A peculiar reworking of Ophiomorpha shafts in the Miocene Nangang Formation, Taiwan

Ludvig Löwemarka* , Yu-Chen Zhenga, Subarna Dasb , Chung-Ping Yeha and Tzu-Tung Chena

aDepartment of Geosciences, National Taiwan University, P.O. Box 13-318, 106 Taipei, Taiwan; bIndian Institute of Technology5 Roorkee, Roorkee, Uttarakhand 247667, India

(Received 14 January 2015; accepted 25 March 2015)

In the Miocene sandstones of the Nankang Formation in north-eastern Taiwan, different varieties of the trace fossilOphiomorpha are abundant. In certain beds, a peculiar reworking of vertical Ophiomorpha shafts was observed. Thisreworking consists of an inner, lined tube positioned in the centre of the shaft. The shaft is lined by thin walls with

10 small knobs and is distinctly different from the shafts of the Ophiomorpha nodosa mazes found in the same beds whichhave thick walls and large knobs. Because both outer and the inner tube walls were constructed by small sub-pellets, adiagenetic origin can be ruled out. The presence of sub-pellets further indicates that the inner tubes were also constructedby crustaceans and not commensal organisms such as worms or fish. The abundance of these vertical shafts suggests thatthey were constructed for a specific purpose, and the similarities in sub-pellets indicate that they likely were constructed

15 by different generations of the same crustacean species. Because brooding chambers were not observed and are rareamong extant marine crustaceans, we suggest that the vertical shafts were constructed to encourage juvenile shrimp toresettle in the parental burrows after they had completed their pelagic larval stages.

Keywords: Miocene; Ophiomorpha nodosa; Shoreface; offshore; Taiwan

Introduction

20 Background and aim

Along the north-east coast of Taiwan, Oligocene to Mio-

cene sediments deposited in littoral to shallow marine

environments have been uplifted and tilted by tectonic

processes related to the collision of a volcanic arc on the

25 Philippine Sea Plate and the Eurasian continental plate

(Suppe, 1984). The intense weathering and erosion

caused by waves and torrential rains have resulted in a

rugged coastline and sparse vegetation cover, providing

detailed exposure of sedimentary and biogenic structures.

30 These sandstones have recorded a set of tectonic and

eustatic sea level changes, allowing a large number of

different environmental settings to be studied. The indi-

vidual beds of these strata often show characteristic

ichnofossil assemblages representing different recurrent

35 environments that are repeated several times in the suc-

cession as the sea level fell and rose. What makes these

sandstones particularly interesting is the fact that many

of the beds are dominated by a single ichnospecies. For

example, in the Yehliu Member of the Taliao Formation,

40 some beds are completely dominated by Schaubcylin-

drichnus, while overlying or underlying beds are domi-

nated by Ophiomorpha (Löwemark & Nara, 2013).

In certain beds of the Nankang Formation, typical

mazes of Ophiomorpha nodosa are common. However,

45 in between these Ophiomorpha mazes, a distinctly differ-

ent kind of Ophiomorpha with considerably thinner and

less knobby walls can be found. These thin-walled

Ophiomorpha often display a peculiar thin-walled inner

tube positioned in the centre of the Ophiomorpha shafts.

50In contrast, the shafts extending from the thick-walled,

knobby Ophiomorpha mazes rarely display this kind of

inner tubes.

The aim of this study was to test whether these inner

tubes are the result of diagenetic processes, if they were

55an integral part of the original Ophiomorpha burrow sys-

tem, or if they represent a secondary reworking of the

tubes by another organism. Furthermore, if the inner

tubes can be shown to be the work of an organism, we

aim to address the possible behaviours that may have

60resulted in the formation of these inner tubes, and the

environmental significance of the presence of these inner

burrows.

Geological setting

Taiwan is situated at the eastern boundary of the Eura-

65sian continent and owes its steep topography to the colli-

sion between the volcanic arc on the Philippine Sea

plate, and the continental margin of the Eurasian plate

(Suppe, 1984). As a result of this collision, two north–

south oriented mountain ranges have formed, the eastern

70representing the volcanic arc of the Philippine Sea plate,

and the western range representing metamorphosed and

uplifted sediment from the Eurasian passive margin.

Because of the north-westward motion of the Philippine

Sea plate, the collision between the two plates is oblique.

75This means that while full collision is taking place in the

central parts, an incipient collision can be found in

the southern parts of the island, and in the north, was

*Corresponding author. Email: loewemark@gmail.com

© 2015 Taylor & Francis

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the collision started, it is now in a post-collisional,

collapsing phase (Shyu, Sieh, Chen, & Liu, 2005; Suppe,

5 1984). During the Penglai orogeny, the strata comprising

Taiwan island were uplifted and deformed (Teng et al.,

1991), resulting in imbricated thrust faults along the

north-east coast (Ho, 1986). The collision in combination

with the opening of the Okinawa trough has resulted in

10 uplifting, faulting and folding of the several thousand

metres thick Cenozoic sediments that were deposited in

a half graben system that developed along the Eurasian

continental margin as a consequence of the opening of

the South China Sea (Chen, 2005).

15 The Miocene strata in Taiwan consist of three main

depositional cycles, each containing a coal-bearing and a

marine unit deposited on the passive margin of the Eura-

sian continent. The study area is located on the north-

east coast in strata belonging to the Nankang Formation

20 (Figure 1), which is encased between the Shitih and the

Nanchuang Formations, extending NE-SW through Tai-

wan (Ho, 1986; Huang, 1990). Mostly, the Nankang

Formation consists of paralic to shallow marine deposits

characterised by strong NW-SE facies changes. It is

25 generally recognised that there are two transgressive–re-

gressive cycles in middle Miocene to upper Miocene.

The Nankang Formation is deposited during the trans-

gressive period, while the underlying Shitih Formation

and the overlying Nanchuang Formation were deposited

30 during regressive periods (Chou, 1970; Hong & Wang,

1988; Huang, 1990). However, more detailed sequence

stratigraphy studies on the north-east coast have

revealed that there are seven smaller transgressive–

regressive cycles within the two major Miocene cycles

35 (Yu & Teng, 1996).

The Miocene age (12–17 Ma) of the Nankang

Formation has been constrained by planktonic foramini-

fers and calcareous nannoplankton; biozone boundaries

of N8/N9 and NN4/NN5 are located in the middle part

40of the Nankang Formation and can be correlated with

the standard outcrops at Chuhuangkeng which contains a

continuous fossils record (Huang, Cheng, & Huang,

1979).

The traditional section of Nangkang Formation

45exposed at north-east coast has been well studied (Ho,

Hsu, Jen, & Fong, 1964; Huang, 1955; Wang, 1953;

Yen & Chen, 1953; Yu & Teng, 1996). The total thick-

ness of the formation is about 500 m; it can be roughly

divided into three parts (Figure 2). Sandstone with

50abundant sea urchin and Mollusca fossils make up the

lower part, a 50 m thick shale and a 29 m thick tuff

constitute the middle part, and the upper sandstone

contains several beds rich in Operculina and mollusca

fossils (Huang et al., 1979).

55Ophiomorpha and burrows of thalassinidean shrimp

The trace fossil Ophiomorpha consists of a tunnel sys-

tem where the walls have been reinforced with pellets,

giving the external wall a knobby appearance, while the

inner wall is typically smooth. The burrows range from

60short vertical or inclined tubes to complex mazes or 3D

boxworks of interconnected shafts and tunnels. Some

workers have related variations in the 3D architecture of

the burrow system to external factors such as substrate

and flow regimes (Bromley, 1996; Frey, Howard, &

65Pryor, 1978). In contrast, Miller and Curran (2001)

found no significant difference in burrow characteristics

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Figure 1. (A) Geological map showing distribution of the Nankang Formation along the north-east Coast of Taiwan. Most observa-tions were made at Fanziao promontory and on a few small islets just next to the Ruibin settlement. (B) The inset map shows thelocation of study area in north-eastern Taiwan.

