Direct Development of the Visual System of the Coral Reef Teleost, The Spiny Damsel, Acanthochromis polyacanthus

Abstract

Unlike most marine teleosts, the coral reef-dwelling spiny damsel, Acanthochromis polyacanthus, lacks a pelagic larva dispersal phase and represents one of few examples of self recruitment onto a natal reef by a marine teleost immediately after hatching. Benthic eggs are protected by the parents, and upon hatching the young remain under parental care for several months. Visual morphogenesis of spiny damsel embryos and juveniles was examined to evaluate the potential visual capabilities of the young after emergence onto the reef. The optic primordia were visible in the embryo as hollow spheres of undifferentiated neuroblasts 2 days after fertilization (daf). Visual morphogenesis proceeded rapidly thereafter in the embryo such that at hatching (between 10 and 12 daf) gross visual morphology was consistent with that reported in the majority of juvenile marine teleosts, reflecting direct development of the retina of the spiny damsel within the egg. At hatching, the outer nuclear layer comprised 2 classes of photoreceptors; cones and rods. Tangential sections of the retina revealed a square cone mosaic in which 4 double cones surrounded a single cone. This arrangement remained unchanged in all later life history intervals examined. Absolute eye size was large compared to larvae of marine pelagic spawners. Eye and lens diameters increased from 0.69 and 0.23 mm, respectively, on the day of hatching (12 daf), to 3.77 and 1.52 mm, respectively, in a fish 131 daf. Angular density of cones increased from 0.25 cones 10′ visual arc⁻¹ in an embryo 8 daf, to 1.14 cones 10′ visual arc⁻¹ in a fish 131 daf, demonstrating the potential for significant increase in spatial resolution with increasing eye size. Convergence ratios of cones to ganglion cells remained relatively constant from the time of hatching, suggesting that the determinate ganglion cell photopic receptive field was established early in development. The increase in the convergence ratios of rods: ganglion cells from 1.4 in the late stages of embryogenesis (10 daf; 2 days prior to hatching) to 4.9 in a fish 103 daf, demonstrated increasing scotopic ganglion cell receptive field size, with increasing age. This was a result of rod cell addition with growth. An increase in the angular density of rods from 0.18 rods 10′ visual arc⁻¹ in an embryo 8 daf, to 4.07 rods 10′ visual arc⁻¹ in a fish 131 daf, and the increase in mean scotopic light path-length from 13.3±1.1μm in an embryo 8 dpf, to 55±5.2 μm a fish 22 dpf, collectively indicate the potential for increasing scotopic sensitivity during growth. On the basis of visual morphology it is predicted that newly hatched spiny damsel juveniles have substantially greater visual capabilities than first feeding larvae with a pelagic dispersal phase. In addition, we propose that the developmental trajectory of the spiny damsel is different from that of pelagic dispersing larvae and does not simply reflect displacement along a common developmental continuum by an extended embryonic duration.