Trilobites are typified by the behavioural and morphological ability to enrol their bodies, most probably as a defence mechanism against adverse environmental conditions or predators. Although most trilobites could enrol at least partially, there is uncertainty about whether olenellids—among the most phylogenetically and stratigraphically basal representatives—could perform this behaviour because of their poorly caudalized trunk and scarcity of coaptative devices. Here, we report complete—but not encapsulating—enrolment for the olenellid genus Mummaspis from the early Cambrian Mural Formation in Alberta, the earliest direct evidence of this strategy in the fossil record of polymerid trilobites. Complete enrolment in olenellids was achieved through a combination of ancestral morphological features, and thus provides new information on the character polarity associated with this key trilobite adaptation.
The ability of trilobites to ventrally flex their segmented bodies (enrol) played a critical role in their long (more than 270 million years) and successful evolutionary history, providing an effective defence against predators and adverse environmental conditions [1,2]. This behavioural strategy generally required precise morphological adaptations, including the presence of trunk tergites with a horizontal hinge near the longitudinal axis (fulcrum), a fused tail shield—the pygidium—equal to or larger in overall size than the cephalic shield (caudalization), and structures that facilitate enrolment and prevent lateral shearing (coaptative devices) [3–7]. Although these features are most commonly found in post-Cambrian—and phylogenetically derived—groups [2,4–7], recent studies show that some middle Cambrian Redlichiina were functionally able to enrol [8,9], hinting at earlier origins for this adaptation. However, the early fossil record of polymerid (i.e. non-eodiscoid) trilobites is typified by olenelloids, a basal group that has traditionally been considered incapable of complete enrolment; i.e. covering the entire underside of the head shield (cephalon) with the ventrally flexed trunk [1,6,10–12].
Here, we describe the functional morphology of enrolled olenellid trilobites from the early Cambrian Mural Formation in Western Canada  and demonstrate that at least some members of this phylogenetically and stratigraphically basal group were capable of complete enrolment. Well-preserved exoskeletons reveal cuticular structures that functioned as simple coaptative devices, and thus provide new information on the polarity of character acquisition required for this important strategy.
2. Material and methods
The material comes from the early Cambrian (Lower Dyeran) Mural Formation, which crops out locally in the Rocky Mountains of Jasper National Park, Alberta [13,14]. On Mumm Peak, it is represented by three members: a lower archaeocyathid limestone (ca 120 m), an intermediate siliciclastic unit (ca 110 m) and an upper dolomite (ca 52 m); decimetre-sized lenses of shell debris within the bedded mudstones attest to occasional storm winnowing in a mid-to-outer shelf environment . Trilobites were collected from mudstones in the lower part of the siliciclastic member, which conformably overlies in situ and reworked archaeocyathid reef-rock. In addition to olenelloids , the siliciclastic member preserves a modestly diverse Burgess Shale-type fauna suggesting rapid burial and negligible transport .
The Mumm Peak trilobite assemblage includes two individuals showing different phases of enrolment, representing two different species of the genus Mummaspis [13,15]. Additional specimens with well-preserved cuticle were examined for coaptative devices. Enrolled specimens were photographed immersed in water; exoskeletal sculpture details were photographed dry. Figured material is housed at the Geological Survey of Canada (GSC), Ottawa.
3. Fossil description
GSC 137152, a specimen of Mummaspis ?muralensis [13,15], shows a ventral view of the cephalon—as evinced by the concavity of the exoskeletal features—and indicates a direct contact between the ventral side of the anterior cephalic margin and the posterior end of the trunk (figure 1a). The first trunk tergite is articulated with the cephalon and also preserved in ventral view; the second and third tergites are missing, probably due to post-burial compaction. Most of the trunk, comprising the 4th–14th tergites plus the macrospine, is symmetrically flexed under the head. The overlap pattern of the tergites demonstrates that this configuration is a result of the ventral flexure of the body. The articulating half ring of the fourth tergite is exposed, indicating that the trunk could be strongly flexed at this region . The macrospine-bearing tergite is in direct contact with the ventral side of the cephalic margin. The tips of the posterior pleural spines extend beyond the anterior cephalic margins, covering most of the ventral side of the head. The spaces left in between the pleural spines, however, shows that M. ?muralensis was incapable of encapsulation; i.e. complete enrolment without open gaps . The overall exoskeletal configuration in GSC 137152 bears a close resemblance to that observed in encapsulated individuals of the redlichiide Eccaparadoxides pradoanus from the middle Cambrian (Drumian) of Spain , and also to completely enrolled specimens of the olenellids Olenellus chiefensis and Olenellus gilberti  from the early Cambrian (Upper Dyeran) of Nevada  (figure 2a; see electronic supplementary material, figure S1).
The second example, an individual of Mummaspis occidens (GSC 137153) , comprises the dorsal view of a cephalon plus the articulated first to fifth trunk tergites (figure 1b). Although the posterior half of the trunk is buried within the rock matrix, the lateral overlapping of the articulating facets in the pleurae indicates that the body is ventrally flexed under the head. The degree of pleural overlap suggests a similar region of maximum body flexure to that observed in GSC 137152. This interpretation is further supported by the burial pattern that follows the axial convexity of the dorsal exoskeleton, indicating that the appearance of the specimen is not a result of disarticulation or breakage. GSC 137153 shows a similar disposition to ventrally flexed specimens of E. pradoanus  and is also comparable to a flexed specimen of the olenellid Nephrolenellus geniculatus from the early Cambrian (Upper Dyeran) of Nevada  (figure 2a; see electronic supplementary material, figure S1).
Mummaspis also exhibits exoskeletal specializations that functioned as simple coaptative devices. Outstretched specimens of Mummaspis truncatooculatus [13,15] with well-preserved cuticle feature prominent postero-laterally oriented ridges in the trunk tergites. These ‘terrace lines’ are restricted to the anterior half on the dorsal surface of each pleural spine, as demarcated by the pleural furrow (figure 1c). On the posterior half of the body, the terrace lines acquire a sub-perpendicular orientation relative to the body axis due to the progressive curvature of the pleural spines. The ventral cuticle (doublure) of each pleural spine, however, features transverse terrace lines (figure 1c). When completely enrolled, the configuration of the terrace lines on the dorsal and ventral articulating surfaces of adjacent pleurae would face each other at approximately right angles (figure 2b). This arrangement duplicates the ‘petaloid facets’ found on the articulating pleural regions in stratigraphically younger trilobites, a coaptative device that facilitates the correct accommodation and gliding of overlapping pleurae during encapsulation [2,3,7,9,19,20].
The cephalic margins in Mummaspis—as well as other olenellids [11,12,18] and redlichiines [8,9]—bear strong parallel terrace lines that, in the anteriormost region, are arranged perpendicular to the body axis (figure 1d). When completely enrolled, these anterior cephalic ridges would have made direct contact with the terrace lines found on the pleural spines of the posterior tergites (figure 2b), resulting in a functional ratchet between these opposite body regions. Such interaction would also have restricted the degree of lateral movement during enrolment, thereby increasing the structural integrity of this configuration against adverse conditions [3,5,7,9,19]. Terrace lines on the cephalon and pygidum that enhance enrolment are known from numerous trilobite groups, but have been documented only in more derived forms with well-caudalized exoskeletons [3,5,7–9,19,20].
Mummaspis from the Mural Formation represents the oldest example of complete enrolment in Redlichiida (figure 2a), and the earliest direct evidence of this behaviour in the fossil record of polymerid trilobites (see electronic supplementary material, table S1). The identification of complete—but non-encapsulating—enrolment in olenellids illuminates the polarity of the morphological features associated with this strategy (figure 2c). Mummaspis and Olenellus [12,18] demonstrate that some micropygous trilobites were able to enrol, and thus this behaviour significantly precedes the general trend to increase body caudalization observed in younger representatives with derived isopygous bodies [1–7,10,19,20]. The presence of differentiated exoskeletal sculpture on the articulating surfaces of olenellids—including the petaloid facets on the trunk pleurae (figure 1c) and shear-resistant structures on the cephalon and posterior spines (figure 1d)—also precedes caudalization. Thus, it appears that terrace lines represent the most ancestral coaptative devices found in polymerid trilobites (figure 2c). Contrary to previous interpretations [1,2,4,10,11], the possession of simple coaptative devices and non-fulcrate trunk tergites did not prevent olenellids from engaging in complete enrolment. However, the fact that Mummaspis and Olenellus could not encapsulate indicates that olenellid enrolment was less complex than that observed in more derived forms [1–7,9,10,19,20]; such simplicity most probably reflects the less escalated palaeoecological nature of the early Cambrian biosphere .
Mummaspis provides a more striking example of complete enrolment in phylogenetically basal trilobites than middle Cambrian Eccaparadoxides (figure 2a,c) , since the partially fulcrate tergites and ‘pseudo-isopygous’ body of the latter are clearly derived compared to the morphology of most redlichiids [10–13,15]. In the wider phylogenetic context of Trilobita, the present findings indicate that olenellid enrolment involved a suite of ancestral characters (figure 2c). By contrast, Redlichiina and other more derived polymerid trilobite groups independently developed analogous morphological adaptations (e.g. fulcrum, increased caudalization, complex coaptative devices) that significantly improved the effectiveness of this strategy, resulting in the ability to encapsulate (figure 2c) [1–9,19,20].
Given the relatively simple morphological adaptations required for olenellid enrolment, the paucity of enrolled individuals in the early fossil record of polymerid trilobites is more likely to be a taphonomic rather than a biological signal. The introduction of more diverse and securely inter-locking mechanisms in derived lineages is certainly responsible in part for the increased occurrence of post-Cambrian enrolled specimens [2,4,8]. By contrast, olenellids could only maintain the enrolled configuration through continuous muscular contraction owing to the limitations of their few and somewhat primitive coaptative devices. After death, the muscles responsible for flexing the trunk would have relaxed, causing the carcass to return to the outstretched position. Thus, the best possibility of preserving enrolled olenellids would require rapid burial of live individuals, as exemplified by the lower siliciclastic member of the Mural Formation . In this context, based on the phylogenetic positions of Mummaspis and Olenellus , it is at least possible that various olenellid groups were capable of complete enrolment and engaged in this behaviour on a regular basis.
The Mural Formation olenellids demonstrate that the minimal behavioural and morphological adaptations required for complete enrolment were well in place by the early Cambrian. Despite humble origins, the adoption of complete enrolment by olenellids pioneered an exceptionally successful behaviour, ultimately leading to the ecological dominance of this archetypical Palaeozoic group during a critical period in the early evolution of animal phyla.
J.O.H. acknowledges funding by CONACYT (Mexico), SEP (Mexico), University of Cambridge Trusts (UK) and Darwin College (UK). J.E. is supported by a Chinese Academy of Sciences Fellowship for Young International Scientists (grant no. 2012Y1ZB0010).
Parks Canada facilitated access for fieldwork.
- Received July 30, 2013.
- Accepted August 29, 2013.
- © 2013 The Author(s) Published by the Royal Society. All rights reserved.