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when comparing different facies in intertidal settings.

Rather, the producers of Ophiomorpha tended to avoid

inhospitable environments than to adapt their burrows to

5 a harsher environment. They further noticed that wall

pellet packing and arrangement varied a lot between dif-

ferent burrow systems, but also within the same system.

Crustacean burrow systems may fill many ethological

functions, and different parts of one system may actually

10 represent quite different behaviours. For example, differ-

ent parts of the burrow system has been attributed to a

number of different behaviours such as deposit feeding

(Bird & Poore, 1999; Griffis & Chavez, 1988; Miller &

Curran, 2001), shelter (Griffis & Chavez, 1988; Grow,

15 1981), storage of plant material for later use or for

gardening of microbes (Dworschak, 2004; Dworschak,

Koller, & Abed-Navandi, 2006; Frey & Howard, 1975;

Gibert & Ekdale, 2010), simple turnover chambers

(Bromley, 1996), or for reproduction purposes (Forbes,

20 1973; Griffis & Chavez, 1988). However, the burrow

systems of crustaceans are also often used and modified

by commensal organisms (Gibert, Netto, Tognoli, &

Grangeiro, 2006; Karplus, Szlep, & Tsurnamal, 1974;

Scheibling et al., 1990). Callianassa major is probably

25 the best known modern analogue of Ophiomorpha pro-

ducing animals, but other groups of crustaceans such as

Upogebia or Axius are also known to produce burrow

systems with knobby walls. The animal secretes mucus

threads that are used to produce pellets of sediment

30grains (Dworschak, 1998) which are used to reinforce

the walls in substrates where the cohesive forces of the

sediment are too weak to keep the tunnels open.

Material and methods

Observations on stratigraphy and trace fossils were pri-

35marily made at Fanziao promontory and on a few small

islets by the Ruibin settlement (Figure 1). The varied

topography caused by the combination of coastal erosion

and several fracture systems allowed observations on

both bedding plane and cross-sections of the 3D burrow

40systems to be made on several hundred specimens.

Diameters and wall thicknesses of outer and inner tubes

were registered using a digital Vernier caliper. A number

of burrows containing inner tubes were sampled for thin

section preparation and XRD analysis in order to allow

45differences in the composition of substrate and wall

material to be assessed.

Results

Description of the Fanziao section

The total length of Fanziao section is approximately 35

50m, made up by massive sandstone with one interbedded

thin mudstone layer (Figure 3). Sandstones are poorly

sorted, and the grain size change is not significant. How-

ever, the sand–mud ratio shows distinct variations, with

upwards increasing sand content from the muddier bot-

55tom part of Fanziao section to the middle part, which is

characterised by muddy sandstones. The muddy mid-part

is overlain by relatively sand-rich beds, with an upward

increasing sand–mud ratio. The top of the sand-rich

section is again overlaid by relative mud-rich sandstones.

60Most of the sedimentary structure have been obliter-

ated due to heavy bioturbation, only swaley cross-

stratifications is present sporadically within sandstones

where they are sandwiched by bioturbated layers. The

thickness of these layers is about 20 cm each, and they

65sometimes form quasi-planar beddings, with obvious

erosional bases visible at the bottom of the structures.

Another dominant sedimentary structure within sand-

stones is mud laminations. These are only centimetre

thick and sometimes appear along with swaley cross-

70stratification. Through the frequency of mud-rich layers,

the relative amount of mud content within the sandstone

could be estimated. Lenticular sandstone beds are found

at the bottom and the top of Fanziao section intercalated

within the muddy sandstone.

75The bioturbation index of sandstones jumps from 1

to 5 in upper thick sandstone section due to interlacing

of swaley cross-stratification layers and bioturbated

layers. The bioturbation index of lenticular sandstone

beds is low (0–1). In contrast, the bioturbation index of

80muddy sandstone is usually high, especially so for the

Figure 2. Simplified stratigraphic column of the NangangFormation, which consists of about one and a half transgres-sive–regressive cycle. The sedimentary environments of theNankang Formation fluctuated between shoreface and wave-dominated outer shelf (Modified from Yu & Teng, 1999).

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muddy bed in the middle part of the section. In addition

to the four Ophiomorpha types described below, the

sandstones at Fanziao contain numerous Bichordites and

Macaronichnus in certain beds, and Rhizocorallium is

5common in the layers where O. nodosa is abundant.

Chondrites and Planolites were occasionally

Figure 3. Stratigraphic column of Fanziao section showing a storm wave-dominated sedimentary environment that fluctuatedbetween lower shoreface and inner offshore. The stratigraphic cycles are reflected in variations in the sand–mud ratio, as well as inthe trace fossil assemblage.

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encountered, and a few structures that could possibly be

attributed to Piscichnus waitemata were seen. Schaub-

cylindrichnus and Thalassinoides were found only within

5 the muddy sandstones and shales. The ichnofacies there-

fore is interpreted as varying between the Skolithos

ichnofacies and Cruziana ichnofacies. Interestingly,

despite the high abundance of crustacean burrows, only

few stingray feeding pits (Piscichnus waitemata) were

10 observed, in stark contrast to the underlying Taliao

Formation where feeding pits of stingray were found to

be targeted directly to the shafts of Ophiomorpha burrow

systems (Löwemark, 2015).

Three key beds were identified; these contain concen-

15 trated shell debris and are located at 2, 17 and 20 m in

the column. The key beds display wavy bedding with

erosional bases. The bed at 2 m showed loading struc-

tures with a vertical extent approaching 50 cm. The two

beds at 17 and 20 m of the column consist of thick sand-

20 stones containing accumulations of complete sea urchin

fossils. The two beds are separated by a fully bioturbated

layer. These key beds allow us to correlate the Fanziao

column to the lower part of Nangang Formation column

described in earlier studies (Yu, 1997; Yu & Teng,

25 1996).

Ophiomorpha morphologies

In the Nankang Formation, at least four distinct morpho-

types of Ophiomorpha-like burrows can be distin-

guished: (A) knobby, thick-walled mazes; (B) thin,

30 straight tubes with regular branches; (C) dense, dendriti-

cally branching tube systems; and (D) thin-walled,

L-shaped shafts (Figure 4).

The tube systems of morphotype A closely corre-

spond to O. nodosa. Walls are generally smooth on the

35 inside and mammillated by coarse pellets on the outside.

The tubes are typically arranged into horizontal mazes

following certain layers, rather than 3D boxworks. Dif-

ferent layers of the maze may be connected with other

horizontal mazes at deeper levels through vertical or

40 inclined shafts. The knobby shafts of O. nodosa are

often vertical in the upper part, but become curved,

approaching the horizontal, in the lower part where they

connect to the maze. Vertical shafts may show large

vertical extent, and the junctions between shafts and

45 maze typically show swellings that may indicate that

they were used as turning chambers. Although the maze

system is somewhat similar to O. irregulaire (Bromley

& Pedersen, 2008), wall lining and pellet shape do not

correspond to O. irregulaire. In most specimen, the wall

50 thickness and pellet size is uniform around the tube, no

spiky pellets or thinner walls on the burrow floor, as

described for O. irregulaire (Lopez-Cabrera & Olivero,

2014), were observed. Furthermore, vertical shafts are

abundant on bedding plane views, in contrast to O.

