Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The impact of deep-tier burrow systems in sediment mixing and ecosystem engineering in early Cambrian carbonate settings


Bioturbation plays a substantial role in sediment oxygen concentration, chemical cycling, regeneration of nutrients, microbial activity, and the rate of organic matter decomposition in modern oceans. In addition, bioturbators are ecosystem engineers which promote the presence of some organisms, while precluding others. However, the impact of bioturbation in deep time remains controversial and limited sediment mixing has been indicated for early Paleozoic seas. Our understanding of the actual impact of bioturbation early in the Phanerozoic has been hampered by the lack of detailed analysis of the functional significance of specific burrow architectures. Integration of ichnologic and sedimentologic evidence from North China shows that deep-tier Thalassinoides mazes occur in lower Cambrian nearshore carbonate sediments, leading to intense disruption of the primary fabric. Comparison with modern studies suggest that some of the effects of this style of Cambrian bioturbation may have included promotion of nitrogen and ammonium fluxes across the sediment-water interface, average deepening of the redox discontinuity surface, expansion of aerobic bacteria, and increase in the rate of organic matter decomposition and the regeneration of nutrients. Our study suggests that early Cambrian sediment mixing in carbonate settings may have been more significant than assumed in previous models.


Bioturbation, involving both particle and solute transport within burrows, into the surrounding sediment and across the sediment-water interface, is one of the most important factors in affecting oxygen concentration in the sediment, chemical cycling, regeneration of nutrients, microbial activity and the rate of organic matter decomposition in modern oceans1,2,3. In addition, burrowing animals represent ecosystem engineers that impact on community structure by either having negative (e.g., influence of infaunal deposit feeders on sessile epifaunal and infaunal suspension feeders) or positive (e.g., influence of infaunal deposit feeders on meiofauna and microbes) effects on other organisms4,5. There is considerable debate regarding the timing of infaunalization and the role that bioturbation may have played in nutrient cycling and sediment mixing during the Cambrian Explosion. Unfortunately, precise evaluation of the actual impact of bioturbation early in the Phanerozoic has been hampered by the lack of detailed analysis of the functional significance of specific burrow architectures preserved in the fossil record. Whereas most research have focused on measuring degree of bioturbation and estimating maximum burrowing depths, the actual role of specific type of burrows in sediment mixing and impact on other organisms has received much less attention. As a result, no attempts have been made in order to establish a link between the functional significance of discrete burrow architectures and their potential impact on sediment properties and the accompanying benthic faunas.

Integration of ichnologic and sedimentologic evidence from North China shows that intense bioturbation, mainly revealed by the ichnogenus Thalassinoides, took place in nearshore carbonate sediments during the early Cambrian, providing evidence of significant infaunalization and sediment mixing. Comparison of these burrow architectures with modern counterparts allows evaluating the role of these deep-tier bioturbators in sediment mixing, geochemical recycling and ecosystem engineering. The aims of this paper are to document the occurrence of pervasive deep-tier Thalassinoides bioturbation in shallow-marine carbonates of the lower Cambrian Zhushadong Formation of North China, and discuss how this style of burrowing may have affected shallow-water carbonate ecosystems and associated sediments.

Geologic setting

The Zhushadong Formation crops out in southwestern Songshan Mountain, western Henan Province (Fig. S1), belonging to the Southern subprovince6,7. The three studied sections are quite continuous and located southwest of Zhengzhou (Figs S1–S2). Two well-preserved trilobite faunas assigned to the Palaeolemis Zone and Redlichnia chinensis Zone indicate a late early Cambrian age (Cambrian Age 4)8,9.

The Zhushadong Formation is a 24–54-m-thick succession of dark-grey and/or light-grey, medium-thick bedded wackestone and dolostone, interbedded with packstone, grainstone and flat pebble conglomerate (Fig. 1). Stromatolites, parallel and convolute lamination are common (Figs S2–S3). Hummocky cross-stratification is present locally. The occurrence of tabular and trough cross bedding, convolute lamination and gypsum breccia10 suggests 2D and 3D dune migration in a restricted shallow-marine environment periodically exposed subaerially in a seasonally dry, probably subarid, climate. The influence of storm activity is suggested by the flat pebble conglomerates and the hummocky cross-stratification, whereas the soft-sediment deformation has been attributed to earthquakes11,12.

Figure 1: Stratigraphic column and ichnofabric data from the lower Cambrian Zhushadong Formation, North China.

(a) Generalized stratigraphic column of the lower Cambrian Zhushadong Formation showing bioturbation index and thickness of bioturbated interval in the Guankou section from the southwestern Songshan Mountain, North China. (b) Table showing bioturbation index, burrow depth, thickness of bioturbated interval and diameter of Thalassinoides in the Zhushadong Formation, Guankou section. Abbreviations: BN = Bed number, SS = sedimentary structures, BI = bioturbation index, BT = thickness of bioturbated interval, BD = burrow depth, D = diameter of Thalassinoides.

