Pelagic or benthic?
Mode of life of the remopleuridid trilobite
Hypodicranotus striatulus
YUTA SHIINO, OSAMU KUWAZURU, YUTARO SUZUKI, SATOSHI ONO & CHIHIRO MASUDA

The mode of life of the remopleuridid trilobite Hypodicranotus striatulus Walcott (1875) was examined hydrodynamically with a special focus on the relationship between the autecological performances of swimming and feeding. To understand the effect of swimming height from the sea bottom on the hydrodynamic performance of the exoskeleton, we
performed computational fluid dynamics simulations on four models at differing distances from the sea bottom. The results indicated that Hypodicranotus could launch itself from the sea bottom with a relatively strong hydrodynamic lift
force from slow walking or swimming speeds. However, the lift force decreased as the swimming height increased atslow swimming speeds. Hence, Hypodicranotus would have had to increase its swimming speed to greater than 0.2 m/s
and to obtain the most stable lift force at a swimming height equal to half of its own body height. Its exoskeletal morphology, with a forked hypostome, enabled it to launch itself at a slow velocity and swim at a modest distance, i.e., close to its
own height, from the sea bottom. Feeding from the median vortex flows along the food groove between the two prongsof the hypostome may have been the best strategy near the sea bottom, where a large amount of food matter would havebeen available. Because arthropod musculature consists of striated muscles, which exhibit inferior endurance,
Hypodicranotus most likely adapted to the near-bottom environment, where it could rest at times on the sea bottom aspart of a nektobenthic mode of life. • Key words: biomechanics, ecomorphology, evolution, hybrid, multi-functionality,
Remopleurididae, Trilobita.
SHIINO, Y., KUWAZURU, O., SUZUKI, Y., ONO, S. & MASUDA, C. 2014. Pelagic or benthic? Mode of life of theremopleuridid trilobite Hypodicranotus striatulus. Bulletin of Geosciences 89(2), 207–218 (5 figures). Czech Geological Survey, Prague. ISSN 1214-1119. Manuscript received January 28, 2013; accepted in revised form November 15,
2013; published online March 11, 2014; issued May 19, 2014.
Yuta Shiino (corresponding author), The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo, Tokyo
113-0033, Japan; y-shiino@um.u-tokyo.ac.jp • Osamu Kuwazuru, Department of Nuclear Power and Energy Safety,
University of Fukui, 3-9-1 Bunkyo, Fukui-shi, Fukui 910-8507, Japan; kuwa@u-fukui.ac.jp • Yutaro Suzuki, Institute of
Geosciences, Shizuoka University, 836 Ohya, Suruga, Shizuoka, 422-8529, Japan; sysuzuk@ipc.shizuoka.ac.jp •Satoshi Ono, Department of Geosciences, Shizuoka University, 836 Ohya, Suruga, Shizuoka, 422-8529, Japan;
r0934002@ipc.shizuoka.ac.jp • Chihiro Masuda, Department of Geosciences, Shizuoka University, 836 Ohya, Suruga,
Shizuoka, 422-8529, Japan; r0234009@ipc.shizuoka.ac.jp

Because evolution has enabled animal lineages to explore arange of adaptive strategies, understanding the autecology
of fossil organisms is necessary to provide insights into
their particular adaptations and how these have evolved.
Swimming trilobites are appropriate candidates for thistype of study because the acquisition of swimming ability
from a benthic lifestyle is a significant autecological innovation (Fortey 1985, 2004). A few decades of research
have demonstrated that “planktonic trilobites” commonly
share certain morphological characteristics, such as adwarfed body size and high spinosity (e.g., Fortey 1985,
2004; Clarkson & Ahlberg 2003; Schoenemann et al. 2008,2010), which are consistent with those of modern planktonic arthropods (e.g., Marshall & Diebel 1995, Land 2000).
DOI 10.3140/bull.geosci.1409