55 irregulaire where vertical shafts are rare (Boyd, McIlroy,

Herringshaw, & Leaman, 2012). The uniform wall

thickness and pellet size in the observed Ophiomorpha

also sets it aside from O. rudis which typically display

smooth walls in the horizontal sections (Riahi, Uchman,

60Stow, Soussi, & Ben Ismail Lattrache, 2014; Uchman,

2009). Although O. nodosa occur abundantly in layers

where the other three morphotypes are common, exam-

ples of connections between the different systems are

dubious. The different morphotypes sometimes cross-cut

65each other, but a reworking of larger Ophiomorpha by

smaller, as seen in e.g. Miocene estuarine sands from

Delaware, USA (Miller & Curran, 2001; Miller, Curran,

& Martino, 1998), was not observed. Inner tubes, as

described in detail below for morphotype D, were only

70seen in a few isolated instances.

Morphotype B consists of long, almost straight seg-

ments of lined tubes. From these straight segments,

sparse branches diverge at about 60 degrees from the

main tube. The branching is often paired and does not

75display the pronounced swellings at the junctions typical

for Ophiomorpha. The tube diameter typically lies

around 1 cm, and the walls have a distinct lining that at

least in some cases seem to be constructed by discrete

pellets, giving the exterior a mammillated appearance.

80Morphotype B was primarily observed in bedding plane

view, but on surfaces with high numbers of straight seg-

ments, high numbers of horizontal cuts of vertical, lined

tubes of the same diameter and morphology could be

observed. This suggests that the Morphotype B was con-

85nected to the sediment surface at regular intervals.

Morphotype C is similar to the straight segments

described above, but displays a considerably denser, den-

dritic branching pattern, and typically has a slightly lar-

ger diameter (1–2 cm) and coarser pellets in the wall

90lining.

Although both morphotype B and C occur abun-

dantly in the same beds as O. nodosa and regularly

cross-cut O. nodosa, no indisputable evidence of any

interconnection was found.

95The fourth morphotype consists of a lined tube that

extends for a considerable vertical distance before

abruptly turning horizontal, giving that tube system an

overall L-shaped appearance (Figure 5). Horizontal parts

are rarely observed even in areas where vertical shafts

100are common, suggesting that the horizontal part is short

and not part of an extensive maze as in the adjacent

O. nodosa. Both lining and pellets are considerably less

pronounced compared to O. nodosa. The tube diameter

is slightly smaller than for O. nodosa, typically ranging

105between 2 and 3 cm. In the vertical shafts, signs of an

inner tube are common. This inner tube is lined by a thin

knobby wall similar in colour to the larger outer wall. A

comparison of paired samples of Ophiomorpha vertical

shaft diameters and the diameters of the inner tubes from

110the same samples reveals a weak correlation between the

two (Figure 6). This weak correlation indicates that the

size of the organism producing the inner tube is largely

independent of the diameter of the vertical shafts.

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In a few instances, thin-walled vertical shafts with

5 inner tubes partly overlap or intergrades to the thick-

walled tube systems of O. nodosa systems were seen

(Figure 7).

Thin section analysis

Results from the thin section analysis show that the

10 grains are sub-rounded to angular, well sorted and that

the grains are dominated by quartz, feldspar and glau-

conite (Figure 8). XRD measurements of the wall lining

show that the matrix primarily consists of goethite, while

in the surrounding substrate and in the tube fill, the

15 matrix is a mixture of clay minerals (Figure 9). The

particles vary in size from silt to medium sand, but most

grains are of fine sand size. There is little difference in

grain size distribution between surrounding substrate,

wall material and tube fill material, but while the sur-

20rounding substrate and the tube fill are grain supported,

the wall material is matrix supported. In the wall

material, matrix makes up about 60–65% of the material.

In both the inner and outer tube walls, sub-pellets sensu

Frey et al. (1978) could be observed. However, there is

25some difference in the arrangement of the sub-pellets. In

the outer wall, the sub-pellets appear to be slightly

larger than the sub-pellets from the inner tube. The

outer wall sub-pellets are also more uniform in size and

appear better organised, while the inner wall sub-pellets

30are less distinct and vary more in size and outline

(Figure 10).

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Figure 4. Photographs of the four morphotypes of Ophiomorpha distinguished at Fanziao. (A) Bedding plane view of O. nodosawhich produces extensive mazes of thickly lined knobby tubes. (B) Bedding plane view of the thin, straight segments with widelyspaced regular branches. (C) Bedding plane view of densely branching, dendritic tube systems. (D) Cross-section view of L-shapedshaft with inner tube. (E) 3D-reconstruction of the four types of Ophiomorpha.

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Discussion

The nature of the inner tube

We initially proposed three potential explanations for the

5 occurrence of the inner tube, a purely diagenetic origin,

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Figure 5. Different aspects of the vertical shafts containing inner tubes. (A) Vertical shaft with inner tube. Where the shaft abruptlyturns horizontal the inner tube expands to fill the entire burrow. The continuation of the system into deeper levels visible in this speci-men was rarely seen in other specimen. (B) Close-up showing the wall of the Ophiomorpha shaft and a distinct inner tube. (C) Bed-ding plane view of Ophiomorpha with a distinct inner tube lined by material of the similar material as the material of the outer wall.(D) The rare occurrence of twin inner tubes in a single shaft (bedding plane view).

Figure 6. Scatter plot showing the relationship between outertube diameter of Ophiomorpha and the diameter of the sec-ondary inner tubes. The low correlation coefficient of 0.13calculated through linear regression suggests that the diameterof the inner tube is largely independent of the diameter of thevertical shafts.

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Figure 7. Two examples were relatively thin-walled verticalshafts possibly connect (A) or overlap (B) with thick-walled,knobby O. nodosa burrows. These possible connections couldindicate that the vertical shafts with inner tubes are an integralpart of the O. nodosa producers reproductive cycle.

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an integral part of the original burrow system, or a sec-

ondary reworking of the initial tube. The diagenetic ori-

gin can be dismissed as the thin section analysis clearly

demonstrates that both the outer and inner walls are con-

5 structed by a large number of sub-pellets (Figure 10).

Furthermore, while the material in the walls is matrix

supported, the sediment in the surrounding substrate and

the fill of both the main shaft and the inner tube are

grain supported. Diagenesis may change the matrix, or

10 sometimes even partly alter grains (Galloway, 1974), but

no known diagenetic processes can rearrange the grains

into sub-pellets. We therefore dismiss diagenesis as cause

for the inner tubes, although diagenetic processes

undoubtedly have altered the matrix and thus enhancing

15 the visibility of the inner tube’s wall material. The inner

tube is also distinctly different from the draft fill

channels described from some callianassid burrows

(cf. Seilacher, 2007). The idea that the inner tube should

be an integral part of the burrow system gains some

20support from the fact that restricted apertures are

often observed in the tube systems of modern crus-

taceans that construct Ophiomorpha-like burrows (e.g.

Frey & Howard, 1975; Swinbanks & Luternauer, 1987).

