Identifying the type of trace fossil

These tiny structures have a unique combination of characteristics that have not been previously described. Several interpretations of the traces can be considered, including origins related to fungi, pedogenic processes, plant roots, and burrows. Of these, some structures can be ruled out on the basis of size. The gut region traces are much larger than individual or paired calcareous needle-fiber structures, which are reported to be no more than 20 μm in diameter (Verrecchia and Verrecchia, Reference Verrecchia and Verrecchia1994). Both needle-fiber structures (Verrecchia and Verrecchia, Reference Verrecchia and Verrecchia1994; Khormali et al., Reference Khormali, Abtahi and Stoops2006) and calcified filaments (Durand et al., Reference Durand, Monger and Canti2010) are inferred to be formed by mineralization of fungal hyphae traces, which are typically on the order of 25 μm across and are rarely greater than 50 μm (Sarjeant, Reference Sarjeant1975). In contrast, the gut region trace fossils are approximately 300 μm in diameter.

Taphonomic, diagenetic, and pedogenic processes can preserve a variety of rhizoliths—organosedimentary structures formed by or around roots (Klappa, Reference Klappa1980). Of these, rhizotubules and calcified roots can most closely resemble the gut region trace fossils. Rhizotubules are mineralized tubes that formed around a root or within the outer portion of voids left by decayed roots (e.g., Klappa, Reference Klappa1980; Kraus and Hasiotis, Reference Kraus and Hasiotis2006; Genise et al., Reference Genise, Bellosi, Verde and González2011). Roots can also become calcified when their tissues are replaced with calcite (Jaillard et al., Reference Jaillard, Guyon and Maurin1991; Khormali et al., Reference Khormali, Abtahi and Stoops2006). Although rhizotubules, calcified roots, and carbonate coatings of void spaces are common pedogenic features of calcareous soils (e.g., Jaillard et al., Reference Jaillard, Guyon and Maurin1991; Khormali et al., Reference Khormali, Abtahi and Stoops2006; Durand et al., Reference Durand, Monger and Canti2010), it should be noted that analyses of JRF 115H gut region samples indicate calcium levels of only 2.5 to 3.0 wt. % (Tweet et al., Reference Tweet, Chin, Murphy and Braman2008). The relatively low calcium content of the gut region substrate is also supported by the fact that no calcite-filled fissures in the substrate were observed.

Root systems are generally characterized by variations in diameter reflected in tapering and branching into smaller structures (e.g., Klappa, Reference Klappa1980; Retallack, Reference Retallack1983). In contrast, the gut region traces do not branch or change diameter, and all documented examples display a narrow range of diameters. In addition, well-preserved root traces can have root hairs (Klappa, Reference Klappa1980), which are not present in the trace fossils of JRF 115H. Thus, although the tubular morphology of the traces is similar to that of rhizotubules, the overall structure and patterns of the traces are different from root systems. The fine scale features of the striae are also distinctively different. Some calcified roots are characterized by discrete calcified cells that are tightly packed in tessellated arrangements (Jaillard et al., Reference Jaillard, Guyon and Maurin1991; Khormali et al., Reference Khormali, Abtahi and Stoops2006), but such cells are not present in the gut region traces. Other examples of calcified root tissues display longitudinal ridges that reflect root epidermal tissues, such as calcified Quaternary-age features figured in Klappa (Reference Klappa1980, fig. 7a). However, the linear features within JRF 115H show negative topography (with sharp edges incised into the substrate), unlike the positive topography (with rounded ridges protruding out of the substrate) illustrated in Klappa’s figures.

Although the color profile of these tiny traces within the gut region substrate superficially resembles the rhizohalos that mark redoximorphic conditions around ancient roots, the features of the gut region trace fossils indicate a different mechanism of formation. Rhizohalos form when soluble iron(II) is flushed out of sediments within the reducing environment of a root channel, while iron exposed to oxygen outside of the root channel is precipitated as insoluble iron(III). This results in a two-toned rhizolith comprised of gray, iron-deficient sediments within a root channel surrounded by oxidized red or brown sediments (Kraus and Hasiotis, Reference Kraus and Hasiotis2006). However, this model does not fit the tiny tubular traces because they are open conduits that would have been exposed to oxygen. Thus the light color of the traces does not indicate a reducing environment and is not equivalent to the light-colored sediment-filled root channels of rhizohalos.

