Feeding Strategy and Locomotion of Cambrian Hyolithides

Home , Balang Formation, Buenellus, Hyolitha, Poleta formation

Available online at www.sciencedirect.com

ScienceDirect

Palaeoworld 27 (2018) 334–342

Feeding strategy and locomotion of Cambrian hyolithides

a,∗ a b c,d b

Hai-Jing Sun , Fang-Chen Zhao , Rong-Qin Wen , Han Zeng , Jin Peng

State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China

Resources and Environmental Engineering College, Guizhou University, Guiyang 550025, China

College of Earth Sciences, University of Chinese Academy of Sciences, No. 19 Yuquan Road, Beijing 100049, China

Department of Paleobiology, National Museum of Natural History, P.O. Box 37012, MRC-121, Washington, DC 20013-7012, USA

Received 7 November 2017; received in revised form 8 March 2018; accepted 26 March 2018

Available online 3 April 2018

Abstract

The Chengjiang (Cambrian Stage 3) and Balang (Cambrian Stage 4) Konservat-Lagerstätten of South China have produced abundant hyolithide

hyoliths; however, little attention has been paid to their feeding strategy and the role it played in the ecosystem. Hyolithides preserved in coprolites

from the Chengjiang Biota and associated with a Tuzoia carcass from the Balang Fauna reveal the ﬂuid feces consuming and scavenging strategies

of this group. Size distribution of hyolithides demonstrates that their dietary habit is ontogenetically dependent, with juveniles having ingested

organic-rich material whereas adult food consumption was more likely by a variety of species-dependent methods The ﬁrst discovery of hyolithides

in association with locomotion traces and burrows indicates they were not only epibenthic vagrants, but also shallow horizontal burrowers. The

new discoveries reported herein enhance our understanding of the feeding strategy and other behaviours of Cambrian hyolithides.

Keywords: Hyolithides; Feeding habit; Trace fossil; Cambrian; Chengjiang Biota; Balang Fauna

1. Introduction quently appear in the gut remains or coprolites of predators as an

important food item (Chen et al., 1996; Chen and Li, 1997; Chen,

Extensive study of exceptionally preserved Cambrian 2004; Vannier and Chen, 2005). Although both qualitative and

Burgess Shale-type biotas offers deep insights into the trophic quantitative analyses have been applied to the Chengjiang Biota

relationships of early life and permits further reconstruction to reconstruct the ecosystem and trophic links among animals

of their ecosystems (Dunne et al., 2008; Vannier, 2012). The (Hu, 2005; Vannier and Chen, 2005; Zhao et al., 2010, 2012,

Chengjiang Biota (Cambrian Stage 3) in Yunnan Province and 2014), little attention has been paid to the feeding behaviours

the Balang Fauna (Cambrian Stage 4) in Guizhou Province, of the hyoliths (Chen, 2004; Vannier and Chen, 2005), and the

South China, are two of the contributors to our understanding role that they played in the ecosystem has long been overlooked.

of Cambrian animals and their interactions. Hyoliths are one of Similarly, with respect to the hyoliths in the Balang Fauna, only

the most numerous and diverse biomineralising animals during limited work has focused on the dietary habit of the hyolithides

the Cambrian, and ranged throughout the Paleozoic until their (Sun et al., 2016) and their biological associations with other

Permian extinction. Hyolithides, as one of the main epifaunal animals (Sun et al., 2017). Deﬁnitive traces produced by these

groups, are abundant in the Chengjiang and Balang lagerstätten animals have remained undocumented until now.

(Peng et al., 2005; Zhao et al., 2010, 2012, 2014), and they fre- Our report focuses on three groups of specimens, two from

the Chengjiang Biota containing hyolithides that we assign to

‘Ambrolinevitus’ ventricosus Qian and the other from the Balang

∗ Fauna that consists of indeterminate individuals. The former two

Corresponding author at: State Key Laboratory of Palaeobiology and Stratig-

are concentrated in fecal deposits, and one of them was described

raphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence

in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, earlier by Chen (2004) and Vannier and Chen (2005). The latter

China. from the Balang Fauna consists of individuals located on and

E-mail address: [email protected] (H.J. Sun).

https://doi.org/10.1016/j.palwor.2018.03.003

H.J. Sun et al. / Palaeoworld 27 (2018) 334–342 335

around a Tuzoia sp. carcass. These specimens allow us to make 2010; Hu et al., 2013; Botting et al., 2015; Martí Mus, 2016;

new interpretations concerning the feeding strategies and other Zhu et al., 2016), and rarely preserved in three dimensions

behaviours of hyolithides, and provide additional details regard- (Sun et al., 2016). Because of inadequate preservation of the

ing the ﬂow of energy within the ecosystem from the perspective hyolithide gut, the feeding habit of these organisms remained

of hyolithide hyoliths. In addition, we provide the ﬁrst report of largely speculative, and no detailed comparison of feeding

traces of hyolithide locomotion and horizontal burrowing. habit between hyolithides and orthothecids was possible. The

hyolithides, with their slow and limited locomotion, were ear-

2. Material and methods lier interpreted as generalized omnivores, including deposit or

detritus feeders (Runnegar et al., 1975; Marek and Yochelson,

The hyoliths from the Chengjiang Biota are preserved in 1976; Dzik, 1980), ﬁlter feeders (Runnegar et al., 1975), and

yellowish-green claystones from the Maotianshan Member of possible grazers (Marek and Yochelson, 1976). Subsequently,

the Yu’anshan Formation in Shankou Village of Anning County serial discoveries of epibionts (bryozoans and tubular corals)

and Ma’anshan Village of Chengjiang County, Yunnan Province, that lived only on the conchs of hyolithides (Marek and Galle,