However, the length of the inner tubes observed in the

25Nankang Formation reach several tens of cm, making it

highly unlikely that the same producer that constructed

the original tube with an inner diameter of 2–3 cm

should be able to maintain a much thinner tube in which

it hardly could fit. Studies on modern crustaceans have

30shown that they need to spend more than 20% of their

time maintaining the burrow system (Gagnon, Beaudin,

Silverberg, & Mauviel, 2013; Stamhuis, Reede-Dekker,

van Etten, de Wiljes, & Videler, 1996). The pelleted nat-

ure of the inner wall clearly indicates that the inner tubes

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Figure 8. Thin sections of Ophiomorpha with inner tube. (i) Idealised cross-section of Ophiomorpha showing the positions of thestudied components. (A) Ambient substrate outside of the outer wall. (B) Outer wall and boundary to ambient substrate. (C) Materialbetween inner and outer wall. (D) Wall of the inner tube. (E) Material inside inner tube. Q = Quartz, F = Feldspar, G = Goethite,Gl = Glauconite. Note the presence of goethite as a major matrix mineral exclusively in both the inner and outer walls, while glau-conite is absent in both the inner and outer walls. The matrix of the substrate and burrow fill consists of mixtures of clay minerals asmatrix. It is evident that both walls are matrix supported, whereas the substrate and burrow fills are grain supported.

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5 were actively maintained. It therefore seems unlikely that

the inner tube should have been constructed by the larger

producer, as it would have had no possibility of

maintaining the upper reaches of the inner tube.

Figure 9. XRD analysis of the different components of the Ophiomorpha shaft and inner tube. The material of ambient substrate(A) and the tube fills (C and E) contains quartz and feldspars, while the wall material of both outer (B) and inner (D) tubes containgoethite. Q = Quartz, F = Feldspar, G = Goethite. Result is shown on 2θ between 20° and 30°.

Figure 10. Both the wall of the outer (A) and the inner (B) tubes display distinct sub-pellets. While the sub-pellets of the outer tubewall are distinct and neatly organised, the sub-pellets of the inner tube wall are less well defined and less organised.

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Consequently, the most probably explanation for the

5 presence of the inner tube is that it was constructed

inside the original, larger Ophiomorpha shaft by another

producer. However, a number of distinct behaviours

resulting in an inner tube produced by a secondary

inhabitant can be conceived. The inner tube could be the

10 result of commensal organisms occupying the same bur-

row system, it could represent the invasion by another

species, or the reoccupation of the burrow by other

organisms after the original producer died or moved on.

The construction of new burrows in an older system has

15 also been documented as the response to erosional events

(Howard, 1978). Another possibility includes the con-

struction of brooding chambers, or burrows constructed

to attract colonisation by juveniles after their pelagic

larval stages.

20 Ethological explanations for the inner tube

Commensalism seems unlikely in our case since the

vertical shaft has been restricted by the construction of

the inner tube, effectively blocking it for usage by its

original producer, thus rather akin to an invasion or hos-

25 tile takeover rather than commensalism. Furthermore,

because the inner tube wall was constructed by sub-pel-

lets of similar size and shape as the outer wall, fish or

vermiform co-habitants are effectively ruled out.

Similar inner tubes were described by Pollard,

30 Goldring, and Buck (1993) and tentatively interpreted to

have been constructed by relocated animals, possibly of

a different species. However, the inner tubes described in

their study differ in several important ways. First, the

material filling the Ophiomorpha consisted of muddy

35 coarse silt, distinctly different from wall material. In the

described burrows, the grain size is similar in wall and

fill, although walls were matrix supported while ambient

sediment was clast supported. Second, Pollard et al.

(1993) makes no mention of a lined wall for the inner

40 shaft. In the studied material, there is a clear tube wall

that appears to be pelleted in a way similar to the outer

wall. If the inner tubes represent invasions or reoccupa-

tion of abandoned burrows by other shrimp species, then

the question arises why almost exclusively in the vertical

45 shafts, and not in the curved shafts of O. nodosa? The

high number of vertical shafts found to contain inner

tubes suggests that they were constructed for a specific

purpose. A secondary reoccupation or invasion of

Ophiomorpha burrows from Pleistocene shallow subtidal

50 or tidal flat environments in North Carolina was rejected

by Curran (1976) because of similarities in wall lining

and tunnel arrangement. In analogue, it seems unlikely

that secondary or commensal organisms would be

responsible for the reburrowing of the Ophiomorpha

55 observed in the Nangang Formation.

Crustacean burrows may fill two functions in the

reproductive cycle: egg incubation (brooding) and

recruiting juveniles returning after their planktonic larval

phase (Atkinson, 1988). Brooding chambers constructed

60by the adults are common among insects and land living

arthropods, but examples from marine crustaceans are

rare (Genise, Bedatou, & Melchor, 2008). Only a small

number of fossil structures related to crustacean burrow

systems have been interpreted as brooding chambers. In

65Pleistocene coastal deposits, burrows of a considerably

smaller diameter were seen to branch off from bulbous

chambers that occurred in close association with O.

nodosa (Curran, 1976; Curran & Frey, 1977), and similar

traces from Miocene strata in Uruguay were similarly

70interpreted as brooding chambers (Verde & Martínez,

2004). Another example of presumed brooding chambers

was described from a Campanian age omission surface

in Israel. These chambers contain a number of small pits

on the floor that presumably held the eggs (Lewy &

75Goldring, 2006). To our knowledge, no unequivocal

brooding chambers have been described for modern mar-

ine crustacean that build knobby-walled tube systems,

but Forbes (1973) showed that the larvae of Callianassa

kraussi live their two larval stages in parent burrows and

80are actually unable to swim. They therefore metamor-

phosed within the parents burrow and excavated small

new burrows directly into the wall of the parent burrow.

Moreover, in certain freshwater shrimp, the brooding and

first juvenile stages take place within the parents’ burrow

85system, from which the juvenile later construct miniscule

burrows radiating out from the main burrow (Suter,

1977).

In the studied material, no chambers similar to the

ones described by Curran (1976), Verde and Martínez

90(2004), or Lewy and Goldring (2006) were observed,

and no burrows were seen to excavate from the tube wall

of the main Ophiomorpha burrows. A brood chamber

origin of the inner tubes therefore seems unlikely.

This only leaves the hypothesis that the vertical

95shafts with inner tubes represent structures built by the

parental crustaceans in order to facilitate the settlement

of juveniles after their pelagic larval stages. If this is the

case, then no brooding chambers would be expected.

Many species of ghost shrimp disperse their larvae in the

100open water where they may migrate shorter or longer

distances before returning to the shelf waters for repro-

duction in later stages of their life cycles (Tamaki et al.,

2010, 2013). In some species, the juveniles have been

seen to return to the adult’s burrow system where they

105produce a set of smaller side burrows within the adult

system before producing their own system (Kornienko,

2013; Shimoda & Tamaki, 2004; Tamaki, Ikebe,

Muramatsu, & Ingole, 1992). For example, burrows by

Upogebia affinis showed smaller burrows made by juve-

110nile shrimp extending from enlarged chambers. These

were interpreted to be excavations by young shrimp.

Because the larvae of U. affinis are free-swimming carni-

vores, the interpretation is that they likely returned after

their larval stage to occupy the parent burrows (Frey &

115Howard, 1975).

The relatively high abundance of vertical shafts with

L-shaped lower parts and the scarcity of observations on

10 L. Löwemark et al.

TGDA 1035208 CE: VA QA: RM

13 April 2015 Initial

horizontal parts of the burrow system suggest that the

system primarily consists of vertical shafts with short

5 horizontal components, in stark contrast to O. nodosa

where the maze systems constitute most of the burrow

system. The fact that the thin-walled L-shaped shafts are

abundant and have short horizontal extensions suggests

that they were constructed for a specific purpose.

