New suspension-feeding radiodont suggests evolution of microplanktivory in Cambrian macronekton

Introduction

The evolution of phytoplanktonic life dates back to at least 1.8 Ga, but it remained essentially represented by simple forms of acritarchs (leiosphaerids) until the end of the Proterozoic Eon¹. During this time interval, eukaryotic life evolved significantly, as evidenced by the emergence of large unicellular forms² (also see ref. ³) or the first macroscopic multicellular organisms⁴, including early animals^5,6. However, these important steps of eukaryotic evolution were apparently confined to the benthic realm, which remained essentially decoupled from primary production in the euphotic zone of the oceans¹. The early Cambrian Period is associated with an even greater modification of marine life—the advent of metazoans and their organisation in complex ecosystems. In less than 30 Myr, most major bilaterian phyla appeared and greatly diversified^7,8, provoking a dramatic change in both the composition and the functioning of the biosphere, which in turn profoundly and irreversibly impacted the Earth system^9,10. For instance, likely triggered by a new ecological force—predation —some of these early Cambrian animals (e.g. scalidophorans) rapidly evolved aptitudes for life within soft substrates¹¹, thus increasing the breadth and depth of eukaryotic colonization of the sea floor, and concomitantly the habitability of the latter¹². Interestingly, phytoplankton also radically changed at that time with the radiation of small, rapidly evolving ornamented acritarchs (acanthomorphs). This has been interpreted as indirect evidence of the introduction of a key component of modern pelagic ecosystems— herbivorous zooplankton¹³. These primary consumers play a critical role in the transfer of energy and biomass from the well-lit surface layer down to the sea floor, repackaging organic matter produced by photosynthesis into larger, more rapidly sinking elements (e.g. carcasses, faecal pellets). The presence of early Cambrian herbivorous zooplankton was demonstrated by the finding of microscopic carbonaceous remains of crustacean filter-feeding apparatuses^14,15. Similar, but larger fossils were also recovered from middle Cambrian strata of the Deadwood Formation in western Canada, which also yielded middle–upper Cambrian remains of omnivorous zooplanktonic crustaceans¹⁶. Although rare, these fossils attest to a complexification of pelagic ecosystems and the onset of a coupling between pelagic and benthic realms in the Cambrian.

Until recently, evidence for a significant contribution of macroscopic animals to the biological pump at that time was meagre. The few nektonic taxa (e.g. chaetognaths, a few arthropods) found in Burgess Shale-type deposits were thought to predominantly live close to the sea floor (demersal zone¹⁷). The description of a lower Cambrian, filter-feeding representative of Radiodonta—distant relatives of spiders, insects, myriapods and crustaceans previously regarded as fearsome apex-predators—radically changed this picture¹⁸. Comparing radiodonts to pachycormid fish, sharks and whales, Vinther et al.¹⁸ concluded that the evolution of suspension-feeding was somewhat predictable in these groups, the ancestors combining predatory habits and large body sizes. This assumption found tremendous support in the discovery of a two metre-long, suspension-feeding radiodont from the Lower Ordovician Fezouata Shale of Morocco¹⁹.

In this contribution, we show that Pahvantia hastata, an as-yet enigmatic arthropod from the middle Cambrian of Utah, was also a suspension-feeding radiodont, although a relatively small one. This taxon illustrates that shortly after the Cambrian explosion, some nektonic animals were likely capable of feeding on microplankton, including large phytoplankton, and therefore of contributing to primary consumption and the establishment of the biological pump in the oceans.

Results

Discussion

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, Amplectobelua^29,30), grasping-crushing (e.g. Amplectobelua³¹), grasping-slicing (e.g. Caryosyntrips, Lyrarapax^27,32), 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).

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.

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. agnostoids^37,38) and lobopodian and scalidophoran worms^39,40. 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 phytoplankton^33,42 (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 crustaceans^45,46. 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. krills^47,48; copepods⁴⁹) or occasionally (e.g. barnacles^50–53) 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) diversity^55,56, which suggests that food availability, more than ancestor size, might have governed the sizes reached by these organisms.

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 appendages^25,27,31. 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.

Methods

Electronic supplementary material

Author contributions

R.L.-A. conceived the project, prepared and photographed the new specimens, and conducted the phylogenetic analysis with inputs from S.P. The latter compiled the data related to the body lengths of radiodonts. R.L.-A. wrote the manuscript with inputs from S.P., who prepared Fig. 5; R.L.-A. prepared the other figures.

Data availability

The data generated or analysed during this study are included in the published article (and its supplementary information files) or available in Dryad Data Repository with the identifier 10.5061/dryad.1cf2fb0 (2018)²⁰. Photographic material of the studied fossils is available from the corresponding author upon request. The specimens of A. benmoulai, A. briggsi, P. hastata, and T. borealis illustrated herein are housed in the collections of the Yale Peabody Museum of Natural History (USA; YPM), the South Australian Museum (Australia; SAM), the University of Kansas Natural History Museum (USA; KUMIP), and the Geological Museum of the University of Copenhagen (Denmark; MGUH), respectively.

Electronic supplementary material

Supplementary Information accompanies this paper at 10.1038/s41467-018-06229-7.