China. Trilobites associated with these individuals are indica- 1976; Malinky, 1990, 2006; Galle and Plusquellec, 2002; Galle

tive of the Eoredlichia-Wutingaspis Zone (Steiner et al., 2001), and Parsley, 2005) indicated that the hyolithides were rheophylic

which correlates with unnamed Cambrian Series 2 Stage 3 organisms and low level ﬁlter feeders (Marek et al., 1997). How-

(Zhao et al., 2012). A specimen from the Balang Fauna is ever, the hyolithide Haplophrentis reesei Babcock and Robison,

preserved in greenish-grey mudstone of the Balang Formation 1988 from the middle Cambrian Spence Shale with its incom-

in the Wenglingtang section in Kaili City, Guizhou Province, plete gut (central string) ﬁlled with sediments was regarded

China, which lies within the Arthricocephalus chauveaui Zone. as a deposit feeder (Babcock and Robison, 1988). An excep-

This zone correlates with unnamed Cambrian Series 2 Stage 4 tionally preserved simple U-shaped and sediment-free gut of

(Yan et al., 2014). For detailed geographical, stratigraphical, and a hyolithide was illustrated by Butterﬁeld (2001, 2003) from

depositional information on these sections see Zhu et al. (2001), the middle Cambrian Mount Cap Formation and interpreted

Peng et al. (2005), Zhao et al. (2012) and Sun et al. (2017). Spec- by him as evidence for a suspension-feeding habit (Butterﬁeld,

imens discussed in this report are housed in the Nanjing Institute 2001). In contrast, a hyolithide reported from the early Cambrian

of Geology and Palaeontology, Chinese Academy of Sciences Chengjiang Biota with a complex folded and sediment-ﬁlled ali-

(specimens with preﬁxes SK and NIGPAS); and the palaeonto- mentary tract was interpreted as herbivore or sediment feeder

logical collection of Guizhou University (specimen with preﬁx (Chen, 2004). Recently, two hyolithides from the base of the

KW). Cambrian Emigrant Formation, USA and the Balang Formation,

Our material was examined and imaged by the standard light China were reported as having a three dimensionally preserved

microscopy, SU3500 Scanning Electron Microscope (SEM) gut consisting of a spiral intestine wound about a nearly straight

with Electron Dispersive X-ray (EDX), digital macrophotogra- rectum (Sun et al., 2016). These specimens support the deposit or

phy [Nikon D300S with an AF-S Micro Nikkor 105 mm f/2.8G detritus-feeding habit of hyolithides as suggested earlier (Marek

lens], and a Carl Zeiss SteREO Discovery V12 microscope and Yochelson, 1976; Babcock and Robison, 1988; Chen, 2004).

linked to an AxioCam HR3 digital microscope CCD camera. A subsequently discovered hyolithide that has an exception-

Photographs were stacked and rendered using Adobe Photoshop ally preserved gut possessing an oesophagus, a central tube,

CS6 and CorelDraw X4 softwares. and lateral winding fecal string was described from the Ordovi-

cian Fezouata Konservat-Lagerstätte of Morocco by Martí Mus

3. Previous work on feeding habit of hyolithide hyoliths (2016). The illustrated tentacled mouth of that specimen was

reconstructed as a generalized organ to adapt to suspension-

The group Hyolitha is usually divided into two subgroups: detritus-deposit feeding spectrum (Martí Mus, 2016). The more

orthothecides and hyolithides. The skeleton of the former con- recently described tentacled Haplophrentis with a U-shaped gut

sists of a conical shell and a planar-retractable operculum, from the Burgess Shale and Spence Shale is illustrated as ben-

whereas the latter is characterised by a conch with a protruding thic suspension feeding lophophorates (Moysiuk et al., 2017).

ligula along the ventral apertural rim, a biplanar operculum, and Therefore it would seem as though the tentacles of hyoliths are

a pair of lateral spines termed helens. In addition to the skeletal organs for food collection from different resources.

differentiations, these two groups have distinct digestive sys-

tems. Usually the content of the gut is in some manner direct 4. Description of specimens and interpretation

evidence for the feeding habit of an animal (Vannier, 2012).

