sign in sign up
<<
Home , Anhanguera (pterosaur), Anurognathus, Archaeopterodactyloidea, Azhdarchoidea, Batrachognathus, Beipiaopterus

Journal of Systematic Palaeontology, Vol. 9, Issue 3, September 2011, 337–353

Evolution of morphological disparity in Katherine C. Prentice, Marcello Ruta∗ and Michael J. Benton School of Earth Sciences, University of Bristol, Wills Memorial Building, Queens Road, Bristol, BS8 1RJ, UK (Received 9 November 2009; accepted 22 October 2010; printed 15 September 2011)

Pterosaurs were important flying for most of the , from the Late to the end of the (225–65 Ma). They varied enormously through time in overall size (with spans from about 250 mm to about 12 m), and in features of their cranial and postcranial skeletons. Comparisons of disparity based on discrete cladistic characters show that the paraphyletic rhamphorhynchoids (Triassic–) occupied a distinct, and relatively small, region of morphospace compared to the derived pterodactyloids (Late –). This separation is unexpected, especially in view of common constraints on anatomy caused by the requirements of flight. Pterodactyloid disparity shifted through time, with different, small portions of morphospace occupied in the and Late Cretaceous, and a much larger portion in the Early Cretaceous. This explosion in disparity after 100 Ma of is matched by the highest diversity of the : evidently, pterosaurs express a rather ‘top heavy’ clade shape, and this is reflected in delayed morphological evolution, again an unexpected finding. The expansion of disparity among pterodactyloids was comparable across subclades: pairwise comparisons among the four pterodactyloid superfamilies show that, for the most part, these significant morphological separation, except in the case of and . Finally, there is no evidence that rhamphorhynchoids as a whole were outcompeted by pterodactyloids, or that pterosaurs were driven to by the rise of . Keywords: pterosaurs; disparity; diversity; rhamphorhynchoids; pterodactyloids; morphospace

Introduction on incomplete remains, especially for Arambourgiania and Hatzegopteryx, there is no question that pterosaurs include Flight evolved several times in the history of vertebrates. the largest flying of all time, exceeding to a consid- Birds, and the wholly extinct pterosaurs illustrate erable degree the largest flying birds, such as the extant the truly astounding range of body sizes, proportions and wandering (up to 3.4 m ; mass 7.36 kg; biomechanical adaptations that permitted the conquest of Henderson 2010) and the late Miocene condor the air. Pterosaurs were the first vertebrates to use powered (6.4 m) (e.g. Chatterjee et al. 2007, and references therein). flight, following several earlier experiments in gliding Among the most remarkable features of pterosaurs among basal diapsid amniotes (e.g. weigeltisaurids in the is their wing skeleton, composed of powerful proximal Late ; kuehneosaurids in the ; see elements (, and ) and an elongate fourth Evans & Haubold 1986; Brinkman 1988; Schaumberg et al. . The wing membrane extended the full length of the 2006; Stein et al. 2008). Pterosaurs range in size from and fourth digit, and attached down the side of the the tiny , with a 250 mm wingspan (Wang body and proximal . A further, smaller membrane 2008), to giants such as , with a wingspan extended in front of the arm from the side of the torso. The estimated at 10–12 m (Fig. 1) and Arambourgiania and earliest known pterosaurs from the Late Triassic, some 225 Hatzegopteryx, which are similar in size or only slightly million old, already possessed these flying adapta- smaller than Quetzalcoatlus (Lawson 1975; Frey & Martill tions. At present, we do not know of any flightless and/or 1996; Buffetaut et al. 2002; for recent estimates of the partly flying precursors. The skeleton evolved a in these taxa, see articles in Hone & Buffe- great deal through the 150 ma of history of the group, taut 2008). Pterosaur body mass is harder to estimate, but with substantial changes in the length of the neck and tail, a recent study (Henderson 2010) using detailed considera- vertebral numbers in the trunk, strengthening elements in tions of anatomy and relative densities in hypothetical slices the regions of the pectoral and pelvic girdles, and details through pterosaur bodies yielded mass estimates from 4 g of the forelimbs and (e.g. Seeley 1901; Unwin () to 544 kg (Quetzalcoatlus), an astonish- 2005). Pterosaur morphological diversity is also evident ing range. Although maximum size estimates are based in their dentition. For example, basal pterosaurs had sharp

∗Corresponding author. Email: [email protected]

ISSN 1477-2019 print / 1478-0941 online Copyright C 2011 The Natural History Museum DOI: 10.1080/14772019.2011.565081 http://www.informaworld.com 338 K. C. Prentice et al.

Figure 1. Extremes in pterosaur morphology. The giant and probably flightless Quetzalcoatlus from the Late Cretaceous of was as tall as a giraffe. The small insectivorous Anurognathus from the Late Jurassic of Germany is seen flying above the artist’s head. Drawings by Mark Witton. and pointed teeth, which in some groups became elon- tionally, pterosaurs have been divided into two suborders, gate and fang-like, presumably for catching fish; later and , with rham- pterosaurs showed a much greater array of tooth morpholo- phorhynchoids forming a paraphyletic assemblage of taxa gies, including with stout mollusc-cracking relative to the monophyletic pterodactyloids. Some 120 teeth, with over a thousand fine teeth for siev- of pterosaurs from 240 localities (Barrett et al. ing out small or larvae from water, and 2008; Butler et al. 2009) have been named since the first with no teeth (Unwin 2005). discovery of a member of this group in 1784; about 40 Pterosaurs form part of the radiation of diap- species are classed as rhamphorhynchoids and 80 as ptero- sids, and appear to be phylogenetically close to dactyloids. Cladistic analyses of pterosaurs (e.g. Kellner according to the majority of cladistic analyses (e.g. Gauthier 2003; Unwin 2003, 2005; Wang et al. 2005; Lu&Ji¨ 1986; Benton & Clark 1988; Sereno 1991; Benton 1999; 2006; Andres & Ji 2008; Lu¨ et al. 2010) have lent support Brochu 2001; Hone & Benton 2007a). However, some to rhamphorhynchoid and pterodactyloid mono- authors have hypothesized that their origins occur deeper phyly. In addition, most analyses retrieve four monophyletic among basal Archosauria (e.g. Bennett 1996), or basal pterodactyloid superfamilies, namely Dsungaripteroidea, Archosauromorpha close to Prolacertiformes (e.g. Peters Ornithocheiroidea, Azhdarchoidea and Ctenochasmatoidea 2000). Hone & Benton’s(2008) weighted supermatrix anal- (Unwin & Lu¨ 1997; Kellner 2003; Unwin 2003; Lu¨ et al. ysis places pterosaurs at the base of Archosauria. Tradi- 2010); however, Bennett (1989) recognized Nyctosauridae Evolution of morphological disparity in pterosaurs 339 instead of Ctenochasmatoidea, and Andres & Ji (2008) each character set (e.g. cranial versus postcranial) entailed erected for the group including in terms of morphological variety of different clades. These ctenochasmatids and their closest relatives. studies are thus necessary in to clarify how changes Rhamphorhynchoids include basal taxa mostly from the in disparity relate to changes in diversity, and whether there Late Triassic and , although some survived might be any validity in commonly assumed explanations into the Late Jurassic and Early Cretaceous (Unwin 2003, and hypothesized scenarios for competitive clade replace- 2005). Pterodactyloids continued to radiate throughout the ments. Points (2) and (3) above are discussed briefly at the Jurassic and Early Cretaceous, with a diversity peak of end of this paper (for additional information see Unwin 20 taxa in the Late Jurassic and 35 in the Early Creta- 2005; McGowan & Dyke 2007; Butler et al. 2009). Points ceous (Butler et al. 2009). Pterosaurs dwindled substan- (1) and (4) form the core of the present investigation. The tially in diversity through the Late Cretaceous, with only issue of how pterosaurs acquired their unique characters the giant azhdarchids and nyctosaurids surviving to the end- is beyond the scope of the present investigation (but see Cretaceous mass extinction (Witton & Naish 2008; Butler et Benton 1999 and references therein). al. 2009; Witton et al. 2009). The pattern of dramatic peaks and drops in species- and -level diversity through the Mesozoic is surely largely artificial (Butler et al. 2009), Material and methods reflecting abundant sampling in Lagerstatten¨ such as the Late Jurassic Solnhofen Formation of Pterosaur data matrix Germany and the Early Cretaceous Santana Formation of Of the numerous cladistic studies available for pterosaurs and Jehol Group of China. However, the startling (e.g. Unwin 2003, 2005; Kellner 2003; Wang et al. 2005; reduction of the group’s diversity to two families in the Andres & Ji 2008; Lu¨ et al. 2008, 2010), we chose that of Late Cretaceous may be genuine (Unwin 2005; Butler Lu¨ & Ji (2006) because it includes the most recent complete et al. 2009). Inadequacies of the fossil record, such as matrix in terms of both taxonomic sampling and charac- missing and incomplete taxa (Butler et al. 2009), are poten- ter selection. In contrast, Andres & Ji’s (2008) analysis tially limiting for studies of diversification through time covers only Pterodactyloidea, while that of Lu¨ et al. (2008) – at least when observed data only are considered, i.e. includes many fewer taxa and characters. The nature of the without phylogenetic interpolation (e.g. Smith 1994) – present article is purely exploratory. Therefore, we have not but less so for considerations of patterns of morphologi- attempted to merge existing datasets, because we wanted to cal evolution, where even a single excellent specimen can avoid the risk of inflating possible errors from incorrect provide a wealth of morphological and phylogenetically coding. In this respect, the data matrix supplied by Lu&Ji¨ informative detail. (2006) represents a ‘baseline’ study, and conclusions from the present work ought to be regarded exclusively in the context of their and character selection. Aims Lu¨ & Ji’s(2006) matrix consists of 56 taxa (three of which are non-pterosaurian outgroups) and 80 skeletal characters. The contrast between the seemingly conserved morphol- In our analyses, all characters were treated as unordered ogy of rhamphorhynchoids and the much greater range of and having equal unit weight, equating to Fitch parsimony, body shapes and sizes among pterodactyloids shows an where it is assumed that all changes between character states apparent match in the number of taxa belonging to the two are equally probable. groups. It is important to understand pterosaur diversity ( = taxonomic abundance) and disparity ( = range of morpho- Disparity logical variety) through the Mesozoic for several reasons: Disparity is a term widely (albeit not always consistently) (1) to shed light on the broad patterns of major evolution- used to describe the range of forms in a group of organisms, ary radiations among , particularly following the or the difference among different body plans (e.g. Gould acquisition of key evolutionary innovations, such as those 1989, 1991; Wills et al. 1994; Foote 1997a). Disparity may related to flight; (2) to assess whether different groups of be measured using one of two broad categories of data. pterosaurs outcompeted each other through the Late Juras- The first category consists of landmarks (widely used in sic and earliest Cretaceous (Colbert 1980; Unwin 1988, geometric morphometrics), outlines (e.g. eigenshape analy- 2005); (3) to consider further the widely held view that sis), or physical measures (e.g. lengths, angles), all of which pterodactyloids were driven to large size in the Late Creta- capture different aspects of shape variation. The second ceous, and eventual extinction, by competition with birds category encapsulates information on shape diversity indi- (Romer 1966; Colbert 1980; Unwin 1988, 2005; Penny rectly, specifically as alternative character conditions or as & Phillips 2004; Slack et al. 2006); and (4) to determine presence/absence scores (including threshold values that whether different portions of pterosaur skeletal anatomy discriminate among different relative proportions), usually experienced differential rates of character change, and what tabulated in a data matrix. 340 K. C. Prentice et al.