Occurrence of Thalassinoides ichnofabric

Well-preserved Thalassinoides systems occur in 0.2–0.3 m thick dolostone beds, locally forming amalgamated units up to 3.3 m thick, from the lower to middle part of the Zhushadong Formation (Fig. 1), forming both boxworks and networks (i.e. mazes)13. Specimens consist of bedding-parallel polygonal networks of 0.4–1.5 cm wide, smooth, unlined (i.e. lacking wall reinforcements), mainly horizontally branching burrows (Fig. 2a–d and Table S1). Locally, short, vertical shafts are seen on bedding surfaces (Fig. 2b). In the more intensely bioturbated beds, bedding-parallel networks are linked by vertical shafts, forming a series of swollen T-junctions, delineating three-dimensional boxworks (Figs 2a and 3 and S4). Most burrows form both Y- and T-junctions but contain no swellings at junctions or elsewhere on the bedding surface. The presence of shafts distinguished the Zhushadong specimens from Thalassinoides horizontalis from the late Cambrian-Early Ordovician of Colorado (Fig. S4)14. The non-bioturbated matrix exhibits a light grey color compared to the dark grey mottled burrows. Burrow fill consists of dolomite crystals, whereas the matrix is made of micrite calcite (Fig. S5)15. Dolomitization linked to burrowing activity has been documented extensively in Thalassinoides-like burrows from the lower Paleozoic16,17.

Figure 2: Thalassinoides in the restricted shallow-marine deposits of the Zhushadong Formation in the Guankou section.

(a) General view of beds showing biooturbation indexes ranging from 2 to 4 from bottom to upper in cross-section view (Bed 8). (b) Thalassinoides network on bedding surface (Bed 9), showing three-dimensional morphology and extensive overlapping. (c) Strong bioturbation (BI 4) in cross-section view (Bed 9). (d) Thalassinoides network as seen on bedding surface (Bed 10), showing horizontal branches. Abbreviations: vs = vertical shaft, Tb = T-branched, Yb = Y-branched, BI = bioturbation index, BT = thickness of bioturbated interval, BD = burrow depth, *maximum burrow depth during multi-layer colonization.

Figure 3: Occurrences of Thalassinoides representing multi-layer colonizers from the restricted platform deposits of the Cambrian Epoch 2 Zhushadong Formation in the Guankou section.

(a) Examples from the lower part of the Zhushadong Formation (Bed 9). (b,c) Middle part of Zhushadong Formation (Bed 12). (d) Upper part of the Zhushadong Formation (Bed 16). Thalassinoides levels indicated by yellow dashed line; shafts connecting multiple layers indicated by white arrows.

To evaluate the degree of infaunalization in the studied Cambrian strata, we have framed our observations within the ichnofabric approach18,19. An ichnofabric refers to any aspect of the texture and internal structure of a substrate resulting from bioturbation and bioerosion at any scale18. To analyze the impact of this specific burrowing style on sediment mixing and on other organisms, we have measured burrow densities and established comparisons with similar burrow systems in the modern.

A total of 34 m of continuous ichnofabric data were collected from the Guankou section (Figs 1 and S2 and Table S1), 53 m in the Lushan section (Fig. S2 and Table S2), and 28 m in the Mianchi section (Figs S2 and Table S3). Most of the lower part of the Zhushadong Formation is essentially unburrowed and preserves a pristine primary fabric, characterized by algal and parallel lamination and planar cross bedding. However, intense bioturbation occurs near the top of the lower part, and in the middle and upper parts (Figs 1 and S2). Maximum penetration of individual burrow shafts is 3.1 cm, but bioturbated zones are amalgamated forming up to 170 cm thick bioturbated intervals (Fig. 1). Also, some of the shafts connect burrow systems formed at different depths, indicating that these are multi-layer colonizers20 able to penetrate more than one event bed. In these cases, maximum burrow depth is 32.4 cm. Beds were most likely deposited by discrete storm events. Thalassinoides records post-storm colonization and intense bioturbation has locally obliterated bedding boundaries, resulting in the amalgamation of bioturbated zones.


Although typical of post-Paleozoic rocks21, Thalassinoides is relatively common in Paleozoic strata as well22. Thalassinoides usually is interpreted as feeding burrow (Fodinichnion), typically produced by infaunal deposit feeders, such as decapod crustaceans23 that develop an ‘underground mining’ strategy. Early Paleozoic occurrences of this ichnogenus predate the oldest known body fossils of burrowing decapods and, therefore, other producers have been suggested14,22,24. Trilobites are known to have produced a wide variety of trace fossils, but their burrows rarely, if ever, have been observed to branch in an anastomosing fashion, like Thalassinoides. In addition, scratch marks, which are diagnostic of trilobite-produced trace fossils, have not been recorded in any of these burrow systems, further arguing against production by trilobites. The occurrence of trilobite body fossils within Thalassinoides has been indicated as evidence of “tunneling” behavior by these organisms24, but exoskeletons (exuvia or dead bodies) are commonly trapped inside burrow galleries, providing a cautionary note in establishing a genetic link between the burrow system and the preserved body fossil25.