Digestive tracts of orthothecides have been well documented 4.1. Specimens from the Chengjiang Biota, Yunnan

from three dimensionally preserved material (Runnegar et al., Province, China

1975; Pojeta, 1987; Kruse, 1997; Horny,´ 1998; Malinky, 2003;

Devaere et al., 2014) and this sediment-ﬁlled folded gut suggests 4.1.1. SK 90001 from Shankou Village in Anning County

a deposit-feeding strategy (Devaere et al., 2014). The inverted pear-shaped aggregate of fossils includes a

On the other hand, the digestive tracts of hyolithides are usu- loosely packed coprolite with a cluster of the brownish coloured

ally compressed in shale (Babcock and Robison, 1988; Mao hyolithide ‘A.’ ventricosus associated with it (Fig. 1A–C). Light

et al., 1992; Butterﬁeld, 2003; Chen, 2004; English and Babcock, grey wrinkled and cracked waptiid carapaces are the dominant

336 H.J. Sun et al. / Palaeoworld 27 (2018) 334–342

Fig. 1. Inverted pear-shaped aggregate containing waptiid remains and the hyolithide ‘Ambrolinevitus’ ventricosus Qian, from the Maotianshan Shale Member of

the Yu’anshan Formation at Shankou Village in Anning County, Yunnan Province, China, SK 90001. (A, B) General view and explanatory diagram, boxes in (A)

show the locations of (C–E). (C) Cluster of hyolithides. (D) Hyolithides within the ﬂuid component of coprolite. (E, F) Colour and stacked SEM photos, hyolithide

conch with possible operculum preserved in association with linear trace fossil, red dotted line indicates the outline of hyolithide skeleton and associated trace.

Abbreviations: co = conical shell, op = operculum, tr = trace fossil. Scale bar = 1 cm for (A, B), 3 mm for (C), 2 mm for (D), and 1 mm for (E, F).

forms within the coprolite, and amorphous remains preserved tal pieces in some specimens strongly suggests these animals

with them may represent the ﬂuid component of the feces were buried in situ.

(Vannier and Chen, 2005) or a taphonomic artefact. A cluster One hyolithide conch and possible incomplete operculum

of ‘A.’ ventricosus is concentrated at one end of the aggre- are located at the end of a tapering and gently curved linear tract

gate and some other individuals are either scattered around or (Fig. 1A, B, E, F). The tract is convex and not aequilate, and the

located within the coprolite. The unsorted, randomly distributed widest part is ca. 1.0 mm, which is slightly narrower than that of

hyolithides (3.5–6.9 mm in length) are usually preserved as the aperture of the associated hyolithide (ca. 1.2 mm). The loca-

conchs with opercula attached (Fig. 1). Articulation of all skele- tion of the hyolithide at the end of the tract, with apex pointing

H.J. Sun et al. / Palaeoworld 27 (2018) 334–342 337

Fig. 2. Aggregate containing waptiid remains and the hyolithide ‘Ambrolinevitus’ ventricosus Qian, from the Maotianshan Shale Member of the Yu’anshan Formation

in Ma’anshan Village of Chengjiang County, Yunnan Province, China, NIGPAS 166947. (A, B) General picture and schematic diagram, details of boxes in (A) are

shown in (C) and (D) respectively. (C) Fragments of waptiid surrounded by hyolithides with their conical shells attached to opercula. (D) Cluster of hyolithides with

some conical shells articulated with opercula. Abbreviations: co = conical shell, op = operculum. Scale bar = 5 mm for (A, B), and 3 mm for (C, D).

toward the tract, and almost corresponding morphologies and These two specimens (SK 90001 and NIGPAS 166947) with

diameters of the body and the fossil tract strongly support the preserved hyoliths located around and within the coprolite seem

notion that the hyolithide was the trace-maker. to support the scenario that the hyolithides were enjoying a

fecal meal. Because no skeletal remains have ever been reported

within the guts of hyolithides, it seems reasonable to suggest that

4.1.2. NIGPAS 166947 from Ma’anshan Village in

‘A.’ ventricosus was feeding on the non-mineralized ﬂuid phase,

Chengjiang County

organic-rich material (Vannier and Chen, 2005) or microbial ﬁlm

The semi-elliptical aggregate with reddish background colour

around the coprolite.

that contrasts markedly with the yellowish surrounding sedi-

ment contains fragments of wrinkled waptiid carapaces, pieces

of bivalved bradoriids and a cluster of hyolithide ‘A.’ ventricosus 4.2. Specimen from the Balang Fauna, Guizhou Province,

exoskeletons (Fig. 2). The shell-free part of the coprolite may China

represent the diffused ﬂuid portion (Vannier and Chen, 2005).

Unsorted (2.2–5.6 mm in length) individuals of ‘A.’ ventricosus This specimen from the Balang Fauna is composed of at least

are scattered within the coprolite without preferred orientation, three distinct animals: Tuzoia sp., the hyolithides, trilobites and

and most of them are preserved as conchs attached with their an organism or organisms that left behind the traces (Fig. 3A,

opercula in place (Fig. 2C, D), which indicates they were buried B). T. sp. is preserved as two valves with some soft parts (e.g.,

in situ. eye and eye stalk), but the valves have been displaced and now

338 H.J. Sun et al. / Palaeoworld 27 (2018) 334–342

Fig. 3. Hyolithides preserved in and around a Tuzoia sp. carcass, from the Balang Formation at Wenglingtang section in Kaili City, Guizhou Province, China, KW-8-6.

