Large tetrapod burrows from the Middle Triassic of Argentina: a behavioural adaptation to seasonal semi-arid climate?
Abstract
We report the discovery of large burrow casts in the early Middle Triassic Tarjados Formation, at Talampaya National Park, north-western Argentina. Facies analysis indicates the burrows are preserved in sandbars deposited by an ephemeral river under semi-arid and seasonal climatic conditions. The structures are mostly preserved in longitudinal cross-section and consist of an opening, an inclined tunnel (ramp), and a terminal chamber. The ramp is 8–14 cm in height, up to 130 cm in length and penetrates 49–63 cm bellow the palaeosurface with an inclination of 22°–30°. We studied burrow cast dimensions, overall architectural morphology, surficial marks, and compared them with other large burrows of both invertebrate and vertebrate origin. A tetrapod origin of the burrow casts was established based on: distinctive architecture, and size, which is more than twice the most common size range for large terrestrial invertebrate burrows. Comparison with other Upper Permian and Triassic tetrapod burrows allows us to identify three general morphological groups: (1) simple inclined burrows; (2) helical burrows; and (3) burrow network complexes, representing different behaviours. A study of tetrapod body fossils preserved within other Upper Permian and Triassic burrows shows that the Tarjados structures were most likely produced by non-mammalian cynodonts. The environmental and climatic context suggests that aridity and seasonality played a fundamental role selecting burrowing behaviour in therapsids and that by the Early–Middle Triassic their burrowing behaviour attained a complexity comparable to modern mammals.
Keywords
Recent fieldwork in the Talampaya National Park (La Rioja Province) provides information about the fossil tetrapods preserved at the initial stages of the Ischigualasto-Villa Unión Basin infill. These new discoveries includes several relatively large burrow casts found in fluvial facies of the Tarjados Formation, and constitute the first time that such burrows have been described in Early-Middle Triassic strata in South America.
In general, reports of large burrows in continental deposits have greatly increased during the last two decades. Recent examples of invertebrate ichnogenera recorded in Mesozoic–Cenozoic fluvial sequences include Camborygma, Loloichnus, Lunulichnus, and Capayanichnus. Their tracemakers were attributed to freshwater crustaceans, such as crayfishes and crabs (Hasiotis & Mitchell 1993; Zonneveld et al. 2006; Bedatou et al. 2008; Melchor et al. 2010). Among vertebrates, lungfish aestivation burrows are perhaps the most numerous (e.g. Vaughn 1964). However, most large burrow casts described from continental successions are interpreted as having been dug by tetrapods, particularly synapsids.
Terrestrial tetrapod burrows have been described from a number of fluvial and aeolian successions dating from the present day back to the Devonian (e.g. Barbour 1895; Olson & Bolles 1975; Voorhies 1975; Martin & Bennett 1977; Smith 1987; Hasiotis et al. 1993, 2004; Groenewald et al. 2001; Miller et al. 2001; Damiani et al. 2003; Hembree et al. 2004; Loope 2006, 2008; Colombi et al. 2008; Hembree & Hasiotis 2008; Sidor et al. 2008; Martin 2009; Schmeisser et al. 2009; Modesto & Botha-Brink 2010; Storm et al. 2010; Bordy et al. 2011; Tałanda et al. 2011). Upper Permian and Lower-Middle Triassic burrows were, until now, only known from south-western Gondwana. They were described from the Teekloof, Balfour, Katberg and Driekoppen formations in the Karoo Basin of South Africa, corresponding to the Pristerognathus, Tropidostoma, Dicynodon, Lystrosaurus, and Cynognathus assemblage zones respectively, (Smith 1987; Groenewald 1991; Groenewald et al. 2001; Damiani et al. 2003; Modesto & Botha-Brink 2010; Bordy et al. 2011) and the Omingonde Formation of Namibia (Smith & Swart 2002) and the Fremouw and Lashly formations of Antarctica (Babcock et al. 1998; Hasiotis et al. 1999; Miller et al. 2001; Sidor et al. 2008). The South American record is scanty. Tetrapod burrows were recently described from the Permian of the Paraná Basin, Brazil (Dentzien-Dias 2010) and one record is only known from the Upper Triassic of Argentina (Ischigualasto Formation) (Colombi et al. 2008). This later occurrence and an example described from the Holy Cross Mountains of Poland (Tałanda et al. 2011) are the only Late Triassic tetrapod burrows described from Pangea.
In this study we analyse the dimensions, overall architectural and surface morphology of the burrow casts and discuss the possible identity of the producer of the Tarjados burrows by comparing them with extant burrows known from modern environments. We also compare the Tarjados burrows with other Upper Permian and Triassic burrows and show how their general morphology relates to the tracemaker and its behaviour. Finally, we review the palaeoenvironmental and palaeoclimatic context in which known Upper Permian and Triassic tetrapod burrows occur wordwide.
