In the mud

Quick... what was Darwin's most popular book? If you answered The Origin of Species, you were wrong. It was his last book, published the year before he died, The Formation of Vegetable Mould Through the Action of Worms With Observation of Their Habits. Darwin noted when he was beginning his career that worms churned up soil, causing heavier objects to sink slowly in the soil. He noted that all soil had passed through the alimentary duct of worms. It started off a fashion of cultivating worms by gardeners that continues to the present day.

Now called "bioturbation", this process has recently been proposed as the reason (or one of several reasons) for the increase in biodiversity in the Cambrian. Three researchers, Filip J.R. Meysman, Jack J. Middelburg and Carlo H.R. Heip, of the Netherlands Institute of Ecology, have a forthcoming paper in Trends in Ecology and Evolution, in which they suggest that the evolution of the reworking of sediments by burrowing animals set off the Cambrian explosion.

In the pre-Cambrian, both plants and animals lived on the surface of the sea floor. This meant that resources available had to be in the sea itself. Many animals lived sedentary lives, attached to the sea floor or to rocks, looking for all the world like plants (making the identification of early chordates difficult, since frond-like animals look just like plants). Mesman et al. argue that a major shift in habitat to include burrowing into the sediments triggered off an increase in ecological complexity, leading to free-swimming organisms, greater plant diversity, and ultimately, us.

Bioturbation results from a range of animal activities. The most eye-catching are those created by larger subterranean mammals, such as insectivorous moles [(a) mole track at Noordhoek beach, Cape Town] and herbivorous pocket gophers Thomomys talpoides macrotis (b) in prairie grasslands. In the marine environment, large-scale burrowing is also present, but less easily detectable [7]. Side-scan sonar has revealed conspicuous trenches (4-m long, by 2-m wide, by 0.4-m deep) created by grey whales in search of benthic amphipods, and long linear traces (0.4-m deep by 50-m long) generated by walruses ploughing the surface sediment in search for bivalves. In seagrass meadows, similar-sized pits and trails are created by herbivores, such as geese and dugong Dugong dugong (c) feeding on rhizomes. On tidal flats, smaller feeding pits (d) (up to 1-m wide and 30-cm deep) are attributed to stingrays such as the blue-spotted stingray Taeniura lymma (e). Small invertebrates have a small per capita impact, but are dominant from a global perspective because of their sheer abundance and ubiquity; examples include ants, termites and the common earthworm Lumbricus terrestris (f). In the marine environment, the predominant bioturbators are deposit-feeding polychaetes and various burrowing crustaceans, such as burrowing shrimp [(g) geochemical gradients created in a laboratory observatory by the shrimp Neotrypaea californiensis.

The authors say

It is hypothesised that there are two important factors driving this 'Cambrian explosion'. The first is the advent of predation, which promoted the development of biomineralised skeletons (bristles, spines, shells, etc.), and began an escalating 'arms race' between predators and their biomineralised prey. The second evolutionary factor is bioturbation, which appeared as a side effect of the skeletons induced by predation: the new armoured arrivals began to 'bulldoze' the ocean floor. In addition to direct defence, skeletal hard parts functioned as anchoring devices or digging tools, which enabled a burrowing life style to evolve. Although the sediment now provided shelter from predators, it was also an incentive for predators to search for such prey. Burrowing also enabled the exploitation of buried organic matter as a food source, leading to the evolution of a new deposit-feeding life style. The colonization of the deeper sediment instigated a true 'burrowing revolution' (also termed 'agronomic' or 'Cambrian substrate' revolution), as the resulting reworking of the sediment involved a dramatic change in the ecological and geochemical functioning of the ocean floor. The microbial mat structure disappeared, disrupted by trilobites and other stiff-legged arthropods, intersected by complex burrow networks and covered with faeces of the newly evolved deposit-feeders. Today, microbial mats only survive in extreme environments that exclude grazers and bioturbators, such as stromatolites, hypersaline lagoons and anoxic basins.

Transition from Ediacaran matground to Cambrian mixground during the burrowing revolution. During the Ediacaran, sediments were covered with microbial mats (a) (Vendian diorama). After the burrowing revolution, the sediment is mixed and intersected by complex burrow networks (b). As a result of burrow flushing, oxygen is now transported deep into the sediment. The lugworm Arenicola marina has a light halo of oxidised sediment around its burrow as opposed to the grey background of reduced sediment.

It's a nice historical irony that Darwin's little worms may have been the latest in a series of lowly but highly significant burrowers, on whom we all rely.