The taphonomic context of the dinosaur carcass is also difficult to reconcile with rhizoliths. The windows of opportunity for root trace formation in JRF 115H were limited to an early interval immediately after death but before deep burial, and a modern interval as the dinosaur remains became exposed to the elements. For both intervals, the primary stumbling block is the condition of JRF 115H itself. The studied samples were collected from what had been the underside of the specimen. If there were sufficient plant growth through the specimen to produce the observed trace fossils near the base of the carcass, then there should be evidence of roots elsewhere in the carcass. Instead, the skeletal remains and integument impressions appear undisturbed by plant growth. Root colonization before deep burial is unlikely because it is implausible for the carcass to have been unburied or shallowly buried long enough for plants to grow into the corpse without it having been significantly altered by decomposition, scavengers, and other surface processes. Once buried, the development of the large carbonate concretions in an otherwise relatively unconsolidated sandstone (Murphy et al., Reference Murphy, Trexler and Thompson2007) also would have served to discourage subsequent root penetration.

Attributing the traces to modern roots is problematic as well. The erosion that brought the carcass to light cut vertically through the pelvic region, but otherwise left the majority of the specimen buried in a hillside several meters from plant growth (Tweet et al., Reference Tweet, Chin, Murphy and Braman2008). There are what appear to be several examples of modern roots or hyphae associated with some of the gut region samples, but these are not preferentially associated with the trace fossils, and instead seem to exploit weak zones. They also are much thinner than the trace fossils, with widths on the order of tens of microns, although the diameters were likely affected by dehydration.

The morphological, geochemical, and taphonomic evidence do not provide a convincing argument for a root origin for the gut region trace fossils. However, the evidence is consistent with the interpretation that the trace fossils reflect the presence and activity of small worms. As noted above, the striae on the traces indicate that sharp points or edges were incised into the substrate, unlike cell impressions of calcified roots (Klappa, Reference Klappa1980; Jaillard et al., Reference Jaillard, Guyon and Maurin1991; Khormali et al., Reference Khormali, Abtahi and Stoops2006). These striae have been formed by external anatomical features of a stationary or burrowing worm. The narrow range of diameters also is more consistent with burrows or worm morphologies than plant roots (Boyd, Reference Boyd1975). As with the potential for root growth, the taphonomic context of the brachylophosaur skeleton indicates that trace-maker activity would have been constrained to the period immediately after death. However, burrowers are mobile, and they may already have been present inside the dinosaur before its death. The horizontal orientation and length of some of the observed trace fossils suggest that they reflect burrowing activity, although it is possible that some of the hollow traces are body molds of the animals, where the remains of a worm supported the three-dimensional shape while the burrow lining was mineralizing. Given these considerations, we infer that the linear features represent trace fossils made by tiny worms.

Taphonomic aspects

The narrow range of burrow diameters and the uniform morphology of burrows suggest that only one type of burrowing worm was present. This apparent monospecific assemblage of bioturbators in the gut contents is consistent with rapid removal of the dinosaur carcass from subaerial exposure, because most terrestrial carcasses immediately attract a varied fauna of invertebrate (Payne, Reference Payne1965; Smith, Reference Smith1986) and vertebrate scavengers.

The thin calcareous layers lining the trace fossils are noteworthy, because calcite is otherwise uncommon in the gut region material (Tweet et al., Reference Tweet, Chin, Murphy and Braman2008). It is possible that the linings represent the diagenetically altered remains of mucosal secretions from the burrowing worms. Mucus is a complex organic material that many burrowing invertebrates, but not terrestrial arthropods, secrete to facilitate movement and strengthen burrow walls in watery environments (Bromley, Reference Bromley1996). Such settings may be comparable to the decaying interior of JRF 115H. Mucus production can facilitate calcite precipitation by serving as a growth medium for calcite-precipitating microorganisms, as described for mucus produced by the modern bivalves Granicorium and Samarangia (Braithwaite et al., Reference Braithwaite, Taylor and Glover2000). Schieber (Reference Schieber2002) suggested that a similar process resulted in pyritization of mucus trails. If bodily remains of the burrowers were present in some of the structures, their bodies could have also provided a growth medium for calcite-precipitating microorganisms. Under this scenario, flattened burrow structures may represent trace fossils that collapsed because they did not have the burrowers’ bodies for support.

