Development of the swimbladder and its innervation in the zebrafish, Danio rerio

Abstract

Many teleosts including zebrafish, Danio rerio, actively regulate buoyancy with a gas-filled swimbladder, the volume of which is controlled by autonomic reflexes acting on vascular, muscular, and secretory effectors. In this study, we investigated the morphological development of the zebrafish swimbladder together with its effectors and innervation. The swimbladder first formed as a single chamber, which inflated at 1-3 days posthatching (dph), 3.5-4 mm body length. Lateral nerves were already present as demonstrated by the antibody zn-12, and blood vessels had formed in parallel on the cranial aspect to supply blood to anastomotic capillary loops as demonstrated by Tie-2 antibody staining. Neuropeptide Y-(NPY-) like immunoreactive (LIR) fibers appeared early in the single-chambered stage, and vasoactive intestinal polypeptide (VIP)-LIR fibers and cell bodies developed by 10 dph (5 mm). By 18 dph (6 mm), the anterior chamber formed by evagination from the cranial end of the original chamber; both chambers then enlarged with the ductus communicans forming a constriction between them. The parallel blood vessels developed into an arteriovenous rete on the cranial aspect of the posterior chamber and this region was innervated by zn-12-reactive fibers. Tyrosine hydroxylase- (TH-), NPY-, and VIP-LIR fibers also innervated this area and the lateral posterior chamber. Innervation of the early anterior chamber was also demonstrated by VIP-LIR fibers. By 25-30 dph (8-9 mm), a band of smooth muscle formed in the lateral wall of the posterior chamber. Although gas in the swimbladder increased buoyancy of young larvae just after first inflation, our results suggest that active control of the swimbladder may not occur until after the formation of the two chambers and subsequent development and maturation of vasculature, musculature and innervation of these structures at about 28-30 dph.

Going with, then against the flow: evidence against the optomotor hypothesis of fish rheotaxis

“…If anything, inflation of the swim bladder should increase the probability of being carried downstream by a current, theoretically making optic flow cues more relevant, not less relevant. Moreover, it is difficult to see how the sequential inflation of the two-chambered swim bladder at approximately 4 (posterior chamber) and 17 (anterior chamber) dpf (Parichy et al, 2009;Robertson, McGee, Dumbarton, Croll, & Smith, 2007) can explain the positive-to-negative shift in the OMR between 11 and 16 dpf.…”

Sensing the strike of a predator fish depends on the specific gravity of a prey fish

“…As our measurements demonstrate (Fig.5), swim bladder inflation decreases the specific gravity of the body in zebrafish by nearly 5% (from 1.063 to 1.011) and thereby causes the body to approach neutral buoyancy. This change is correlated with an increase in the frequency of spontaneous swimming as a larva begins to forage for food (Robertson et al, 2007). The approach towards neutral buoyancy has the benefit of reducing the demand to generate propulsive forces to overcome gravity.…”

“…In zebrafish, swim bladder inflation occurs within 2days of hatching [by 4days post-fertilization (dpf)], when larvae begin to actively forage (Robertson et al, 2007;Lindsey et al, 2010). The swim bladder fills to ~5% of body volume with oxygen-rich gas that has a density that is 1000 times less than the surrounding tissue (Scholander et al, 1951;Alexander, 1966;Robertson et al, 2008;Lindsey et al, 2010).…”

PFOS affects posterior swim bladder chamber inflation and swimming performance of zebrafish larvae

“…The swim bladder of zebrafish consists of two chambers separated by a narrow duct. The posterior chamber is developed and inflated around 4 dpf and operates as a hydrostatic organ to regulate buoyancy while the anterior chamber is developed and inflated around 20 dpf and functions primarily as an acoustic resonator aiding hearing (Finney et al, 2006;Robertson et al, 2007). This study focusses on the effects of PFOS on swim bladder development during the embryonic and larval stages.…”