The two categories of data type are both relevant to anal- i.e. cranial (characters 1–43), total postcranial (characters yses of morphospace occupation and patterns of within- 44–80), forelimb (characters 59–76), and hindlimb (charac- and between-group disparity, and are complementary rather ters 77–80), all from Lu¨ & Ji (2006). As concerns character than mutually exclusive (e.g. Wills et al. 1994; Ruta 2009). partitions, we point out that comparisons among different Descriptors in the first category may not necessarily corre- plots of taxa in morphospace are of a semiqualitative nature. spond to heritable traits in the cladistic sense (i.e. hier- Multivariate treatments of Euclidean inter-taxon distances archical internested sets of shared derived features that differ, as they are conducted on subsets of the original data change their condition at different levels of a phylogeny), matrix. For convenience, we discuss these different plots at and there is no consideration of whether they might repre- once (e.g. rarefaction curves of mean disparity values for sent primitive or derived conditions. Cladistic characters each data partition), but the reader should not draw general- permit ready comparisons among taxa from different and ized conclusions from such comparisons as input data differ morphologically varied taxonomic groups (Wills et al. with each partition. 1994; Wills 2001). Such taxonomic groups need not be The analytical protocols are similar to those used by Wills clades (Wills 2001); thus, any assemblage of taxa may be et al. (1994), Brusatte et al (2008a), Ruta (2009) and others. compared with any other such assemblage. As an exam- The original data matrix of Lu¨ & Ji (2006) was transformed ple, a researcher may identify clusters of taxa display- using the software MATRIX(Wills 1998) to produce a tabu- ing some functional, ecological, geographical or temporal lation of inter-taxon Euclidean distances. The multivariate cohesion that relates to the macroevolutionary questions package (Bouxin 2005) was used to perform a under consideration. For these reasons, the most obvious principal coordinates analysis (PCoA) on such distances, comparison among pterosaurian groups is between rham- using the centroid of all taxa as the origin of the multivariate phorhynchoids and pterodactyloids. Discrete monophyletic axes, and with Lingoes’ (1971) method of negative eigen- groups within rhamphorhynchoids – such as those retrieved value correction. From the PCoA outputs (PCo scores, i.e. in some cladistic analyses – are not amenable to compar- coordinates of taxa on the multivariate PCo axes), disparity isons as the taxonomic samples are too small. Cladistic indexes were calculated. There is no single best measure characters further document unique morphological features of disparity that is not affected by sample size, number of of clades, and thus permit exploration of supposed key characters, and/or percentage of missing data (Ciampaglio adaptations or key innovations, i.e. those morphological et al. 2001). Therefore, two metrics were used here: (1) the novelties that are often hypothesized to have driven, or sum of variances, which is used to measure the dispersal of ensured, the success of a particular clade (discussions in taxa within morphospace (Foote 1997b; Ciampaglio et al. Gould 1991; Wills et al. 1994; Foote 1996; Erwin 2007). 2001; Villier and Korn 2004; Erwin 2007; Ruta 2009); and The present study uses discrete characters to summarize (2) the sum of ranges, which indicates the amount of overall patterns of morphological evolution among major groups morphospace occupation (Wills et al. 1994; Wills 1998). of pterosaurs. The results (i.e. quantification of disparity; The PCoA outputs were analysed using the software models of morphospace occupation) are contingent upon RARE (Wills 1998), which produced the disparity metrics the data matrix employed, and ought to be regarded as and the rarefaction disparity profiles. The settings were: (1) empirical (sensu McGhee 1999; see also Wills et al. 1994; use of the first two PCo axes for representations of taxa Brusatte et al. 2008a, b; Ruta 2009). By empirical, we in morphospace; (2) bootstrapping re-sampling using 1000 mean that disparity values and morphospace occupation replicates; (3) 95% confidence intervals; and (4) reconstruc-

are determined by the chosen parameters (taxa and char- tion of full rarefaction profiles using a minimum of two acters) and are thus data-dependent (namely, based upon taxa, and a maximum corresponding to the total number observed morphologies). of taxa being examined in each calculation. Rarefaction curves (e.g. Foote 1992), shown exclusively for the sum of Disparity protocols in the present study ranges, are used to standardize disparity measures accord- Disparity values were compared according to various parti- ing to sample size, and help visualize the rate at which tions of our taxonomic and character samples: (1) disparity mean disparity values change with increasing numbers of in the two major groups, Rhamphorhynchoidea and Ptero- taxa (Gotelli & Colwell 2001). dactyloidea; (2) disparity through geological time, with taxa To evaluate the statistical significance of the degree of assigned to Triassic, Jurassic, Early Cretaceous and Late separation among groups in morphospace, we employed Cretaceous time bins; such bins provide the best balance npMANOVA (non-parametric multivariate analysis of between sample size and time resolution (Foote 1994); variance; Anderson 2001) with calculations performed in (3) disparity in the four major pterodactyloid subclades, PAST (Hammer et al. 2001). The npMANOVA is designed Dsungaripteroidea, Ornithocheiroidea, Azhdarchoidea, and to test for the significance of differences among the Ctenochasmatoidea (after Unwin & Lu¨ 1997; Kellner 2003; variances of groups, but it is more versatile than standard Unwin 2003); and (4) disparity based upon characters MANOVA in that it can be applied to samples of values associated with different regions of the skeletal system, that do not conform to a normal distribution. Finally, to Evolution of morphological disparity in pterosaurs 341 assess the proximity of the problematic pterodactyloid taxon youngi to either Ctenochasmatoidea or Ornithocheiroidea, a Kruskal–Wallis test was carried out using PCo Euclidean distances.