The well-preserved state of many of these tiny, thin-walled structures indicates that they were formed after the carcass had reached its final resting place. Burrows probably would not have been preserved with such fidelity if they had been made when the body was being transported or when the gut region material was very fluid. The poorly preserved trace fossils thus may represent burrowing before the onset of optimal conditions for preservation. The post-mortem gut region material would have presented a clay-rich burrowing environment with abundant mm-scale plant fragments and less abundant silt- to sand-sized mineral clasts (Tweet et al., Reference Tweet, Chin, Murphy and Braman2008).

Burrower identity

Although it often is difficult to assign burrows to a specific group of animals (Bromley, Reference Bromley1996), in this case the field of candidates can be constrained by the size, morphology, and lining features of the burrows. The fluvial burial setting of JRF 115H offers additional clues, if the worms immigrated into the carcass from the local environment. The diameters of the burrows restrict the size of the burrowers to animals with an adult or larval diameter of approximately 0.3 mm, which is near the upper end of the meiofaunal range (Higgins and Thiel, Reference Higgins and Thiel1988). The striking uniformity of burrow diameters suggests that the animals were either at adult size, or did not grow significantly during the time period when the trace fossils were being made.

The trace fossils do not exhibit a regularly sinusoidal morphology, which suggests that they were not made by animals that move by longitudinal flexure, such as some nematodes (Moussa, Reference Moussa1970; Chamberlain, Reference Chamberlain1975; Robinson, Reference Robinson2004). Similarly, the traces do not show meniscate or annulated burrow fill, which suggests that they were not made by animals that move by strong peristaltic motions, such as some annelids and insect larvae. However, the absence of features pointing to longitudinal or peristaltic motions could be a function of preservation and/or substrate.

The striae in the mineralized walls are interpreted as bioglyphs (Ekdale and de Gibert, Reference Ekdale and de Gibert2010) that might have been produced by bristle-like external features dragged through the substrate or deposited mucus. There is no evidence for significant appendages, such as hard mandibles or legs, because major distortions or marks incised in the walls are absent. These features suggest that the ancient burrowers had circular cross-sections and smooth exteriors, except for possible fine bristle-type structures.

These lines of evidence indicate that the trace makers were vermiform, meiofaunal-scale animals with small external projections. These animals would have been either endoparasites in the brachylophosaur, or else migrants from the freshwater channel sediment that moved into the dinosaur carcass. As previously noted, the distinctive calcareous lining of the trace fossils may indicate that the burrowers produced mucus. Of modern meiofaunal groups, one group that includes taxa that fit these characteristics is Phylum Annelida (Higgins and Thiel, Reference Higgins and Thiel1988). A group of tiny oligochaete annelids, the enchytraeids, presents one possible analogue for the tiny Cretaceous burrowers. They are mucus-producing, setae-bearing worms of appropriate size and terrestrial habits, and they ingest decaying plant matter (O’Connor, Reference O’Connor1967; Dasch, Reference Dash1983). Roundworms of the Phylum Nematoda also fit some of the characteristics of the trace fossils. However, roundworms are less likely because modern examples usually are smaller than 300 μm in diameter (Goodey, Reference Goodey1963), and their typical mode of locomotion is sinusoidal. It also is possible that the trace makers represent an extinct lineage of soft-bodied worms.

Burrower paleobiology

There are several behaviors that can motivate organisms to associate with carcasses, including scavenging, sheltering, and predation on other carcass fauna (Payne, Reference Payne1965). Remnant populations of parasites, as well as their eggs, also might be present in a fresh carcass. Sheltering cannot be ruled out based on the physical evidence, but it seems unlikely that the carcass would be found by one specific type of tiny animal in need of shelter but not by a wider spectrum of animals in need of a meal. Given the lack of morphologic diversity in the trace fossils, predation on other fauna is also unlikely. An additional possibility is that the trace makers could have been associated with debris introduced into the carcass, perhaps as enchytraeid-like animals feeding on dead vegetal matter.

In the absence of well-preserved body fossils of the burrowers or unambiguous morphologic features in the fossil traces, evaluating the likelihood of specific motives must be done through consideration of the taphonomic conditions and the nature of the available resources. It is reasonable to consider the trace makers in terms of being allochthonous (scavengers) or autochthonous (remnant parasites or hatched eggs). For either allochthonous or autochthonous burrowers, a large dinosaur such as JRF 115H would have presented a tremendous resource, both in life and death.