Other malacostracans or even unrelated clades, such as worm-like organisms, may have been involved in the production of these structures, representing examples of behavioral convergence14,22. Within the former, phyllocarids which are known since the Cambrian and were common through the Paleozoic26, have been suggested as possible producers of Paleozoic Thalassinoides14,22. Although there is evidence that some of these crustaceans were deposit feeders which may have burrowed efficiently26,27,28, it is uncertain if they may have been able to produce branching burrows. Another group of shrimp-like arthropods known since the early Cambrian are waptiids29,30,31. Based on morphologic evidence, it has been suggested that waptiids may have been able to burrow in various type of substrate31, although it remains unclear if they may have produced Thalassinoides-like systems.

The list of Cambrian representatives of worm-like bioturbators is extensive, including priapulids32 and sipunculans33. However, these typically produced simple, unbranched burrows, rather than Thalassinoides-like galleries. Enteropneusts, which are known since the Cambrian34,35,36, are other potential candidates. Modern enteropneusts are efficient deposit-feeding bioturbators, capable of producing not only U-shaped burrows37,38,39, but also branching burrow systems occupying mid to deep tiers40. In fact, the ichnogenus Balanoglossites has been attributed in some cases to the work of enteropneusts41,42,43,44, resulting in structures which are remarkably similar to those referred to as Thalassinoides in lower Paleozoic rocks44. However, an epifaunal suspension-feeding mode of life has been indicated as a primitive trait36, therefore casting some doubts about the potential of Cambrian representatives to produce burrow systems.

Unlike the three-dimensional Thalassinoides (i.e. boxworks) (circa 1 m deep) in Upper Ordovician and younger strata17,45, Thalassinoides from the lower and middle Cambrian strata of the Great Basin are characterized by forming discrete small two-dimensional networks and, more rarely, three-dimensional boxworks, which produced little to negligible bioturbation46. The two-dimensional Thalassinoides continued to dominate through the Early Ordovician14. In fact, it is the increase in the size of Thalassinoides and the switch in dominance from networks to boxworks that have been deemed responsible for the increase in the extent and depth of bioturbation that took place in carbonate settings between the Middle and Late Ordovician46.

However, the occurrence of high-density and deep-tier Thalassinoides mazes penetrating several storm layers in the lower Cambrian of China suggests that these evolutionary innovations took place in proximal areas of this carbonate platform earlier than commonly assumed based on previously available information. In fact, our study suggests that deep-tier, intense bioturbation by the producers of Thalassinoides mazes is a consequence of the Cambrian Explosion47 rather than of the Great Ordovician Biodiversification Event48 as previously implied46,47,48,49. Invoking taphonomic or environmental reasons to explain the discrepancy between extent and depth of bioturbation between burrow systems from the Cambrian of China and occurrences elsewhere is unsupported by sedimentologic data, because a similar duration of colonization windows is expected in all these shallow-marine, storm-affected carbonate settings. In the same vein, comparable colonization windows may have resulted in broadly similar population densities of the tracemakers.

Interestingly, boxwork architectures seem to have been restricted to the proximal platform deposits represented in the Zhushadong Formation (Figs 2 and 3, S2, and S6–7), with the overlying middle to upper Cambrian Mantou and Zhangxia formations containing only shallow Thalassinoides networks in more open platform deposits, albeit reaching BI up to 3 (Figs S8 and S9). Therefore, information from the lower Cambrian of North China supports the model of onshore origination of evolutionary innovations and their subsequent offshore expansion50,51,52,53.

The timing of infaunalization and its consequences in terms of sediment mixing and biogeochemical cycling during the early Paleozoic is at present a matter of debate54,55,56,57,58. It has been recently argued that sediment mixing has been suppressed during most of the early Paleozoic being limited until the late Silurian56,57. With the exception of the classic Skolithos sandstone of nearshore to subtidal settings59,60,61, burrows tend to occupy shallow tiers in the Cambrian54,56,57. Because these are produced by sessile infaunal organisms (e.g., long vermiform soft-bodied animals, such as lophophorate phoronids and tantacular-crowned polychaetes62), their impact on sediment mixing has been typically dismissed56. However, other studies have indicated that the establishment of this infauna may have been instrumental in increasing the complexity of the trophic web, resulting in coupling of benthos and plankton54.

As with the case of Skolithos, Thalassinoides is produced by stationary organisms and not by sediment bulldozers. However, this type of galeries represents the activities of deep bioturbators that are able to transport sediment to the surface from below and solutes within the burrow and into the host sediment by increasing the area of sediment-water interface1,2,3,63,64,65,66. In modern environments, burrow systems similar to those from the Cambrian of China strongly affect nitrogen fluxes across the sediment-water interface and supply oxygen and other oxidants to microbial communities on the burrow walls67. This style of bioturbation induces N2 fixation68. Also, as a result of burrow construction and maintenance, ammonium is transported into the overlying water63. In unlined burrow systems, such as these Cambrian Thalassinoides, pump takes place both into and out of the sediment, further underscoring the effects of biogenic advection of porewater69. In addition, high densities of burrows, such as those documented here, impact on organic carbon fluxes and increase dissolved inorganic nitrogen fluxes with respect to unburrowed sediments67. Software ImageJ analysis used to calculate spacing among Cambrian burrows (Fig. S10 and Table S4) indicates that these are commonly within 5 mm of each other, allowing their oxygenated zone to meet even in the case of low-porosity, fine-grained sediment70. Experimental studies have shown that, even in the absence of significant sediment movement, the effect of burrowing is not restricted to the sediment adjacent to the bioturbator, extending instead laterally to a distance equivalent to several times the length of the producer70. The fact that the studied Cambrian deposits display relatively high porosities promotes even further solute transport into the surrounding sediment. In addition to solute transport, this style of bioturbation results in significant particle transport71.