Geological setting
In Argentina, the non-marine Triassic sedimentary record is preserved in a series of extensional basins located along the western margin of southern South America (e.g. Stipanicic 2002). Among them, the Ischigualasto-Villa Unión Basin infill is a nearly continuous continental Triassic succession that includes up to 6000 m of alluvial, fluvial and lacustrine deposits (e.g. Stipanicic & Bonaparte 1979; Stipanicic 2002). Its outcrops are widely distributed in the provinces of San Juan and La Rioja in northwestern Argentina (Fig. 1). The sequence is lithostratigraphically divided into several units: at the base, the Talampaya and Tarjados formations (Romer & Jensen 1966) unconformably rest on Palaeozoic deposits and they are unconformably covered by the Agua de la Peña Group (e.g. Stipanicic 2002; Mancuso 2005). The Ischigualasto-Villa Unión Basin is widely known for its rich tetrapod content (e.g. Bonaparte 1997; Marsicano et al. 2001; Langer et al. 2010), nearly all described from to the upper part of the succession (Agua de la Peña Group). The lower part (Talampaya and Tarjados formations) is nearly devoid of fossil remains that, until the present study consisted of a manus-pes print of a non-mammalian therapsid (Talampaya Formation) and fragmentary skeletal remains of dicynodonts from the Tarjados Formation (Cox 1968; Bonaparte 1997; Mancuso et al. 2010).
The basal contact of the Tarjados Formation was interpreted as an erosional unconformity over the thick red ephemeral fluvial deposits of the Talampaya Formation (Caselli et al. 2004). A regional unconformity constitutes the upper contact of the Tarjados Formation with the overlying tuffaceous sandstone and siltstone at the base of the Agua de la Peña Group (the Chañares Formation) (Rogers et al. 2001). The Tarjados Formation is divided in two members (Romer & Jensen 1966), which consist of thinning and fining-upward successions of sandstone and mudstone (Table 1, Fig. 2). Both members are interpreted as deposited by ephemeral fluvial systems interbedded with eolian sandstone and playa lake deposits (Caselli 2000; Nucci & Caselli 2000; Caselli et al. 2004), the most distinctive difference between them being their contrasting colour. Thus, reddish colours characterize the Lower Member and white/grey hues characterize the Upper Member where the burrows are preserved (Fig. 2).
| Interpretation of facies | Lithology | Structures | Bedding |
|---|---|---|---|
| Lower member | |||
| Fluvial system (∼25 m) | Moderate red medium to fine-grained sandstone (St, Sp) | Trough and planar cross-stratication | Lenticular to tabular beds with 0.5–1 m thick |
| Moderate red mudstone (Fm) | Massive, horizontal lamination, mudcracks | Tabular beds with 0.1–0.4 m thick and laterally persistent for hundreds of metres | |
| Playa lake (∼8 m) | Moderate reddish brown fine-grained sandstone and mudstone (Fl, Fm) | Massive, horizontal lamination, mudcracks, carbonate concretions | Tabular bed with up to 8 m thick and laterally persistent for hundreds of metres |
| Unconfined ephemeral flows associated with floodplain and eolian deposits (∼120 m) | Moderate red fine- to medium-grained sandstone (Sh, Sp) | Horizontal lamination, planar cross-stratification | Lenticular to tabular beds with 0.5–3 m thick |
| Moderate red mudstone (Fl, Fm) | Massive, horizontal lamination, mudcracks | Tabular beds with 0.05–0.2 m thick and laterally persistent for tens of metres | |
| Moderate red well-sorted fine sandstone (Sap) | Asymptotic planar cross-stratification | Tabular to lenticular beds with 0.2–0.5 m thick | |
| Upper member | |||
| Ephemeral fluvial system (∼100 m) | Moderate red intraformational conglomerate (Gm) | Irregular to sub-rounded mudstone clasts | Lenticular beds with 0.2–0.6 m thick, with erosional basal boundaries |
| Light greenish grey fine- to medium-grained sandstone (St, Sp, Sh, Sm) | Planar and trough cross-stratification, horizontal lamination and, massive structure occasionally mottled coloured | Tabular to lenticular beds with 0.05-0.6 m thick, with erosional and/or non-erosional basal boundaries | |
| Moderate red mudstone, subordinate fine-grained sandstone light greenish grey banding mudstone (Fl, Fm) | Horizontal lamination, desiccation cracks, occasionally mottled coloured | Tabular beds with 0.5–1 m thick, and extent laterally for tens of metres, and have non-erosional boundaries | |
Palaeoenvironment
In the Río Gualo area (Fig. 1), we recorded the sedimentological section (Fig. 2). The sequence is characterized by interbedded tabular sandstones and mudstones with lenses of conglomerate (Table 1, Fig. 3). These intraformational conglomerate (Gm) lenses generally form lag deposits at the base of the channels (Fig. 3A, B).They are characterized by irregular to sub-rounded moderate red (5R4/6) mudstone clasts, ranging from 2 to 30 cm in diameter however towards the top of the Upper Member conglomerate is dominated by rounded quartz pebbles. The S facies (Table 1) is dominated by 1–2 m-thick lenticular and tabular beds of normally graded light greenish grey (5GY8/1) fine- to medium-grained sandstone with planar (Sp) and trough cross-stratification (St) and horizontal lamination (Sh) and, occasionally, massive structure (Sm) (Fig. 3A, C). The large burrow casts, fossil footprints, and root casts occur in this facies. Facies F (Table 1) is characterized by tabular beds of horizontal laminated moderate red (5R4/6) mudstone (Fl), subordinate fine-grained sandstone, locally with mottled colour. The mudstone intervals vary between 0.5 and 1 m in thickness and commonly show light greenish grey (5GY8/1) banded beds and different hierarchies of desiccation cracks (Fig. 3A, D). Invertebrate dwelling structures, such as Palaeophycus isp. and Arenicolites isp, are commonly present in this facies as well as isolated large burrow casts.