◦

(A, B) General view and line drawing, boxes in (A) indicate the locations of (C–E) (rotate 180 ), white arrow shows the location of (G). (C) Cluster of hyolithides,

white arrow indicates incomplete hyolithide conchs, yellow and red arrows indicate the locations of (H) and (I). (D) SEM photo, a possible hyolithide conch buried in

the T. sp. carcass with shell partially exposed (white arrow) in association with trace fossil. (E) A hyolithide conch preserved in association with trace fossil, white box

shows the location of (F). (F) SEM photo, the anterior part of hyolithide conch is buried beneath the reticulate pattern. (G) SEM photo, a hyolithide conch preserved

with an associated operculum. (H) SEM photo, an operculum with a pair of platyclavicles. (I) A hyolithide with conch, articulated operculum and a preserved tubular

gut, box indicates the area of elemental mapping shown in (J–O). Abbreviations: ca = cardinal shield, co = conical shield, es = eye stalk, ey = eye, us = undetermined

structure. Scale bar = 1 cm for (A, B), 2 mm for (C, E), 300 ␮m for (D), 500 ␮m for (F, G, I), and 200 ␮m for (H). (For interpretation of the references to color in this

ﬁgure legend, the reader is referred to the web version of this article.)

one valve partially overlaps the other. Reticulate patterns and the to each other (Fig. 3G, I). The hyolithides are scattered on one

meandering trace fossil Gordia cover the outer surface of the T. of the valves and around the left side of the T. sp. skeleton. Char-

sp. carapace. Linear traces on the T. sp. skeleton vary dramati- acters stated above indicate that the hyolithides are preserved in

cally in both length and width. Without key external characters situ, and the occurrence of the trace fossils and hyolithides within

preserved, the hyolithides cannot be conﬁdently identiﬁed. They the T. sp. carapace suggests T. sp. had already died prior to burial,

are small (1.0–5.6 mm in length) and considered to represent but not too long before, because the labile soft parts of the animal

a juvenile stage, because usually this morphotype found in the still can be observed in places. A mineralized tubular gut pre-

Balang Fauna exceeds 10 mm in length (Sun et al., 2017). Speci- served within the conch of an articulated hyolithide individual

mens are preserved as conchs (Fig. 3C, E) and opercula (Fig. 3H) (Fig. 3I) is sediment free and covered by iron oxides (Fig. 3J–O).

unattached, but in some cases both skeletal pieces are connected This demonstrates that the hyolithides were unlikely sediment

H.J. Sun et al. / Palaeoworld 27 (2018) 334–342 339

Fig. 4. (A) Reconstruction of general morphology of hyolithides (Martí Mus and Bergström, 2005; Moysiuk et al., 2017). (B, C) Hypothesized model of furrow

constructed by hyolithide, arrows indicate the directions of sediment movement; (B) front view of apertural part; (C) cross section of conical shell near apex.

Abbreviations: co = conical shell, he = helen, op = operculum, te = tentacle.

digesters but instead probably fed on the decaying organic-rich knowledge of hyolithide behaviour and aids in improving our

soup and microbial ﬁlm around the dead body. understanding of the association of speciﬁc traces with their

The aperture of one hyolithide is buried beneath the reticu- makers.

late sculpture of Tuzoia (Fig. 3E, F). Its apertural width is ca. Specimens from the Chengjiang Biota and the Balang Fauna

0.9 mm, which is more or less consistent with the size of the possess tracts and/or burrows that may likely have been produced

tract (0.5–0.9 mm wide) associated with it. The tract, preserved by the hyolithides and burrows constructed by hyolithides are

in concave hyporelief, is aligned with the hyolithide conch, shallow. Because the hyolithides are small, it is not surprising

strongly suggesting that the trace was produced by the move- that their slender helens have been unable to leave any traces

ment of the hyolithide. At least some, if not all, of the burrows in the thick skeletal or sediment matrix. Although hyolithides

were constructed by them. Although the apex of the hyolithide are usually interpreted as epibenthic vagrants, the specimens

is slightly displaced from the tract, this may have been the result described herein provide evidence that they were also able to bur-

of subsequent taphonomic processes. Another specimen buried row horizontally and to a shallow depth within substrate. In this

with T. sp. is an incomplete conch exposed in a gently curved scenario (Fig. 4), helens could have provided locomotion, while

burrow (Fig. 3D). It further suggests that the hyolithides were the operculum and protruding soft parts may have served to aid

scavenging on the decaying soft parts beneath the cuticle of the in digging (Fig. 4A, B). The mouth, circled with tentacles (Martí

T. sp. carcass. Mus, 2016; Moysiuk et al., 2017), would have been responsible

for collecting organic material to ingest (Fig. 4A, B). On the orig-

inal tract surface, there should be sculptures present that were

5. Discussion

generated by matrix being pushed laterally and forward (Fig. 4B,

C) and by the ornamentation on the venter of hyolithides as

5.1. Traces of hyolithides

they moved through the substrate. However, details within the

traces are usually absent, which may have resulted from the

Trace-body fossil assemblages are common in the Burgess

overlying sediment having overprinted the ﬁne details (Collette

Shale-type deposits (Zhang et al., 2007; Wang et al., 2009;

et al., 2010). These smooth and sinuous traces were constructed

Conway Morris and Peel, 2010; Mángano, 2011; Fatka and

by hyolithides probably to feed within the organic-rich matrix.