This analogy between extinct and modern taxa facilitates
predictions about the mode of life of these propulsioninefficient swimming trilobites. However, the autecological characteristics of propulsion-efficient swimming trilobites remain enigmatic, particularly those of the remopleuridid trilobites. Even the generalised life mode of theseanimals has been classified into contrasting categories, as
either benthic or pelagic (e.g., Whittington 1952,
Bergström 1973, Fortey 1985, Amati et al. 2009). To resolve this question, it is necessary to provide a consistent
explanation for the inter-related traits of swimming capability, habitat and the corresponding biological performancemeasures within the framework of the animal body plan.
The remopleuridid trilobite Hypodicranotus striatulus
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D

A

B

C

Figure 1. Morphology of Hypodicranotus striatulus. • A, B – dorsal and antero-lateral views of Hypodicranotus striatulus (MCZ-115910).
• C – hypostome (MCZ-100987). • D – dorsal view of a left-half broken specimen (MCZ 100988) with the hypostome partially exposed on the left side.

Walcott (1875) was a propulsion-efficient swimming animal with a hydrodynamically sophisticated morphology in
the Ordovician sea (Fig. 1, Shiino et al. 2012). Its
exoskeletal form was highly streamlined to avoid flow
detachment, and the long, bilaterally pronged hypostome
reduced viscous drag while maintaining a modest lift force
over a wide range of swimming speeds (Shiino et al. 2012).
In addition to this hydrodynamic morphology, Hypodicranotus exhibited notable adaptations for feeding whileswimming, using the flow of water through its food groove
to consume tiny, suspended organic particles (Fig. 2,
Shiino et al. 2012). Water flows during swimming also
contributed to the respiratory ventilation of the animal(Fig. 2, Shiino et al. 2012). The occurrence of Hypodicranotus fossils in a variety of sedimentary facies andtheir inter-provincial palaeobiogeography has been interpreted to indicate a pelagic swimmer (Brett et al. 1999,
Amati et al. 2009). In contrast, the food source utilised inthis feeding style might limit adaptation to a specific environment. Therefore, it is necessary to determine how habitat differences would affect the balance of feeding, respiration and swimming behaviour that the organism needed inorder to prosper.
The aim of this study was to examine the swimming
performance of an exoskeletal model with respect to its
swimming speed and height above the sea bottom. Computational fluid dynamics (CFD) simulations were performed
to determine where the animal would have obtained themost efficient drag and lift forces. Based on the simulation
results, we discuss the mode of life of Hypodicranotus witha special focus on the relationship between swimming capability and integrated aspects of biological performance.

Materials and methods
The CFD simulation methods used here have been fully
described in previous reports by our group (Shiino et al.
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2009, 2012; Shiino & Kuwazuru 2010, 2011a, b). The methodology is briefly described below.

Fossil specimens
A complete, articulated dorsal exoskeleton and a hypostome of the Ordovician remopleuridid trilobite Hypodicranotus striatulus Walcott (1875) from the Trenton
Group, New York, United States of America, were used forthe simulation (Fig. 1A–C). These specimens are housed in
the Museum of Comparative Zoology at Harvard University (MCZ-100987, MCZ-115910). The dorsal exoskeletal
specimen is 25.5 mm long and 17.0 mm wide, and the hypostome is 17 mm long and 7.6 mm wide. Additionally, an
exoskeletal model with a hypostome was reconstructed based on specimen MCZ 100988 (Fig. 1D).

Computational fluid dynamics (CFD)
simulations
Water flows around the exoskeleton with the hypostome
attached in its original position were simulated by solving
the incompressible Navier-Stokes (NS) equations for unsteady viscous fluids. The simulation was performed
using the commercial computational fluid dynamics code
SCRYU/Tetra 9.0 (Software Cradle Co., Ltd., Tokyo, Japan), which employs the finite-volume method (e.g., Adkins & Yan 2006, Shiino et al. 2009). To implement a
three-dimensional model of Hypodicranotus for analysis
in the CFD simulation, we constructed a polycarbonate
exoskeletal replica using the vacuum-forming method(Shiino et al. 2009, Shiino 2010) and obtained sequential
cross-sectional images of the replica using an
SMX-225CT microfocus X-ray CT system (Shimadzu
Corporation, Tokyo, Japan). Subsequently, the volumetric data were translated into surface morphological data inYuta Shiino et al.  Pelagic or benthic? Mode of life of Hypodicranotus