Results

The two major pterosaur suborders Morphospace occupation for all 53 pterosaur taxa (Fig. 2) shows substantial differences between the two major subor- ders. The principal coordinates axes 1 and 2 represent cumu- latively 9.23% of overall variance (PCO 1: 5.22%; PCO 2: 4.01%) with negative eigenvalue correction, and 62.39% of overall variance (PCO 1: 37.56%; PCO 2: 24.83%) without correction; for disparity calculations, we also considered PCO 3 (2.82% of overall variance with negative eigenvalue correction, 12.37% without). Rhamphorhynchoids occupy a much more restricted and compact area of morphospace than pterodactyloids, where their distribution also appears Figure 2. Empirical two-dimensional morphospace for all 53 to be more even. The rhamphorhynchoid region of pterosaurian taxa included in this study, based on principal coor- morphospace also encompasses the three outgroup taxa. dinates 1 and 2. Red squares, rhamphorhynchoids; blue circles, Pterodactyloids show a broader and more heterogeneous pterodactyloids; yellow squares, outgroups. The two pterosaurian scatter of taxa; in particular, we note the occurrence of suborders occupy remarkably different regions of morphospace in terms of size, and spread of taxa. Note also how the primitive rham- several extreme morphologies (‘outliers’) that contribute phorhynchoids are proximal to the outgroups. Numbered taxa are: substantially to the total range of this suborder. Outgroups (n = 3: 1, Ornithosuchus longidens;2,Herrerasaurus Rarefaction plots (Fig. 3A) indicate that rhamphorhyn- ischigualastensis;3, taylori); Rhamphorhynchoids choids (given the chosen dataset) achieved maximal dispar- (n = 13: 4, buffarinii;5, pilosus;6, ity very rapidly, despite their small sample size, and macronyx;7, banthensis;8,Rham- phorhynchus longicaudus;9, muensteri; 10, the values for the sum of ranges are consistently much crassirostris; 11, Dendrorhynchoides curviden- smaller than those of pterodactyloids for comparable taxon tatus; 12, volans; 13, ningchen- numbers. Fig. 4A quantifies mean disparity values for gensis; 14, Anurognathus ammoni; 15, Campylognathoides liasi- the two groups. The rarefaction profile for pterodacty- cus; 16, ranzii); Pterodactyloids (n = 40: 17, loids increases steeply up to and well beyond the maxi- Liaoxipterus brachyognathus; 18, mesembrinus; 19, Liaoningopterux; 20, blittersdorffi; 21, Feilongus mum sample of rhamphorhynchoids, and the curve never youngi; 22, sethi; 23, Tapejara imperator; 24, quite flattens out. This suggests the interesting possibility Anhanguera santanae; 25, Anhanguera piscator; 26, Nurhachius that additional pterodactyloid taxa would increase overall ignaciobritoi; 27, latidens; 28, Haopterus gracilis; disparity of the group even further, although this hypothesis 29, Noripterus complicidens; 30, Pteranodon longiceps; 31, requires a stringent test in the light of a more comprehensive gui; 32, Eopteranodon lii; 33, Phobetor parvus; 34, Sinopterus dongi; 35, Chaoyangopterus zhangi; 36, taxonomic sample. leonardi; 37, Eoazhdarcholia oxiensis; 38, ; 39, Huaxiapterus jii ; 40, Dsungaripterus weii; 41, Gallodactylus canjuerensis; 42, gracilis; 43, Boreopterus cuiae; 44, Disparity through time Jidapterus edentus; 45, Zhejiangapterus linhaiensis; 46, Quet- Through geological time, pterosaurs show highest dispar- zalcoatlus sp.; 47, Pterodactylus antiquus; 48, Pterodactylus ity in the Early Cretaceous (Fig. 3B, 4B). However, these kochi; 49, rhamphastinus; 50, Germanodacty- results may indicate that taxa are considerably undersam- lus cristatus; 51, Cycnorhamphus suevicus; 52, pled during time intervals other than the Early Cretaceous. gracile; 53, Pterodaustro guinazui; 54, Azhdarcho lancicollis; 55, chenianus; 56, Eosipterus yangi). These were the times of the rise and decline of pterosaurs as a whole, when numbers of specimens and numbers of species were low (Butler et al. 2009). It will therefore be through geological time (data not shown for brevity), rham- interesting to see whether new finds of Triassic and Late phorhynchoids from the Triassic, Jurassic and Early Creta- Cretaceous pterosaurs have a more marked effect on total ceous all significantly overlap in morphospace, indicating morphospace than new Late Jurassic and Early Cretaceous no significant change in patterns of morphospace occu- finds. Fig. 4B shows mean disparity values in the four time pation through time (p < 0.05). However, pterodactyloids intervals of interest. When the two suborders are compared show a different pattern: the large Early Cretaceous region 342 K. C. Prentice et al.

Figure 3. Rarefaction curves of mean disparity value of the sum of ranges, calculated for different subdivisions of the pterosaurian data set. Comparisons of rarefaction curves are illustrated for: A, the suborders Pterodactyloidea and Rhamphorhynchoidea; B, four major time intervals; C, four superfamilies of Pterodactyloidea; D, four categories of morphological characteristics for all pterosaurs.

Figure 4. Morphological disparity for different subdivisions of the pterosaurian dataset. Mean disparity values, based on the sum of ranges, are shown together with error bars representing 95% confidence intervals, obtained with 1000 bootstrap replicates. Comparisons of mean disparity values are illustrated for: A, the two suborders of pterosaurs; B, four major time intervals; C, four superfamilies of Pterodactyloidea; D, four categories of morphological characteristics for all pterosaurs. Abbreviations: Azhdarc., Azhdarchoidea; Ctenoch., Ctenochasmatoidea; Dsungar., Dsungaripteroidea; E. Cretac., Early Cretaceous; L. Cretac., Late Cretaceous; Ornitho., Ornithocheiroidea. Evolution of morphological disparity in pterosaurs 343 of morphospace overlaps with both Jurassic and Late Creta- general conclusions regarding the separation among the ceous regions (Jurassic, p = 0.4095; Late Cretaceous, four superfamilies. Thus, if Feilongus youngi is placed in p = 1), but these two are significantly separate (p = 0.0225), the Ctenochasmatoidea, then there is no significant separa- indicating a substantial shift in morphospace through tion between Ornithocheiroidea and Ctenochasmatoidea (p time. = 0.063), but if it is placed in the Ornithocheiroidea, then a significant separation occurs between those superfamilies Pterodactyloid superfamilies (p = 0.0078). Finally, a Kruskal–Wallis test devised to test Rarefaction curves for the four pterodactyloid superfami- differences in mean values of PCo Euclidean distances of lies are shown in Fig. 3C. The curves for Azhdarchoidea and Feilongus from Ornithocheiroidea and Ctenochasmatoidea, Ctenochasmatoidea are tightly appressed to one another, returned a non-significant result (p = 0.847). and are almost invariably higher than the curves that relate to Ornithocheiroidea and Dsungaripteroidea. Furthermore, Character partitions all curves rise quite steeply and never reach a plateau. Once again, we stress that the comparisons among mean Comparisons among mean disparity values for the four disparity values for pterosaurs as a whole using character superfamilies (Fig. 4C) show that Dsungaripteroidea are partitions (Fig. 4D) and rarefaction curves based upon those considerably less disparate than other groups (certainly partitions (Fig. 3D) are only of a semiqualitative nature. The given their more limited taxonomic samples). However, results from the partitions have been plotted together only we note that confidence intervals around the mean values for convenience. Thus, observed differences merely reflect for the four superfamilies largely overlap one another. the different sizes of the character submatrices: hindlimb The areas of morphospace occupied by the four super- (4), forelimb (18), cranial (43) and total postcranial (37). families are colour-coded in Fig. 5. A npMANOVA test The only noteworthy point is the fact that, when hindlimb indicates that the Ornithocheiroidea, Azhdarchoidea and characters are used, the rarefaction curve does not plateau Ctenochasmatoidea are all significantly separated from out. However, in the case of each of the remaining parti- < each other in morphospace (p 0.05), but that there is tions, increasing the number of taxa does not result in a no significant separation between the Dsungaripteroidea remarkable increase in mean disparity values, and all curves = and Azhdarchoidea (p 1). The controversial inter- tend to reach a plateau. Fig. 6 shows two-dimensional plots pretation of one particular taxon, Feilongus youngi,as for all the rhamphorhynchoids and pterodactyloids consid- either an ornithocheiroid or a ctenochasmatoid impacts the ered in this study, based upon different character partitions (see also discussion below). Note how, in most cases, the two suborders are clearly separate, suggesting that different character subsets yield a similar signal.