Kozák, 2014), and similar sinuous traces have been frequently

Other than vermiform animals, hyolithides can also produce lin-

described on discoidal animals (Wang et al., 2009; Lin et al.,

ear and meandering burrows, which provides a hint to identify

2010), bivalved arthropods (e.g., Isoxys, Tuzoia and Waptia, etc.;

trace producers of similar tracts in other Burgess Shale-type

Zhang et al., 2007; Wang et al., 2009; Mángano, 2011), and

deposits.

some other skeletal animals (e.g., echinoderms, brachiopods,

The horizontal burrowing and partly infaunal mode of life of

hyoliths and trilobites, etc.; Babcock and Peel, 2007; Lin et al.,

the hyolithides probably served as adaptations for stability on the

2010; Peel, 2010; Mikulásˇ et al., 2012; Sun et al., 2015),

sea ﬂoor, given that the ventral surfaces of many hyolith species

but identifying the trace-maker is always difﬁcult. Ideally, a

are rounded and convex. Partial burial within the sediment would

trace-maker preserved in its ﬁnal tract provides unequivocal

have inhibited movement by currents or other organisms on the

evidence of the organism that made the trace, because the

seaﬂoor. The partly infaunal life habit described herein contrasts

differences in required preservation conditions of traces and

with that proposed by Sysoyev (1959) and Fisher (1962) in which

trace-makers, trace and trace-maker associations are not very

they regarded conical hyoliths as occupying burrows with apex

common in the fossil record (Babcock, 1996; Zhang et al., 2006;

oriented downward and only the aperture exposed above the

Collette et al., 2010; Lei et al., 2014). However, the specimen

sediment. There is no evidence for a vertical emplacement of

described herein constitutes one of those exceptional cases in

the hyolithide conch for any of the specimens described herein.

which traces can be reasonably attributed to a trace-maker, in

this instance a hyolithide. This adds signiﬁcant detail to our

340 H.J. Sun et al. / Palaeoworld 27 (2018) 334–342

Fig. 5. Size distribution of hyolithides preserved on the specimens SK 90001 and NIGPAS 166947 from the Chengjiang Biota and KW-8-6 from the Balang Fauna.

5.2. Feeding strategy of hyolithides and their role in the occurrences (Hou et al., 1999; Chen, 2004; Vannier and Chen,

ecosystem 2005; Simões and Acenolaza,˜ 2009; Hu et al., 2013), which sug-

gests that many hyolithide species had high reproductive rates.

Hyolithides rooted in lophophorates are constrained as Ontogenetic change of feeding strategy of hyolithides acceler-

suspension feeders by Moysiuk et al. (2017). However, the ated the juvenile maturation process and assisted with group

gut-content in a juvenile individual recovered from the Balang survival under pressure from predation and famine.

Fauna (Figs. 3I–O, 5) indicates a scavenging strategy. The The tentacles of hyolithides (Moysiuk et al., 2017) are not

hyolithide ‘A.’ ventricosus preserved within the coprolite from restricted to function as suspension feeding apparatus from our

the Chengjiang Biota represents a fecal decomposing strategy evidence; rather, they are generalized feeding organs adapted to

and possibly represents a later span of ontogenetic stages, owing a variety of feeding strategies (Martí Mus, 2016) as mentioned

to the absence of conchs smaller than 2 mm (Fig. 5). Previ- above. The hyolithides transformed particulate food (protista,

ous reports of conch diameters of ‘A.’ ventricosus from the fungi, carrion, feces and possible algae, etc.) from the water col-

Chengjiang Lagerstätte usually range from 4.5 to 7 mm (Hou umn, sediment-water interface, or animal corpses into biomass.

et al., 1999; Luo et al., 1999; Chen, 2004). The forgoing discus- Then they in turn became available as food for Ottoia, Sidneyia

sion tends to favour the changes in feeding strategy associated and other predators (Conway Morris and Whittington, 1985;

with the ontogeny depending on the species of hyolithides. Vannier and Chen, 2005; Vannier, 2012). Through this detrital

The simple sediment-free U-shaped or tubular gut indicates pathway (Moore et al., 2004), particle-based energy was brought

that it was more effective for the animal to digest highly organic- into the community and ecosystem, which might further affect

rich material or small food grains (main ways: suspension the evolution of the digestive system and feeding modes within

feeding or scavenging) during the early ontogeny, but with the the system (Vannier, 2012). Furthermore, hyolithides feeding on

increase in gut volume, hyolithides would have been able to feces or corpses of other animals would have reduced the organic

digest nutrition-poor particles and yet satisfy their nutritional carbon accumulation and oxygen consumption, thereby poten-

requirements by increased volume of ingested food in their tially affecting the carbon and oxygen cycles in their ecosystems.

long alimentary tract. Under this framework, on the one hand, The feeding strategy of hyolithides highlights an essential func-

individuals at different ontogenetic stages having distinct feed- tion in the ﬂow of energy within the Cambrian marine ecosystem

ing habits can reduce the intra-population competition on food and added to its trophic complexity. This demonstrates the simi-

sources; on the other hand, selectivity of certain food sources larity of trophic organization within ecosystems of the Cambrian

for juveniles can efﬁciently absorb and take in nutrition to grow and those of the Recent (Moore et al., 2004; Dunne et al., 2008;

more rapidly. Hyoliths were one of the main prey items of Cam- Vannier, 2012). This observation also brings new thoughts on

brian predators (Conway Morris and Whittington, 1985; Vannier the feeding strategy, food sources, and feeding mechanism of

and Chen, 2005; Vannier, 2012). If hyoliths used any type of early lophophorates.