This style of burrowing may have also played a role in promoting the presence of some organisms, while excluding others. By increasing porosity and penetrability into the substrate, bioturbation may have triggered burrowing activities by other organisms5. In fact, Planolites, a simple trace fossil attributed to deposit feeders, commonly co-occur in the muddy layers intercalated with the Thalassinoides-bearing beds (Fig. S7b). Also, bioturbation may have been conducive to the establishment of microbes, meiofauna and tiny animals within the burrows5,71,72. There is increased evidence that tiny animals73,74 and meiofauna75,76,77 have been important components of Cambrian marine ecosystems. On the contrary, sediment remobilization by these deposit feeders may have been detrimental for colonization of sessile suspension feeders, a phenomenon referred to as trophic group amensalism4,78. In addition, sediment turnover may have negatively impacted on larval recruitment and epifaunal grazers by diminishing microbial films on the sediment surface5. Neither suspension-feeder burrows, nor grazing trails have been recorded in these Cambrian carbonates.

To summarize, these bioturbators not only have significantly modified the primary sedimentary fabric, but also may have efficiently contributed to nutrient recycling, acting as ecosystem engineers as well. Some of the effects of bioturbation may have included promotion of nitrogen and ammonium fluxes across the sediment-water interface, average deepening of the redox discontinuity surface, expansion of aerobic bacteria, and increase in the rate of organic matter decomposition and the regeneration of nutrients. Our analysis suggests that sediment mixing in early Cambrian proximal shallow-marine carbonate settings may have been more intense than previously assumed. This is consistent with the results of recent global studies based on comprehensive ichnologic compilations54 and geochemical analysis55 through this critical interval of the history of the biosphere.


Bed-by-bed sedimentologic logging was performed in three sections, Guankou, Lushan, and Mianchi. Facies analysis follows the standard practice of describing lithology, sedimentary structures, bed geometry, bed contacts and fossil content, followed by interpretation in terms of depositional processes and sedimentary environments. Ichnologic analysis involves trace-fossil sampling, study of density, abundance and distribution of biogenic structures; measurement of degree of bioturbation; and relationships among trace fossils, physical sedimentary structures, and bedding types in each sedimentary layer. Detailed maps and photographic panels of the ichnofossil-bearing strata were prepared. Software ImageJ analysis was used to calculate spacing among burrows. Thin sections were produced in order to analyze burrow fills and walls.

To assess degree of bioturbation, bioturbation index (BI)19 was used. This index measures the extent to which the primary sedimentary fabric is still visible. BI = 0 represents no bioturbation (0%), and a pristinely preserved primary fabric. BI = 1 (1–4%) characterized sparse bioturbation with few discrete biogenic structures locally overprinting the well-preserved sedimentary fabric. BI = 2 (5–30%) is typified by low bioturbation in sediment with well-preserved sedimentary structures. BI = 3 (31–60%) refers to sediment with discrete trace fossils, moderate bioturbation and still distinguishable bedding contacts. BI = 4 (61–90%) is characteristic of intense bioturbation, high trace-fossil density, common overlap trace fossils, and primary sedimentary structures mostly erased. BI = 5 (91–99%) represents sediment having intense bioturbation and a completely disturbed bedding. BI = 6 (100%) comprises completely bioturbated and reworked sediment, revealed by repeated overprinting of trace fossils. Bioturbation index was assessed for each bed.

Tier classification is based on current schemes54. The shallow tier is represented by structures emplaced in the upper 6 cm of the substrate, the mid tier comprises those produced within 6–12 cm of the substrate, the deep tier consists of those formed below 12–100 cm, and the ultra-deep tier is represented by those traces emplaced below 100 cm. The 6-cm boundary is taken to approximately coincide with a depth above which organisms are challenged by environmental disturbance instead of by maintaining contact with the sediment-water interface; below this boundary, these difficulties are reversed in severity. Below the 12-cm boundary, stresses linked to limited food supply and oxygen content, and increased substrate compaction are the dominant limiting factors. Structures produced below 100 cm are virtually unknown prior to the Mesozoic Marine Revolution27.

Additional Information

How to cite this article: Zhang, L.-J. et al. The impact of deep-tier burrow systems in sediment mixing and ecosystem engineering in early Cambrian carbonate settings. Sci. Rep. 7, 45773; doi: 10.1038/srep45773 (2017).

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.


  1. 1

    Aller, R. C. Bioturbation and remineralization of sedimentary organic matter: effects of redox oscillation. Chem. Geol. 3–4, 331–345 (1994).