10 Because any sign of brooding chambers is absent, we

propose that the purpose of the vertical shafts was to

provide optimal conditions for juvenile shrimp after they

finished their pelagic larval stages. The relatively thin

wall of the vertical shaft, in comparison with O. nodosa,

15 could indicate that the structure was in use over a much

shorter time period than the shafts of O. nodosa, consis-

tent with having been constructed for the specific pur-

pose of attracting juvenile shrimp. This hypothesis gains

support from the observation that the sub-pellets of the

20 outer and inner wall appears to have been constructed in

a similar way, suggesting that they were produced by the

same species. This kind of behaviour where the adult

crustacean constructs a burrow in order to attract juve-

niles has actually been observed in O. puerelis (Gibert

25 et al., 2006). Although morphologically very different

from the observed inner tubes, this could be considered

a modern analogue for the observed recolonisation of the

vertical shafts.

It has been shown for modern thalassinid shrimp that

30 substrate plays a significant role in determining the bur-

row morphology (Griffis & Chavez, 1988). The same

species produce different morphologies in different sub-

strates. It consequently seems unlikely that the same spe-

cies would produce different types of burrows in the

35 same substrate, unless the burrow systems filled entirely

different purposes. The burrows with inner tube therefore

likely are either constructed by another species or con-

structed for a specific purpose. The similarities in the

construction and the possible connections between the

40 shafts with inner tubes and O. nodosa mazes indicate

that these two burrows may be part of the same system,

but fill two different purposes: the mazes are feeding

structures (cf. Bromley, 1996) while the vertical shafts

are built to attract recolonisation by juveniles.

45 Diagenetic alteration of the tube material

The outer and inner walls thus appear to have been con-

structed by the same organism, but why is the wall mate-

rial cemented by goethite, a mineral rare in the substrate

matrix and in the tube fills? Several reasons can be put

50 forward to explain the accumulation of goethite

(FeOOH) as a major matrix mineral in both the walls. A

simple argument would be attributed to selective uptake

of iron rich compounds from deposits in cracks and

fissures due to the input of Fe-rich waters by the trace

55 maker (Ter & Buckeridge, 2012). Another possibility

would be that the trace maker was perhaps feeding on

the microbes that had been cultivated in the walls of

the burrow (Uchman, 2009). Studies on extant

Thalassinidean ghost shrimp have revealed slightly

60reducing conditions in the wall material related to the

organic material in the mucus (Bird, Boon, & Nichols,

2000). Microbial growth accelerates the oxidation of

Fe2+ to Fe3+ by acting as a catalyst (Weber et al., 2012),

as the microbes require Fe2+ for obtaining their energy at

65depths where the availability of organic carbon is mini-

mal. This implies that the overall environment in the

walls was oxidising, with the available oxidising pore

waters giving rise to iron bearing hydroxides and oxyhy-

droxide minerals such as goethite. Goethite deposition

70can also be supported by the presence of glauconite in

certain parts of the trace fossil outside of the walls. This

indicates that there was an abundance of iron-rich clays

which degraded to give rise to glauconite and probably

goethite because of the overall oxidising conditions and

75also due to abundance of iron (McConchie, Ward,

Mccann, & Lewis, 1979). Glauconite is formed under

reducing conditions, while the presence of goethite in

the walls suggests an oxidising environment in the walls.

Consequently, glauconite is primarily absent from the

80walls.

Paleoenvironmental setting and significance

Although there is no significant change in lithology in

the Fanziao section, cyclic changes were observed in

sand–mud ratio and trace fossil assemblage. Through

85these observations, the sedimentary environment of these

kinds of massive sandstones traditionally described as

offshore transition zone (Yu, 1997; Yu & Teng, 1996)

can be separated into two sub-sedimentary environments:

lower shoreface and inner offshore. The lower shoreface

90begins at the lower limit of the fair-weather wave base

(Reinson, 1984) and the inner offshore lays beneath it,

above the storm wave base, thus both are affected by

storm wave process. Here, the differences in trace fossil

suites are used to draw the boundary between them fol-

95lowing Pemberton et al. (2001, 2012).

The inner offshore facies is made up by muddy sand-

stone and shale intercalated by lenticular coarser grain

sandstone beds. Higher mud content represents more

distal environments further away from the sediment

100source. The lenticular sandstone beds are usually inter-

preted as tempestites (Huang et al., 1979; Yu & Teng,

1996) where the bioturbation is less intense due to rapid

deposit rate (MacEachern & Bann, 2008) and contain

only vertical dwelling traces such as Ophiomorpha,

105representing opportunistic colonisation of the sandy sub-

strate following storms (Pemberton & MacEachern,

1995; Pemberton, MacEachern, & Ranger, 1992). During

fair-weather periods, mud and sand were constantly dis-

turbed by animals, forming intensely bioturbated layers

110with overprinted burrows where it is difficult to identify

all the trace fossils (Figure 11). For example, at 18 m in

the column, a fully bioturbated bed lays right on top of a

thick storm bed of cumulated fossils, only Thalassi-

noides and vertical shafts of Ophiomorpha can be

Geodinamica Acta 11

TGDA 1035208 CE: VA QA: RM

13 April 2015 Initial

5 identified, indicating a subsequent calm period. The trace

fossil suite of the inner offshore muddy sandstones con-

tains Thalassinoides, Schaubcylindrichnus, Chondrites

and vertical Ophiomorpha shafts. Schaubcylindrichnus

burrows were found only in these muddy sandstones,

10 which help to divide sedimentary environment.

The lower shoreface is made up by thick massive

sandstones, displaying swaley cross-stratifications charac-

terised by strongly erosional amalgamated bed sets and

intensively burrowed beds followed by swaley cross-

15 stratifications. This results in rapid bioturbation index

shifts from 1 to 5. Low bioturbation index occurs in the

layers with swaley cross-stratifications containing few

vertical dwelling trace fossils. Beds with high bioturbation

index sit right on top of the swaley cross-stratifications

20 and extend until the next bed with swaley cross-stratifica-

tion. Disparate trace fossil suites were observed in the

different layers within the massive sandstones. These

characteristics represent frequent periodic storm deposits,

where the storms tended to destroy fair-weather benthic

25 communities (Frey, Pemberton, & Saunders, 1990;

Pemberton, 1992; Pemberton & Robert, 1984). Different

trace fossil suites emplaced during storm period and fair-

weather periods, respectively, allow the deposits to be

separated. Fair-weather period deposits consist of

30 O. nodosa, vertical Ophiomorpha shafts, Rhizocorallium

and Chondrites, indicating an impoverished Cruziana

ichnofacies. Sometimes wavy remnants are inserted in the

amalgamated sandstone beds. Storm period deposits

consist of vertical Ophiomorpha shafts, Bichordites,

35Macaronichnus and Phycosiphon, representing the

Skolithos ichnofacies. Within the Macaronichnus–

Ophiomorpha ichnofabric, Macaronichnus burrows

probably represent an opportunistic behaviour (Curran,

1985; Pollard et al., 1993). In this environment,

40Bichordites is also an opportunistic trace fossil similar to

Macaronichnus, colonising the layers right above the

swaley cross-stratification. Moreover, the morphology of

Ophiomorpha tends to switch from horizontal O. nodosa

to vertical shafts. The shift in orientation being a response

45as energy levels increased (Howard & Frey, 1975).

The peculiar Ophiomorpha with inner tubes were

found within storm layers in the lower shoreface

environment where they coexist with Bichordites and

Macaronichnus, but are located in the upper part of the

50layer.

We speculate that the occurrence of the vertical

Ophiomorpha shafts with inner tubes found in the storm

beds is related to the need to provide additional possibili-

ties for the juveniles after the storms had temporarily

55destroyed the original opening of the O. nodosa maze

system.