chemical strategies to resist predation, we have no direct or indi-

rect evidence of it so far. Although hard skeletons can serve as Acknowledgements

predation-resistant devices, the mobility and agility of hyoliths

were very limited. A good strategy for the survival of this group

We acknowledge Prof. Jun-Yuan Chen for assistance and

and its response to predation would have been a high reproduc-

access to the specimens of the Chengjiang Biota. Dr. John

tive rate and rapid maturation. Such a predation-defense strategy

Malinky is thanked for his helpful suggestions and revisions.

has also been suggested for trilobites (Babcock, 2003). A great

This manuscript also beneﬁted from constructive reviews from

number of monospeciﬁc hyolithides are known from abundant

Dr. Martin Valent. This research was supported partly by grants

H.J. Sun et al. / Palaeoworld 27 (2018) 334–342 341

from the Strategic Priority Research Program (B) of the Chinese Galle, A., Parsley, R.L., 2005. Epibiont relationships on hyolithids demonstrated

by Ordovician trepostomes (Bryozoa) and Devonian tabulates (Anthozoa).

Academy of Sciences (XDB18000000); the National Natural

Bulletin of Geosciences 80, 125–138.

Science Foundation of China (41602002, 41472012, 41672005);

Galle, A., Plusquellec, Y., 2002. Systematics, morphology, and paleobiogeogra-

and the Key Laboratory of Economic Stratigraphy and Palaeo-

phy of Lower Devonian tabulate coral epibionts: Hyostragulidae fam. nov.

geography, Nanjing Institute of Geology and Palaeontology, on hyolithids. Coral Research Bulletin 7, 53–64.

Chinese Academy of Sciences (2016KF08). Horny,´ R.J., 1998. Lower Ordovician Nephrotheca sarkaensis (Orthothecida,

Hyolitha) with fossilized intestinal contents in situ (Sárka Formation,

Bohemia). Journal of the National Museum (Prague) Natural History Series

167, 95–98.

Hou, X.G., Bergström, J., Wang, H.F., Feng, X.H., Chen, A.L., 1999. The

References Chengjiang Fauna — Exceptionally Well-Preserved Animals from 530 Mil-

lion Years Ago. Yunnan Science and Technology Press, Kunming, 257 pp.

Babcock, L.E., 1996. Phylum Arthropoda, Class Trilobita. In: Feldmann, R.M., Hu, S.X., 2005. Taphonomy and palaeoecology of the Early Cambrian

Hackathorn, M. (Eds.), Fossils of Ohio. Ohio Division of Geological Survey Chengjiang Biota from eastern Yunnan, China. Berliner Palaobiologische

Bulletin 70, pp. 90–113. Abhandlungen 7, 182–185.

Babcock, L.E., 2003. Trilobites in Paleozoic predator-prey systems, and their Hu, S.X., Zhu, M.Y., Luo, H.L., Steiner, M., Zhao, F.C., Li, G.X., Liu, Q.,

role in reorganization of early Paleozoic ecosystems. In: Kelley, P.H., Zhang, Z.F., 2013. The Guanshan Biota. Yunnan Science and Technology

Kowalewski, M., Hansen, T.A. (Eds.), Predator–prey Interactions in the Press, Kunming, 204 pp.

Fossil Record. Kluwer Academic/Plenum Press, New York, pp. 55–92. Kruse, P.D., 1997. Hyolith guts in the Cambrian of northern Australia — turning

Babcock, L.E., Peel, J.S., 2007. Palaeobiology, taphonomy and stratigraphic sig- hyolithomorphs upside down. Lethaia 29, 213–217.

niﬁcance of the trilobite Buenellus from the Sirius Passet Biota, Cambrian Lei, Q.P., Han, J., Ou, Q., Wan, X.Q., 2014. Sedentary habits of anthozoa-like

of North Greenland. Memoirs of the Association of Australasian Palaeon- animals in the Chengjiang Lagerstätte: Adaptive strategies for Phanerozoic-

tologists 34, 401–418. style soft substrates. Gondwana Research 25, 966–974.

Babcock, L.E., Robison, R.A., 1988. Taxonomy and paleobiology of some Mid- Lin, J.P., Zhao, Y.L., Rahman, I.A., Xiao, S.H., Wang, Y., 2010. Bioturbation

dle Cambrian Scenella (Cnidaria) and hyolithids (Mollusca) from western in Burgess Shale-type Lagerstätten — Case study of trace fossil–body fos-

North America. The University of Kansas Paleontological Contributions: sil association from the Kaili Biota (Cambrian Series 3), Guizhou, China.

Paper 121, 1–22. Palaeogeography, Palaeoclimatology, Palaeoecology 292, 245–256.

Botting, J.P., Muir, L.A., Jordan, N., Upton, C., 2015. An Ordovician variation Luo, H.L., Hu, S.X., Chen, L.Z., Zhang, S.S., Tao, Y.H., 1999. Early Cam-

on Burgess Shale-type biotas. Scientiﬁc Reports 5, 9947. brian Chengjiang Fauna from Kunming Region, China. Yunnan Science and

Butterﬁeld, N.J., 2001. Cambrian food webs. In: Briggs, D.E.G., Crowther, P.R. Technology Press, Kunming, 189 pp.