The fining-upward succession that comprises the Tarjados Upper Member is interpreted as having been deposited by an ephemeral river and it is characterized by the repeated facies sequences of 1.5–4 m thickness (Fig. 3A). Each facies sequence starts with an intraformational conglomerate (Gm), followed by planar/trough cross-stratified medium-grained sandstone (Sp/St) that passes upward to planar cross-stratified (Sp) and horizontal laminated (Sh) fine-grained sandstone, and occasionally massive sandstone with mottled colour. The S facies are interpreted as emergent downstream prograding sand bars of ephemeral channels. The sequence terminates with horizontal laminated mudstones (Fl), commonly showing light greenish grey banding, desiccation cracks, and root marks, interpreted as deposited in a floodplain alluvium (e.g. Fisher et al. 2007; Pace et al. 2009).
The stacking pattern of Tarjados Upper Member strata displays lateral and vertical variations. Laterally, the intraformational conglomerates can be absent, thus the succession starts with lenticular, erosively-based, channel bodies without lag, or lenticular to laterally extensive non-erosively-based channels. Both erosive and non-erosive channels are overlain by downstream prograding bar deposits. This lateral variation is related to the dynamics of the fluvial system, recording differences between primary (with erosive base) and secondary channels, channel migration behaviour, and waning discharge with emergence during periods when the stream system avulsed or dried up (e.g. Fisher et al. 2007). The vertical variation of facies sequences is commonly an upward reduction in the F facies and the amount of the mudstone clasts within the channel lags. A gradual decrease in the intrafomational clasts within channel lags strongly suggests a decrease of accommodation space in the basin during the deposition of the Tarjados Upper Member (e.g. Wright & Marriott 1993).
As previously mentioned, the Tarjados Formation has been interpreted as deposited by ephemeral fluvial systems based on its repetitive fining-upward vertically stacked beds of sandstone and mudrock. The presence of hiatus surfaces in the sandstone bar deposits, evidenced by the tetrapod footprints and burrows, root casts, and colour mottling, strongly suggest periodic fluvial activity, with alternating periods of flooding and subaerial exposure. Moreover, the light colour mottling and banding in some mudstone beds, and different hierarchies of desiccation cracks, carbonate concretions, and root marks also suggest that the water table was subject to seasonal vertical fluctuations. The small-scale sand dunes that migrated on the floodplains and the extensive mudcracks indicate prolonged dry conditions. Taken together, this evidence suggests that water supply in the Tarjados Basin was strongly seasonal, characterized by the alternation of short wet and long dry seasons, most probably under an overall semi-arid climatic regime.
Tarjados burrow morphology
Six large burrow casts are analysed in this study. Four of them are preserved in longitudinal and transverse cross-sectional views (Figs 4–6), and two as 3-D internal casts (Fig. 7); all of them remain in the field (detail measurements of each burrow are presented on Table 2).
| Burrow # | Opening diameter | Ramp | Terminal chamber | Length | Deep | Incl | Orient. | ||
|---|---|---|---|---|---|---|---|---|---|
| Height | Width | Height | Width | ||||||
| 1 | 13 | – | – | – | 129 | 55 | 22° | NE | |
| 2 | 20 | 14 | – | 16 | – | 136 | 63 | 30° | NE |
| 3 | – | – | – | 11 | 26 | – | – | – | – |
| 4 | 16 | 8–13 | - | 15.5 | 25 | 122 | 49 | 24° | SW |
| 5 | – | – | – | 14 | 24 | – | – | – | E-NE |
| 6 | – | – | – | 10 | 27 | – | – | – | E-NE |
Inclined large burrow casts
The burrow casts are inclined structures (Fig. 4) and consist of an upper proximal portion (opening), a descending tunnel (ramp), and a lowermost terminal chamber. The preserved length of the burrows ranges from 122 to 136 cm, including the terminal chamber when present (burrows 2 and 4). The penetration depth ranges from 49 to 63 cm and the inclination varies from 22° to 30° (Table 2).
Branching is absent and although the outer contact is sharp and well-defined, with no impressions of a burrow lining were observed. The outer contacts of burrows 1–3 are coated by a thin gypsum deposit interpreted as a secondary, more recent precipitation, which is common in the study area (Fig. 4). The gypsum deposit makes it difficult to see the surface markings on the burrow casts in the field.
In burrows 2 and 4 the proximal entrance of the burrow is preserved. It is funnel-shaped and tapers towards the ramp (Fig. 4C, D) and ranges from 16 to 20 cm in height. The inclined ramp has roughly parallel walls and has a height range of 8–14 cm, with an average height of 13 cm. In burrow 1, an expansion in height of the middle portion of the ramp (22 cm in height) is recorded and this is interpreted as a medial chamber (Fig. 4A, B). The height of the ramp decreases slightly from the opening down to the domed terminal chamber (Fig. 4C, D) where the height again increases (Table 2). Due to the orientation of the burrow casts to the plane of the cliff exposure the transverse cross-section of the terminal chamber is only observed in burrow # 3, where it is elliptical with a bilobate ventral surface (Fig. 6).