Monofor

print

colour o

nline

Figure 11. A 3D ichnofabric model of the lower shoreface environment in the Fanziao section. A transition layer of post-stormdeposits (middle) is encased by two fair-weather layers. Biogenic features of the fair-weather beds are dominated by Cruzianaichnofacies, while in contrast, the ichnofacies of the post-storm bed is more Skolithos like.. In the fair-weather deposit (bottom andtop beds), the trace fossil suite is made up of O. nodosa, Rhizocorallium, Chondrites and two additional types of thinner Ophiomor-pha, indicating Cruziana ichnofacies. The middle layer represents post-storm deposit and can be sub-divided into two parts: the lowerpart consists of swaley cross-stratification with rare vertical Ophiomorpha shafts, while the upper part is fully bioturbated by Bi-chordites and Macaronichnus. This suggests that these trace fossils represent an opportunistic colonisation of the substrate and thatthe colonising window of Bichordites and Macaronichnus is shorter than for Ophiomorpha. Consequently, a succession from swaleycross-stratification, Bichordites and Macaronichnus burrows to Ophiomorpha burrows can be expected. If fair-weather conditionsextend long enough, an assemblage typical of the Cruziana ichnofacies will develop (top layer). In reality, the middle layer that repre-sents frequent or severe storm-dominated conditions (Pemberton et al., 2001) may be much thicker than the beds with well-developedCruziana facies and actually make up most of the massive sandstones in the Fanziao section. Either the time between two storms istoo short for a biological assemblage to form, or the storms were so strong that the original substrate was swashed away. Evidence offrequent storm events are seen in the recurring superimposed succession of storm deposits that cut off the tops of the trace fossils.

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12 L. Löwemark et al.

TGDA 1035208 CE: VA QA: RM

13 April 2015 Initial

Conclusions

Based on detailed field observation on the morphology

of the different types of Ophiomorpha, and on thin sec-

5 tion and XRD analysis of tube walls and tube fill materi-

als, several facts can be established:

• The presence of pellets in the wall of the inner

tube effectively rules out a diagenetic origin of the

10 inner tube.

• The inner tubes are constructed by similar sub-

pellets as the outer tubes, suggesting that both

walls were constructed by similar or related

organisms.

15 • The abundance of the vertical, L-shaped shafts

suggest that they were constructed for a specific

purpose.

Based on these facts, we propose that the vertical

shafts were constructed by the adult crustaceans in order

20 to facilitate the resettlement of juvenile shrimp returning

to the sea floor after finishing their pelagic larval stages.

The inner tubes therefore represent a phase of tube con-

struction by the juveniles before they were large enough

to roam the maze system together with the adult

25 crustaceans.

Acknowledgements

Wen-Shan Chen and Chi-Yu Lee (National Taiwan University),Huei-Fen Chen (National Taiwan Ocean University) andCai-Run Yu (Chinese Culture University) are thanked for assis-

30 tance with the mineralogical evaluations. Jorge Villegas Martínand one anonymous reviewer are cordially thanked for their con-structive comments. This field work of this study was funded byMOST (Ministry of Science and Technology) in Taiwan.

Disclosure statement

35 No potential conflict of interest was reported by the authors.

Funding

This field work of this study was funded by MOST (Ministryof Science and Technology) in Taiwan.

ORCID

40 Ludvig Löwemark http://orcid.org/0000-0002-3337-2367

Subarna Das http://orcid.org/0000-0003-0905-1755

References

Atkinson, R. J. A. (1988). Physiological ecology of burrowingdecapods. In A. A. Fincham & P. S. Rainbow (Eds.),

45 Aspects of decapod crustacean biology (pp. 201–226).London: Zoological Society of London.

Bird, F. L., Boon, P. I., & Nichols, P. D. (2000). Physicochemi-cal and microbial properties of burrows of the deposit-feeding Thalassinidean ghost shrimp Biffarius arenosus

50 (Decapoda: Callianassidae). Estuarine, Coastal and ShelfScience, 51, 279–291. doi:10.1006/ecss.2000.0676

Bird, F. L., & Poore, G. C. B. (1999). Functional burrowmorphology of Biffarius arenosus (Decapoda: Callianassi-dae) from southern Australia. Marine Biology, 134, 77–87.

55doi:10.1007/s002270050526Boyd, C., McIlroy, D., Herringshaw, L. G., & Leaman, M.

(2012). The recognition of ophiomorpha irregulaire on thebasis of pellet morphology: Restudy of material from thetype locality. Ichnos, 19, 185–189. doi:10.1080/

6010420940.2012.734880Bromley, R. G. (1996). Trace fossils: Biology, taphonomy and

applications. London: Chapman and Hall. 361 pp.Bromley, R. G., & Pedersen, G. K. (2008). Ophiomorpha

irregulaire, Mesozoic trace fossil that is either well under-65stood but rare in outcrop or poorly understood but common

in core. Palaeogeography, Palaeoclimatology, Palaeoecol-ogy, 270, 295–298. doi:10.1016/j.palaeo.2008.07.017

Chen, W.-S. (2005). Characteristic trace fossils from shorefaceto offshore environments of an Oligocene succession,

70Northeastern Taiwan. TAO, 16, 1097–1120.Chou, J. T. (1970). A stratigraphy and sedimentary analysis of

the Miocene in northern Taiwan. Petroleum Geology of Tai-wan, 7, 145–189.

Curran, H. A. (1976). A trace fossil brood structure of probable75callianassid origin. Journal of Paleontology, 50, 249–259.

Curran, H. A. (1985). The trace fossil assemblage of a Creta-ceous nearshore environment: Englishtown formation ofdelaware, U.S.A. In K. A. Curran (Ed.), Biogenic struc-tures: Their use in interpreting depositional environments

80Society of Economic Paleontologists and Mineralogists,Special Publication (pp. 264–276).

Curran, H. A., & Frey, R. W. (1977). Pleistocene trace fossilsfrom North Carolina (USA), and their Holocene analogues.In T. P. Crimes & J. C. Harper (Eds.), Trace fossils (vol. 2,

85pp. 139–162). Seel House Press.Dworschak, P. C. (1998). The role of tegumental glands in bur-

row construction by two mediterranean callianassid shrimp.Senkenbergiana maritima, 28, 143–149.

Dworschak, P. C. (2004). Biology of Mediterranean and Carib-90bean Thalassinidea (Decapoda). In A. Tamaki (Ed.), Pro-

ceedings of the Symposium on “Ecology of largebioturbators in tidal flats and shallow sublittoral sediments– from individual behavior to their role as ecosystem engi-neers” (pp. 15–22). Nagasaki: Nagasaki University.

95Dworschak, P. C., Koller, H., & Abed-Navandi, D.(2006). Corallianassalongiventris and Pestarella tyrrhena(Crustacea, Thalassinidea,Callianassidae). Marine Biology,148, 1369–1382.

Forbes, A. T. (1973). An unusual abbreviated larval life in the100estuarine burrowing prawn Callianassa kraussi (Crustacea:

Decapoda: Thalassinidea). Marine Biology, 22, 361–365.doi:10.1007/BF00391395

Frey, R. W., & Howard, J. D. (1975). Endobenthic adaptationsof juvenile thalassinidean shrimp. Bulletin of the Geologi-

105cal Society of Denmark, 24, 283–297.Frey, R. W., Howard, J. D., & Pryor, W. A. (1978). Ophiomor-

pha: Its morphologic, taxonomic, and environmental sig-nificance. Palaeogeography, Palaeoclimatology,Palaeoecology, 23, 199–229.

110Frey, R. W., Pemberton, S. G., & Saunders, T. D. A. (1990).Ichnofacies and bathymetry: A passive relationship. Journalof Paleontology, 64, 155–158.