(Eds.), Palaeobiology II. Blackwell Science, Oxford, pp. 40–43. Mángano, M.G., 2011. Trace-fossil assemblages in a Burgess Shale-type deposit

Butterﬁeld, N.J., 2003. Exceptional fossil preservation and the Cambrian Explo- from the Stephen Formation at Stanley Glacier, Canadian Rocky Mountains:

sion. Integrative and Comparative Biology 43, 166–177. unraveling ecologic and evolutionary controls. In: Johnston, P.A., Johnston,

Chen, J.Y., 2004. The Dawn of Animal World. Jiangsu Science and Technology K.J. (Eds.), Proceedings of the International Conference on the Cambrian

Press, Nanjing, 366 pp. Explosion. Palaeontographica Canadiana 31, 89–107.

Chen, J.Y., Li, C.W., 1997. Biology of the Chengjiang fauna. Bulletin of the Malinky, J., 1990. Solenotheca, new hyolitha (Mollusca) from the Ordovician of

National Museum of Natural Science 10, 11–106. North America. Proceedings of the Biological Society of Washington 103,

Chen, J.Y., Zhou, G.Q., Zhu, M.Y., Yeh, K.Y., 1996. The Chengjiang Biota: A 265–278.

Unique Window of the Cambrian Explosion. National Museum of Natural Malinky, J.M., 2003. Ordovician and Silurian hyoliths and gastropods reassigned

Science, Taichung, 222 pp. from the Hyolitha from the Girvan district, Scotland. Journal of Paleontology

Collette, J.H., Hagadorn, J.W., Lacelle, M.A., 2010. Dead in their tracks — 77, 625–645.

Cambrian arthropods and their traces from intertidal sandstones of Quebec Malinky, J.M., 2006. Revision of Hyolitha from the Ordovician of Estonia.

and Wisconsin. Palaios 25, 475–486. Palﬁontologische Zeitschrift 80, 88–106.

Conway Morris, S., Peel, J.S., 2010. New palaeoscolecidan worms from the Mao, J.R., Zhao, Y.L., Yu, P., Qian, Y., 1992. Some middle Cambrian hyolithids

Lower Cambrian: Sirius Passet, Latham Shale and Kinzers Shale. Acta from Taijiang, Guizhou. Acta Micropalaeontologica Sinica 9, 257–265.

Palaeontologica Polonica 55, 141–156. Marek, L., Galle, A., 1976. The tabulate coral Hyostragulurn, an epizoan with

Conway Morris, S., Whittington, H.B., 1985. Fossils of the Burgess Shale: bearing on hyolithid ecology and systematics. Lethaia 9, 51–64.

A National Treasure in Yoho National Park, British Columbia. Geological Marek, L., Yochelson, E.L., 1976. Aspects of the biology of Hyolitha (Mollusca).

Survey of Canada, Ottawa, 31 pp. Lethaia 9, 65–82.

Devaere, L., Clausen, S., Alvaro, J.J., Peel, J.S., Vachard, D., 2014. Terreneu- Marek, L., Parsley, R.L., Galle, A., 1997. Functional morphology of hyolithids

vian orthothecid (Hyolitha) digestive tracts from northern Montagne Noire, based on ﬂume studies. Vestníkˇ Ceského Geologického Ústavu 72, 351–358.

France; taphonomic, ontogenetic and phylogenetic implications. PLoS One Martí Mus, M., 2016. A hyolithid with preserved soft parts from the Ordovician

9, e88583. Fezouata Konservat-Lagerstätte of Morocco. Palaeogeography, Palaeocli-

Dunne, J.A., Williams, R.J., Martinez, N.D., Wood, R.A., Erwin, D.H., 2008. matology, Palaeoecology 460, 122–129.

Compilation and network analyses of Cambrian food webs. PLoS Biology Martí Mus, M., Bergström, J., 2005. The morphology of hyolithids and its

6, 0693–0708. functional implications. Palaeontology 48, 1139–1167.

Dzik, J., 1980. Ontogeny of Bactrotheca and related hyoliths. Geologiska Mikulás,ˇ R., Fatka, O., Szabad, M., 2012. Paleoecologic implications of ichno-

Föreningen i Stockholm Förhandlingar 102, 223–233. fossils associated with slightly skeletonized body fossils, middle Cambrian

English, A.M., Babcock, L.E., 2010. Census of the Indian Springs Lagerstätte, of the Barrandian area, Czech Republic. Ichnos 19, 199–210.

Poleta Formation (Cambrian), western Nevada, USA. Palaeogeography, Moore, J.C., Berlow, E.L., Coleman, D.C., Ruiter, P.C., Dong, Q., Hastings,

Palaeoclimatology, Palaeoecology 295, 236–244. A., Johnson, N.C., McCann, K.S., Melville, K., Morin, P.J., 2004. Detritus,

Fatka, O., Kozák, V., 2014. A new type of entombment of Peronopsis (Agnos- trophic dynamics and biodiversity. Ecology Letters 7, 584–600.

tida) in a hyolithid conch. Carnets de Géologie [Notebooks on Geology] 14, Moysiuk, J., Smith, M.R., Caron, J.-B., 2017. Hyoliths are Palaeozoic

191–198. lophophorates. Nature 541, 394–397.

Fisher, D.W., 1962. Small conoidal shells of uncertain afﬁnities. In: Moore, R.C. Peel, J.S., 2010. Articulated hyoliths and other fossils from the Sirius Passet

(Ed.), Treatise on Invertebrate Paleontology. Miscellanea. Geological Soci- Lagerstätte (early Cambrian) of North Greenland. Bulletin of Geosciences

ety of America and University of Kansas Press, Lawrence, pp. W98–W143. 85, 385–394.