Discoveries and changing patterns of disparity We were interested in the impact of discovery of new pterosaur taxa on the overall pattern of morphospace occu- pation. To this purpose, we divided the pterosaur sample

from Lu¨ & Ji (2006) into five time bins of approximately five decades each encompassing the dates on which taxa were named. We then processed cumulative taxon samples through time so that, for instance, time bin 3 includes all taxa from that time interval plus those from all preceding intervals. We constructed cumulative rarefaction curves for each set of calculations and built cumulative morphospaces accordingly. We stress that these calculations rely upon the inter-taxon Euclidean distances from the whole Lu&Ji¨ (2006) matrix. In short, we did not recalculate Euclidean distances for subsets of taxa from the full data matrix. Instead, we performed PCoA on the original Euclidean Figure 5. Empirical two-dimensional morphospace for all ptero- distances, but excluding every time those taxa that did not dactyloids included in this study, based on principal coordinates 1 and 2; the four pterodactyloid superfamilies are colour-coded, as belong to the cumulative time bin samples (see also Wills follows: Ornithocheiroidea in blue, Ctenochasmatoidea in yellow, et al. 1994; Ruta 2009). Azhdarchoidea in red, Dsungaripteroidea in green. The species It is not unexpected that morphospace occupation Feilongus youngi is marked by an orange circle. changed and expanded as successive cohorts of newly 344 K. C. Prentice et al.

Figure 6. Empirical two-dimensional morphospace for all 53 pterosaurs included in this study, produced using different character partitions, and based on principal coordinates 1 and 2. The rhamphorhynchoid morphospace areas (red) are always smaller than those of pterodactyloids (blue) for: A, total postcranial; B, hindlimb; C, forelimb; and D, cranial character sets. named pterosaurs were added to the sample (Fig. 7A–E); Discussion the profiles of disparity at each sampling interval also show a dramatic increase (Fig. 7F). Progressively higher curves Comparing rhamphorhynchoids and in the diagram refer to cumulative numbers of taxa. The pterodactyloids curves for the last two time bins are closely appressed and The two pterosaur suborders clearly differ in many respects, much higher than those related to the previous bins. This and analysis of disparity adds to this picture. The differ- suggests that recently described taxa have impacted levels ences cannot be explained by group status (paraphyletic of disparity considerably. Outstanding pterosaur finds from rhamphorhynchoids versus monophyletic pterodactyloids), China are likely to have contributed to this effect, causing a number of taxa (rarefaction shows rhamphorhynchoids are doubling in mean disparity for comparable numbers of taxa at maximal disparity, given the sample size), geological from previous time periods. duration (both groups existed for approximately the same Evolution of morphological disparity in pterosaurs 345

Figure 7. A–E, progressive occupation of morphospace through research time. The plots of principal coordinates axes 1 and 2 show sequential changes in morphospace occupation as new pterosaurian discoveries are accrued, through research time, up to A, 1840; B, 1870; C, 1973; D, 1997; and E, 2005. F, rarefaction of the five samples, from time bin 1 (pterosaurs named up to 1840) to time bin 5 (pterosaurs named 1998–2005), showing the substantial effect of new taxa, but with evidence of levelling-off from 1974 onwards (time bins 1 + 2 + 3 + 4). Pterosaur taxa from each time bin are colour coded, as follows: 1812–1849 (green), 1851–1875 (yellow), 1876–1973 (light blue), 1974–1997 (purple), and 1998–2005 (dark blue). time: 100 ma for rhamphorhynchoids; 105 ma for ptero- ing, especially in light of the common constraints on dactyloids), or geographical range (both groups existed morphology imposed by flight (Hazlehurst & Rayner 1992; essentially worldwide). Norberg 1994). Of course, our study uses discrete charac- The complete separation of the rhamphorhynchoid and ters as a basis for disparity calculations, and it might be pterodactyloid regions of morphospace (Fig. 2) is intrigu- argued that shared shape characters, such as those imposed 346 K. C. Prentice et al. on the by flight demands, could only be detected by that the shorter innermost part of the wing in rhamphorhyn- physical shape measurements. However, McGowan & Dyke choids indicates mixed gliding and flapping flight capabil- (2007) identified significant differences in disparity among ities, while the longer innermost part of the wing in ptero- the forelimbs and hindlimbs of pterosaurs, birds and bats, dactyloids indicates static and dynamic soaring. based on measurements of relative proportions of different The two suborders may have differed also in their modes components of the skeleton. This result differed from of . For example, Unwin (1987, 2005) those of Rayner (1988) and Hazlehurst & Rayner (1992), suggested that rhamphorhynchoids had limited walking who found considerable overlap among pterosaurs, birds abilities on the ground, but were able to climb trees or and bats in forelimb proportions. Thus, the differences cliffs. Pterodactyloids, on the other , may have been found by McGowan & Dyke (2007) could be accounted good walkers, some were possibly waders, and others may for by the fact that they coded a mixture of forelimb and have stalked their prey on foot (Langston 1981; Unwin hindlimb characters. Our study by anatomical partition (Fig. 2005; Witton & Naish 2008). Agile walking required a 6) confirms the conclusion of McGowan & Dyke (2007), forelimb that was strong enough to support the anterior albeit in the light of cladistic features rather than physical part of the body while enabling movement. Further, Einars- measurements: the two pterosaur suborders occupy separate son (2006) noted that rhamphorhynchoids had longer claws areas of morphospace based on all four anatomical char- on their fingers than their toes, interpreted as an adaptation acter partitions, including forelimb characters, and exhibit for climbing trees, whereas pterodactyloids had claws of only a slight overlap when cranial characters alone are used equal length fore and aft, and so probably could not climb. (Fig. 6D). The two suborders differ also in cranial characters, One possible conclusion from our results is that rham- although our disparity analyses show a slight overlap in phorhynchoids and pterodactyloids differed substantially in morphospace (Fig. 6D). The two taxa that come closest their mode of flight. In plots of aspect ratio against wing are the rhamphorhynchoid Rhamphorhynchus muensteri loading for several species of pterosaurs, Hazlehurst & and the pterodactyloid Gallodactylus anjuersensis, both Rayner (1992) found that rhamphorhynchoids generally had characterized by the possession of long teeth that were lower wing loadings than pterodactyloids, indicating slower well spaced on the jaw line – an adaptation for catching flight speeds, greater manoeuvrability, and better soaring fish. Rhamphorhynchoids had a limited range of dentitions, performance. Hazlehurst & Rayner (1992) reconstructed mainly consisting of long needle-shaped teeth projecting rhamphorhynchoids with short and deep wing profiles from the jaw margins, although some basal forms such compared to the relatively longer and narrower wings of as Eudimorphodon show heterodont dentition. Pterodacty- pterodactyloids, a standard view at the time (Wellnhofer loids, on the other hand, exhibit a wide spectrum of tooth 1978; Padian & Rayner 1993). These authors suggested that shapes and sizes, including closely spaced needle-like teeth, pterodactyloid wing membranes had no connection to the well spaced needle-like teeth, baleen-like slender teeth (e.g. hindlimb, and so wing depth was no greater than the length Pterodaustro) for straining food from water, teeth occur- of the torso. The posterior margin of the rhamphorhynchoid ring only in sections of the jaws, and even no teeth at wing membrane attached to the leg, perhaps as far down as all in pteranodontids and azhdarchids. Rhamphorhynchoids the ankle, thus potentially doubling the depth of the wing. were largely fish-eaters, although some (e.g. Anurognathus) However, this apparent distinction between deep-winged may have been insectivores. The diet of different species of rhamphorhynchoids and slender-winged pterodactyloids pterodactyloids, on the other hand, probably included fish, may not be so sharp after all: the Vienna specimen of shellfish, fruit, carrion and insect and larvae Pterodactylus shows its wing membrane attached to the (Unwin 2005). (Unwin 2005; Witton 2008). Further morphological disparity among pterodactyloids There are other differences between rhamphorhynchoids is seen in the astonishing diversity of cranial crests, some and pterodactyloids. For example, the hindlimb to fore- on the snout and others on the back of the head, some limb ratios of rhamphorhynchoids are similar to those made entirely from bone and others supporting a membrane, seen in bats, whereas those of pterodactyloids are much which would have been highly visible (Fig. 8). It has been higher (Dyke et al. 2006). In addition, pterodactyloids could suggested that the head crests might offer some aerody- extend their more extensively than rhamphorhyn- namic advantages (e.g. in Nyctosaurus and Pteranodon choids, thus straightening the leading edge of the wing to [Bramwell & Whitfield 1974; Xing et al. 2009]), but a greater degree (Witton 2008). Furthermore, most ptero- generally the crests make little difference to the aerody- dactyloids had lost the fifth toe, a long structure in more namic performance of the head, based on wind tunnel basal pterosaurs that may have helped support a substantial experiments (Elgin et al. 2008). It is thus reasonable to membrane between the hind legs. Such differences in wing conclude that such crests were used primarily for signalling, shape have led to the suggestion that members of the two perhaps in . The extravagant diversity of suborders used different modes of flight (Dyke et al. 2006; pterodactyloid (Wellnhofer 1978) may reflect higher Einarsson 2006). In particular, Einarsson (2006) suggested levels of sexual selection among pterodactyloids than Evolution of morphological disparity in pterosaurs 347