    ADS  Google Scholar 

  2. 2

    Meysman, F. J., Middelburg, J. J. & Heip, C. H. Bioturbation: a fresh look at Darwin’s last idea. Trends Ecol. Evol. 21, 688–695 (2006).

    PubMed  Google Scholar 

  3. 3

    Kristensen, E. et al. What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar. Ecol. Prog. Ser. 446, 285–302 (2011).

    ADS  Google Scholar 

  4. 4

    Jones, C. G., Lawton, J. H. & Shachak, M. Organisms as ecosystem engineers. Oikos 69, 373–386 (1994).

    Google Scholar 

  5. 5

    Pillay, D. & Branch, G. M. Bioengineering effects of burrowing Thalassinidean shrimps on marine soft-bottom ecosystems. Oceanogr. Mar. Biol. Annu. Rev. 49, 137−192 (2011).

    Google Scholar 

  6. 6

    Zhang, W. & Jell, P. A. Cambrian trilobites of north China-Chinese Cambrian trilobites housed in the Smithsonian Institution. 1–332. (Beijing, Science Press, 1987).

  7. 7

    Zhang, W. In Biostratigraphy of China(eds Zhang, W., Chen, P. & Palmer, A. R. ) 55–119 (Beijing, Science Press, 2003).

  8. 8

    Pei, F. Division and correlation of the North China type Cambrian biostratigraphic units of Henan Province. Henan Geology 18, 97–106 (2000).

    Google Scholar 

  9. 9

    Peng, S. Review on the studies of Cambrian trilobite faunas from Jiangnan slope belt, South China, with notes on Cambrian correlation between South and North China. Acta Palaeontol . Sinica 48, 437–452 (2009).

    Google Scholar 

  10. 10

    Zhu, Y. & Ma, L. Division and correlation of Lower Cambrian and its sedimentary evolution in North China. Geol. Rev. 54, 731–740 (2008).

    Google Scholar 

  11. 11

    Tian, H., Lü, M., Zhang, B. & Sang, Z. Sm-Nd age dating and its significance of chert in soft sediment deformation structures from the Lower Cambrian Zhushadong Formation, Jinan of Shandong Province. J. Palaeogeogr. 17, 45–50 (2015).

    Google Scholar 

  12. 12

    Yang, W., Wang, M. & Qi, Y. Earthquake-induced Soft-sediment Deformation Structures in the Dengfeng Area, Henan Province, China: Constraints on Qinling Tectonic Evolution during the Early Cambrian. Acta Geol. Sin-Engl. 89, 1835–1846 (2015).

    Google Scholar 

  13. 13

    Ekdale, A. A., Bromley, R. G. & Pemberton, S. G. Ichnology, the use of trace fossils in sedimentology and stratigraphy. 1–317 (Tulsa, Oklahoma, Society of Economic Paleontologists and Mineralogists Short Course No. 15, 1984).

  14. 14

    Myrow, P. M. Thalassinoides and the enigma of early Paleozoic open–framework burrow systems. Palaios 10, 58–74 (1995).

    ADS  Google Scholar 

  15. 15

    Qi, Y., Meng, Y., Dai, M. & Li, D. Biogenic leopard patch structures from the Zhushadong Formation (Cambrian Series 2), Dengfeng area, Western Henan. Geol. Sci. Technol. Infor. 33, 1–8 (2014).

    CAS  Google Scholar 

  16. 16

    Gingras, M. K., Pemberton, S. G., Muelenbachs, K. & Machel, H. Conceptual models for burrow-related, selective dolomitization with textural and isotopic evidence from the Tyndall Stone, Canada. Geobiology 2, 21–30 (2004).

    CAS  Google Scholar 

  17. 17

    Jin, J., Harper, D. A. T., Rasmussen, J. A. & Sheehan, P. M. Late Ordovician massive-bedded Thalassinoides ichnofacies along the palaeoequator of Laurentia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 367–368, 73–88 (2012).

    Google Scholar 

  18. 18

    Bromley, R. G. & Ekdale, A. A. Composite ichnofabrics and tiering of burrows. Geol. Mag. 123, 59–65 (1986).

    ADS  Google Scholar 

  19. 19

    Taylor, A. M. & Goldring, R. Description and analysis of bioturbation and ichnofabric. J. Geol. Soc. 150, 141–148 (1993).

    ADS  Google Scholar 

  20. 20

    Uchman, A. Tiering patterns of trace fossils in the Palaeogene flysch deposits of the Carpathians, Poland. Geobios 28, 389–394 (1995).

    Google Scholar 

  21. 21

    Buatois, L. A. et al. In The trace-fossil record of major evolutionary events, vol. 2: Mesozoic and Cenozoic. (eds Mángano, M. G. & Buatois, L. A. ). Topics in Geobiology 40, 19–177 (Springer, 2016).

    Google Scholar 

  22. 22

    Carmona, N. B., Buatois, L. A. & Mángano, M. G. In Trace Fossils in Evolutionary Palaeoecology (eds Webby, B. D., Mángano, M. G. & Buatois, L. A. ). Fossils & Strata 51, 141–153 (Wiley, 2004).

