Coupled exuviae of the Ordovician Ovalocephalus (Pliomeridae, Trilobita) in South China and its behavioral implications

Introduction

The biomineralized or chitinous exoskeleton of arthropods hinders the growth of their bodies; therefore, individuals must shed their old shells many times during growth and development (Moussian, 2013; Daley & Drage, 2016). Trilobites, as an extinct group of arthropods, also needed to shed their shells as they grew (Fortey, 2014). Different trilobites exhibited different molting techniques (Henningsmoen, 1975); most trilobites shed their shells through separating the librigenae from the cranidium (McNamara & Rudkin, 1984; Whittington, 1990), whereas for trilobites with librigenae fused with the cranidium, separation of the cephalon from the thoracopygon usually occurred during molting (Speyer, 1985; Wang & Han, 1997), and some genera had multiple exuvial modes (Brandt, 1993; Budil & Bruthansová, 2005). In addition to ecdysis reflecting the ontogenetic development process of trilobites, some exceptionally preserved trilobite specimens also contain behavioral information. For example, some trilobites shed their shells by hiding in empty shells or burrows of other animals (Davis, Fraaye & Holland, 2001; Chatterton, Collins & Ludvigsen, 2003; Chatterton & Fortey, 2008; Zong, Fan & Gong, 2016), and even molted infaunally (Rustán et al., 2011), reflecting the hiding behavior of trilobites. Some phacopids may also have exhibited asymmetric behaviors during molting (Zong & Gong, 2017). Other trilobites collectively shed their shells, which may have been related to molting–mating behavior (Speyer & Brett, 1985; Speyer, 1990).

South China is an important area for trilobite fossils, and abundant Ordovician trilobites have been collected from Hubei Province (Lu, 1975; Zhou & Zhen, 2008). However, there are few reports on exuvial specimens and correlation research. Only photographs of exuvial specimens were attached to the identification of genera and species in the paleontological literature; these exuvial specimens have not been systematically described, their patterns have not been classified and explained, and the behavioral strategy of these trilobites during molting has not been analyzed (Han & Wang, 2000). Here, I collected many exuviae of Ovalocephalus tetrasulcatus (Phacopida, Pliomeridae) from the Upper Ordovician in central Hubei. Some of the specimens were found with two or three in a line, or preserved partly or even completely overlapping; these patterns are regarded as representing the active behavior of trilobites during molting, and may be related to the herding behavior of some trilobites. They provide new material for understanding exuvial techniques of trilobites, and the behavior of trilobites when molting.

Materials & Methods

All specimens were collected from the Upper Ordovician Linhsiang Formation of the Daozimiao section in Jinshan County, central Hubei (GPS: N 30°59′51.49″, E113°06′26.04″) (Fig. 1). The Linhsiang Formation is widely distributed in the middle Yangtze region, and is mainly composed of yellow-green calcareous mudstones with a few siliceous mudstones in the Daozimiao section, but differs from the nodular muddy limestones of the Linhsiang Formation in the type section in Linxiang, Hunan Province. In the Daozimiao section, the Linhsiang Formation is conformably underlain by the muddy limestones of the Upper Ordovician Pagoda Formation and overlain by the graptolite shales of the Upper Ordovician Wufeng Formation. The 1.5-m-thick calcareous mudstones from the top of the Linhsiang Formation (Fig. 1D) yield an abundant and diverse trilobite fauna, including members of the Metagnostidae, Cyclopygidae, Phillipsinellidae, Encrinuridae, Telephinidae, Raphiophoridae, Cheiruridae, Dionididae, Trinucleidae, Asaphidae, Pliomeridae, and Remopleurididae. In addition, the Foliomena fauna (brachiopods) (Zhan & Jin, 2005), ostracods, echinoderms, machaeridians, and trace fossils are also found in the same horizon. Based on the trilobite assemblage, the age of the top of the Linhsiang Formation is constrained to the middle Katian (early Ashgill) (Zhou, Zhou & Xiang, 2016).