Figure 8. Diversity of cranial characters in pterosaurs, showing variations in jaw shape, presence and absence of teeth, proportions, and crests on the snout and back of the skull. Pterosaurs shown are: A, Dimorphodon; B, Rhamphorhynchus; C, ; D, Pteranodon; E, Pterodactylus; F, Pterodaustro; G, Dsungaripterus; H, ; I, Thalassodromeus. Drawing by Mark Witton. rhamphorhynchoids, and a consequent explosion in cranial Rhamphorhynchoids occupy a small area of crests. Further, the great disparity in pterodactyloid jaws morphospace, largely reflecting their conservative and dentitions may indicate a broadening of dietary body plans (but also the small number of taxa relative to regimes, perhaps reflecting new opportunities as fishes pterodactyloids). The extremes in morphospace are marked and diversified during the Cretaceous (Lloyd et al. by the piscivorous Dimorphodon and the insectivorous 2008). Batrachognathus. In general, the rhamphorhynchoids The size of the pterodactyloid region of morphospace remained relatively small, the largest wingspans probably is substantial, when compared to that of rhamphorhyn- reaching 2 m (Kellner 2003). Among other variations, choids (Fig. 2), and this is based mainly on the aston- Anurognathus had a short tail (Bennett 2007) and Austri- ishingly disparate Early Cretaceous pterodactyloids. An adactylus possessed a head crest, both features being more example is Tapejara imperator, with its remarkable sail- typical of pterodactyloids. like head crest and perhaps an unusual diet of fish and The three outgroups, Scleromochlus, Herrerasaurus fruit (Wellnhofer & Kellner 1991), unlike the other periph- and Ornithosuchus, fall within the rhamphorhynchoid eral pterosaurs, which were . The Late Creta- morphospace region (Fig. 2). These outgroups show an ceous pterodactyloids occupy a tiny area of the Early Creta- approximate ordering in their similarity to rhamphorhyn- ceous morphospace, and yet these pterosaurs were some of choids that roughly matches their closeness of relationship the most extreme, including the giant pteranodontids, and (however, note that proximity in morphospace is not neces- the truly huge azhdarchids. The latter include the largest sarily matched by phylogenetic closeness; Wills 2001). known pterosaur, Hatzegopteryx thambema, with an esti- Thus, Scleromochlus is either the of pterosaurs mated wingspan of 10–12 m and a 3-m-long head, one of (Sereno 1991) or a basal avemetatarsalian close to the origin the largest of all terrestrial vertebrates. It is thought that this of both pterosaurs and dinosauromorphs (Benton 1999). pterodactyloid inhabited inland areas, stalking its prey on Herrerasaurus is a basal , and Ornithosuchus is foot (Witton & Naish 2008), and perhaps flew only rarely. the most distantly related, being a crurotarsan on the 348 K. C. Prentice et al. crocodilian line of archosaurian evolution (Sereno 1991; history, but more or less matches diversity changes (Butler Benton 1999). Scleromochlus coincides with the rham- et al. 2009). The two pterosaur suborders, however, peaked phorhynchoid morphospace region for cranial, total in diversity and disparity at different times: the rham- postcranial, and hindlimb characters (Fig. 6A, B, D); not phorhynchoids in the Jurassic and the pterodactyloids in unexpectedly, there are significant differences in forelimb the Early Cretaceous. characters (Fig. 6C). Herrerasaurus and Ornithosuchus Comparing pterosaur diversity and disparity through occur close together in morphospace, but they differ from time is dogged by sampling problems, although conclusions rhamphorhynchoids in all character partitions except the differ on whether or not these present a serious obstacle for cranial set (Fig. 6D). studies of pterosaur evolution (Butler et al. 2009; Dyke et al. 2009). Evidence of an incompletely sampled fossil record is The pterodactyloid subclades seen from a collector curve of pterosaurs through research Despite some differences, recent cladistic analyses (Kell- time (Dyke et al. 2009): the curve rises rapidly, with no sign ner 2003; Unwin 2003, 2005; Wang et al. 2005; Lu&¨ of an asymptote that might indicate saturation in new finds. Ji 2006; Andres & Ji 2008; Lu¨ et al. 2010) divide Further, rarefaction of numbers of species against numbers pterodactyloids into four subclades, generally arranged of specimens show that all bins are undersampled (Dyke cladistically as (Ornithocheiroidea + (Ctenochasmatoidea et al. 2009). However, there is good congruence between + (Dsungaripteroidea + Azhdarchoidea))). Our disparity the implied order of branching in two current results suggest that all four superfamilies occupy differ- of pterosaurs (Kellner 2003; Unwin 2003) and the strati- ent regions of morphospace, except for a significant over- graphical order of the (Dyke et al. 2009). Further, lap of Dsungaripteroidea and Azhdarchoidea, although study of the accumulation history of new pterosaur species this is not immediately apparent when viewing the region through research time (Dyke et al. 2009) shows that as new of morphospace of all pterodactyloids. Individual charac- species are discovered, the number of known formations ter partitions, however, result in more substantial overlap and sites yielding pterosaur fossils has also increased – this among the subclades, the only significant separation being would not be expected if the bulk of the record came from for Azhdarchoidea relative to other subfamilies based upon just a few exceptional faunas. cranial characters. The raw data on pterosaur species is affected by fossil A final brief comment concerns the phylogenetic posi- Lagerstatten,¨ sites of exceptional preservation, such as the tion of Feilongus youngi from the Early Cretaceous. The Formation from the Late Jurassic of affinities of this taxon are disputed, as it has been regarded Germany and the Jehol Group from the mid-Cretaceous of either as a ctenochasmatoid (Wang et al. 2005) or as China. These yield rich pterosaur faunas, some 15 species an ornithocheiroid (Lu¨ & Ji 2006). In the morphospace in the former, and more than 30 in the latter. Other spans of plots, Feilongus usually falls within the range of the Mesozoic time may entirely lack pterosaur remains, or yield Ornithocheiroidea for all characters (Fig. 5) and for Early little more than scraps. Phylogenetic evidence in the form Cretaceous taxa only, but its position is less clear in of ‘ghost lineages’ and ‘range extensions’ (Smith 1994) the morphospace plots of individual character partitions. may be used to fill some gaps. Such phylogenetic diver- The inclusion of Feilongus in either Ornithocheiroidea or sity estimates (PDEs) provide some correction of the raw Ctenochasmatoidea does not affect the statistical signifi- diversity data (e.g. Ruta & Benton 2008), but the effec- cance of the overlap between the two superfamilies when tiveness of this method diminishes as the gaps expand all pterodactyloids are considered, but it does when only (Benton 1987). Further corrections can be applied that take Early Cretaceous pterosaurs are considered. account of the distribution of pterosaur-bearing formations (Butler et al. 2009) to provide a modelled diversity esti- Evolution of diversity and disparity mate (MDE), a residual ‘unexplained diversity signal’ that It has commonly been observed that diversity (that is, represents variation in diversity that cannot be accounted species richness) and disparity (that is, morphological vari- for by simple variation in the number of pterosaur-bearing ety) are decoupled (Wills et al. 1994; Wagner 1995; Foote formations. 1997; Wills 2001; Erwin 2007). However, Dyke et al. These three measures of pterosaur diversity through time (2009) found that the high diversity of pterodactyloids – the raw data, the PDE, and the MDE – all show a major in the Early Cretaceous was mirrored by high levels of peak in the Early Cretaceous (Fig. 9), and this was the limb disparity. If diversity and disparity were evolving time of highest disparity. Disparity measures could not in tandem in pterosaurs, this result would be somewhat be broken down meaningfully into shorter time intervals, unusual because disparity usually peaks early in a clade’s and so this result is only suggestive. However, it seems history (Foote 1997; Erwin 2007). evident that the rhamphorhynchoids did not achieve high Here, we confirm Dyke et al.’s(2009) finding that overall diversity or disparity, and it was only after 90–100 ma of disparity (not just forelimb disparity) peaked in the Early evolution that pterosaurs achieved maximum diversity and Cretaceous (Fig. 9). This peak occurs late in the clade’s disparity. Evolution of morphological disparity in pterosaurs 349