The burrows are preserved in medium-grained massive sandstones (burrows 2–4, Figs 4C, D, 6) and medium-grained planar cross-stratified sandstones, both interpreted as facies of exposed portions of mid-channel bars (Fig. 4; burrow 1). Two types of burrow infill are recognized; massive sandstone throughout the burrow (burrows 2–4, Figs 4C, D, 6) and massive sandstone with internal erosional surfaces (burrow 1, Fig. 4A, B). With the latter angular mudstone clasts occur within the terminal portion. The internal discontinuity within the burrow fill represents a break in sediment supply and suggests two stages of burrow infilling (Fig. 4A, B). The surface also involves an expansion in height of the ramp (medial chamber) and is here interpreted as evidences for re-occupation of an abandoned, half filled burrow (Fig. 4A, B).
All studied burrows dip with an inclination of 22°–30° and with burrows 1 and 2 the entrance is oriented to the NE, while the entrance to burrow 4 is orientated to the SW (Table 2). All of them are aligned perpendicular to the palaeo-downstream direction.
Isolated terminal chamber internal casts
Burrow casts 5 and 6 are short tunnels with parallel walls (ramp) that expand into a dome-shaped terminal chamber (Fig. 5). The height of the terminal chambers range from 10 to 14 cm, while its width varies between 24 and 27 cm (Table 2). The structures are preserved as three-dimensional internal casts filled with highly bioturbated, fine-grained sandstone. These casts occur at the horizon with the floodplain mudstones and are infilled with bioturbated sandstone from the overlying bed (Fig. 5). The invertebrate bioturbation is of simple dwelling structures, mostly Palaeophycus isp., although identification of individual trace fossils is difficult.
Similar to the inclined large burrows these are also oriented to the E-NE and perpendicularly to the palaeo-downstream direction (Table 2).
Discussion
Distinguishing invertebrate and tetrapod burrows
There is no single morphological feature that uniquely links large burrow structures to tetrapods. When body-fossils are not preserved inside the burrow, there are a number of characteristics that should be studied in order to resolve the question of the original digger (Table 3). The distinction between invertebrate and tetrapod makers of large burrows is based mostly on the comparisons with modern fossorial animals, the burrow dimensions, the overall architecture, and the presence of marks on the burrow walls (e.g. Groenewald et al. 2001; Miller et al. 2001; Hasiotis et al. 2004; Loope 2006; Sidor et al. 2008).
| Morph. Group | Age | Unit | Location | Name | Overall architectural morphology | Surface features | Dimensions cm | Animal in burrow | Reference | ||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Architecture | Orientation | Cross-Section | Branching | Diam. | Depth/length | ||||||||
| Simple inclined burrows | Middle/Late Permian | Paraná Basin | Brazil | Small Burrows | Simple straight to slightly curved with enlarged entrance | Inclined 30º | – | No | – | 4–7 | –/30–60 | No | Dentzien-Dias (2010) |
| Middle/Late Permian | Paraná Basin | Brazil | Medium Burrows | Simple straight to slightly curved with terminal chamber | Inclined 40º | Elliptical, Few ventrally bilobate | No | – | 9–15 | –/33–98 | No | Dentzien-Dias (2010) | |
| Early Triassic | Balfour and Katberg Formations | South Africa | Large scale Scoyenia | Simple straight with terminal chamber | Inclined 0º–10º | – | No | Scratch marks on lateral walls | 20–45 | –/30 | Dicynodont (Lystrosaurus, Dicynodon) | Groenewald (1991) | |
| Early Triassic | Balfour and Katberg Formations | South Africa | Histioderma | Simple straight with terminal chamber | Inclined 40° | – | No | Scratch marks on lateral walls | 20–50 | –/100 | ?Dicynodont (Lystrosaurus) | Groenewald (1991) | |
| Early Triassic | Balfour and Katberg Formations | South Africa | Small-scale Scoyenia | Simple, strait | Inclined 20°–30° | – | No | – | 3 | –/30 | Unidentified bone fragments | Groenewald (1991) | |
| Early Triassic | Balfour Formations | South Africa | NMQR 3606 | Relatively straight. Entry, ramp and terminal chamber | Inclined 12º | Elliptical | No | No | 12 × 34 | – | Dicynodont (Lystrosaurus) | Modesto & Botha-Brink (2010) | |
| Early Triassic | Fremouw Formation | Antarctica | Type L burrow | Simple. Rarely J shaped | Inclined to subhorizontal | Circular –elliptical. Few ventrally bilobate | Rare, horizontal and vertical | Scratch marks tangential to long axis | 2–6.5 | 15/– | No | Miller et al. (2001) | |
| Early Triassic | Fremouw Formation | Antarctica | Type G Burrow | Simple, strait to slightly curved. One possibly helically coiled | Subhorizontal to gently inclined | Elliptical | Rare | Scratch marks tangential to long axis | 8–19 | 8 –25/– | No | Miller et al. (2001) | |
| Early Triassic | Katberg Formation | South Africa | Very large burrow | Single, relatively straight. Entry, ramp and rounded terminus | Sub–horizontal. Inclined 30º | Circular to slightly elliptical | no | Vertical and horizontal scratch marks on lateral walls | 25–40 | 150/300 | No | Bordy et al. (2011) | |
