Although imperfectly understood, the morphology of Pahvantia frontal appendages strongly suggests that they were used for the capture of microscopic food particles suspended in the water column. The number (>50 per row), morphology (thin and long), and distribution (even and dense) of the putative setae indicate that they formed a filtering apparatus (Fig. 1c–e), rather than manipulated moving macroscopic preys. Except for the proximal endites (Fig. 1f), likely used to comb the filtering setae and transfer food particles to the mouth, the frontal appendage of Pahvantia is devoid of the robust spines (endites and auxiliary spines) characterizing radiodont appendages with inferred grasping (e.g. Anomalocaris, Amplectobelua29,30), grasping-crushing (e.g. Amplectobelua31), grasping-slicing (e.g. Caryosyntrips, Lyrarapax27,32), or sediment sifting (e.g. Hurdia, Peytoia23) functions.

Suspension-feeding habits have been inferred for two, possibly three radiodonts exhibiting fundamentally different organisation of the frontal appendages. In the early Cambrian Tamisiocaris, and possibly Anomalocaris briggsi, suspended particles (including mesoplankton) were trapped by a net formed by the numerous, needle-like auxiliary spines fringing the anterior and posterior margins of long and delicate endites18 (Fig. 3a, b). In contrast, the Early Ordovician Aegirocassis was equipped with long, plate-like endites similar to those of Hurdia and Peytoia, except that numerous moveable setae project from the anterior margin in place of stout auxiliary spines19 (Fig. 3c). Each seta bears two rows of spinules (Fig. 3d), representing an additional order of complexity compared to the filtering apparatus of Tamisiocaris. With its long plate-like endites bearing anterior setae only, the frontal appendage of Pahvantia is strongly reminiscent of that of Aegirocassis, except for an additional row of setae per endite, and apparent lack of spinules (Fig. 3e).

Fig. 3 Endite morphologies in suspension-feeding radiodonts. Photographs of specimens immersed in dilute ethanol (a) or dry (b–e). a, b Endites with numerous auxiliary spines. a Early Cambrian Tamisiocaris borealis (MGUH30501; image: J. Vinther). b Early Cambrian Anomalocaris briggsi (SAM P47020a; image: J. Paterson). c, d Endite with numerous complex setae, Early Ordovician Aegirocassis benmoulae (images: P. Van Roy). c General view (YPM522227). d Detail of the setae and their spinules (YPM527125). e Endite with numerous simple setae, middle Cambrian Pahvantia hastata (KUMIP314089). Scale bars represent 1 cm (c, d) and 2 mm (a, b, e). as auxiliary spines, en endites, se setae, sp spinules Full size image

The highly complex filtering apparatus of the Ordovician taxon likely evolved in relation to gigantism, the presence of spinules allowing its mesh size to approach that of Tamisiocaris (490 µm), despite a huge difference in appendage size—a single endite of Aegirocassis is as long as the whole appendage of the early Cambrian species. Compared to the giant Moroccan species, Pahvantia has an inferred body length ten times smaller20 and despite a simpler structure, a filtering system with a mesh size seven times smaller (c. 70 µm). This latter difference is important, for it suggests that Pahvantia was able to sieve much smaller organisms/particles out of the water column. Following Vinther et al.’s methodology18, a minimum size between 70 µm (mesh size) and 100 µm (linear regression; Fig. 4) can be inferred for the suspended elements captured by the middle Cambrian radiodont. This corresponds to the size of large microplanktonic organisms, which nowadays essentially include autotrophic (phytoplankton) and heterotrophic (protozooplankton) unicellular eukaryotes33 (Fig. 4). In other words, Pahvantia might have been both a primary and secondary consumer, and therefore contributed to a more efficient transfer of biomass and energy from the euphotic zone to benthic environments.

Fig. 4 Size of the particles captured by suspension-feeding radiodonts. With a mesh size of 70 µm (red dashed line), P. hastata might have fed on microplankton, including phytoplankton. The mesh size was closed to 500 µm (blue dashed line) in both Aegirocassis and Tamisiocaris, which therefore likely grazed on mesoplankton. Grey area depicts prey-size variation for a given mesh size in modern suspension feeders. Diagram on the left is modified after ref. 18. Size distribution of main plankton types (right) is derived from ref. 63 Full size image

Indeed, even if relatively small for a radiodont (<25 cm), Pahvantia was a ten to thousand times larger than any mesoplanktonic (0.02–2 cm) primary consumers, and therefore produced much larger and more rapidly sinking faecal pellets and carcasses. Larger organic remains have shorter residence times in the water column and consequently greater chances to reach the sea floor and become food for benthic organisms34. Thus, the large faecal pellets of Pahvantia were probably consumed by a variety of coprophagous animals, such as hyoliths, ptychopariid trilobites, and agnostoid arthropods35, all abundant components of the Wheeler fauna36. Likewise, its carcasses likely supplied sustenance to mobile scavengers attracted from afar, including some arthropods (e.g. agnostoids37,38) and lobopodian and scalidophoran worms39,40. Moreover, the efficiency of energy transfer between any two trophic levels is only 10% on average41, and so by shortening the food chain connecting primary production and benthic organisms, Pahvantia might have more efficiently contributed to the flux of energy from pelagic to benthic realms than free-swimming animals feeding on mesoplankton (e.g. Tamisiocaris).