Figure 9. Comparison of diversity and disparity change through time shows some evidence of coupling of the two, and a coordinated rise in disparity and diversity in the Early Cretaceous. The disparity measures (sum of ranges, left-hand scale) are from Fig. 4. The diversity measures (number of lineages, right-hand scale) are plotted at a much finer time scale (stratigraphical sub-stages), and the two curves show raw number of species (solid line) and modelled diversity estimate, based on the number of pterosaur-bearing formations (dashed line). The diversity curves are from Butler et al. (2009). The slow rise of the pterosaurs is surprising. Given that Competitive displacement they were the first vertebrates known to achieve true flap- Morphospaces need not equal ecospaces (Hulsey & Wain- ping flight, it might have been assumed that the clade would wright 2002; Wainwright 2007), especially because there expand rapidly in diversity and disparity, but pterosaurs can be a disconnection between morphological diversity apparently existed as a narrow spindle-shaped clade for up and functional diversity: many different morphological to 100 ma in the Late Triassic, Jurassic, and early part of combinations may have the same functional property. This the Early Cretaceous, before expanding rapidly in the late highlights the danger of assuming that groups of organ- Early Cretaceous, and then declining after perhaps 25 ma of isms that occupy different morphospaces were biologically high diversity and disparity. As noted, of course, the rarity (in the broadest sense of the word) different, especially if of Triassic and Jurassic pterosaurs could be a problem of those morphospaces are based on different characters from substantial undersampling of the rock record, and new finds those that might be effective in any competitive interac- of Lagerstatten¨ of these ages could demonstrate this. But, tions. However, this issue can be partly circumvented by if the pterosaur clade is truly ‘top heavy’ (Gould et al. considering all aspects of morphology as well as the func- 1977), then it presents an interesting contrast to the major- tions associated with the characters used to construct the ity of disparity studies to date that focus on ‘bottom heavy’ morphospaces (McGowan & Dyke 2007). clades, where diversity and disparity expanded rapidly early In the case of pterosaurs, there were formerly two widely in clade history. held assumptions: that rhamphorhynchoids, and rham- A more exhaustive treatment of the decoupling of phorhynchids in particular, were outcompeted by ptero- diversity–disparity curves ought to await a broader, dactyloids, and the latter, in turn, were driven to extinction synthetic overview of the group as a whole. by the emergence of birds in the Cretaceous (Colbert 1980; Palaeobiological–functional studies of pterosaurs are still Unwin 1988, 2005; Penny & Phillips 2004; Slack et al. in their infancy, although considerable progress is being 2006). Both purported replacements pass the basic tests made in these areas. A firmer grasp of the factors underly- for a candidate competitive replacement (CCR; Benton ing such a decoupling are beyond the scope of the present 1996a, b), in that the organisms in each group overlap article, but we do hope that our finds will initiate a survey in time and space and in some aspects of their assumed of the causal explanations. ecology. 350 K. C. Prentice et al.

Rhamphorhynchoids and pterodactyloids overlapped in between adults of contemporaneous birds (smaller) and time for at least 30 ma, from the Late Jurassic to late pterosaurs (larger) (Hone & Benton 2007b). Early Cretaceous (150–120 ma ago). At the beginning In simple terms, there is no evidence for a classic ‘double of this time span, in the Late Jurassic Solnhofen Lime- wedge’ pattern of decline in pterosaur diversity and increase stone Formation of Germany, numerous species of each in diversity (Butler et al. 2009), as suggested by Slack group lived side by side, including Rhamphorhynchus and et al. (2006). However, we note that, although the ‘double Pterodactylus. The last rhamphorhynchoid, the insectivo- wedge’ pattern has been suggested as typical of long-term rous anurognathid Dendrorhynchoides from the late Early competition between major groups (references in Benton Cretaceous Jehol Group of China, is significantly separated 1996a, b), a truly competitive displacement of one group in morphospace from pterodactyloids. The long coexis- by another might in fact happen so rapidly that it would tence of the two groups through the Late Jurassic and Early look more like a sudden (geologically speaking) event. Cretaceous does not indicate whether competition did or did not occur, but it does show that rhamphorhynchoids History counts were not simply driven to extinction by the emergence of The plots of pterosaurs in morphospace based on the the first pterodactyloids. During Solnhofen Limestone and chronology of their discoveries reveal interesting patterns. Jehol Group times, numerous pterosaurs coexisted – both In the first plot (Fig. 7A), very few taxa are represented, rhamphorhynchoids and pterodactyloids – each presum- but these already show a disjoint distribution. With addi- ably occupying a discrete segment of ecospace as a result tion of taxa from the second time bin (Fig. 7B), the disjoint of character displacement and avoidance of competition. pattern is maintained, and repeated in both groups, which The complete separation between the morphospace appear juxtaposed to one another. Inclusion of taxa from regions occupied by the two suborders (Fig. 1), and the the third time bin (Fig. 7C) impacts very little on the recip- near-complete separation of morphospace areas for differ- rocal position and distribution of taxa from the previous ent character sets (Fig. 6), suggest substantial morphologi- intervals, but note the overlap between the light blue taxa cal differentiation between rhamphorhynchoids and ptero- and each of the groups from the preceding intervals. In the dactyloids. This indicates, but does not prove (Wainwright fourth time bin (Fig. 7D), the distribution of taxa changes 2007), that species within each suborder were distinct on substantially, but we still see taxa from the first two time several grounds, either because they had different funda- bins as two juxtaposed groups, though they now appear to mental characteristics that had always kept them apart, be rotated. A common pattern, also found with taxa from or because of character displacement under competition. the third time bin, is the diffusion in morphospace. Also, One complicating factor we have not been able to include taxa from the fourth time bin tend to overlap other groups is ontogeny. There is a suggestion (Unwin 2005) that to a very limited degree. With the inclusion of taxa (Fig. many pterosaurs changed their diets and other ecological 7E) from the final time bin, we note an equally rapid spread characteristics during growth. This means that niches or within morphospace, and a large amount of overlap with morphospace regions cannot be defined in a restricted way (mostly) groups from the third and fourth time bins. for any species, and we cannot rule out the possibility that Taken together, these observations highlight the tremen- juveniles of different species might have competed whereas dous impact of pterosaur discoveries over the last decades. the adults did not, or that juveniles of one species might have Disparity augments significantly at the transition from the competed with adults of another. second to the third, and from the third to the fourth time bins. Birds arose in the Late Jurassic and diversified in the Furthermore, taxa appear progressively more dispersed in Cretaceous, and their rise in morphological and taxonomic morphospace, indicating that new discoveries have intro- diversity has sometimes been hypothesized to correlate duced a remarkable array of new and widely disparate inversely with that of pterosaurs, suggesting the possibility morphological types. Such finds are generally in agree- of competitive displacement (Colbert 1980; Unwin 1988). ment with previous authors’ observations of the impact McGowan & Dyke (2007) showed that birds, bats and of palaeontological practice and knowledge on modalities pterosaurs all differ substantially in limb disparity, which of occupation and structuring of morphospace (e.g. Foote suggests different locomotory modes. Further, diverse birds 1997b; Nardin et al. 2005). and pterosaurs apparently coexisted for a long time. We know that the Jehol Group in China, spanning some 11 Supplementary material ma, has yielded large numbers of birds and pterosaurs that Supplementary material for this paper is available via the presumably occupied different ecological niches, the birds Supplementary Content on the article’s online page. flitting amongst the trees and feeding largely on insects and fruit (two species fed on fishes), and the pterosaurs swoop- ing over the lake and feeding on fishes and aquatic inverte- Acknowledgements brates around the margins (Zhou 2004). These mixed faunas suggest that birds and pterosaurs divided ecospace success- We thank Lorna Steel and an anonymous reviewer for fully, and there was generally a substantial size difference helpful comments. MR is funded by a NERC Advanced Evolution of morphological disparity in pterosaurs 351