Gagnon, J.-M., Beaudin, L., Silverberg, N., & Mauviel, A.(2013). Mesocosm and in situ observations of the burrow-

115ing shrimp Calocaris templemani (Decapoda: Thalassinidea)and its bioturbation activities in soft sediments of the Lau-rentian Trough. Marine Biology, 160, 2687–2697.doi:10.1007/s00227-013-2262-0

Galloway, W. E. (1974). Deposition and diagenetic alteration120of sandstone in Northeast Pacific Arc-Related basins:

AQ3

AQ4

AQ5

AQ6

Geodinamica Acta 13

TGDA 1035208 CE: VA QA: RM

13 April 2015 Initial

Implications for graywacke genesis. Geological Society ofAmerica Bulletin, 85, 379–390. doi:10.1130/0016-7606(1974)85<379:dadaos>2.0.co;2

Genise, J. F., Bedatou, E., & Melchor, R. N. (2008). Terrestrial5 crustacean breeding trace fossils from the Cretaceous of

Patagonia (Argentina): Palaeobiological and evolutionarysignificance. Palaeogeography, Palaeoclimatology,Palaeoecology, 264, 128–139. doi:10.1016/j.-palaeo.2008.04.004

10 Gibert, J. M. D., & Ekdale, A. A. (2010). Paleobiology of thecrustacean trace fossil Spongeliomorpha iberica in the Mio-cene of Southeastern Spain. Acta Palaeontologica Polo-nica, 55, 733–740. doi:10.4202/app.2010.0010

Gibert, J. M. d., Netto, R. G., Tognoli, F. M. W., & Grangeiro,15 M. E. (2006). Commensal worm traces and possible juve-

nile thalassinidean burrows associated with Ophiomorphanodosa, Pleistocene, southern Brazil. Palaeogeography,Palaeoclimatology, Palaeoecology, 230, 70–84.

Griffis, R. B., & Chavez, F. L. (1988). Effects of sediment type20 on burrows of Callianassa californiensis Dana and C.

gigas Dana. Journal of Experimental Marine Biology andEcology, 117, 239–253. doi:10.1016/0022-0981(88)90060-3

Grow, L. (1981). Burrowing behaviour in the crayfish, Cam-barus diogenes diogenes girard. Animal Behaviour, 29,

25 351–356. doi:10.1016/S0003-3472(81)80094-2Ho, C. S. (1986). Introduction to the geology of Taiwan:

Explanatory text of the geologic map of Taiwan (p. 163).Taipei: Central Geologic Survey, MOEA.

Ho, C. S., Hsu, M. Y., Jen, L. S., & Fong, G. S. (1964).30 Geology and coal resources of the northern coastal area of

Taiwan. Bulletin of the Geological Survey of Taiwan, 15,1–23.

Hong, E., & Wang, Y. (1988). Basin analysis of the upperMiocene-lower Pliocene series in northwestern foothills of

35 Taiwan. Ti-Chih, 8, 1–20.Howard, J. D. (1978). Sedimentology and trace fossil. In P. B.

Basan (Ed.), Trace fossil concepts (pp. 11–42). OklahomaCity: Sepm Short Course, SEPM, .

Howard, J. D., & Frey, R. W. (1975). Estuaries of the Georgia40 coast, U.S.A.: Sedimentology and biology. II. Regional ani-

mal-sediment characteristics of Georgia estuaries. Sencken-bergiana Maritima, 7, 33–103.

Huang, C. K. (1955). Gold-copper deposits in the Chinkuashihmine, Taiwan, with special reference to the mineralogy.

45 Acta geologica Taiwanica, 7, 1–20.Huang, C. Y. (1990). Upper Miocene stratigraphy and the

horizon of post- Lushanian fauna turnover in NortheasternTaiwan. Proceedings of the Geological Society of China,33, 303–328.

50 Huang, C. Y., Cheng, Y. M., & Huang, T. (1979). Preliminarybiostratigraphic study of the Nankang Formation in theShuinantung section, northern Taiwan. Ti-Chih (InChinese), 2, 1–11.

Karplus, I., Szlep, R., & Tsurnamal, M. (1974). The burrows of55 alpheid shrimp associated with gobiid fish in the northern

Red Sea. Marine Biology, 24, 259–268. doi:10.1007/BF00391901

Kornienko, E. S. (2013). Burrowing shrimp of the infraordersGebiidea and Axiidea (Crustacea: Decapoda). Russian

60 Journal of Marine Biology, 39, 1–14. doi:10.1134/S1063074013010033

Lewy, Z., & Goldring, R. (2006). Campanian crustacean bur-row system from Israel with brood and nursery chambersrepresenting communal organization. Palaeontology, 49,

65 133–140. doi:10.1111/j.1475-4983.2005.00532.xLopez-Cabrera, M. I., & Olivero, E. B. (2014). Ophiomorpha

irregulaire and associated trace fossils from the upper creta-ceous of Patagonia, Argentina: Palaeogeographical and

ethologicalsignificance. Spanish Journal of Palaeontology,7029, 33–44.

Löwemark, L. (2015). Evidence for targeted elasmobranchpredation on thalassinidean shrimp in the Miocene Taliaosandstone formation, NE Taiwan. Lethaia. doi:10.1111/let.12101

75Löwemark, L., & Nara, M. (2013). Morphological variabilityof the trace fossil Schaubcylindrichnus coronus as aresponse to environmental forcing. Palaeontologica elec-tronica, 16, 5A.

MacEachern, J. A., & Bann, K. L. (2008) The role of ichnology80in refining shallow marine facies models. In G. Hampson,

R. Steel, P. Burgress, & R. Dalrymple (Eds.), Recentadvances in models of siliciclastic shallow-marine stratigra-phy (pp. 73–116). SEPM Special Publication.

McConchie, D. M., Ward, J. B., Mccann, V. H., &85Lewis, D. W. (1979). A Mössbauer investigation of

glauconite and its geological significance. Clays and ClayMinerals, 27, 339–348.

Miller, M. F., & Curran, H. A. (2001). Behavioral plasticity ofmodern and Cenozoic burrowing thalassinidean shrimp.

90Palaeogeography, Palaeoclimatology, Palaeoecology, 166,219–236.

Miller, M. F., Curran, H. A., & Martino, R. L. (1998).Ophiomorpha nodosa in estuarine sands of the lower Mio-cene Calvert formation at the Pollack Farm Site, Delaware.

95In B. R. N. (Ed.), Geology and paleontology of the lowerMiocene Pollack Farm Fossil Site, Delaware (pp. 41–46).Delaware Geological Survey.

Pemberton, G. S., Spila, M., Pulham, A. J., Saunders, T.,MacEachern, J. A., Robbins, D., & Sinclair, I. K. (2001).

100Ichnology and sedimentology of shallow to marginal mar-ine systems: Ben Nevis & Avalon Reservoirs, Jeanne d’ArcBasin, Short Course Notes 15. Geological Association ofCanada, 343 pp.

Pemberton, S. G. (Ed.). (1992). Applications of ichnology to105petroleum exploration. Calgary: SEPM – Society for Sedi-

mentary Geology.Pemberton, S. G., & MacEachern, J. A. (1995). The ichnologi-

cal signature of storm deposits: The use of trace fossils inevent stratigraphy. In C. E. Brett (Ed.), Paleontological

110event horizons – Ecological and evolutionary implications(pp. 73–109). New York, NY: Columbia University Press.

