multiple lines of evidence indicate erect hindlimbs across Pterosauria, including all known non-pterodactyloids.

Discussion

Other indications of terrestrial competency in non-pterodactyloids

The terrestrial proficiency of early pterosaurs

Concluding remarks

Additional Information and Declarations

Competing Interests

The author declares there are no competing interests.

Author Contributions

Mark P. Witton conceived and designed the experiments, performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.

Funding

The author declares there was no funding for this work.

 
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Several papers and a website by Peters (see below) address several problems ignored by this manuscript/paper including:

  1. Basal pterosaur ichnites (they are known, have been published and non are quadrupedal, some are digitigade)
  2. The origin of pterosaurs (among bipedal fenestrasaurs each with uropatagia, trailing each hind limb. Objections to this scenario by Hone and Benton (2007, 2008)...
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