Perhaps one of the most important adaptations of Cambrian brachiopods was the ability to attach to hard substrates, in particular sponges6,11,19, raising the individuals above the seafloor to avoid biofouling, turbidity and lowering competition by implementing a tiering system. Attachment to larger motile organisms would not only provide the advantages listed above, but could potentially increase nutrient availability by transporting the individuals to more habitable parts of the benthic environment where both hosts and symbionts would benefit from low turbidity levels and higher access to food sources (i.e., in areas with bacterial mats uncovered by silt in the case of Wiwaxia). The current generated by the movement of Wiwaxia may have also been sufficient to improve the food supply and remove waste products produced by the brachiopod. In addition, brachiopods have been documented in unidentified coprolites and in the gut of Ottoia prolifica32, a priapulid worm from the Burgess Shale32 suggesting brachiopods were common prey items. Wiwaxia sclerites were also identified in the gut contents of Ottoia, however, based on size inconsistencies it was suggested that Ottoia scavenged on decaying wiwaxiids rather than preying on live specimens33. Attaching to larger, motile animals, such as Wiwaxia would have certainly acted as a deterrent and made it more challenging for benthic predators to eat the brachiopods.

This relationship also sheds some indirect light on the timing and mode of growth of the scleritome of Wiwaxia and points to the uniqueness and limitations of this scleritome for brachiopods to attach to it. All Wiwaxia specimens described herein are well over 25 mm in length, a dimension considered to represent the beginning of the adult phase when the scleritome becomes less variable21,26. Assuming that the attached brachiopods are a few months old, this puts some minimal time constraints between two consecutive molting events in adult Wiwaxia specimens. This also suggests that juvenile Wiwaxia specimens were less likely to be suitable habitats for brachiopods presumably because the rate of shedding and replacing sclerites was higher in smaller individuals to accommodate for an increased number and variety of sclerites26, thus reducing the time for larval brachiopods to settle. In addition, the size of the three attached brachiopod shells are comparable possibly suggesting that other Nisusia specimens, larger than the ones already documented, are unlikely to be found in association with other Wiwaxia scleritomes. Owing to the fact that such associations remain extremely rare (i.e. among hundreds of articulated Wiwaxia specimens, only three occurrences exist, a fourth specimen housed at the Cincinnati Museum18 is inconclusive), points out to the nature of the symbiosis, which must have been facultative for both species and of limited evolutionary advantage for the brachiopod, since growth to adult stage might not have been possible due to periodic shedding of the sclerites.

Attachment of invertebrates to mobile organisms, although considerably rare in the fossil record, is a strategy adopted by a wide variety of organisms in modern marine communities. Bryozoans in particular are common epibionts on motile organisms, attaching themselves to crabs34,35, cephalopods36, sea turtles37 and sea snakes38. Poriferans, hydrozoans, scyphozoans, sea anemones, anthozoans, nematodes, nemertians, annelids, barnacles, molluscs and echinoderms have also been reported in modern marine settings as epibionts on copepods, crabs, isopods, lobsters and shrimp as well as on gastropod shells34. No records of extant brachiopods living as epibionts on mobile hosts has been found, instead extant brachiopods have been reported predominantly acting as the role of host and are commonly encrusted by bryozoans39, bivalves40, polychaetes41 and internally inhabited by crustaceans42.

Many of the mobile hosts mentioned above are arthropods (e.g. crabs, lobsters, isopods) and the frequent moulting of the arthropod host would obviously have a negative impact on the attached epibiont, as the exoskeleton is removed. The benefits that may accrue from attaching to a moulting organism to some degree must offset the potential shortened life span, at least in the bryozoan/crab symbiotic relationship that appears to have repeatedly evolved, suggesting that a real benefit exists for the bryozoans34,43. A moulting episode would not necessarily lead directly to the death of the symbiont, but it would increase the symbiont's exposure to scavengers and other organisms that may consume the moulted shell. Competition for suitable substrate space is intense in modern communities43,44 and exploitation of mobile hosts may lessen the competition for substrate by providing additional unoccupied substrate space. Mobile hosts, due to the difficulty of settling on a free moving organism, are typically less occupied, (in terms of the number of epibionts and percentage of the host covered by epibionts) when compared to sessile substrates34,38,43 providing a substrate where interactions with other attached organisms will be minimal45.

It is difficult to determine if the pelagic larvae of Nisusia actively sought out Wiwaxia for settlement rather than fortuitously settling on Wiwaxia because the sclerite provided a suitable attachment surface. Over 200 specimens of Nisusia from the Burgess Shale Formation have been examined and only 18 individuals are preserved directly attached to a form of substrate. Of those 18 individuals, attachment to the sponge Pirania is the most common (67%, 12 of the 18 specimens) and three specimens are attached to Hazelia, Chancelloria and a tube belonging to Selkirkia (one specimen on each substrate type). The three Nisusia specimens attached to Wiwaxia (17% of total attached Nisusia specimens) represent the second most favoured substrate of the preserved specimens available. The most common brachiopod in the Burgess Shale Formation preserved attached to substrate, is the paterinate brachiopod Micromitra, where over 50 specimens have been recorded (Topper, unpublished). Pirania once again, is the most heavily favoured substrate with over 60% of Micromitra individuals attached to the sponge. Despite the abundance of Micromitra specimens, no individuals are attached to Wiwaxia sclerites, in fact N. burgessensis is the only species that is found to be directly attached to Wiwaxia out of the eight species of brachiopods documented from the Burgess Shale Formation.

In total, out of the 87 specimens of brachiopod (across all brachiopod species documented from the Burgess Shale) found to be directly attached to substrate, 57 specimens are attached to the sponge Pirania. Brachiopod specimens are also attached to a variety of disarticulated skeletal elements and to other brachiopod individuals, however Wiwaxia is the only mobile organism in the community that is preserved with brachiopods attached. Other organisms in the Burgess Shale community may have moved too rapidly or lived too high in the water column to allow settlement (free swimmers like the anomalocaridids), lacked appropriate sclerites to attach to (soft bodied organisms such as Nectocaris and Odontogriphus) or been too small to allow settlement and development (e.g. Marrella and Scenella). Admittedly this is but a few examples of the some 170 species documented from the Burgess Shale18, however it does accentuate the combination of characters possessed by Wiwaxia that would have allowed for a suitable settlement point for brachiopod larvae.

Conclusions

This unique association of brachiopods attaching onto Wiwaxia represents the oldest commensal relationship of sessile organisms fixed on a mobile organism in the fossil record, predating the previous oldest occurrence by approximately 200 million years14. This commensal and facultative relationship would have benefited the brachiopod in a variety of ways but would have been temporary and potentially limited by the timing of scleritome ecdysis. Possible advantages include; (1) obtaining an attachment on a hard substratum, (2) reaching an elevated position above the sediment surface and a variety of potential food supplies due to locomotion of the host (3) avoidance of biofoul and sedimentary disturbance (4) less competition by settlement on unoccupied space and (5) added protection. It would be hard to imagine given the small size of the brachiopods relative to the size of Wiwaxia that the symbiont negatively impacted the host, especially with Wiwaxia episodically shedding its sclerites and spines. This commensal association is unique for a species of brachiopod, fossil or living and suggests that complex forms of symbiotic relationships were already well established by the Cambrian period.