A

B

C

D

Figure 2. Flows around the hypostome-bearing model. • A – flow vectors in median cross sectional view. • B – flow vectors around the median crosssection in antero-lateral view. • C – vector representations of flows on the internal surface. The hypostome is shown as a transparency. • D – schematic illustration of ambient and secondary flows. Swimming provides biological benefits in the form of feeding using the food groove and respiration using thecounter-currents along the inferred trilobite gills (after Shiino et al. 2012).

the Standard Triangulation Language (STL file type)using the image-processing function of the image-based
structural analysis software VOXELCON 2005 (Quint
Corporation, Japan). The STL file was transferred into
SCRYU/Tetra, and finite-volume meshes of tetrahedral
elements were generated automatically (Shiino et al.
2009).
The Reynolds-averaging method can be used to decompose the pressure and velocity in the NS equations into atime average and a fluctuation component, resulting in the
Reynolds-averaged Navier-Stokes (RANS) equations(e.g., Bertram 2000). Along with the RANS equations, weemployed an improved k-å turbulence model based on the
turbulent kinetic energy k and its dissipation rate å, which is
known as the AKN model (Abe et al. 1992, 1995). The
AKN model is applicable to consider near-wall eddy viscosity in flow fields with a low Reynolds number (Abe etal. 1992, 1995); thus, it is suitable to simulate flows around
our Hypodicranotus model (Shiino et al. 2012). The total

simulation time was set at 15 seconds because the fluid
structure reached a stable condition with or without vortex
fluctuations, similar to a Karman vortex, within this time
period. We used a constant time step of 0.003 seconds toobtain a reasonable computation time. Our preliminary
analyses confirmed the accuracy of simulations using theseparameters (Shiino et al. 2012).
To examine the hydrodynamic properties of the exoskeleton at different distances from the sea bottom, we
adopted an analysis domain consisting of a cuboid spacethat extended a distance of 10 times the model length in thedownstream direction; 5 times the model width and heightin the lateral and upward directions, respectively; and 3
times the model length in the upstream direction (Fig. 3).
The distance between the model and the bottom of thespace was set at 0.2, 0.5 and 1.0 times the model height(L3; 8.1 mm) (Fig. 3). To evaluate the effect of flow velocity (i.e., coasting speed) on the hydrodynamic properties ofthe exoskeleton, we simulated 11 different uniform inlet
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Figure 3. Schematic illustrations of the analysis domain for the computational fluid dynamics simulation showing the distances from the bottom examined in this study.

velocities, ranging from 0.01 to 0.5 m/s (corresponding toReynolds numbers of 270 to 13500, where the body lengthof 25.5 mm was adopted as a representative length). The
outlet pressure was fixed to zero. The boundary conditionof the bottom was set as a moving wall whose direction andspeed were concordant with the inlet flow (Fig. 3). Allother parameters of the CFD simulation matched thoseused in our previous studies (Shiino et al. 2009, 2012;
Shiino & Kuwazuru 2010, 2011a, b).

