Multi-Aged Small Pterosaur Track Assemblage from the Upper Cretaceous of Korea

The pterosaur is the earliest and largest powered �ying vertebrate, even earlier and larger than the other extant archosaurian group, birds. However, evidence for this �ying reptile, including the diversity of the small-sized pterosaur after the mid-Cretaceous, and their ecology, has remained elusive. Here we present numerous and dense pterosaur track assemblages from the Hwasun Seoyuri tracksite in the Upper Cretaceous Jangdong Formation of the Neungju Basin in Korea. The pterosaur track assemblage, assigned to Pteraichnus isp., consists of various sized, randomly oriented manus-dominated tracks with several pes claw marks. These features commonly indicate the semi-aquatic behavior and multi-age gregariousness of pterosaurs. The supposed trackmaker of pterosaur tracks would be the small-sized pterodactyloid that inhibited the Late Cretaceous Korean Peninsula, but that has not previously been reported. This ichnological evidence for the global distribution of small-sized pterosaurs could be interpreted to mean that the pterosaur fauna in the Late Cretaceous was more distributed and diverse than was previously known.


Introduction
The pterosaurs is the extinct ying archosaurs, which existed from the Late Triassic to the terminal Cretaceous, and they were the rst powered-ying vertebrates, even earlier than the extant powered-ying archosaur group birds [1][2][3] .The smallest pterosaurs know so far has a wingspan reaches under 1 meter, while the largest pterosaur had exceeded 10 meters in their wingspan 4 .This ying reptile had been one of the most important components of the Mesozoic ecosystems 5 , but there are many unresolved enigmas about pterosaurs concerning their ecology and evolution.Despite the abundance of information that can be obtained from pterosaur body fossils, studies of pterosaur tracks are essential in that they could provide vivid information about the ethology and ecology of the living organisms.Here, we report an assemblage of small pterosaur tracks, mainly consisting of manus tracks, from the Hwasun Seoyuri tracksite in the Upper Cretaceous Jangdong Formation of the Neungju Basin, Korea.This is the rst evidence for the lineage of the small-size pterosaur was survived in the East Asia after the mid-Cretaceous period.The purpose of this paper is to shed light on the trackmaker's ecology, and the distribution and diversity of the small-sized pterosaurs in the Late Cretaceous East Asia.
The Hwasun Seoyuri tracksite belongs to the Jangdong Formation which consists of silty mudstones and ne sandstones with pyroclastic materials from alluvial plain and sand at 8 .The tracks with various sedimentary structures, including desiccation cracks, ripple marks, and sulfate and halite casts in the Jangdong Formation suggest that this basin was lled under arid to semi-arid conditions 9 .The age of the Jangdong Formation is inferred to be 94 Ma based on the U-Pb dating of zircons 8 .
The Hwasun Seoyuri tracksite contains about 1,500 dinosaur tracks organized into more than 60 trackways on ve different beds, and most of them are attributed to theropod 10,11 (Figs.1b & c).After that, various paleontological studies were conducted in this site including the enigmatic theropod trackway 12 , theropod acceleration phase using the trackway 13 , and pes-only sauropod and ornithopod trackways 14 .This tracksite was originally used as a quarry, but it is now designated as the Natural Monument No. 487 of Korea and part of the Mudeungsan UNESCO Global Geopark.

Materials And Methods
Pterosaur tracks occurred on 10 abandoned slabs and a single bed located above the dinosaur tracks bearing beds of the Hwasun Seoyuri tracksite (Fig. 1d).Most of the pterosaur tracks described in this study were found at isolated slabs, but several tracks were discovered on the outcrop.Tracks in the slabs are preserved as a positive hyporelief at the laminated tuffaceous ne sandstone-mudstone couplets.
The surface of slabs remains mild straight or sinuous ripple.The cross-sections of the slabs consist of aser or wavy-bedded ne sandstone to mudstone.All pterosaur track-bearing slabs were stored in the Korea Dinosaur Research Center, Chonnam National University, Gwangju, Korea, under the designated number KDRC-HW-PT number.
A total of 221 footprints were measured (Supplementary Table S1) and terms for descriptions of the pterosaur tracks followed by Pascual Arribas and Sanz Péres 15 and Billon-Bruyat and Mazin 16 .The photographs of the slabs and tracks were taken with a digital camera SONY alpha 7 Mark and digital lenses SEL80M29G, and SEL2470Z.The footprints were rst drawn by Procreate for iPad, and images were created in Adobe Photoshop 2021 and Adobe Illustrator 2021.The guidelines for creating 3D images were outlined by Falkingham et al. 17 and Romilio 18 .All photographs were converted into the 3D models using Agisoft Metashape Professional (v.1.7.1) and visualized using Paraview (v.5.9.0).

