Development of respiratory structures in embryos and first and second instars of the bark scorpion, Centruroides gracilis (Scorpiones: Buthidae)

Abstract

The SEM was used to study the development of respiratory structures in successive stages in relation to the overall changes occurring in the scorpions. Book lung development is a slow process, starting with spiracles and a sac-like atrium in the early embryo and continuing lamellar formation to 150 or more in the adult. In the embryo, the primordial epithelial cells become aligned in a planar pattern as they secrete granules of material that aggregate spontaneously to form the cuticular walls of the lamellae. A blade-like structure is formed consisting of cells sandwiched within the two cuticle walls they secreted. These cells are in the primordial air channel. The adjacent hemolymph channel is nearly devoid of cells, but cross-bridges develop and help stabilize the cuticle walls and maintain the width of the channel. The cells in the primordial air channel undergo cytolysis, leaving it open for air except for cuticular cross-bridges. Development continues in the newborn (first instars); the air channels of some lamellae still contain cells and are not yet functional for gas exchange. The first instars are weak and relatively inactive. They climb up on the mother's dorsum until the first molt (about 8 days). With the cuticular walls of the lamellae in place, cells adhering to the wall in the hemolymph channel produce a thin, new tissue layer (epithelium) on the lamellar wall facing the hemolymph channel. This layer has many discontinuities as though it is slowly developing. Formation of the tissue layer and cytolysis of the cells in the air channels continue through the first molt in which little book lung cuticle is shed as exuvium. The air channels of the second instars (foraging nymphs) are now cell free and open for air passage except for the cross-bridges. The tissue layer is still incomplete and continues to be formed. It may provide the hypodermal primordium for cuticle replacement in later molts, but development was not studied beyond the second instar except for comparison with book lungs in the adult. The blade-like lamellae in the adult are larger and more numerous than in the second instar, but in the anterior book lung the shape of the cuticle wall and cross-bridges and the widths of the air and hemolymph channels are about the same as in the second instar. The air channels in the posterior part of the lamellae have distinctive, vein-like space-holders. The similarity of the adult anterior lamellae with those in the second instar suggests retention of this part through the 4-5 molts to maturation, and/or cell processes like those in the embryo are repeated, but this needs to be examined in further studies of cell and cuticle changes before and during the molts.

Chelicerata

“…The development of scorpion and spider book lungs is uniform and fi rst becomes apparent as an ectodermal invagination at the posterior margin of an opisthosomal segment (Laurie 1890 ;Purcell 1909 ;Farley 2008 ). This invagination then increases in size, forming a pulmonary sac, while the limb bud itself ingresses into the ectoderm of the segment (Farley 2011 ).…”

Book lung development in the embryo, postembryo and first instar of the cobweb spider, Parasteatoda tepidariorum C. L Koch, 1841 (Araneomorphae, Theridiidae)

“…In more advanced embryos, the first indication of respiratory structures are bilateral spiracles at the posterior margin of developing opisthosomal sternites (Farley, 1999(Farley, , 2001a(Farley, ,b,c, 2005(Farley, , 2008(Farley, , 2011. Those observations are from representative species from basal scorpion families Buthidae, Vaejovidae and Iuridae (Fet et al, 2000;Coddington et al, 2004).…”

“…Kjellesvig-Waering (1986) suggested that marginal spiracles in fossil scorpions were openings for passage of water to gills above the posterior edge of abdominal plates or sternites. Many scorpion embryos of diverse taxa were examined with SEM (Farley, 1999(Farley, , 2001a(Farley, ,b,c, 2005(Farley, , 2008(Farley, , 2011, but no indication of such opening or gills was observed.…”

“…A single terrestrialization event is proposed for arachnids with book lungs, since the adult organs have numerous features that appear to be homologous in the diversity of animals that have book lungs (Scholtz and Kamenz, 2006). This study is part of a comparative investigation of the development of book gills in the horseshoe crab (Farley, 2010(Farley, , 2012 and book lungs in scorpions (Farley, 2005(Farley, , 2008(Farley, , 2011 and spiders. Light and transmission electron microscopy are used herein to extend and clarify the earlier light microscopic studies of spider book lung development (Kishinouye, 1891;Simmons, 1894;Purcell, 1895Purcell, , 1909Montgomery, 1909;Janeck, 1909;Ivani c, 1912;Kassianow, 1914;Versluys and Demoll, 1923;Dawydoff, 1949).…”

“…As reviewed earlier (Farley, 2008(Farley, , 2010(Farley, , 2011(Farley, , 2012, lamellate respiratory organs are present in some arthropod chelicerates, and similarities in the structure of these organs is sometimes used as an indication of evolutionary relationships. The internal book lungs of arachnids are hypothesized to have been derived from the external book gills of an ancient ancestor with respiratory organs like those of the horseshoe crab (e.g., Kassianow, 1914;Versluys and Demoll, 1923;Anderson, 1973;Dunlop, 1998).…”