Evaluation of the bottom effect
To qualitatively examine the bottom effect on the swimming capability of Hypodicranotus, we calculated the dragand lift forces as functions of the distance from the bottom.
Propulsion-efficient swimming organisms, including Hypodicranotus, reduce their drag forces to swim easily andto obtain a modest lift force to stabilise the body horizontally (Shiino et al. 2012). To compare the hydrodynamic
effects of different distances from the sea bottom at different coasting speeds, we normalised the drag and lift forcesby the drag predicted from the nominal hydrodynamic
pressure. We refer to the resulting normalised drag coefficient as Cd and the lift coefficient as Cl. The coefficientswere calculated as Cd = 2Fd / ñ vex2S and Cl = 2Fl / ñ vex2S,
where Fd is the drag force, Fl is the lift force, ñ is the massdensity of the fluid, vex is the inlet velocity and S is the projected frontal area of the model (Vogel 1994). The projected frontal area of the hypostome-bearing model was
85.47 mm2, as estimated using the SCRYU/Tetra postprocessing function.
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Results
Drag and lift forces and coefficients
The drag and lift forces and the corresponding coefficientsfor all simulated cases are shown in Fig. 4. The drag force
increased as the coasting speed increased (Fig. 4A), whereas its coefficient decreased monotonically (Fig. 4B). The
drag forces and coefficients were similar regardless of theswimming height, except at the shortest distance from thebottom (Fig. 4A, B: 0.2L3). The pattern of drag forces andcoefficients suggests that efficient swimming could beachieved at all the heights except the lowest level (0.2L3).
By lifting its body away from the bottom, the animal could
quickly decrease its drag and obtain suitable swimming
conditions.
The lift forces and coefficients differed dramaticallywith respect to the distance from the bottom (Fig. 4C, D).
The lift force increased as the coasting speed increased(Fig. 4C), whereas its coefficient decreased (Fig. 4D). At acoasting speed of 0.15 m/s, the lift force and coefficient increased as the body approached the bottom, suggesting ahighly efficient launching ability in the initial stage ofswimming near the bottom. At coasting speeds greater than
0.2 m/s, the simulated results always showed stable lift
coefficients, indicating that the lift force could be readily
controlled by altering the swimming speed. The lift force
and coefficient were maximised near the swimming heightof 0.5L3. Thus, the bottom effect is expected to produce
higher lift forces at higher velocities (Fig. 4C, D). At velocities near 0.1 m/s, the variation in the lift coefficient wassmooth at the swimming height closest to the bottom

Yuta Shiino et al.  Pelagic or benthic? Mode of life of Hypodicranotus

A

C

B

D

Figure 4. Drag and lift forces and coefficients at different velocities and distances from the bottom. The results for the hypostome-bearing model withno bottom effect (open circles) are from Shiino et al. (2012). • A – drag forces. • B – drag coefficients. • C – lift forces. • D – lift coefficients.

(0.2L3) but not at swimming heights farther from the bottom (0.5L3, 1.0L3) because the flow behind the body fluctuated due to turbulence. In other words, the flow changes
from laminar to turbulent at this velocity. However, this effect strongly depends on the angle of the tail, which wasmodelled after the subject fossil.
The evidence presented here indicates that at the sea
bottom, the drag force is relatively high, but the lift force isalso high. Near the sea bottom, the drag force quickly declines to the magnitude it would exhibit without a bottom
effect, and the lift force becomes stable at relatively highvelocities. At lower coasting speeds (less than 0.15 m/s),
the pressure beneath the model increased because flows
tended to be stagnant, decreasing in velocities. This flow

condition can provide higher lift coefficients near the sea
bottom. At higher coasting speeds (more than 0.2 m/s),
smooth flows beneath the model resulted in higher velocities, which created lower lift coefficients (Fig. 4D). A significant reduction of fluid pressure would be expected at
the swimming height closest to the bottom (0.2L3) due toflows through the constricted space responding to the Venturi effect and therefore causing the lift coefficient to drastically decrease as the coasting speed increases (Fig. 4D).
A swimming height of 0.5L3 provides the maximum efficiency needed to obtain lift force. At higher levels, the lift
force also decreases and approaches the magnitude it
would exhibit without a bottom effect (Fig. 4: open circles
in each plot).
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Discussion
Launching to swimming
The results presented above clearly show that Hypodicranotus could swim most effectively, with lower drag andhigher lift, at close distances from the bottom but not in theupper water column. Because Hypodicranotus can be regarded as a nektobenthic swimmer in terms of its hydrodynamic properties, it is necessary to explain the effect when
they launched from the sea bottom.
It is generally accepted that moving the metameric appendages could provide a propulsive force for swimming(Bergström 1969, 1973; Whittington 1975). Because trilobite appendages exhibit little specialisation along the body,metachronal movements would result in drag-based propulsion, a so-called serial paddling, which are a typicalmode of appendage movement observed in extant isopods
and horseshoe crabs (Azuma 2006). Serial paddling is theultimate transformation of accelerated level-bottom walking by marine arthropods. Therefore, it is expected that
Hypodicranotus launched from the sea bottom with the aidof a relatively high lift force when walking.
According to Shiino et al. (2012), the presence of soft
tissues may affect the magnitude of drag force to some degree. Taking the hydrodynamic influence of the appendages into consideration, the space between the body and thesea bottom would significantly decrease. In this condition,
the lift force increases at lower coasting speeds by means offlow stagnation, while it decreases at higher coasting
speeds, in comparison with the present simulation model.
The sudden reduction of the lift coefficient at the swimming height closest to the sea bottom (0.2L3) would be further emphasised by the Venturi effect as mentioned above.
Such instability of the lift coefficient near the bottom
seems to be unreasonable for coasting-swimming.
Metamerically arranged and laterally deflected trilobite
appendages facilitate smooth fluid flows under the pleuralfold. This grants Hypodicranotus stability while swimming and a way to lift their body above the sea bottom during resting or walking. Our results suggest Hypodicranotus
could move through a stable and smooth sequence of walking, launching and swimming at a height equal to half of its
own body height (0.5L3).