Pterosaur Tracks In The Hwasun Seoyuri Tracksite
Hundreds of pterosaur tracks, mainly manus-dominated, were found on 10 isolated slabs (KDRC-HW-PT01 -PT10) originating in the same layer and a single bed in the outcrop of the Hwasun Seoyuri tracksite (Fig. 2).most of the tracks do not make consecutive trackways (Fig. 3), it is di cult to recognize the gait pattern.
Several slabs are displaying the randomly oriented and densely overlapped tracks.Although the morphology of imprints is well-preserved, anatomical details such as skin or digital pad impressions are not discerned because of subsequently formed evaporite traces.
The manus imprints are asymmetrical tridactyl digitigrade (Figs.4a-c & 4a′-c′).Three digits radiate from a metacarpophalangeal joint.The length of digit I and digit are almost the same in their mean value (Digit I: 14.06 mm, Digit : 14.12 mm).Also, the length of digit is always longer than the other digits (mean value: 26.07 mm).Digit I is oriented anterior-laterally with a slightly inward curve on the tip.Digit is oriented posterior-laterally and shows an intermediate imprint.Digit , the longest imprint, is oriented posteriorly, and there is no digit impression in any tracks.Although the depression in small-size tracks is subequal, depression in the metacarpophalangeal joint is deeper than digital impressions in medium to large-sized tracks (Figs.4g-j).In the width of the digits, it is observed that the diminutive tracks (length less than 30 mm) have narrow or slender width of digits that may be derived from the collapse of the substrate 19  The pes imprints are more obscure and rarer than the manus imprints (Figs.4d-f & 4d′-f′).The preserved pedal imprints show asymmetrical and plantigrade tetradactyl or pentadactyl morphology.The form of the pes is rectangular and elongated form.There is no impression of soft tissues or webbing in the pes imprints.Although some tracks show the digit V impression (Figs.4d & d′), most of the pes cannot be identi ed as the trace of digit V.The length ratios of digit to digit IV are broadly similar, but digit I is always shorter than the others.The pes phalanges and claw marks are found in some slabs (Figs.4k-n).
; and (5) Rhamphichnus 24 .Among these taxa, pterosaur tracks in the Hwasun Seoyuri tracksite can be regarded as Pteraichnus based on their size and morphology.After the rst de nition of Pteraichnus in Stokes 21 , the diagnosis of Pteraichnus has been amended twice by Lockley et al. 25 and Billon-Bruyant and Mazin 16 .The amended diagnosis could be roughly de ned as "digitigrade, tridactyl, elongated, and asymmetrical manus; plantigrade, tetradactyl, elongated, and subtriangular pes", and the pterosaur tracks in the Hwasun Seoyuri tracksite can be referred to as Pteraichnus.The tracks in this study have distinctive size, morphological characters, and spatial gaps from previously reported other Pteraichnus ichnotaxa.However, it is hard to be con dent about whether all tracks are attributed to the same species of trackmaker or not because they have a wide size variation and do not make an obvious trackway.Therefore, we refer to Pteraichnus in the Hwasun Seoyuri tracksite only as Pteraichnus isp., without assignment to either known Pteraichnus ichnospecies or novel ichnospecies.

Discussion
Semi-aquatic behavior The interpretation of Pteraichnus isp.assemblage in the Hwasun Seoyuri tracksite is that manus tracks account for most of the samples.Several manus-dominated pterosaur ichnites have been reported in various geological time and space, and there are two possibilities for interpreting this imbalance in proportions.The rst possibility is a difference in load between forelimbs and hindlimbs [26][27][28] .Given the center of mass position in pterodactyloid located at the front of its body, the manus-dominated tracks would come from the division of body mass 29 .Because forelimbs support a higher portion of the weight than hind limbs, the manus imprints could have a higher potential of preservation than the pes 30 .However, while the various size of manus imprints (length from 20.14 to 55.85 mm; width from 6.38 to 25.67 mm) are found in most slabs, pes imprints are very rare, regardless of size.For example, the slab KDRC-HW-PT04 shows relatively larger manus imprints (length larger than 60 mm) with smaller manus imprints (length smaller than 25 mm), but no pes imprints are observed except for one partially preserved pes imprint (Figs.3d & e).Therefore, considering that only the manus imprints remain common in populations of various sizes, it is unlikely that the proportion of weight on the manus and pes may have resulted from this uneven preservation.
Another possibility is the semi-aquatic behavior of the trackmaker.Lockley and Wright 29 suggested that manus-dominated tracks and partially preserved or scratched pes marks might be attributed to swimming or semi-oating behavior when they touched the subaquatic sediments by forelimbs and paddling by hind limbs.Pteraichnus isp. in this study are also discovered with scratched lines probably pes claw marks (Figs. 4k-n).Moreover, the ripple marks and absence of desiccation marks also indicate a shallow lake margin, but a subaquatic (or brie y exposed) depositional environment.Also, most of the pterosaur tracks in the Hwasun Seoyuri tracksite are irregularly distributed, and overlapping one another.The randomly oriented tracks of pterosaurs have commonly been explained as the feeding and semi-oating behavior in shallow water 25 .When the trackmaker pterosaur was buoyant on the water surface, their forelimbs could touch the sediments without the pes imprints, while eating 31,32 .However, the swimming or oating behavior of pterosaurs is not fully understood.Hone and Henderson 33 stated that the pterosaurs might not be as stable on the water surface as the modern water bird due to their unstable body balance and low rostrum position.5][36][37] ), at least some pterosaurs are believed to have been familiar with semi-aquatic life.