| Middle Triassic | Lashly Formation | Antarctica | Tetrapod ichnogenus B | Simple with terminal chamber | Horizontal to gently inclined | Elliptical to ventrally bilobate | No | Scratch marks on lateral walls and floor | 5 | – | No | Sidor et al. (2008) | |
| Late Triassic | Keuper Formation | Poland | Large burrow casts | Straight to slightly curve, terminate in chambers | Inclined 18–36º | Elliptical | Rare | No | 7 –9 | 60–120/100–375 | No | Tałanda et al. (2011) | |
| Helical burrows | Late Permian | Teekloof Formation | South Africa | Helical burrow (daimonelices) | Helically spiraled with horizontal terminal chamber | Vertical. Ramp angle 10º–32º | Plano-convex to ventrally bilobated | No | Scratch marks on lateral walls and floor | 6–16 | –/50–75 | Dicynodont (Diictodon) | Smith (1987) |
| Early Triassic | Balfour and Katberg Formations | South Africa | Gyrolothes/Daimonelix | ?Helical, loosely coiled | Ramp angle 10º–15º | – | No | Scratch marks on lateral walls | 20–45 | – | Unidentified bone fragments | Groenewald (1991) | |
| Burrow networks complexes | Early Triassic | Balfour and Katberg Formations | South Africa | Thalassinoides | Complex net-like pattern of interconnected tunnels | Horizontal | – | Numerous | No | 3–15 | – | No | Groenewald (1991) |
| Early Triassic | Driekoppen Formation | South Africa | Burrow complexes | Enlarged entrance, tunnels as network complex with terminal chambers. | Inclined 1°–23° | Ventrally bilobate –oval | Numerous, curved | Scratch marks along the bases | 5–12 | – | Cynodont (Trirachodon) | Groenewald et al. (2001) | |
| Late Triassic | Ischigualasto Formation | Argentina | Large diameter burrow | Vertical shaft, tunnels as network complex with intermediate and terminal chamber | Horizontal to subhorizontal | Elliptical | Numerous, winding | Scratch marks on lateral and dorsal walls. Poorly defined | 10 | – | No | Colombi et al. (2008) | |
| Terminal chambers | Permo-Triassic | Balfour Formations | South Africa | Trinaxodon burrow cast | Terminal chamber | – | Ventrally bilobate | – | Scratch marks on lateral and dorsal walls | – | – | Cynodont (Thrinaxodon) | Damiani et al. (2003) |
| Early Triassic | Fremouw Formation | Antarctica | Tetrapod ichnogenus A | Terminal chamber | Subhorizontal | Ventrally bilobate | No | Scratch marks on lateral walls | 15.7 | – | No | Sidor et al. (2008) | |
To interpret the putative producer of a trace fossil, the size of the burrow is the first useful parameter. In solitary species the burrow dimensions closely match with the size of the tracemaker. In general, the diameter of their burrows are as small as possible to reducing the energy used in excavation (Anderson 1982; White 2005). In the Tarjados large burrows the height of the ramp and the terminal chamber ranges from 10 to 15 cm (Table 2), thus providing an approximate idea of the dimension of the tracemaker, and if a tetrapod produced the burrow, that measure would be the approximate hip height (or slightly less if the animal kept a crouching position inside the tunnel).
In non-marine environments, burrowing invertebrates have a size range that slightly overlaps that of tetrapods (Table 3). To date all the burrows containing tetrapod skeletal remains are more than 5 cm in diameter, and commonly more than 10 cm, whereas invertebrate burrows are typically 2–5 cm wide. The most common diameter of burrows attributed to crayfish, such as Camborygma from the Upper Triassic Chinle Formation, have a diameter range of 0.5–12.5 cm but most commonly vary between 2 and 5 cm (Hasiotis & Mitchell 1993). Other burrows attributed to crayfish, such as Loloichnus from the Late Jurassic–Late Cretaceous of Patagonia, ranges from 1 to 2.5 cm (Bedatou et al. 2008). Although the dimensions of burrows are not completely diagnostic for distinguishing those produced by invertebrates and tetrapods, the architectural morphology of the burrows is more enlightening.
Several architectural morphologies can be recognized in burrows attributed to tetrapods (Fig. 8). Many Permian and Triassic burrows that have tetrapod occupants are elliptic to circular in cross-section and in many cases the ventral surface is bilobate, as in the Tarjados burrows (Table 3, Fig. 6). However, the cross-sectional profile varies along the burrow systems (Hasiotis et al. 2004), thus the presence of a bilobate floor depends on the portion of the burrow that is preserved. The significance of the bilobate floor is uncertain. Based on the large size of their burrows (diameter approximately 30 cm), and the small size of the individuals preserved inside the burrows (skull width approx. 10 cm), Groenewald et al. (2001) proposed that the bilobate bottom was related to a two-way traffic. In contrast, Damiani et al. (2003) proposed that it might represent paths worn down by the tracemaker’s feet. Accordingly, documentation of burrow casts of extant skinks, which have a longitudinal median groove, are produced by the sprawling stance of one individual (Hasiotis et al. 2004).