    Google Scholar 

  23. 23

    Nickell, L. A. & Atkinson, R. J. A. Functional morphology of burrows and trophic modes of three thalassinidean shrimp species, and a new approach to the classification of thalassinidean burrow morphology. Mar. Ecol. Prog. Ser. 128, 181–197 (1995).

    ADS  Google Scholar 

  24. 24

    Cherns, L., Wheeley, J. R. & Karis, L. Tunneling trilobites: Habitual infaunalism in an Ordovician carbonate seafloor. Geology 34, 657–660 (2006).

    ADS  Google Scholar 

  25. 25

    Buatois, L. A. & Mángano, M. G. Ichnology: Organism-substrate Interactions in Space and Time. 1–358 (Cambridge University Press, 2011).

  26. 26

    Collette, J. H. & Hagadorn, J. W. Early evolution of phyllocarid arthropods: phylogeny and systematics of Cambrian-Devonian archaeostracans. J. Paleontol. 84, 795–820 (2010).

    Google Scholar 

  27. 27

    Hannibal, J. T. & Feldmann, R. M. Arthropod trace fossils, interpreted as echinocarid escape burrows from the Chagrin Shale (Late Devonian) of Ohio. J. Paleontol. 57, 705–716 (1983).

    Google Scholar 

  28. 28

    Vannier, J., Boissy, P. & Racheboeuf, P. R. Locomotion in Nebalia bipes: a possible model for Palaeozoic phyllocarid crustaceans. Lethaia 30, 89–104 (1997).

    Google Scholar 

  29. 29

    Vannier, J. & Chen, J. Early Cambrian food chain: new evidence from fossil aggregates in the Maotianshan Shale biota, SW China. Palaios 20, 3–26 (2005).

    ADS  Google Scholar 

  30. 30

    Caron, J. B. & Vannier, J. Waptia and the diversification of brood care in early arthropods. Current Biology 26, 69–74 (2016).

    CAS  PubMed  Google Scholar 

  31. 31

    Strausfeld, N. J. Waptia revisited: intimations of behaviors. Arthropod Struct. Dev. 45, 173–184 (2016).

    PubMed  Google Scholar 

  32. 32

    Vannier, J., Calandra, I. & Gaillard, C., Zylińska. Pirapulid worms: Pioneer horizontal burrowers at the Precambrian-Cambrian boundary. Geology 38, 711–714 (2010).

    ADS  Google Scholar 

  33. 33

    Huang, D. Y., Chen, J. Y., Vannier, J. & Saiz Salinas, J. I. Early Cambrian sipunculan worms from southwest China. Proc. R. Soc. Lond. B. 271, 1671–1676 (2004).

    Google Scholar 

  34. 34

    Caron, J. B., Morris, S. C. & Cameron, C. B. Tubicolous enteropneusts from the Cambrian period. Nature 495, 503–506 (2013).

    ADS  CAS  PubMed  Google Scholar 

  35. 35

    Nanglu, K., Caron, J. B. & Cameron, C. B. Using experimental decay of modern forms to reconstruct the early evolution and morphology of fossil enteropneusts. Paleobiology 41, 460–478 (2015).

    Google Scholar 

  36. 36

    Nanglu, K., Caron, J. B., Morris, S. C. & Cameron, C. B. Cambrian suspension-feeding tubicolous hemichordates. BMC biology 14, 56 (2016).

    PubMed  PubMed Central  Google Scholar 

  37. 37

    Duncan, P. B. Burrow structure and burrowing activity of the funnel feeding Enteropneust Balanoglossus aurantiacus in Bogue Sound, North Carolina, USA. Mar. Ecol. 8, 75–95 (1987).

    ADS  Google Scholar 

  38. 38

    Mauviel, A., Juniper, S. K. & Sibuet, M. Discovery of an enteropneust associated with a mound-burrows trace in the deep sea: ecological and geochemical implications. Deep Sea Res. 34, 329–335 (1987).

    ADS  Google Scholar 

  39. 39

    Dobbs, F. C. & Guckert, J. B. Microbial food resources of the macrofaunal-deposit feeder Ptychodera bahamensis (Hemichordata: Enteropneusta). Mar. Ecol.-Progr. Ser. 45, 127–136 (1988).

    ADS  Google Scholar 

  40. 40

    Romero-Wetzel, M. B. Branched burrow-systems of the enteropneust Stereobalanus canadensis (Spengel) in deep-sea sediments of the Vöring-plateau, Norwegian sea. Sarsia 74, 85–89 (1989).

    Google Scholar 

  41. 41

    Mägdefrau, K. Über einige Bohrgänge aus dem Unteren Muschelkal von Jena. Pal. Z. 14, 150–160(1932).

    Google Scholar 

  42. 42

    Kaźmierczak, J. & Pszczołkowski, A. Burrows of enteropneustain Muschelkalk (Middle Triassic) of the Holy Cross Mountains, Poland. Acta Palaeontol. Pol. 14, 299–317 (1969).

    Google Scholar 

  43. 43

    Knaust, D. In Trace fossils. Comcepts, problems, prospects(ed. Miller, W. III ), 502–517 (2007).