Fossil evidence
and relevant sedimentary environment
Based on its lack of lithofacies dependency, it has beensuggested that Hypodicranotus was a pelagic swimmer(Amati et al. 2009). The relevant sedimentary environments of Hypodicranotus fossils suggest habitats ranging
from shallow-ramp to slope settings (Amati et al. 2009), in212

dicating that the animal was not particularly adapted to thesedimentary facies and bottom environments (Amati &Westrop 2006, Amati et al. 2009). This evidence was adopted to infer a pelagic life style (Fortey 1985). Many modern
organisms with swimming capability are widely distributed across provinces and habitat depths, unlike sessile benthic organisms. Nevertheless, not all modern swimming organisms are pelagic. Thus, the inference that an organismwith no obvious dependence on the conditions of the sea
bottom must be pelagic may mislead autecological interpretation. For example, the benthic shrimp species Solenocera melantho is distributed at depths of 70 to 400 m in its
shelf to lower-slope habitat (Chan 1998). Although thisspecies is restricted to the Western Pacific, the genus Solenocera exhibits a wider range of depths across its global
distribution (e.g., Kunju 1970, Holthuis 1980). Similarly,
the isopod species Bathynomus doederleinii inhabits
depths of 100 to 686 m in the Western Pacific, and the genus Bathynomus ranges from 70 to 2140 m in depth acrossthe Atlantic, Pacific and Indian Oceans (Schotte et al.
1995). Both of these modern arthropods are regarded asbenthic animals with some degree of swimming ability.
Thus, it is difficult to determine whether motile fossil organisms were pelagic or benthic based solely on their facies
dependency, or lack thereof.
Characteristic wide distribution patterns, regardless of
depth and bottom conditions, might be closely related tothe autecological properties of an organism. For example,
the extant shrimp Solenocera depends on a variety of foodsources, including fish, decapods, foraminifers andmolluscs (Dineshbabu & Manissery 2009). These highlyvariable food sources depend on the benthic environment
to which each species is adapted (Dineshbabu & Manissery2009), resulting in a wide range of habitats and depth distributions for the genus. The isopod Bathynomus, which employs a sit-and-wait foraging strategy, also occupies a wide
range of habitats because it can remain stationary, consuming little energy, until a dead organism such as a fish or awhale falls through the water column nearby (e.g., Johansen & Brattegard 1998, Lowry & Dempsey 2006, Matsui etal. 2011). In general, carnivorous arthropods such as Limulus use endites for grasping and ascending food particles
toward mouth openings. This is achieved mechanically by
repeated adductive motion of adaxial podomeres. In
Hypodicranotus, the long, forked hypostome with its rigid
connection to the cephalic shield would cover the adaxial
podomeres of the appendages. Thus, the use of these appendages for predation would be structurally unreasonable.
Instead, Hypodicranotus may have fed efficiently by capturing suspended particles from the water flowing along its
food groove, as discussed previously (Shiino et al. 2012).
The water flowing along the food groove could transportcomparatively small organic particles. In any facies or sedimentary environment, organic particles are abundant

