Microanatomy of Early Devonian book lungs

Abstract

The book lungs of an exceptionally preserved fossil arachnid (Trigonotarbida) from the Early Devonian (approx. 410 Myr ago) Rhynie cherts of Scotland were studied using a non-destructive imaging technique. Our three-dimensional modelling of fine structures, based on assembling successive images made at different focal planes through the translucent chert matrix, revealed for the first time fossil trabeculae: tiny cuticular pillars separating adjacent lung lamellae and creating a permanent air space. Trabeculae thus show unequivocally that trigonotarbids were fully terrestrial and that the microanatomy of the earliest known lungs is indistinguishable from that in modern Arachnida. A recurrent controversy in arachnid evolution is whether the similarity between the book lungs of Pantetrapulmonata (i.e. spiders, trigonotarbids, etc.) and those of scorpions is a result of convergence. Drawing on comparative studies of extant taxa, we have identified explicit characters (trabeculae, spines on the lamellar edge) shared by living and fossil arachnid respiratory organs, which support the hypothesis that book lungs were derived from a single, common, presumably terrestrial, ancestor.

Physical gills in diving insects and spiders: theory and experiment

“…Therefore, insects eventually die if the tracheal system becomes flooded, or even if the spiracles are wetted. The situation is similar in spiders, which also evolved from air-breathing ancestors (Kamenz et al, 2008). They exchange gases in internal book lungs that connect to the atmosphere through spiracles on the abdomen.…”

Early Terrestrial Animals, Evolution, and Uncertainty

“…The presence of two pairs of lungs on the same body segments as some extant forms provides a strong argument that they are most closely related to a group known as the tetrapulmonate arachnids, which includes the spiders, whip scorpions, whip spiders, and short-tailed whipscorpions (Dunlop 2010). Indeed, the fine structure of the book lungs from a Devonian trigonotarbid, examined using threedimensional reconstruction techniques, is shared with living tetrapulmonates (Kamenz et al 2008). The youngest fossil member of the group dates from 290 million years ago (Rößler et al 2003).…”

“…These translucent rocks were formed in a hydrothermal hot spring setting in which silica-rich water inundated and silicified nearby vegetation, including a number of the animals-all arthropods-creating a near-perfect record of this early terrestrial ecosystem . The incredibly well-preserved fossils are studied in slides made from the rock and often display the internal anatomy (e.g., book lungs, the respiratory organs of arachnids; Kamenz et al 2008). Animals described to date include arachnids , primitively flightless hexapods (springtails and a bristletail or silverfish), as well as true insects Engel and Grimaldi 2004), centipedes (Shear et al 1998), and freshwater Crustacea, including extinct relatives of fairy shrimp and tadpole shrimp (Trewin and Fayers 2007).…”

Tomographic techniques for the study of exceptionally preserved fossils

“…fluorescent organic samples, it has been applied to Precambrian microfossils preserved in chert (Schopf et al 2006, see also figure 3d ) and to isolated siliceous microfossils (O'Connor 1996). Conventional microscopy can also provide sufficient separation of focal planes for tomography, as demonstrated by the reconstruction of arachnid respiratory structures from the Devonian Rhynie chert Lagerstätte (Kamenz et al 2008). Optical tomography is non-destructive and can resolve sub-micron scale structure.…”

“…Identification of outlines can theoretically be automated, but high noise levels in most palaeontological data make this impractical; manual placement of curves, using a raster tomogram as a guide, is the norm (e.g. Kamenz et al 2008). To produce a model, corresponding curves are surfaced with a triangle mesh.…”