If the trace fossils were produced by allochthonous burrowers, conditions must have protected the carcass from other opportunistic allochthonous fauna. As noted, most terrestrial carcasses quickly attract a varied fauna of invertebrate and vertebrate scavengers, yet there is only evidence for one type of animal associated with JRF 115H after its death. Considering that JRF 115H was most likely buried rapidly, we can envision a scenario where worms living in the channel sands found the carcass after it was buried beyond the reach of other potential scavengers. Alternatively, an adventitious burrower scenario could account for the absence of scavengers if it is posited that the only means of access to the carcass was through introduced debris, which transported the trace makers. It should be noted, however, that the taphonomy of the carcass suggests that the plant debris in the gut region of JRF 115H represents dinosaur gut contents rather than allochthonous debris (Tweet et al., Reference Tweet, Chin, Murphy and Braman2008). If the trace fossils were produced by autochthonous animals, the burrowers would have been either active parasites that survived the host’s death, transport, and burial, or else newly hatched parasites that emerged after the dinosaur’s death. Both possibilities are conceivable if the carcass remained largely intact after death, and if the chain of taphonomic events occurred rapidly enough.

Although there is little physical evidence to favor either autochthony or allochthony, autochthonous burrowing by remnant parasites presents a more parsimonious explanation of the condition that a single type of burrower was present in a largely undisturbed carcass. The absence of other types of bioturbation is striking, because the resources of a carcass accessible to tiny meiofaunal-scale burrowers also should have been within reach of larger burrowers that had the ability to cover more territory.

The possibility that these tiny trace fossils reflect the activity of parasitic worms inside the gut of a dinosaur is tantalizing. However, other possible scenarios to explain these intriguing trace fossils cannot be ruled out entirely.

Paleobiologic implications of the paired trace fossils

One of the most interesting characteristics of the burrows is their common occurrence in distinctive pairs with shared walls. The relative timing of pair formation is uncertain, although paired trace fossils showing identical changes in direction and the absence of distortion in the shared walls suggest that the pairs were formed by two animals aligned or moving together. Cross-cutting relationships might provide clues as to whether the paired traces were simultaneously created, but examples are equivocal. Fig. 3.1 shows a set of paired traces oriented left–right and another set, oriented top–bottom, which is clearly cut by a horizontal trace that likely represents one member of the horizontal pair.

Several plausible scenarios can be constructed for the sequence of events that resulted in the paired burrow configuration, some invoking pairs of burrowers moving at the same time, and others invoking burrowers active at different times running up against previous burrows. However, the presence of at least 13 pairs in the group of 280 observed traces suggests that coincidental formation is unlikely. Although it is not uncommon for burrows to be closely associated—for example in some types of feeding traces—the actual sharing of walls as seen here is exceedingly rare. It is more typical for burrowers to avoid other burrows (Seilacher, Reference Seilacher1967). It is conceivable that the parallel trace fossils represent a feeding strategy to concentrate foraging in areas of proven food supply, but it seems unlikely that such a strategy would be necessary in this case, because the organic fraction of the gut region material of JRF 115H appears to have been relatively homogeneous. Some other benefit seems more likely. Recurring simultaneous formation of parallel trace fossils appears to reflect intentional contact. Although some types of worms are known to aggregate in large groups, including some nematodes (Croll, Reference Croll1971) and enchytraeid annelids (O’Connor, Reference O’Connor1967; Dasch, Reference Dash1983), there are few reports in the scientific literature describing social interactions of worms. One potential motive is reproduction. Certain kinds of worms reproduce by lining up next to each other, such as has been observed in extant earthworms (Edwards and Bohlen, Reference Edwards and Bohlen1996) and some nematodes (Huettel, Reference Huettel2004: fig. 5.5).

Aside from the distinctively paired burrows, most of the gut region trace fossils are simple and gently curved, and appear to lack complex branching patterns or regular meanders. The majority of these trace fossils thus appear to be feeding traces (fodinichnia). However, it also is possible that parts of the trace fossils might represent body impressions of dead burrowers preserved within the substrate (mortichnia).