The surface markings on tetrapod burrow casts appear to be most likely preserved at the base and lateral walls of the excavations, and they are aligned with the long axis of the burrow (Table 3). However, many burrow casts lack surface marks and it has been proposed that the absence of these interpreted scratch marks could be related to the age of the burrows, as the continuous use could erase the original marks (Modesto & Botha-Brink 2010). Unfortunately, the way that the Tarjados burrows are exposed (longitudinal cross-sectional view) and the presence of intense bioturbation in the terminal chamber casts precludes the observation of any surficial marks.
Burrows attributed to freshwater decapod crustaceans are potentially comparable to those of tetrapods, although most of them are predominantly vertically orientated. Loloichnus includes thick-walled Y-shaped burrows (Bedatou et al. 2008) and Camborygma are vertical straight shafts with a single terminal chamber, or complex structures with multiple entrances and chambers that commonly lack of a major horizontal component (Hasiotis & Mitchell 1993; Hasiotis et al. 1993) (Fig. 7A, B). Burrows that display a simple vertical architectural morphology with a bulbous terminus are generally identified as lungfish aestivation burrows but are often confused with those attributed to crayfish (Fig. 7C) (Hasiotis et al. 1993). In fact, is this type of morphology that clearly separate lungfish burrows from those produced by tetrapods (see Hasiotis et al. 1993). Other burrows attributed to decapod crustaceans are included in the ichnogenera Lunulichnus and Capayanichnus, the latter interpreted as produced by freshwater crabs (Fig. 7D, E). They are predominantly simple, vertically orientated, and lack terminal enlargements. In some cases, Capayanichnus have an overall ‘L’ shape (Zonneveld et al. 2006; Melchor et al. 2010).
Based on the characters discussed above, it is possible to attribute the large burrows recorded from the Tarjados Formation to the digging behaviour of tetrapods based on: 1, their distinctive architectural morphology, as a simple inclined tunnel with a bilobate floor and a domed terminal chamber; and 2, their size, which is more than twice the most common size range described for large terrestrial invertebrate burrows.
Comparison with other permian and triassic burrows attributed to tetrapods
May it help in the identification of the burrow producer to consider the Tarjados burrows and other terrestrial burrows of the same age? Is the morphology of Permian and Triassic burrows characteristic of any particular tetrapod group? As a first attempt to answer these questions we analysed the reported examples of Permian and Triassic burrows from Gondwana interpreted to be produced by tetrapods (Table 3). The observed variability is resolved into three general morphological groups (Fig. 8) occurring throughout the fossil record: (1) simple inclined burrows; (2) helical burrows; and, (3) burrow network complexes. Also, isolated terminal chambers are recorded (see Table 3), although they cannot be positively assigned to any of the aforementioned morphological groups.
The results indicate that there is no strong correspondence, but a subtle coincidence, between the burrow morphology and the taxonomic group of tetrapods preserved inside. For example, dicynodonts are recorded within simple inclined and helical burrows, and cynodonts are preserved within network complexes and isolated terminal chambers. Because of the scarcity of body fossils preserved within burrows, any conclusions based on these associations are still highly speculative. The morphology of burrow system reflects how it was used and ultimately the biology of its tracemaker (Eisenberg & Kinlaw 1999). Most of the reported Permian and Triassic burrows consist of simple inclined tunnels (Fig. 8C, Table 3). The inclined burrows of the Tarjados Formation fall in this morphological group.
Today, similar tunnels are dug by semi-fossorial animals that use burrows as climatic shelters (Kinlaw 1999), such as those constructed by the gopher tortoise (Gopherus polyphemus) (Hansen 1963; Doonan & Stout 1994), the American alligator (Alligator mississipiensis) (Voorhies 1975) and many carnivorous mammals (Voorhies 1975). The curved shaft of the helical burrows (Fig. 8B) may save horizontal space and avoid neighbouring burrows (Martin & Bennett 1977), provide more effective protection from predators, and complicate the flow of air thereby limiting circulation and increasing heat interchange (Meyer 1999). Modern mammals that dig helical burrows include gophers, golden moles, and kangaroo rats (Butler 1995). Recent examples of burrow network complexes (Fig. 8A) are typically permanent residences for their producers and are used for several purposes, including storage, latrines, breeding, and foraging (Kinlaw 1999). Modern producers of such burrows include the plains vizcacha (Lagostomus maximus) and the tucu-tucu (Ctenomys mendocinus) of Argentina (Mares et al. 1989; Albanese et al. 2010), and the prairie dog (Cynomys leucurus) of North America (Sheets et al. 1971).
The triassic tetrapod burrowers and possible tarjados tracemakers
Among the Triassic burrows that contain skeletal remains, only a few can be confidently considered to preserve the remains of the original tracemaker (i.e. a skeleton or skeletons that are articulated in life position and with body sizes consistent with the diameter of the burrow) (Smith 1987; Groenewald 1991; Groenewald et al. 2001; Smith & Swart 2002; Damiani et al. 2003; Retallack et al. 2003; Modesto & Botha-Brink 2010). At present, the identified tracemakers are members of the therapsid clade, cynodonts and dicynodonts (see Table 3). The best-known examples are the cynodonts Trirachodon (Groenewald et al. 2001; Smith & Swart 2002) and Thrinaxodon (Damiani et al. 2003). Among dicynodonts, disarticulated remains of Lystrosaurus and Dicynodon sp. were found in simple inclined burrows (Groenewald 1991; Modesto & Botha-Brink 2010), although the evidence used to identify these taxa as the original diggers not strong.