This hypothesis of a Cambrian nektonic organism like Pahvantia being an omnivorous suspension-feeder relies on the inferred minimum size of the particles trapped by its filtering apparatus, and the fact that it falls within the size range of modern marine phytoplankton33,42 (Fig. 4). This observation logically raises the question of whether phytoplanktonic organisms in Cambrian marine environments were comparable in size to modern ones. Unfortunately, little is known of the organisms responsible for marine primary production in the Early Palaeozoic, except that they were not coccolithophorids, diatoms or dinoflagellates, and that the role of green algae might have been greater than today43. Only the phytoplankton producing resistant cysts have left a trace in the fossil record in the forms of acritarchs. These organic-walled microfossils provide the only estimates of the sizes reached by primary producers at that time. According to Huntley et al.44, average acritarch size dramatically increased during the Cambrian, reaching 55 µm during the 500–485 Ma time interval (i.e. shortly after the deposition of the Wheeler Formation). Extrapolating from the mean size (<10 µm) and size distribution of modern phytoplanktonic species42, this average value for acritarchs suggests an upper size range of Drumian (c. 502 Ma) phytoplankton exceeding the mesh size (70 µm) of the filtering apparatus of Pahvantia. This seems all the more likely given that this estimated mesh size represents a maximum value, which only considers the distance between two adjacent setae of a given row. This assessment, measured in a single sub-adult specimen, omits the possibility that more distant elements (e.g. setae on adjacent endites) might have overlapped in the original three-dimensional organisation of the filtering basket, thus creating a finer filtering mesh19. Likewise, mesh size might have increased during the ontogeny of Pahvantia, as it does in some extant crustaceans45,46. Lastly, it cannot be entirely ruled out that spinules were present but not preserved in the middle Cambrian radiodont, which would considerably reduce the mesh size of the filtering net. In Aegirocassis, these structures are only conspicuous in a couple of particularly well-preserved specimens19, and both are substantially much larger than the single, strongly flattened Pahvantia appendage described herein. Considering these possible biases, it is particularly likely that this macroscopic nektonic organism grazed on large phytoplankton, especially during the early phases of its life.

The description of a Drumian suspension-feeding radiodont illustrates that this feeding strategy evolved at least twice, possibly three times, in the history of this group: Tamisiocaris (early Cambrian), Pahvantia (middle Cambrian), and Aegirocassis (Early Ordovician). The three taxa are all retrieved within a clade regrouping Tamisiocarididae and Hurdiidae, with Tamisiocaris belonging to the former and Aegirocassis and Pahvantia to the latter. An ancestor-descendant relationship between Pahvantia and Aegirocassis seems unlikely according to the association of the latter taxon with Peytoia in some of the retrieved trees of the parsimony analyses. This polyphyletic origin of filter-feeding in radiodonts mirrors the situation observed in recent crustaceans, where this feeding mode is known in representatives of at least fifteen orders46. This reflects the fact that microscopic suspension-feeding and macroscopic raptorial predation are two extremes of the same spectrum, which essentially differ in the size of the particles/organisms caught, rather than in the mechanics of feeding. This is well-illustrated by extant crustaceans with complex filtering apparatuses, which nonetheless commonly (e.g. krills47,48; copepods49) or occasionally (e.g. barnacles50,51,52,53) engage in raptorial predation, or by the progressive shift from filter-feeding to raptorial predation during ontogeny in some fairy shrimps54, barnacles52, or krills47. Actually, there might be a positive correlation between body size and contribution of animal-derived food to the diet in crustaceans, with larger taxa/individuals preying more and targeting larger preys. This led Riisgård46 to hypothesize the existence of a physiological limitation to body size in filter-feeding crustaceans, especially herbivorous ones. In short, feeding in these organisms is constrained by the size of the filtering surface, while metabolism (especially respiration) is related to body volume; a surface increasing slower than a volume, there should be a maximum body size beyond which suspension-feeding cannot compensate metabolic cost. The discovery of a 200 cm-long, filter-feeding Ordovician radiodont indicates that the relationship between body size and feeding strategy was more complicated in these extinct organisms. Vinther et al.’s suggestion18 – somewhat reverse to Riisgård’s hypothesis—that suspension feeding animals evolved from large predators might also be nuanced. Indeed, albeit reaching a large body size compared to most middle Cambrian animals, Pahvantia remains one of the smallest radiodonts20 (Fig. 5). Moreover, the sizes of the presently-known filter-feeding radiodonts positively correlate with phytoplankton (acritarch) diversity55,56, which suggests that food availability, more than ancestor size, might have governed the sizes reached by these organisms.

Fig. 5 Diversity of sizes and feeding habits in radiodonts. As exemplified by Aegirocassis and Pahvantia, there is no obvious relationships between size and feeding strategy in this group. Raptorial predators are represented in red, sediment sifters in purple, and suspension feeders in blue Full size image

Thus, there are no clear relationships between body size, feeding strategies, and phylogenetic affinities in radiodonts (Fig. 5), which actually attests to the great adaptability of these extinct organisms. This is particularly well-illustrated by the wide range of morphologies and functions displayed by their frontal appendages25,27,31. The description of a microplanktonic-feeder representative adds to an ever-growing body of evidence suggesting that radiodonts, as both juveniles and adults27, contributed in various ways to the emergence of modern-style marine ecosystems in the Cambrian, including in the coupling of pelagic and benthic realms.