Yuta Shiino et al.  Pelagic or benthic? Mode of life of Hypodicranotus

around the sediment-water interface (Boucot 1981, Nowell
et al. 1981, Snelgrove 1998). Although Hypodicranotus isa benthic dweller with a strong swimming capability, not apelagic swimmer, a weaker dependence on particular foodresources would enable this animal to occupy a wide range
of depths.
Further explanation is required for the inter-provincial
distribution pattern of Hypodicranotus, which is related tolarval dispersal ability rather than swimming capability
and related biological performances. The morphologicallyand taxonomically related genus Remopleurides has
protaspides of nonadult-like globular forms called
asaphoid protaspides. Unique to this form is the planktonic
protaspid growth stages, and earlier meraspid stages(Chatternton & Speyer 1997). A number of studies haveprecluded a benthic life style on the basis that the larval
body size was less than a millimetre, with three dimensionally extending long spines (e.g., Whittington 1959,
Fortey & Chatterton 1988, Chatterton & Speyer 1997, Park
& Choi 2011). These morphological features fulfil the general requirement for a planktonic life style because it had alarge surface area in relation to its volume (e.g., Ruppert etal. 2003).
With these facts in mind, one may imagine that themorphological characteristics of larval stages have facilitated the inter-provincial distribution pattern of remopleuridids. However, the explanation is not so simple because there still remains the problem of inter-provincial
distribution of Hypodicranotus. The fossil occurrencesof Hypodicranotus are known from North America, theUnited Kingdom, the Ural Mountains of Siberia andKolyma of eastern Russia (Ludvigsen & Chatterton1991). The palaeogeographic position of the Kolyma
Terrain during the Ordovician appears to be the Mediterranean Province, possibly near Laurentia (Zhang &Barnes 2007, Rasmussen & Harper 2011). In contrast to
the case of Hypodicranotus, the genus Remopleurides
likely had a broad distribution (Amati et al. 2009) evenfor supposed propulsion-efficient swimmers. The relationship between swimming capability and distribution
may not be linear and needs to be further examined toreach an appropriate understanding of the remopleuridid
mode of life.

Biological aspects of swimming
With this mechanical interpretation of swimming, the biological traits of trilobites may provide further insight into
their modes of life. The swimming method of serial paddling takes advantage of acceleration at comparatively
slow speeds for short durations (Vogel 1994, Azuma
2006). The cessation of swimming in Hypodicranotus
might have resulted in sinking towards the bottom. There-

fore, the serial paddling observed in arthropods would beincompatible with a pelagic mode of life without morphological adaptation enabling the frictional retardation ofsinking. To explore the pelagic habitat, propulsionefficient swimming animals may acquire lift-based swimming abilities, such as the undulating fins of fish, thatenables them to swim faster and for longer durations (Vogel 1994, Azuma 2006). Alternatively, propulsion-efficient swimming abilities may be lost, as observed in immobile planktonic animals.
The body plan of Hypodicranotus provides further
evidence of its swimming ability. In arthropods, themuscular system consists only of striated muscles (Doritet al. 1991). This type of muscle provides instantaneous
locomotive force but is not effective for endurance(Dorit et al. 1991). Therefore, Hypodicranotus would
need to rest in the water column if it were a pelagic
swimmer. This behaviour appears unlikely due to themorphological features described above. Indeed, planktonic locomotion is efficient for pelagic arthropods.
Slowly moving the appendages through the water may
enable some arthropods to float because their exoskeletons can withstand considerable fluid resistance(e.g., Marshall & Diebel 1995). In addition, exposing theappendages could obtain the effective drag force that
contributes to further enhancement of the floating modeof life. In the case of Hypodicranotus, the long, forked
hypostome covered the venter to reduce the drag force(Shiino et al. 2012), which seems in opposition to this direction of morpho-functional strategy.