Based on the study of their anatomy, several Early to early Middle Triassic tetrapods were proposed to have evolved burrowing adaptations such as the procolophonid Procolophon, as well as several dicynodont and cynodont taxa. The presence of large unguals (for scratch digging) and the pronounced overbite in procolophonids (i.e. to reduce the ingestion of dirt) were interpreted tentatively as burrowing adaptations (De Braga 2003). Moreover, Abdala et al. (2006) reported a multitaxon aggregation of the procolophonid Owenetta kitchingorum and the cynodont Galesaurus planiceps, and suggested shelter-sharing based on the high degree of articulation of the skeletal remains and the preservation of delicate bones in situ. Nevertheless, procolophonids have not yet been found in an unequivocal burrow structure, and a shelter-sharing behaviour does not confirm that these amniotes were diggers. Most dicynodonts exhibit postcranial features suitable for digging and a fossorial way of life, such as robust humerus relative to the femur, short antebrachium, and large broad manus with sharp broad claws (Yalden 1996; Ray & Chinsamy 2003).
However, the best-preserved dicynodont found in a burrow, the Late Permian Diictodon (Smith 1987), challenges this generalization. This taxon posses a slender humerus and poorly developed olecranon process, as occur in other similarly sized Permian dicynodonts (Angielczyk pers comm. 2011). Nevertheless, Diictodon shows other features suitable for digging such as cylindrical body, short limbs with smaller distal segment compared to the proximal, stout metacarpals, and long and wide manus, among others (Ray & Chinsamy 2003). The skeletons of non-mammaliaform cynodonts have no anatomical features that particularly suggest a burrowing lifestyle, nevertheless some taxa have been found articulated within burrows (Groenewald et al. 2001; Damiani et al. 2003). Botha & Chinsamy (2004) studied the bone histology of Trirachodon, and some relatives, in order to explore a correlation with lifestyle habits. Comparisons of relative bone wall thickness (RBT) to extant burrowing tetrapods reinforced the inference of a burrowing lifestyle for Trirachodon. The same was suggested for the South American non-mammalian cynodont Andescynodon due to its thick bone walls (Chinsamy & Abdala 2008). According to the discussion above, both therapsisds (non-mammalian cynodonts and dicynodonts) and parareptiles (procolophonids) are potential tracemakers of Permian-Triassic burrows based on overall morphology and/or bone histology. Nevertheless, dicynodonts were the only confidently identified tracemakers of Permian burrows, and non-mammalian cynodonts to Triassic burrows.
The Tarjados Formation has yielded only fragmentary skeletal remains of relatively large dicynodonts and vertebrae of a medium size archosaur (Cox 1968; Mancuso et al. 2010). Both of these taxa are too large to be the producers of the burrows described herein. Stratigraphically equivalent faunas are known in Argentina from the Lower-Middle Triassic Puesto Viejo Group (southern Mendoza) and the Middle Triassic Cerro de las Cabras Formation (Cuyana Basin). From these faunas, several dicynodonts were described (e.g. Bonaparte 1978; Domnanovich 2010). However, all taxa and unidentified remains correspond to medium-to-large sized animals, too big to be the putative tracemackers of the Tarjados burrows. Several non-mammalian cynodonts also are known from the same levels (the traversodontid Pascualhnathus polanskii, Rusconiodon mignoney and Andescynodon mendozensis, Cynognathus crateronotus, the gomphodontids Diademodon tetragonus, and Cromptodon mamiferoides; see Abdala & Ribeiro 2010). Some of them display sizes that fit the range of the Tarjados burrows, such as Pascualhnathus, Rusconiodon, Andescynodon and Cromptodon. Moreover and as discussed above, Andescynodon has been suggested to have fossorial behaviour based on bone histology (Chinsamy & Abdala 2008).
In the Paraná Basin of southern Brazil equivalent Lower–Middle Triassic levels have yielded tetrapods that also could represent potential tracemakers. The record of non-mammalian therapsids consist of an isolated stapes assigned to a dicynodont (Schwanke & Kellner 1999; Langer & Lavina 2000), and the non-mammalian cynodont Luangwa sudamericana (Abdala & Ribeiro 2010); only the latter has a size that matches the Tarjados burrows. The Brazilian beds have also yielded the parareptile Procolophon (see Cisneros 2008), already mentioned as a probable digger (De Braga 2003), and it also displays sizes that fit the Tarjados excavations.
Based on these observations, non-mammalian cynodonts can be suggested as likely tracemakers of the Tarjados burrows due to their size and the interpreted burrowing behaviour of some taxa (Fig. 9). Although non-mammalian cynodonts are unknown from the Tarjados Formation they are fairly diverse in the overlying succession, the Middle-Late Triassic Agua de la Peña Group. The possibility that the burrows were produced by a parareptile (Procolophon, or a close relative with equivalent behaviour and size) is not completely ruled out; although parareptiles are at present unknown from Argentina and their burrowing behaviour is weakly supported.