  44. 44

    Knaust, D. & Dronov, A. Balanoglossites ichnofabrics from the Middle Ordovician Volkhov formation (St. Petersburg Region, Russia). Stratigr. Geo. Correl. 21, 265–279 (2013).

    Google Scholar 

  45. 45

    Sheehan, P. M. & Schiefelbein, D. R. J. The trace fossil Thalassinoides from the Upper Ordovician of the eastern Great Basin; deep burrowing in the early Paleozoic. J Paleontol. 58, 440–447 (1984).

    Google Scholar 

  46. 46

    Droser, M. L. & Bottjer, D. J. Ordovician increase in extent and depth of bioturbation: Implications for understanding early Paleozoic ecospace utilization. Geology 17, 850–852 (1989).

    ADS  Google Scholar 

  47. 47

    Mángano, M. G. & Buatois, L. A. In The trace-fossil record of major evolutionary events, vol. 1: Precambrian and Paleozoic(eds Mángano, M. G. & Buatois, L. A. ). Topics on Geobiology 39, 73–126 (Springer, 2016).

    Google Scholar 

  48. 48

    Mángano, M. G., Buatois, L. A., Wilson, M. & Droser, M. In The trace-fossil record of major evolutionary events, vol. 1: Precambrian and Paleozoic (eds Mángano, M. G. & Buatois, L. A. ). Topics in Geobiology 39, 127–156 (Springer, 2016).

    Google Scholar 

  49. 49

    Droser, M. L. & Bottjer, D. J. Trends in depth and extent of bioturbation in Cambrian carbonate marine environments, western United States. Geology 16, 233–236 (1988).

    ADS  Google Scholar 

  50. 50

    Mángano, M. G. & Buatois, L. A. Timing of infaunalization in shallow-marine early Paleozoic communities in high-latitude Gondwanic settings: Discriminating evolutionary, environmental and paleogeographic controls. Paleontol. Electr. 14, 1–21 (2011).

    Google Scholar 

  51. 51

    Sepkoski, J. J. & Sheehan, P. M. Jr. In Biotic interactions in Recent and fossil benthic communities(eds Tevesz, M. J. S. & McCall, P. L. ) 673–718 (Plenum, New York, 1983).

  52. 52

    Jablonski, D., Sepkoski, J. J. Jr. & Sheehan, P. M. Onshore-offshore patterns in the evolution of Phanerozoic shelf communities. Science 222, 1123–1124 (1983).

    ADS  CAS  PubMed  Google Scholar 

  53. 53

    Droser, M. L. & Bottjer, D. J. Trends and patterns of Phanerozoic ichnofabrics. Annu. Rev. Earth Pl. Sc. 21, 205–225 (1993).

    ADS  Google Scholar 

  54. 54

    Mángano, M. G. & Buatois, L. A. Decoupling of body-plan diversification and ecological structuring during the Ediacaran-Cambrian transition: evolutionary and geobiological feedbacks. P. Roy. Soc. B-Biol. Sci. 281, 20140038 (2014).

    Google Scholar 

  55. 55

    Boyle, R. A. et al. Stabilization of the coupled oxygen and phosphorus cycles by the evolution of bioturbation. Nature Geosci. 7, 671–676 (2014).

    ADS  CAS  Google Scholar 

  56. 56

    Tarhan, L. G. & Droser, M. L. Widespread delayed mixing in early to middle Cambrian marine shelfal settings. Palaeogeogr. Palaeoclimatol. Palaeoecol. 399, 310–322 (2014).

    Google Scholar 

  57. 57

    Tarhan, L. G., Droser, M. L., Planavsky, N. J. & Johnston, D. T. Protracted development of bioturbation through the early Palaeozoic Era. Nature Geosci. 8, 865–869 (2015).

    ADS  CAS  Google Scholar 

  58. 58

    Buatois, L. A. et al. Relict ecosystems at the dawn of the Phanerozoic revolution. Nature Commun. 5, 3544 (2014).

    ADS  Google Scholar 

  59. 59

    Desjardins, P. R., Mangano, M. G., Buatois, L. A. & Pratt, B. R. Skolithos pipe rock and associated ichnofabrics from the southern Rocky Mountains, Canada: colonization trends and environmental controls in an early Cambrian sand-sheet complex. Lethaia 43, 507–528 (2010).

    Google Scholar 

  60. 60

    Droser, M. L. Ichnofabric of the Paleozoic Skolihtos ichnofacies and the nature and distribution of Skolithos piperock. Palaios 6, 316–325 (1991).

    ADS  Google Scholar 

  61. 61

    Droser, M. L., Hughes, N. C. & Jell, P. A. Infaunal communities and tiering in Early Palaeozoic nearshore clastic environments: trace-fossil evidence from the Cambro-Ordovician of New South Wales. Lethaia 27, 273–283 (1994).

    Google Scholar 

  62. 62

    Pemberton, S. G. & Frey, R. W. Quantitative methods in ichnology: spatial distribution among populations. Lethaia 17, 33–49 (1984).

    Google Scholar 

  63. 63

    Ziebis, W., Forster, S., Huettel, M. & Jørgensen, B. B. Complex burrows of the mud shrimp Callianassa truncata and their geochemical impact in the sea bed. Nature 382, 619–622 (1996).