Feasible autecologyof Hypodicranotus striatulus
As discussed above, swimming capability and geologicalevidence indicate that Hypodicranotus was a non-pelagic
swimmer. Because this animal may have adapted to the benthic environment through its propulsion-efficient swimming
capability, further explanations of its adaptations to the nektobenthic lifestyle are needed. The feeding strategy of Hypodicranotus (see Fig. 2) would be beneficial in the benthic environment, where a large amount of detritus is available forfeeding (e.g., Shiino et al. 2011). The feeding method resembles that of tadpole shrimp, in which beating the metameric appendages to swim generates flows along the foodgroove, and these secondary flows raise a plume of food materials from the substrate-water interface (Fryer 1988). Thus,
the morphology of Hypodicranotus was adapted to collect
food particles by antero-dorsally directing vortex flows
along the food groove. This process would be most efficientin nektobenthic environments.
In addition to this feeding strategy, the ability to swim
provided a new defensive strategy for trilobites. Through213

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enrolment, some benthic trilobites could entirely encapsulate the non-mineralised parts of their bodies, protecting
them against predatory attack (e.g., Esteve et al. 2010,2011; Feist et al. 2010). We argue that this defensive strategy provided a secondary benefit for trilobites and other arthropods with enrolment or volvation abilities. Predatorsthat use vision to detect potential prey depend on motion-capture perception; thus, they are unlikely to perceive
static, enrolled individuals as potential prey. This defensive strategy is similar to thanatosis (e.g., Nishino & Sakai
1996). Instead of compromising its enrolment ability(Hegna 2010), the swimming ability of Hypodicranotus
provided an active escape mechanism, as observed in modern arthropods (e.g., Jacklyn & Ritz 1986). Given the advantages of swimming for feeding and respiration, otheraspects of biological performance, including escape behaviour, were functionally integrated with the propulsion-efficient swimming system of Hypodicranotus within its trilobite body plan.
In summary, our simulations revealed that Hypodicranotus could obtain a large and stable lift force for effortless swimming near the sea bottom. Instead of enhancing
swimming performance, the swimming movement of
Hypodicranotus would generate postero-anteriorly directed vortex flows beneath the ventral side of the dorsal
tergites, which would initially appear to be disadvantageous (Shiino et al. 2012). Importantly, however, the animal could divert these hydrodynamic handicaps for feeding and respiration (Suzuki & Bergström 2008, Shiino etal. 2012), thus functionally integrating the swimming,
feeding and respiratory systems as well as protection(Fig. 5). Its weak dependence on specific food resources
enabled this species to occupy a broad range of habitats despite its nektobenthic mode of life.

Propulsion-inefficiency or -efficiency
in trilobite swimming
Because swimming behaviour is heavily influenced by surrounding viscous fluids, morphological characteristics greatly influence swimming capability and mode of life.
Swimming trilobites could be subdivided into two broadtypes of exoskeletal morphology. One is the morphology
with proportionally large cephalon against whole exoskeletal body plus spherical eyes as observed in Carolinites,
Opipeuterella, Cyclopyge, Telephina and Symphysops.
This morphological type must be a propulsion-inefficientswimmer because of its great surface friction. The locomotion would be slow, and the swimming speed would be
only several body lengths per second. The locomotion may
immediately stop at the conclusion of beating the appendages, and thus, its seemingly planktonic mode of life. The
other morphological type is likely to be a propulsion214

efficient swimmer because of the streamlined exoskeleton,
allowing the locomotion of coasting or grinding. The number and the size of ommatidia differ greatly from that of
propulsion-inefficient swimmers. Assuming these morphological requirements, remopleuridids such as Amphitryon, Remopleurides and Hypodicranotus are certainly
candidates for propulsion-efficient swimmers.