Multi-aged Gregarious Flocks
Another characteristic of pterosaur tracks in this study is the high densities of various size imprints in the limited space.The average density of tracks in the Hwasun Seoyuri tracksite is 143/m², while the highest dense slab shows 175/m².Moreover, the manus and pes imprints in this study show a great amount of variability in both size and morphology.Given that the high density of over 100/m² of pterosaur tracks has been referred to as the gregarious behavior of the trackmaker 38 , the trace-bearing slabs with varioussized tracks suggest a multi-aged pterosaurian ock(s).Among the measurable manus samples (162 specimens), the maximum-minimum ratios of length and width are 2.77 and 3.48, respectively, and this indicates that these size variables are originated from heterogeneous samples (> 2).To gure out whether this heterogeneity originated from generation or not, the normality of samples was tested for the length and width of the manus.Both data are showing the normality with unimodal without any data transformation (Length: Shapiro-Wilk's W = .991,p = 0.382; Width: Shapiro-Wilk's W = .990,p = 0.342) (Fig. 5).The normality and unimodal distribution make it possible to deduce that the tracks originated from the same population 39,40 .Thus, the normality and heterogeneity of pterosaur track assemblage would originate from the ontogenic stages from a single population of pterosaur ock.
Many studies provide a glimpse of multi-aged gregarious behavior, from a hatchling age to adult.Multiaged Caiuajara dobruskii bonebeds from Brazil indicate that this species was living in ocks from a very young age 41 .3][44][45][46] ), and gregarious nesting (e.g. 46).Therefore, the previously known ecology of pterosaurs and wide variation of track size support that they may have been made by a multi-aged pterosaur ock.Nevertheless, we could not exclude the possibility that some of the different-sized tracks could be attributed to multiple taxa of pterosaurs because many kinds of seabirds consist of multi-species feeding ock 47 , and even if they are each the groups of different species, they could make footprints in the same area if they shared ecological space.
However, given that the size of footprints is widely distributed and do not making speci c groups, it can be deduced that most of the footprints are attributed to the multi-aged ock of pterosaur.It is hard to assume the ontogenetic stages of the tracks in this study with only footprints.It may include the entire ontogenetic stages from hatchlings to the adults or may contain partial stages, such as juveniles to subadults.Naish et al. 46 compared the small-sized pterosaur (Sinopterus dongi) and medium-sized pterosaur (Pterodaustro guinazui) of hatchling and adult, and their wingspan hatchling-adult ratio is 7.6 and 10.34, respectively.Given the pterosaurs show isometric ontogeny 45 , the size of digits measured from tracks could re ect the hole size of the trackmaker.The result that the maximum-minimum ratio of pterosaur manus tracks (manus: 2.77; pes: 3.28) indicates that it covers a considerable portion of the entire pterosaur's life span.