Research Fellowship (ARF NE/F014872/1). We thank sity patterns: implications for hypotheses of bird/pterosaur Mark Witton for his artwork in figures 1 and 8. This paper is competitive replacement. Paleobiology, 35, 432–446. based on work by KP carried out as part of the requirements Chatterjee, S., Templin, R. J. & Campbell, K. E., Jr 2007. The aerodynamics of Argentavis. The world’s largest flying bird of the MSc in Palaeobiology at the University of Bristol. from the Miocene of . Proceedings of the National Academy of Sciences, USA, 104, 12398–12403. References Ciampaglio, C. N., Kemp, M. & McShea, D. W. 2001. Detect- ing changes in morphospace occupation patterns in the fossil Anderson,M.J.2001. A new method for non-parametric multi- record: characterization and analysis of measures of disparity. variate analysis of variance. Austral Ecology, 26, 32–46. Paleobiology, 27, 695–715. Andres, B. & Ji, Q. 2008. A new pterosaur from the Colbert, E. H. 1980. Evolution of the vertebrates. 3rd edition. Province of China, the phylogeny of the Pterodactyloidea, Wiley Interscience, New York, 510. pp. and convergence in their cervical vertebrae. Palaeontology, Dyke,G.J., Nudds, R. L. & Rayner, J. M. V. 2006. Limb dispar- 51, 453–469. ity and wing shape in pterosaurs. Journal of Evolutionary Barrett, P. M., Butler, R. J., Edwards, N. P. & Milner, A. Biology, 19, 1339–1342. R. 2008. Pterosaur distribution in time and space: an atlas. Dyke, G. J., McGowan, A. J., Nudds, R. L. & Smith, D. 2009. Zitteliana, Series B, 28, 61–107. The shape of pterosaur evolution: evidence from the fossil Bennett, S. C. 1989. A pteranodontid pterosaur from the Early record. Journal of Evolutionary Biology, 22, 890–898. Cretaceous of Peru, with comments on the relationships of Einarsson, E. 2006. Morphological and functional differences Cretaceous pterosaurs. Journal of , 63, 669–677. between rhamphorhynchoid and pterodactyloid pterosaurs Bennett, S. C. 1996. The phylogenetic position of the Pterosauria with emphasis on flight. Journal of Paleontology, within the Archosauromorpha. Zoological Journal of the 26, 58A. Linnean Society, 18, 261–308. Elgin, R. A., Grau, C. A., Palmer, C., Hone, D. W.E, Greenwell, Bennett, S. C. 1999. Pterosaurs. Pp. 996–1004 in R. Singer (ed.) D. & Benton, M. J. 2008. Aerodynamic characters of the Encyclopaedia of paleontology. Fitzroy Dearborn, Chicago. cranial crest in Pteranodon. Zitteliana, Series B, 28, 167–174. Bennett, S. C. 2007. A second specimen of the pterosaur Anurog- Erwin, D. H. 2007. Disparity: morphological pattern and devel- nathus ammoni. Palaontologische¨ Zeitschrift, 81, 376–398. opmental context. Palaeontology, 50, 57–73. Benton,M.J.1987. Mass among families of non- Evans, S. E. & Haubold, H. 1986. A review of the Upper Permian marine : the data. Memoires´ de la Societ´ eG´ eologique´ genera Coelurosauravus, Weigeltisaurus and Gracilisaurus. de France, 150, 21–32. Zoological Journal of the Linnean Society, 90, 275–303. Benton,M.J.1996a. On the nonprevalence of competitive Foote, M. 1992. Rarefaction analysis of morphological and taxo- replacement in the evolution of tetrapods. Pp. 185–210 in nomic diversity. Paleobiology, 18, 1–16. D. Jablonski, D. H. Erwin & J. H. Lipps (eds) Evolutionary Foote, M. 1994. Morphological disparity in - paleobiology. University of Chicago Press, Chicago. crinoids and the early saturation of morphological space. Pale- Benton, M. J. 1996b. Testing the roles of competition and expan- obiology, 20, 320–344. sion in evolution. Proceedings of the Royal Society Foote, M. 1996. Evolutionary patterns in the fossil record. Evolu- of London, Series B, 263, 641–646. tion, 50, 1–11. Benton, M. J. 1999. Scleromochlus taylori and the origin of Foote, M. 1997a. The evolution of morphological diversity. dinosaurs and pterosaurs. Philosophical Transactions of the Annual Review of Ecology and Systematics, 28, 129–152. Royal Society of London, Series B, 354, 1423–1446. Foote, M. 1997b. Sampling, taxonomic description, and our Benton, M. J. & Clark, J. 1988. Archosaur phylogeny and the evolving knowledge of morphological diversity. Paleobiol- relationships of the Crocodylia. Pp. 295–338 in M. J. Benton ogy, 23, 181–206. (ed.) The phylogeny and classification of the tetrapods. Volume Frey, E. & Martill, D. M. 1996. A reappraisal of Arambourgia- 2. Systematics Association Special Volume 35A, Oxford nia (Pterosauria, Pterodactyloidea): one of the world’s largest University Press, Oxford. flying animals. Neues Jahrbuch fur¨ Geologie und Palaontolo-¨ Bouxin, G. 2005. Ginkgo, a multivariate analysis package. Jour- gie, Abhandlungen, 199, 221–247. nal of Vegetation Science, 16, 355–359. Gauthier, J. A. 1986. Saurischian monophyly and the origin of Bramwell, C. D. & Whitfield, G. R. 1974. of birds. Memoirs of the California Academy of Sciences, 8, Pteranodon. Philosophical Transactions of the Royal Society 1–55. of London, Series B, 267, 503–581. Gotelli, N. J. & Colwell, R. K. 2001. Quantifying biodiversity: Brinkman, D. 1988. A weigeltisaurid from the Lower procedures and pitfalls in the measurement and comparison Triassic of British Columbia. Palaeontology, 31, 951–955. of species richness. Ecology Letters, 4, 379–391. Brochu, C. A. 2001. Progress and future directions in archosaur Gould, S. J. 1989. Wonderful life: the Burgess Shale and the . Journal of Paleontology, 75, 1185–1201. nature of history. Norton, New York, 352. pp. Brusatte, S. L., Benton,M.J., Ruta, M. & Lloyd, G. T. 2008a. Gould,S.J.1991. The disparity of the Burgess Shale arthropod Superiority, competition, and opportunism in the evolutionary fauna and the limits of cladistic analysis: why we must strive radiation of dinosaurs. Science, 321, 1485–1488. to quantify morphospace. Paleobiology, 17, 411–423. Brusatte,S.L., Benton, M. J., Ruta, M. & Lloyd, G. T. Gould,S.J., Raup, D. M., Sepkoski Jr., J. J., Schopf, T. J. M. & 2008b. The first 50 Myr of dinosaur evolution: macroevolu- Simberloff, D. S. 1977. The shape of evolution: A comparison tionary pattern and morphological disparity. Biology Letters, of real and random clades. Paleobiology, 3, 23–40. 4, 733–736. Hammer, Ø., Harper, D. A. T. & Ryan, P. D. 2001. PAST: Buffetaut, E., Grigorescu, D. & Csiki, Z. 2002. A new giant Paleontological Statistics Software Package for Education and pterosaur with a robust skull from the latest Cretaceous of Data Analysis. Palaeontologica Electronica 4(1), 9. pp. Romania. Naturwissenschaften, 89, 180–184. Hazlehurst, G. A. & Rayner, J. M. V. 1992. Flight characteristics Butler, R. J., Barrett, P. M., Nowbath, S. & Upchurch, P. 2009. of Triassic and Jurassic Pterosauria: an appraisal based on Estimating the effects of sampling biases on pterosaur diver- wing shape. Paleobiology, 18, 447–463. 352 K. C. Prentice et al.