The 1.5-m-thick trilobite-bearing calcareous mudstones are homogeneous, without bedding structures. There are no cross-bedding and graded bedding visible in the longitudinal sections of the rocks, but a small amount of authigenic pyrites is preserved in this interval (Figs. 2A–2D). This evidence suggests the calcareous mudstones formed in a relatively calm and deepwater environment, which is consistent with the results of the characteristics of the brachiopod association found in the same interval (Zhan & Jin, 2005). Ovalocephalus tetrasulcatus (Kielan 1960) is the only pliomerid trilobite in the Linhsiang Formation of Jingshan. Ovalocephalus is largely restricted to peri-Gondwana, but is widely distributed in the Ordovician of China (Zhou, Yuan & Zhou, 2010). In the Linhsiang Formation of Jingshan, most specimens of Ovalocephalus tetrasulcatus are articulated or nearly articulated exoskeletons, as well as enrolled specimens. This pattern suggests that the trilobites were not transported by current before burial, and were buried in situ. Although some biotic burrows can be observed in the calcareous mudstones (Figs. 2E, 2F), no traces of burrows have been found near the trilobites (Figs. 2B, 2C), which rules out the likelihood that trilobites were affected by biotic disturbance before burial or preserved in burrows.

I collected more than 100 specimens containing articulated or nearly articulated exoskeletons from the calcareous mudstones at the top of the Linhsiang Formation of Jingshan, including 13 specimens that showed two exoskeletons end to end or overlapping one another, and three specimens that show three exoskeletons end to end or two of them overlapping one another, which obviously differed from isolated single exoskeletons preserved in the same interval. The fossils in Fig. 3 were whitened with magnesium oxide powder, and all photographs were captured using a Nikon D5100 camera with a Micro-Nikkor 55 mm F3.5 lens. The axial azimuth measurements of the trilobites and the rose chart were completed in CorelDRAW X7.

Results

In the present work, complete exoskeletons include all specimens with articulated cephala, thoraces, and pygidia or enrolled exoskeletons, indicating that they are fossilized carapaces of Ovalocephalus tetrasulcatus. Among these nearly complete exoskeletons, a portion of them are articulated thoraces and pygidia, but with the cephala separated and preserved nearby (Fig. 3A), which are considered exuviae (Han & Wang, 2000). Another kind has librigenae separated from the cranidia, but the cranidia and thoracopyga are still articulated, or the cranidia are separated from the thoraces and slightly rotated. These specimens include those with two librigenae separated from cranidia, but still preserved nearby (Fig. 3B), and a portion of these librigenae were inverted or rotated (Fig. 3D); in addition, some specimens have one librigena separated from the cranidium and inverted, but another still in situ (Fig. 3C). Both types of inverted or rotated librigenae separated from the cranidium are similar to the exuvial mode of many trilobites (Henningsmoen, 1975; McNamara & Rudkin, 1984), indicating that they are most likely exuviae of Ovalocephalus tetrasulcatus, rather than corpses that were broken up by bottom currents and/or organisms, and the natural decomposition of the corpses. This indicates that there is more than one exuvial mode in Ovalocephalus tetrasulcatus; i.e., separation of the cephalon from the thoracopygon, separation of the librigenae from the cranidium, or both existing at the same time. A similar diversity of exuvial patterns has been found in other phacopid trilobites (Brandt, 1993; Budil & Bruthansová, 2005; Chen, 2011).

In the sixteen specimens with two or three exoskeletons partly superimposed or end to end, all the specimens show separation of the cephalon or librigenae, and the separated cephala or librigenae are still preserved near the thoracopyga (Fig. 4), indicating that all of these specimens are exuviae of Ovalocephalus tetrasulcatus. The central axis of the most frontal Ovalocephalus tetrasulcatus in the exuvial clusters was used as the directrix to calculate the axial azimuth of the posterior trilobites. The results showed that there was an obvious dominant orientation; that is, the axial azimuth of the trilobites in these clusters had obvious consistency (Fig. 5), indicating they were not the result of accidental burial events. The separated librigenae preserved near the cranidia may also preclude them from being the result of postmortem transport. Therefore, these exuviae are inferred to have been caused by the active behavior of trilobites.

Discussion

Conclusions

The exuviae of Ovalocephalus tetrasulcatus from the Upper Ordovician Linxiang Formation presented two types: separation of the librigenae from the cranidium, and separation of the cephalon from the thoracopygon, reflecting the diversity of the exuvial modes. Some specimens have two or three exuviae arranged end to end, and some have partly and even completely superimposed exuviae together in clusters. The preserved patterns and burial conditions indicate that these specimens are products of the active behavior of trilobites, rather than mechanical transport by currents, unexpected burial in the middle of the act of molting, or collective molting before mating. The preserved patterns and overlapping phenomena of the exuviae indicate that these clusters were formed by two or three trilobites lining up to shed their shells in a long and narrow feature of seafloor topography. They likely represent the behavioral response that the trilobites chose to follow in certain risky life activities, indicating that herding behavior existed in these Ordovician trilobites.