About The Trackmaker
With the discovery of many pterosaur tracksites worldwide, there have been various attempts to nd evidence for estimating possible trackmakers.The rst approach for identifying the trackmaker is integrating the osteological data of pterosaurian body fossils with information preserved in trace fossils, and diverse variates can be considered for the suspected trackmaker 48 .The manus and pes anatomy of Pteraichnus isp.In the Hwasun Seoeyuri tracksite shows the fully laterally rotated manus imprints and anteriorly oriented tetradactyl pes, and they are representative features of pterodactyloid, rather than nonpterodactyloid 24 .However, while most other information which could identify the trackmaker is obtained from pes imprints, it is hard to make a comparison that Pteraichnus isp.assemblage in the Hwasun Seoyuri tracksite mainly consists of manus imprints with rarely and partially preserved pes imprints.Therefore, only the information about manus and pes size is used in this study to identify the trackmaker.
Another approach for estimating the possible trackmaker is integrating osteological gures obtained from trace fossils with pterosaurian body fossil records in the vicinity.Nevertheless, the pterosaur body fossil records in the Korean Peninsula are very rare, including partially preserved wing nger phalanxes and isolated teeth of borepteridae in the Hasandong Formation (Aptian) [58][59][60][61] , with represents a geological time gap from the Hwasun Seoyuri tracksite.Despite expending the scope to the Upper Cretaceous strata of East Asia, the pterosaur fossil records are not su cient to be a candidate for Pterichnus isp. in this study, because of the lack of skeleton record or of not being of comparable size for the trackmaker.Therefore, the pterodactyloid, which was not reported as a skeleton fossil record, existed in the Late Cretaceous Korean Peninsula, and produced Pteraichnus isp. in the Hwasun Seoyuri tracksite.
Small-sized pterosaur distribution in the Late Cretaceous.
3][64][65][66][67][68][69][70][71][72] ).3][64][65] ); in particular, this tendency was reinforced in small pterosaurs (e.g. 2,65).However, McGowan and Dyke 69 stated that birds and pterosaurs occupied different ecological niches in that they had a difference in limb morphospace.Moreover, the declines in pterosaur diversity and disparity could be attributed to sampling bias derived from exceptional pterosaur fossil-rich deposits (Lagerstätten) 67,68 .Nevertheless, Benson et al. 70 argued the increase of pterosaur body size was coincident with avian radiation, and it derived to pterosaur gigantism, which made it vulnerable to extinction.However, Longrich et al. 71 's work demonstrated that at least some pterosaurian families had not declined until the K-Pg extinction, and several new pterosaur taxa have recently been found in the Upper Cretaceous deposits in a range of sizes from relatively small to huge as the number of samples increases 72 .Thus, a multi-pronged approach to elucidating the diversity and radiation of the Late Cretaceous pterosaur is needed.
The small-sized pterosaur, which is small enough to make the tracks in this study, had been hardly reported until the 2000s.However, a few small-sized pterosaurs were discovered recently in the North American and Afro-Arabian continents, such as Piksi barbarulna in Montana 73 , the tiny azhdarchoid pterosaur in British Columbia, Canada 74 , Alcione elainus in Morocco 71 , and Mimodactylus libanensis in Lebanon 54 .Several pterosaur ichnofossil records have been reported in the Late Cretaceous and continue to the end-Cretaceous 75 .−80 ), but tracks of small-sized pterosaur are also only reported in Morocco 79 and Korea (in this study) (Fig. 6).In particular, Pteraichnus isp. in the Hwasun Seoyuri tracksite is the rst evidence that the small-sized pterosaur continued into the Late Cretaceous East Asia (Fig. 7).The small-sized pterosaur fossil records after the mid-Cretaceous are on the rise for both body and trace fossils.Although the number of samples is small, these samples are not only relatively diverse among the lineages that survived to the end of the Cretaceous, but are also widely distributed worldwide.Hence, considering this tendency, although the pterosaur gigantism continued to the end of the Cretaceous, the small-sized diversity of pterosaurs was maintained and survived until the Late Cretaceous East Asia, rather than the conventional ideas.

Conclusion
Small-sized pterosaur tracks are preserved from the Upper Cretaceous Jangdong Formation of the Neungju Basin, Korea, where abundant dinosaur trackways had been reported.These pterosaur tracks are assigned to Pteraichnus isp., and are some of the smallest pterosaurian tracks in the Late Cretaceous.
The track assemblage consists of manus-dominated tracks with probably claw marks.Manus-dominated tracks have been interpreted as an imbalance of body mass or aquatic behavior, such as swimming or semi-oating on the surface.Such randomly oriented tracks also indicate the possibility of swimming, or oating behavior with feeding.The high density of variable-sized tracks could be inferred as gregarious behavior of a pterosaur multi-aged ock(s) (Fig. 8).Comparable-sized pterosaurs with the candidate for Pteraichnus isp. in the Jangdong Formation have only been reported in North America and Afro-Arabia.Therefore, Pteraichnus isp. in the Hwasun Seoyuri tracksite would be attributed to the not-yet found pterosaurian that lived in the Late Cretaceous Korean Peninsula.Pteraichnus isp. in this study could be the rst ichnological evidence for small-sized pterosaurs that were widely distributed not only in North America, Arabia, and North Africa, but also in East Asia.

Figure 1 Location
Figure 1

Figure 5 Frequency
Figure 5

Figure 6 Comparison
Figure 6