Terrestrial burrowing: a response to climate?
Most vertebrate burrows recorded in Devonian to Permian strata are interpreted as aestivation burrows of animals that lived in water bodies that seasonally dried out (e.g. Olson & Bolles 1975; Hasiotis et al. 1993; Hembree et al. 2004; Storm et al. 2010). Truly terrestrial burrows excavated subaerially, and attributed to tetrapods, are recorded since the Permian and have been interpreted as seasonal or permanent refuges for protection from predation, rearing of young, hibernation, and/or food storage, among others (Boucot 1990; Kinlaw 1999). Today, burrowing behaviour is common amongst tetrapods on arid or semiarid environments, in a large number of mammals, reptiles, amphibians, and a few birds (e.g. Voorhies 1975; Kinlaw 1999).
Tarjados burrows are preserved on the top of sandbars in ephemeral river channels deposited under seasonally dry conditions. The orientation of the burrows perpendicular to the channel flow direction might minimize their flooding when fluvial discharge occurred. This type of behaviour is observed in extant rodents as tuco-tucos (Ctenomys) in northwestern Argentina (e.g. Talampaya National Park) (V.K. pers. obs. 2011) that orientate their burrows perpendicularly to the stream direction in ephemeral rivers beds. Also, it is well known that not randomly distributed burrows can be related to environmental factors such as shading from sunlight and shielding from cold winds (Kay & Whitford 1978; Best 1988; Baumgardner 1991). For example, the cavy Microcavia australis orients active holes to the E thus, avoiding cold SE and S winds as is observed at the Reserve of Ñacuñán in centralwestern Argentina (Taraborelli et al. 2009). Also, a southern orientation is notably rare among savanna burrows of nine-banded armadillos (Dasypus novemcinctus) from northern Belize (Platt et al. 2004), and in other species of armadillos, as Dasypus hibridus, from Uruguay (González et al. 2001).
Today, burrow and soil temperatures are affected by fluctuation in ambient temperature. The soil temperatures in depths greater than 50 cm below ground are almost constant both diurnally and seasonally (Burda et al. 2007). The ground depth of the Tarjados burrows is on that range (49–63 cm) thus suggesting that they might be emplaced at that depth to maintain a more or less constant temperature. This is also consistent with the general idea that the more vertical burrows might be constructed for safety, thermoregulation, and canalization in the case of flooding. In contrast, the horizontal arrangement is more determined by the abundance and distribution of food resources and foraging strategies (e.g. Heth 1989; Spinks et al. 2000; Šumbera et al. 2003; Burda et al. 2005).
The environmental context of most of studied Permian and Triassic burrows is semiarid-arid and/or marked seasonality (Smith 1987; Miller et al. 2001; Smith & Swart 2002; Damiani et al. 2003; Smith & Botha 2005; Colombi et al. 2008; Dentzien-Dias 2010). This is congruent with the monsoonal circulation and strong seasonality postulated for the supercontinent of Pangea during Late Permian and Triassic times (e.g. Robinson 1973; Kutzbach & Gallimore 1989; Parrish 1993; Scotese et al. 1999; Sellwood & Valdes 2006). Such climatic regime would have resulted in increasing aridity in the low- and mid-latitude continental interiors, and polewards expansion of relative aridity and strong seasonality of rainfall (Parrish 1993). In that context, it has been suggested that burrowing played a significant role in allowing tetrapods to tolerate the increasing aridity in southern Gondwana and also with the high carbon dioxide and low oxygen levels associated to the end-Permian extinction event (Retallack et al. 2003; Smith & Botha 2005; Smith & Botha-Brink 2009). This hypothesis agrees with modern studies which postulate that the possession of a cool, moist burrow with stable temperatures underground is especially critical for survival in arid and semi-arid zones that are hot and dry with greatly fluctuating temperatures on the surface (Kinlaw 1999).
It is evident that aridity and seasonality played a fundamental role in selecting for burrowing behaviour, at least, among Permian and Triassic tetrapods. Moreover, the evidence suggests that the burrowing behaviour was present in therapsids as early as the middle/late Permian. By this time burrowing was already present with two types of structures, simple inclined and helical burrows (see Table 3). During the Early–Middle Triassic burrow architecture became more elaborate including not only 3D burrow complexes but also orientated simple burrows which are specialized shelters (avoiding excessive sunlight, cold wind, and/or flooding events). This would imply that during the early Mesozoic burrowing behaviour in basal therapsids already attained a complexity comparable to modern mammal examples.
Acknowledgments
We are very thankful to Kenneth Angielcyk, Nicholas Minter, and Luis Buatois for their critical comments on the early version of the manuscript. We are also very grateful to the two reviewers, R.M.H. Smith and an anonymous one, for improving the final version of the manuscript. Funding for this research was provided by projects UBACyT 20020100100728 (C.M.), PROSUL – CNPq 490340/2006-7 (C.S.), and PIP 11420090100209 (A.M.). This is the contribution R-22 of the Instituto de Estudios Andinos Don Pablo Groeber.
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Received: 1 March 2012
Accepted: 14 June 2012
Published online: 22 October 2012
Issue date: 1 April 2013
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