    ADS  CAS  Google Scholar 

  64. 64

    François, F., Poggiale, J.-C., Durbec, J.-P. & Stora, G. A new approach for the modeling of sediment reworking induced by a macrobenthic community. Acta Biotheor. 45, 295–319 (1997).

    Google Scholar 

  65. 65

    Solan, M. & Wigham, B. D. Biogenic particle reworking and bacterial-invertebrate interactions in marine sediments. Coast. Estuar. Stud. 60, 105–124 (2005).

    Google Scholar 

  66. 66

    Herringshaw, L. G. & McIlroy, D. Bioinfiltration: Irrigation-driven transport of clay particles through bioturbated sediments. J. Sediment. Res. 83, 443–450 (2013).

    ADS  Google Scholar 

  67. 67

    D’Andrea, A. F. & DeWitt, T. H. Geochemical ecosystem engineering by the mud shrimp Upogebia pugettensis (Crustacea: Thalassinidae) in Yaquina Bay, Oregon: Density-dependent effects on organic matter remineralization and nutrient cycling. Limnol. Oceanogr. 54, 1911–1932 (2009).

    ADS  Google Scholar 

  68. 68

    Bertics, V. J. et al. Burrowing deeper into benthic nitrogen cycling: the impact of bioturbation on nitrogen fixation coupled to sulfate reduction. Mar. Ecol. Prog. Ser. 409, 1–15 (2010).

    ADS  CAS  Google Scholar 

  69. 69

    Woodin, S. A., Wethey, D. S. & Volkenborn, N. Infaunal hydraulic ecosystem engineers: Cast of characters and impacts. Integr. Comp. Biol. 50, 176–187 (2010).

    PubMed  Google Scholar 

  70. 70

    Zorn, M. E. et al. Microscale oxygen distribution in various invertebrate burrow walls. Geobiology 4, 137–145 (2006).

    Google Scholar 

  71. 71

    Wethey, D. S., Volkenborn, V. & Reise, K. Pore-water advection by hydraulic activities of lugworms. Arenicola marina: A field laboratory and modeling study. J. Mar. Res. 66, 255–273 (2008)

    Google Scholar 

  72. 72

    Branch, G. M. & Pringle, A. The impact of the sand prawn Callianassa kraussi Stebbing on sediment turnover and on bacteria, meiofauna, and benthic microflora. J. Exp. Mar. Biol. Ecol. 107, 219–235 (1987).

    Google Scholar 

  73. 73

    Haug, J. T. et al. A Marrella-like arthropod from Cambrian of Australia: A new link between ‘Orsten’-type and Burgess Shale assemblages. Acta Palaeontol. Pol. 58, 629–639 (2012).

    Google Scholar 

  74. 74

    Han, J. et al. Tiny sea anemone from the Lower Cambrian of China. Plos One 5, e13276 (2010).

    ADS  PubMed  PubMed Central  Google Scholar 

  75. 75

    Maas, A. et al. The ‘Orsten’-More than a Cambrian Konservat-Lagerstätte yielding exceptional preservation. Palaeoworld 15, 266–282 (2006).

    Google Scholar 

  76. 76

    Mass, A. et al. Maotianshan-Shale nemathelminths–Morphology, biology, and the phylogeny of Nemathelminthes. Palaeogegr. Palaeoclimatol. Palaeoecol. 254, 288–306 (2007).

    ADS  Google Scholar 

  77. 77

    Harvey, T. H. P. & Butterfield, N. J. Exceptionally preserved Cambrian loriciferans and the early animal invasion of the meiobenthos. Nature Ecol and Evol 1, doi: 10.1038/s41559-016-0022 (2017).

  78. 78

    Rhoads, D. C. & Young, D. K. The influence of deposit feeding organisms on sediment stability and community trophic structure. J. Mar. Res. 28, 150–178 (1970).

    Google Scholar 

Download references


Financial support for this study was provided by the Natural Science Foundation of China (41472083, 41602112, 41290260), China Postdoctoral Science Foundation Funded Project (2016M592288), the Key Scientific Research Fund of University of Henan Province (17A17001), the Specialized Research Fund for the Doctoral Program of Higher Education (20114116110001, 20134116120002) and Program for Innovative Research Team (in Science and Technology) in University of Henan Province (16IRTSTHN014) to Zhang and Qi, and by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants 311727-15 and 311726-13 awarded to Mángano and Buatois, respectively. Francis MacDonald, Peter Sheehan and Jean Vannier provided very useful feedback. We also thank the two Nature Scientific Reports reviewers and the editor for their valuable comments.

Author information




Li-jun Zhang, Luis A. Buatois, and Gabriela Mángano conceived the study. Y.-A. Qi, Y. Meng and D. Li contributed to the field work and thin-section data. All authors participated in data preparation, discussion and interpretation.

Corresponding author

Correspondence to Luis A. Buatois.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, LJ., Qi, YA., Buatois, L. et al. The impact of deep-tier burrow systems in sediment mixing and ecosystem engineering in early Cambrian carbonate settings. Sci Rep 7, 45773 (2017).

Download citation

Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing