Collective behaviour in 480-million-year-old trilobite arthropods from Morocco

Abstract

Interactions and coordination between conspecific individuals have produced a remarkable variety of collective behaviours. This co-operation occurs in vertebrate and invertebrate animals and is well expressed in the group flight of birds, fish shoals and highly organized activities of social insects. How individuals interact and why they co-operate to constitute group-level patterns has been extensively studied in extant animals through a variety mechanistic, functional and theoretical approaches. Although collective and social behaviour evolved through natural selection over millions of years, its origin and early history has remained largely unknown. In-situ monospecific linear clusters of trilobite arthropods from the lower Ordovician (ca 480 Ma) of Morocco are interpreted here as resulting either from a collective behaviour triggered by hydrodynamic cues in which mechanical stimulation detected by motion and touch sensors may have played a major role, or from a possible seasonal reproduction behaviour leading to the migration of sexually mature conspecifics to spawning grounds, possibly driven by chemical attraction (e.g. pheromones). This study confirms that collective behaviour has a very ancient origin and probably developed throughout the Cambrian-Ordovician interval, at the same time as the first animal radiation events.

Figure 1

General morphology and parameters of the raphiophorid trilobite Ampyx priscus Thoral, 1935, from the Lower Ordovician (Upper Tremadocian-Floian) Fezouata Shale of Morocco (Zagora area). (a–d) BOM 2481, overall morphology and details of genal spines. (e) Parameters used in measurements. (f,g) MGL 096718, genal spine showing internal mineralized infilling. (h) AA.OBZ2.OI.1, transverse thin section through right genal spine (see general view in Supplementary Fig. 8d). (i) MGL 096727, genal spine. (j) ROMIP 57013, external mould of glabellar and genal spine showing longitudinal ridge. a–d,f,g,i,j are light photographs. Abbreviations are as follows: α, angle between the longitudinal axis of two successive individuals; D, distance between two successive individuals in clusters (joins central part of occipital rings); df, dorsal furrow; dil, dorsal inner lobe; dol, dorsal outer lobe; ges, genal spine; gl, glabella; gls, glabellar spine; if, mineralized infilling; io, iron oxide; Lg, length of glabella; Lges, length of genal spine; Lgls, length of glabellar spine; Lp, length of pygidium; om, organic matter; py, pygidium; su, suture; TL, total length; vf, ventral furrow; vil, ventral inner lobe; vol, ventral outer lobe; Wc, width of cranidium; Wg, width of glabella; Wo, width of occipital ring; Wp, width of pygidium; 1–6, 1st to 6th thoracic segment. Scale bars: 1 cm in a–c, f, i, j; 5 mm in  g,h; 1 mm in d.

Figure 2

Linear clusters of the raphiophorid trilobite Ampyx priscus Thoral, 1935, from the Lower Ordovician (upper Tremadocian-Floian) Fezouata Shale of Morocco (Zagora area). (a,b) AA.TER.OI.12 (see Supplementary Fig. 2a). (c) MGL 096727 (see Supplementary Fig. 5a). (d) AA.TER.OI.13 (see Supplementary Fig. 2b). (e) BOM 2461 (see Supplementary Fig. 2f). (a,e) are light photographs. Line drawings from photographs. Segmented blue lines in (b–d) join the central part of occipital rings of trilobites. Red arrows indicate the position of polished section in Fig. 3. Abbreviations are as follows: (x), Asaphellus aff. jujuanus (asaphid trilobite); (y), juvenile asaphid trilobite. Scale bars: 1 cm.

Figure 3

Sediment associated with trilobite clusters. (a,b) AA.TER.OI.13 (see also Supplementary Figs 8–10), part and counterpart, from the Lower Ordovician (upper Tremadocian-Floian) Fezouata Shale of Morocco (Zagora area). (c) Polished section, general view. (d,e) Thin sections showing details of sedimentary structure. (f) Thin section showing grain size and local enrichment in organic matter (lower part). Red arrows indicate bedding plane with Ampyx clusters. Location of thin sections indicated by green lines and numbers (see also Supplementary Figs 9–11). Scale bars: 10 cm in a, b; 1 cm in c–e; 50 µm in f.

Figure 4

Scenario to explain the in situ preservation of the Ampyx linear clusters from the Lower Ordovician (Upper Tremadocian-Floian) of Morocco. (a) Deposition of a distal tempestite (event layer 1). (b) Epibenthic (e.g. trilobites) and shallow endobenthic (e.g. possible worms) organisms settle and generate bioturbation above red-ox boundary. (c) Second storm event layer entombs epibenthic fauna in situ; red-ox boundary moves upwards (white arrows). (d) New faunal recolonization. According to Vaucher et al., distal storm deposits are relatively thin (less than 5 cm) and consist of a waning (base) and waxing (top) phases (subdivision not represented in this diagram), and depositional environment is that of the distal lower shoreface with a possible water depth of approximately 30–70 m. Bioturbation is based on polished and thin sections (Fig. 3 and Supplementary Figs 8 and 9). Abbreviations are as follows: bt, bioturbation; tr, trilobite group (Ampyx); trc, trilobite carcasses (Ampyx); w, worm; wsi, water-sediment interface.

Figure 5

Two non-exclusive hypotheses to explain the linear clusters of Ampyx priscus from the Lower Ordovician of Morocco. (a–c) Response to oriented environmental stress (e.g. storms); hydrodynamic signal (higher current velocity represented by white arrows) received by motion sensors triggers re-orientation of individuals; mechanical stimulation and/or possible chemical signals cause gathering, alignment and locomotion in group. (d–f) Seasonal reproductive behaviour; chemical signals (e.g. pheromones; see red circles and red arrows) cause attraction and gathering of sexually receptive individuals (males and females) and migration to spawning grounds. The alignment of individual may have been controlled by mechanical stimuli (as in a–c). Olfactive and mechanical sensors were probably located on the antennules (pink areas 4, 5), and genal and glabellar spines (green areas 1–3), respectively. The exact location of mechanoreceptors is uncertain (possibly on high-relief exoskeletal features such as the glabella).