Henderson, D. M. 2010. Pterosaur body mass estimates from Penny, D. & Phillips, J. M. 2004. The rise of birds and : three-dimensional mathematical slicing. Journal of Vertebrate are microevolutionary processes sufficient for macroevolu- Paleontology, 30, 768–785. tion? Trends in Ecology and Evolution, 19, 516–522. Hone, D. W. E. & Benton, M. J. 2007a. An evaluation Peters, D. 2000. A reexamination of four prolacertiforms with of the phylogenetic relationships of the pterosaurs among implications for pterosaur phylogenesis. Rivista Italiana di archosauromorph . Journal of Systematic Palaeontol- Paleontologia e Stratigrafia, 106, 293–336. ogy, 5, 465–469. Rayner, J. M. V. 1988. The evolution of vertebrate flight. Biolog- Hone, D. W. E. & Benton, M. J. 2007b. Cope’s Rule in the ical Journal of the Linnean Society, 34, 269–287. Pterosauria, and differing perceptions of Cope’sRule at differ- Romer, A. S. 1966. Vertebrate paleontology. 3rd edition. Univer- ent taxonomic levels. Journal of Evolutionary Biology, 20, sity of Chicago Press, Chicago, 468. pp. 1164–1170. Ruta, M. 2009. Patterns of morphological evolution in major Hone, D. W. E. & Benton, M. J. 2008. Contrasting total-evidence groups of Palaeozoic Temnospondyli (Amphibia: Tetrapoda). and supertree methods: the origin of the pterosaurs. Zitteliana, Special Papers in Palaeontology, 81, 91–120. Series B, 28, 35–60. Ruta, M. & Benton, M. J. 2008. Calibrated diversity, tree Hone, D. W. E. & Buffetaut, E. (eds). 2008. Flugsaurier – topology and the mother of mass extinctions: the lesson of pterosaur papers in honour of Peter Wellnhofer. Zitteliana, temnospondyls. Palaeontology, 51, 1261–1288. Series B, 28, 1–264. Schaumberg, G., Unwin, D. M. & Brandt, S. 2006. New infor- Hulsey, C. D. & Wainwright, P. C. 2002. Projecting mechanics mation on the anatomy of the Late Permian gliding reptile into morphospace: disparity in the feeding system of labrid Coelurosauravus. Palaontologische¨ Zeitschrift, 81, 160–173. fish. Proceedings of the Royal Society of London, Series B, Seeley, H. G. 1901. Dragons of the air: an account of extinct 269, 317–326. flying reptiles. Appleton, New York, 272. pp. Kellner, A. W.A. 2003. Pterosaur phylogeny and comments on the Sereno, P. 1991. Basal archosaurs: phylogenetic relationships and evolutionary history of the group. Pp. 105–137 in E. Buffe- functional implications. Journal of Vertebrate Paleontology, taut & J.-M. Mazin (eds) Evolution and palaeobiology of Memoir, 2, 1–53. pterosaurs. Geological Society of London, London. Slack, K. E., Jones, C. M., Ando, T., Harrison, G. L., Fordyce, Langston, W. 1981. Pterosaurs. Scientific American, 244, R. E., Arnason, U. & Penny, D. 2006. Early penguin 122–136. fossils, plus mitochondrial genomes, calibrate avian evolu- Lawson, D. A. 1975. Pterosaurs from the latest Cretaceous of tion. Molecular Biology and Evolution, 23, 1144–1155. West Texas: discovery of the largest flying creature. Science, Smith, A. B. 1994. Systematics and the fossil record: document- 187, 947–948. ing evolutionary patterns. Blackwell Scientific Publications, Lingoes, J. 1971. Some boundary conditions for a monotone London, 232 pp. analysis of symmetric matrices. Psychometrika, 36, 195–203. Stein, K., Palmer, C., Gill, P. G. & Benton, M. J. 2008. The Lloyd, G. T., Davis, K. E., Pisani, D., Tarver, J. E., Ruta, M., aerodynamics of the British Late Triassic Kuehneosauridae. Sakamoto, M. Hone, D. W. E., Jennings, R. & Benton, M. Palaeontology, 51, 967–981. J. 2008. Dinosaurs and the Cretaceous terrestrial revolution. Unwin, D. M. 1987. Pterosaur locomotion: Joggers or waddlers? Proceedings of the Royal Society of London, Series B, 275, Nature, 327, 13–14. 2483–2490. Unwin, D. M. 1988. Extinction and survival in birds. Pp. 295–318 Lu,¨ J. & Ji, Q. 2006. Preliminary result of a phylogenetic analy- in G. P. Larwood (ed.) Extinction and survival in the fossil sis of the pterosaurs from western Liaoning and surrounding record. Oxford University Press, Oxford. areas. Journal of the Paleontological Society of Korea, 22, Unwin, D. M. 2003. On the phylogeny and evolutionary history 239–261. of pterosaurs. Pp. 139–190 in E. Buffetaut & J.-M. Mazin Lu,¨ J., Unwin, D. M., Xu, L. & Zhang, X.-l. 2008. A new (eds) Evolution and palaeobiology of pterosaurs. Geological azhdarchoid pterosaur from the Lower Cretaceous of China Society of London, London. and its implications for pterosaur phylogeny and evolution. Unwin, D. M. 2005. The pterosaurs from deep time. Pi Press, New Naturwissenschaften, 95, 891–897. York, 352. pp. Lu,¨ J., Unwin, D.M., Jin, X., Liu, Y. & Ji, Q. 2010. Evidence Unwin, D. M. & Lu,¨ J. 1997. On and the rela- for modular evolution in a long-tailed pterosaur with a ptero- tionships of pterodactyloid pterosaurs. Historical Biology, 12, dactyloid skull. Proceedings of the Royal Society, Series B, 199–210. 277, 383–389. Villier, L. & Korn, D. 2004. Morphological disparity of McGhee, G. R. Jr. 1999. Theoretical morphology. The concept ammonoids and the mark of the Permian mass extinctions. and its applications. Columbia University Press, New York, Science, 306, 264–266. 378. pp. Wagner, P. J. 1995. Testing evolutionary constraint hypothe- McGowan, A. J. & Dyke, G. J. 2007. A morphospace-based ses with early Paleozoic gastropods. Paleobiology, 21, test for competitive exclusion among flying vertebrates: did 248–272. birds, bats and pterosaurs get in each other’s space? Journal Wainwright, P. C. 2007. Functional versus morphological diver- of Evolutionary Biology, 20, 1230–1236. sity in macroevolution. Annual Review of Ecology, Evolution, Nardin, E., Rouget, I. & Neige, P. 2005. Tendencies in paleonto- and Systematics, 38, 381–401. logical practice when defining species, and consequences on Wang, X. L. 2008. Discovery of a rare arboreal forest-dwelling biodiversity studies. Geology, 33, 969–972. flying reptile (Pterosauria, Pterodactyloidea) from China. Norberg, U. M. 1994. Wing design, flight performance, and habi- Proceedings of the National Academy of Sciences, USA, 105, tat use in bats. Pp. 205–239 in P. C. Wainwright & S. M. 1983–1987. Reilly (eds). Pp.. University of Chicago Press, Chicago, Wang, X. L., Kellner,A.W.A., Zhou, Z. & Campos, 376. pp. D. A. 2005. Pterosaur diversity and faunal turnover in Padian, K. & Rayner, J. M. V. 1993. The wings of pterosaurs. Cretaceous terrestrial ecosystems in China. Nature, 437, American Journal of Science, 293, 91–166. 875–879. Evolution of morphological disparity in pterosaurs 353

Wellnhofer, P. 1978. Pterosauria. Handbuch der Palaoherpetolo-¨ Witton, M. P. 2008. A new approach to determining pterosaur gie 19. Gustav Fischer, Stuttgart, 82 pp. body mass and its implications for pterosaur flight. Zitteliana, Wellnhofer, P. & Kellner,A.W.A.1991. The skull of Tapejara Series B, 28, 143–158. wellenhoferi Kellner (Reptilia, Pterosauria) from the Lower Witton, M. P. & Naish, D. 2008. A reappraisal of azhdarchid Cretaceous Santa Formation of the , north- pterosaur functional morphology and paleoecology. PLoS eastern Brazil. Mitteilungen der Bayerischen Staatssamm- ONE, 3, e2271. fuer Palaeontologie und Historische Geologie, 31, 89– Witton, M. P., Martill, D. M. & Green, M. 2009. On ptero- 106. dactyloid diversity in the British Wealden (Lower Cretaceous) Wills, M. A. 1998. and recent disparity: the picture and a reappraisal of “Palaeornis” clifti Mantell, 1844. Creta- from priapulids. Paleobiology, 24, 177–199. ceous Research, 30, 676–686. Wills, M. A. 2001. Morphological disparity: a primer. Pp. 55–144 Xing, L., Wu, J., Lu., Y., Lu,¨ J. & Ji, Q. 2009. Aerodynamic char- in J. M. Adrain, G. D. Edgecombe & B. S. Lieberman (eds). acteristics of the crest with membrane attachment on Creta- Fossils,phylogeny, and form – an analytical approach. Kluwer ceous pterodactyloid Nyctosaurus. Acta Geologica Sinica, 83, Academic, New York. 25–32. Wills, M. A., Briggs,D.E.G& Fortey, R. A. 1994. Disparity as Zhou, Z. 2004. Vertebrate radiations of the Jehol biota and an evolutionary index – a comparison of Cambrian and recent their environmental background. Naturwissenschaften, 49, arthropods. Paleobiology, 20, 93–130. 754–756.