342 H.J. Sun et al. / Palaeoworld 27 (2018) 334–342

Peng, J., Zhao, Y., Wu, Y., Yuan, J., Tai, T., 2005. The Balang Fauna — a new Wang, Y., Lin, J.P., Zhao, Y.L., Orr, P.J., 2009. Palaeoecology of the trace fossil

early Cambrian Fauna from Kaili City, Guizhou Province. Chinese Science Gordia and its interaction with nonmineralizing taxa from the early Middle

Bulletin 50, 1159–1162. Cambrian Kaili Biota, Guizhou Province, South China. Palaeogeography,

Pojeta, J., 1987. Phylum Hyolitha. In: Boardman, R.S., Cheetham, A.H., Rowell, Palaeoclimatology, Palaeoecology 277, 141–148.

A.J. (Eds.), Fossil Invertebrates. Blackwell, Palo Alto, pp. 416–444. Yan, Q.J., Peng, J., Zhao, Y.L., Wen, R.Q., Sun, H.J., 2014. Restudy of sedimen-

Runnegar, B., Pojeta, J., Morris, N.J., Taylor, J.D., Taylor, M.E., McClung, G., tary and biostratigraphy of the Qiandongian (Cambrian) Balang Formation

1975. Biology of the Hyolitha. Lethaia 8, 181–191. at Jianhe, Guizhou, China — example for the Jiaobang Section of the Balang

Simões, M.G., Acenolaza,˜ G.F., 2009. Hyolith-dominated shell beds from the Formation. Geological Review 60, 893–902.

Lampazar Formation in NW Argentina: patterns and processes of origin in Zhang, X.G., Hou, X.G., Bergström, J., 2006. Early Cambrian priapulid worms

the Late Cambrian (Furongian) seas of western Gondwana. Memoirs of the buried with their lined burrows. Geological Magazine 143, 743–748.

Association of Australasian Palaeontologists 37, 453–462. Zhang, X.G., Bergström, J., Bromley, R.G., Hou, X.G., 2007. Diminutive trace

Steiner, M., Zhu, M.Y., Weber, B., Geyer, G., 2001. The Lower Cambrian of East fossils in the Chengjiang Lagerstätte. Terra Nova 19, 407–412.

Yunnan: trilobite-based biostratigraphy and related faunas. In: Zhu, M.Y., Zhao, F.C., Zhu, M.Y., Hu, S.X., 2010. Community structure and composi-

Van Iten, H., Peng, S.C., Li, G.X. (Eds.), The Cambrian of South China. tion of the Cambrian Chengjiang biota. Science China Earth Sciences 53,

Acta Palaeontologica Sinica 40, pp. 4–39. 1784–1799.

Sun, H.J., Babcock, L.E., Peng, J., Zhao, Y.L., 2015. Hyolithids and associated Zhao, F.C., Hu, S.X., Caron, J.-B., Zhu, M.Y., Yin, Z.J., Lu, M., 2012. Spatial

trace fossils from the Balang Formation (Cambrian Stage 4), Guizhou, China. variation in the diversity and composition of the Lower Cambrian (Series 2,

Palaeoworld 24, 55–60. Stage 3) Chengjiang biota, Southwest China. Palaeogeography, Palaeocli-

Sun, H.J., Babcock, L.E., Peng, J., Zhao, Y.L., 2016. Three-dimensionally pre- matology, Palaeoecology 346, 54–65.

served digestive systems of two Cambrian hyolithides (Hyolitha). Bulletin Zhao, F.C., Caron, J.-B., Bottjer, D.J., Hu, S.X., Yin, Z.J., Zhu, M.Y., 2014.

of Geosciences 91, 51–56. Diversity and species abundance patterns of the early Cambrian (Series 2,

Sun, H.J., Babcock, L.E., Peng, J., Kastigar, J.M., 2017. Systematics and palaeo- Stage 3) Chengjiang Biota from China. Paleobiology 40, 50–69.

biology of some Cambrian hyoliths from Guizhou, China, and Nevada, USA. Zhu, M.Y., Zhang, J.M., Li, G.X., 2001. Sedimentary environments of the Early

Alcheringa 41, 79–100. Cambrian Chengjiang Biota: sedimentology of the Yu’anshan Formation in

Sysoyev, V.A., 1959. Ekologiya khiolitov. Doklady Akademiya Nauk SSSR 127, Chengjiang County, eastern Yunnan. In: Zhu, M.Y., Van Iten, H., Peng, S.C.,

892–895 (in Russian). Li, G.X. (Eds.), The Cambrian of South China. Acta Palaeontologica Sinica

Vannier, J., 2012. Gut contents as direct indicators for trophic relationships in 40, pp. 80–105.

the Cambrian marine ecosystem. PLoS One 7, e52200. Zhu, X.J., Peng, S.C., Zamora, S., Lefebvre, B., Chen, G.Y., 2016. Furongian

Vannier, J., Chen, J.Y., 2005. Early Cambrian food chain: new evidence from (upper Cambrian) Guole Konservat-Lagerstätte from South China. Acta

fossil aggregates in the Maotianshan Shale Biota, SW China. Palaios 20, Geologica Sinica (English Edition) 90, 30–37. 3–26.