Fusion of locomotor maneuvers, and improving sensory capabilities, give rise to the flexible homing strikes of juvenile zebrafish

Abstract

At 5 days post-fertilization and 4 mm in length, zebrafish larvae are successful predators of mobile prey items. The tracking and capture of 200 μm long Paramecia requires efficient sensorimotor transformations and precise neural controls that activate axial musculature for orientation and propulsion, while coordinating jaw muscle activity to engulf them. Using high-speed imaging, we report striking changes across ontogeny in the kinematics, structure and efficacy of zebrafish feeding episodes. Most notably, the discrete tracking maneuvers used by larval fish (turns, forward swims) become fused with prey capture swims to form the continuous, fluid homing strikes of juvenile and adult zebrafish. Across this same developmental time frame, the duration of feeding episodes become much shorter, with strikes occurring at broader angles and from much greater distances than seen with larval zebrafish. Moreover, juveniles use a surprisingly diverse array of motor patterns that constitute a flexible predatory strategy. This enhances the ability of zebrafish to capture more mobile prey items such as Artemia. Visually-guided tracking is complemented by the mechanosensory lateral line system. Neomycin ablation of lateral line hair cells reduced the accuracy of strikes and overall feeding rates, especially when neomycin-treated larvae and juveniles were placed in the dark. Darkness by itself reduced the distance from which strikes were launched, as visualized by infrared imaging. Rapid growth and changing morphology, including ossification of skeletal elements and differentiation of control musculature, present challenges for sustaining and enhancing predatory capabilities. The concurrent expansion of the cerebellum and subpallium (an ancestral basal ganglia) may contribute to the emergence of juvenile homing strikes, whose ontogeny possibly mirrors a phylogenetic expansion of motor capabilities.

Limitations of Neural Map Topography for Decoding Spatial Information

“…Catching performance in other fish species improves rapidly during development, mainly due to the strike speed (Drost, 1987). The hunting accuracy rate has not been thoroughly studied throughout zebrafish gestational development, but is 50% for 8 dpf larvae (Westphal and O'Malley, 2013). However, it is not clear whether it is strike speed or aiming accuracy that constrains this performance rate.…”

Automated detection of feeding strikes by larval fish using continuous high-speed digital video: a novel method to extract quantitative data from fast, sparse kinematic events

“…A very similar case is the development of a crack in solid surfaces in response to stress (Matsuyama et al, 2010), which is a highly nonlinear and unpredictable physical process that should benefit from an automatic marking of the events for the consequent analysis of, for instance, initial crack size, its location and its speed of propagation. High-speed cameras are a common tool in the study of feeding kinematics (Ferry-Graham et al, 2002;Oufiero et al, 2012;Wainwright and Bellwood, 2002;Wainwright et al, 2007Wainwright et al, , 2001Westphal and O'Malley, 2013); they are often used to record short videos (lasting a few seconds) and the analysis is usually focused on feeding kinematics and prey response. Here, we use a digital videorecording system that is geared to collect continuous high-speed videos and facilitate the unbiased identification and isolation of behavioral events in the field of view.…”

Probing the xeno-oestrogenic impact of sediment cores contaminated by the pulp and paper industry: induction of aromatase cyp19a1b in late larval zebrafish

“…The 20dpfZF instead is an actively foraging life-stage (Westphal and O'Malley 2013), still widely ecological alternative for chemical fate-based experimentation, and an authentic fish species in subtropics. While the fish early life-stage toxicity test required experimentation to end prior to 30 dph (OECD TG 210), zebrafish between 20-25 dpf (dph = 3 + dpf) age during experimentation were effectively responsive to estrogenic signals.…”