Pemberton, S. G., MacEachern, J. A., Dashtgard, S. E., Bann,K. L., Gingras, M. K., & Zonneveld, J.-P. (2012). Chapter19 – Shorefaces. In K. Dirk & G. B. Richard (Eds.),

115Developments in sedimentology (pp. 563–603). Elsevier.Pemberton, S. G., MacEachern, J. A., & Ranger, M. J. (1992).

Ichnology and event stratigraphy: The use of trace fossilsin recognizing tempestites. In S. G. Pemberton (Ed.), Ap-plication of Ichnology to Petroleum Exploration. A Core

120Workshop. SEPM Core Workshop Notes (pp. 85–117).Pemberton, S. G. F., & Robert, W. (1984). Quantitative meth-

ods in ichnology: Spatial distribution among populations.Lethaia, 17, 33–49.

Pollard, J. E., Goldring, R., & Buck, S. G. (1993). Ichnofabrics125containing Ophiomorpha: significance in shallow-water

facies interpretation. Journal of the Geological Society,London, 150, 149–164.

Reinson, G. E. (1984). Barrier-island and associated strand-plain systems. In R. G. Walker (Ed.), Facies models

130(pp. 119–140). Geoscience Canada, Reprint Series 1.Geological Society of Canada, St. John’s.

Riahi, S., Uchman, A., Stow, D., Soussi, M., & Ben IsmailLattrache, K. (2014). Deep-sea trace fossils of theOligocene–Miocene Numidian Formation, northern Tunisia.

135Palaeogeography, Palaeoclimatology, Palaeoecology, 414,155–177. doi:10.1016/j.palaeo.2014.08.010

AQ7

AQ8

AQ9

AQ10

AQ11

AQ12

AQ13

AQ14

14 L. Löwemark et al.

TGDA 1035208 CE: VA QA: RM

13 April 2015 Initial

Scheibling, R., Evans, T., Mulvay, P., Lebel, T., Williamson,D., & Holland, S. (1990). Commensalism between an epi-zoic limpet, Patelloida nigrosulcata, and its gastropod

5 hosts, Haliotis roei and Patella laticostata, on intertidalplatforms off Perth, Western Australia. Marine andFreshwater Research, 41, 647–655. doi:10.1071/MF9900647

Seilacher, A. (2007). Trace fossil analysis. Berlin: Springer.10 Shimoda, K., & Tamaki, A. (2004). Burrow morphology of the

ghost shrimp Nihonotrypaea petalura (Decapoda: Tha-lassinidea: Callianassidae) from western Kyushu, Japan. Mar-ine Biology, 144, 723–734. doi:10.1007/s00227-003-1237-y

Shyu, J. B. H., Sieh, K., Chen, Y.-G., & Liu, C.-S. (2005).15 Neotectonic architecture of Taiwan and its implications for

future large earthquakes. Journal of Geophysical Research:Solid Earth, 110, B08402. doi:10.1029/2004JB003251

Stamhuis, E. J., Reede-Dekker, T., van Etten, Y., de Wiljes, J.J., & Videler, J. J. (1996). Behaviour and time allocation of

20 the burrowing shrimp Callianassa subterranea (Decapoda,Thalassinidea). Journal of Experimental Marine Biologyand Ecology, 204, 225–239. doi:10.1016/0022-0981(96)02587-7

Suppe, J. (1984). Kinematics of arc-continent collision, flipping25 of subduction, and back-arc spreading near Taiwan.

Memoir of the Geological Society of China, 6, 21–33.Suter, P. (1977). The biology of two species of Engaeus

(Decapoda: Parastacidae) in Tasmania. II. Life history andlarval development, with particular reference to E. cis-

30 ternarius. Marine and Freshwater Research, 28, 85–93.doi:10.1071/MF9770085

Swinbanks, D. D., & Luternauer, J. L. (1987). Burrow distribu-tion of Thalassinidean Shrimp on a Fraser Delta Tidal Flat,British Columbia. Journal of Paleontology, 61, 315–332.

35 doi:10.2307/1305325Tamaki, A., Ikebe, K., Muramatsu, K., & Ingole, B. (1992).

Utilizatiqn of adult burrows by juveniles of the ghostshrimp, Calllanassa poalica Ortmann: Evidence from resincasts of burrows. Researches on Crustacea, 21, 113–120.

40 Tamaki, A., Mandal, S., Agata, Y., Aoki, I., Suzuki, T.,Kanehara, H., Aoshima, T., Fukuda, Y., Tsukamoto, H., &Yanagi, T. (2010). Complex vertical migration of larvae ofthe ghost shrimp, Nihonotrypaea harmandi, in inner shelfwaters of western Kyushu, Japan. Estuarine, Coastal and

45 Shelf Science, 86, 125–136. doi:10.1016/j.ecss.2009.11.005

Tamaki, A., Saitoh, Y., Itoh, J.-I., Hongo, Y., Sen-ju, S.-S.,Takeuchi, S., & Ohashi, S. (2013). Morphological characterchanges through decapodid-stage larva and juveniles in theghost shrimp Nihonotrypaea harmandi from western

50Kyushu, Japan: Clues for inferring pre- and post-settlementstates and processes. Journal of Experimental Marine Biol-ogy and Ecology, 443, 90–113. doi:10.1016/j.jembe.2013.02.038

Teng, L. S., Wang, Y., Tang, C. H., Huang, T. C., Yu, M. S., &55Ke, A. (1991). Tectonic aspects of the Paleogene deposi-

tional basin of northern Taiwan. Proceedings of the Geo-logical Society of China, 34, 313–316.

Ter, P. C., & Buckeridge, J. S. J. S. (2012). Ophiomorphabeaumarisensis isp. nov., a trace fossil from the late Neo-

60gene Beaumaris Sandstone is the burrow of a tha-lassinidean lobster. Proceedings of the Royal Society ofVictoria, 124, 223–231.

Uchman, A. (2009). The Ophiomorpha rudis ichnosubfacies ofthe Nereites ichnofacies: Characteristics and constraints.

65Palaeogeography, Palaeoclimatology, Palaeoecology, 276,107–119. doi:10.1016/j.palaeo.2009.03.003

Verde, M., & Martínez, S. (2004). A new ichnogenus for crus-tacean trace fossils from the upper Miocene Camachoformation of Uruguay. Palaeontology, 47, 39–49.

70doi:10.1111/j.0031-0239.2004.00346.xWang, Y. (1953). Geology of the Chinkuashih and Chiufen dis-

tricts, Taipei hsien, Taiwan. Acta geologica Taiwanica, 5,47–67.

Weber, K. A., Spanbauer, T. L., Wacey, D., Kilburn, M. R.,75Loope, D. B., & Kettler, R. M. (2012). Biosignatures link

microorganisms to iron mineralization in a paleoaquifer.Geology, 40, 747–750. doi:10.1130/g33062.1

Yen, T. P., & Chen, P. Y. (1953). Explanatory text of the geo-logic map of Taiwan, Tatunshan Sheet. (9 pp.). Geological

80Survey of Taiwan.Yu, N. T. (1997). Sequence stratigraphy of the middle to upper

Miocene strata, northern Taiwan: A preliminary study. Pro-ceedings of the Geological Society of China, 40, 685–707.

Yu, N. T., & Teng, L. S. (1999). Depositional environments of85the Taliao and Shihti Formations, northern Taiwan. Bulletin

of the Central Geological Survey, Taiwan, 12, 99–132.Yu, N. T., & Teng, S. L. (1996). Facies characteristics and

depositional cycles of middle and upper Miocene strata ofthe Western Foothills, northern Taiwan. Ti-Chih, 15, 29–60.

AQ15

Geodinamica Acta 15

TGDA 1035208 CE: VA QA: RM

13 April 2015 Initial