Future perspectives in understanding
the biophysiological performanceof fossil organisms
Understanding the morphological functions that characterise animal adaptations makes it possible to reconstruct thebiological traits of fossil organisms (e.g., Shiino & Suzuki
2007, 2011; Lerosey-Aubril et al. 2011; Shiino & Kuwazuru 2011a). Because we cannot reliably test or confirm thelifestyles of fossil organisms, it has been suggested thatknowledge about their morphological functions represents
the only source of information in understanding the autecological properties of fossil organisms. However, all animals must be treated as multifunctional entities to ensure
the consistent integration of the various aspects of their
biological performance. As the present study demonstrates, a plausible autecological scenario must explain multiple inter-related performance traits (e.g., Hughes & Chapman 1995, Suzuki et al. 2008, Kaji et al. 2011, Fujiwara &Hutchinson 2012, Matsumura & Yoshizawa 2012).
Earlier misinterpretations of morphological functions
were caused by the lack of reliable quantitative analyses,
which can enhance our understanding of adaptive functional capabilities (Briggs et al. 1991). Trilobite morphotypes have been inferred to represent adaptations to specific lifestyles (Fortey & Owens 1990), and these
inferences provide working hypotheses about the palaeoecological characteristics of these organisms. However,exceptions to the rule of morphological adaptation, especially in swimming trilobites (Fortey 1985, p. 418 in
Hughes 2007), invalidate the one-sided approach tomorphotypic properties.
In the family Remopleurididae, Remopleurides hascomparatively stout genal spines that extend postero-laterally and a long thoracic mid-axial spine on the eighth thoracic segment (e.g., Nikolaisen 1988). These morphological features would retard the sinking rate, as observed inplanktonic animals, and are apparently different than theadaptive features of Hypodicranotus. Although the morphological features of Remopleurides seem to suggest aplanktonic mode of life, their habitat was restricted aroundthe inner shelf, unlike a simple pelagic animal (Hansen etal. 2011). The ball-socket structure of articulation between
thoracic segments in Remopleurides is visibly bloated(Nikolaisen 1988); the excessive development may haveYuta Shiino et al.  Pelagic or benthic? Mode of life of Hypodicranotus

Figure 5. Morpho-functional diagram of Hypodicranotus. The exoskeletal characteristics enhance the swimming ability of the animal, thus generating
vortex flows within the area surrounded by the exoskeleton (see also Shiino et al. 2012). This adaptation converts the apparently disadvantageous formation of vortex flows into a benefit for feeding and respiration, thus constituting a biological system with hybrid functionality. Some functional properties,
indicated by question marks, remain uncertain.

an unknown role other than trilobite volvation. Given themorphological disparity of terrace ridges on the hypostome
between Remopleurides and Hypodicranotus, there is amajor difference in adaptive features between the two. The
unusual swimming trilobite, Hypodicranotus exemplifies
morphological adaptation for efficient swimming performance while maintaining homeostasis.
Considering that animals integrate a variety of biological performance traits within their bodies, othermorphological features with functional roles can be understood in terms of their relevant autecological properties (Fig. 5). During swimming, Hypodicranotus may
depend on its eyes to determine its swimming direction
and speed in response to ambient conditions. Therefore,
the visual system should be adapted to faster swimmingnear the sea bottom because arthropods optimise their
sensory traits in response to relevant adaptive strategies(e.g., Clarkson 1967, 1975; McCormick & Fortey 1999;
Schoenemann et al. 2010; Ono 2011). The strip-like visual surface of the eyes with many thousands of tinylenses arranged in an almost vertical fashion (Whittington 1952) enables it to have lateral and forward view likeother benthic trilobites and to see its surroundings inhigh resolution. This may partially support our hypothesis. Additional morphological characteristics, such as
the pattern of terrace ridges, the form of the genal spines,
the mode of articulation and the prominent thoracic
mid-axial spine located on the eighth thoracic segment,
may also have contributed to the swimming performanceof the animal as well as to its homeostasis. A pair of pits
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on the ventral side of the cephalic doublure may haveplayed a role in an unknown biological system, possibly
related to a specific behaviour. Future biomechanicalanalyses will help to elucidate how the hybrid functionality of the remopleuridid morphology has evolved under genetic and autecological constraints.

Acknowledgements
We are grateful to Jessica Cundiff and Tsuyoshi Takahashi (Harvard University) for a greatly appreciated arrangement to makeplaster figures of fossil specimens. We thank Brigitte Schoenemann (The University of Bonn) and Rudy Lerosey-Aubril(Senckenberg Research Institute) for thorough discussions, critical comments and encouragement at TRILO 2012. We thank Paul
Hille (Utrecht University) for providing information of fossil
specimens. Thanks are also due to two reviewers, Richard Fortey(Natural History Museum) and Nigel Hughes (University of California Riverside). Funding was provided in part by the Kurata
Grants from the Kurata Memorial Hitachi Science and Technology Foundation, and by the JSPS KAKENHI Grant Number
24840018 and 25630047.

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