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

Westphal RE, O'Malley DM - Front Neural Circuits (2013)

Bottom Line: At 5 days post-fertilization and 4 mm in length, zebrafish larvae are successful predators of mobile prey items.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Natural Sciences, North Shore Community College Lynn, MA, USA.

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.

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Changes in zebrafish morphology and predatory behavior across ontogeny. Four developmental stages (early larval, late larval, juvenile, and adult) are defined based upon total length, which defines the start of each stage. Each stage is accompanied by a representative image of a fish and the typical age at which it begins. Zebrafish develop gradually, i.e., without a distinct metamorphosis, but major changes in body form occur throughout these stages, including changes to fins, bones and body form. Morphological change is accompanied by behavioral changes, which are summarized. The early larval micrograph is courtesy of Dr. Edward Devlin.
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Figure 1: Changes in zebrafish morphology and predatory behavior across ontogeny. Four developmental stages (early larval, late larval, juvenile, and adult) are defined based upon total length, which defines the start of each stage. Each stage is accompanied by a representative image of a fish and the typical age at which it begins. Zebrafish develop gradually, i.e., without a distinct metamorphosis, but major changes in body form occur throughout these stages, including changes to fins, bones and body form. Morphological change is accompanied by behavioral changes, which are summarized. The early larval micrograph is courtesy of Dr. Edward Devlin.

Mentions: Many physiological, morphological and behavioral changes occur throughout zebrafish ontogenesis (see e.g., Nüsslein-Volhard and Dahm, 2002; Webb and Shirey, 2003; Ghysen and Dambly-Chaudière, 2004; Hernández et al., 2005; Larson et al., 2006; Bae et al., 2009; Valente et al., 2012), with especially substantial growth from the age of first predation (about 5 dpf) to the late juvenile stage (summarized in Figure 1). One of the most conspicuous morphological developments is differentiation of the fins. Larval fish hatch with a single primordial fin fold which is eventually replaced by the caudal, dorsal, and anal fins (Nüsslein-Volhard and Dahm, 2002; McHenry and Lauder, 2006; Danos and Lauder, 2007). Concurrently, the paired pectoral fins develop from a simple endoskeletal disc to a more complex fin, including twelve actinotrichia (fin rays) in each of the bilateral pectoral fins. This is accompanied by the differentiation of pectoral fin-associated muscles and neurons (Thorsen and Hale, 2005, 2007; Green and Hale, 2012). In addition to these changes in the appendicular skeleton and associated musculature, the jaw is also gaining new function: premaxillary protrusion is facilitated by the ossification of the kinethmoid bone during late larval developmental (Hernández, 2000; Hernández et al., 2002; Staab and Hernández, 2010). Moreover, the body form is becoming more streamlined (McHenry and Lauder, 2006).


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

Westphal RE, O'Malley DM - Front Neural Circuits (2013)

Changes in zebrafish morphology and predatory behavior across ontogeny. Four developmental stages (early larval, late larval, juvenile, and adult) are defined based upon total length, which defines the start of each stage. Each stage is accompanied by a representative image of a fish and the typical age at which it begins. Zebrafish develop gradually, i.e., without a distinct metamorphosis, but major changes in body form occur throughout these stages, including changes to fins, bones and body form. Morphological change is accompanied by behavioral changes, which are summarized. The early larval micrograph is courtesy of Dr. Edward Devlin.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3675323&req=5

Figure 1: Changes in zebrafish morphology and predatory behavior across ontogeny. Four developmental stages (early larval, late larval, juvenile, and adult) are defined based upon total length, which defines the start of each stage. Each stage is accompanied by a representative image of a fish and the typical age at which it begins. Zebrafish develop gradually, i.e., without a distinct metamorphosis, but major changes in body form occur throughout these stages, including changes to fins, bones and body form. Morphological change is accompanied by behavioral changes, which are summarized. The early larval micrograph is courtesy of Dr. Edward Devlin.
Mentions: Many physiological, morphological and behavioral changes occur throughout zebrafish ontogenesis (see e.g., Nüsslein-Volhard and Dahm, 2002; Webb and Shirey, 2003; Ghysen and Dambly-Chaudière, 2004; Hernández et al., 2005; Larson et al., 2006; Bae et al., 2009; Valente et al., 2012), with especially substantial growth from the age of first predation (about 5 dpf) to the late juvenile stage (summarized in Figure 1). One of the most conspicuous morphological developments is differentiation of the fins. Larval fish hatch with a single primordial fin fold which is eventually replaced by the caudal, dorsal, and anal fins (Nüsslein-Volhard and Dahm, 2002; McHenry and Lauder, 2006; Danos and Lauder, 2007). Concurrently, the paired pectoral fins develop from a simple endoskeletal disc to a more complex fin, including twelve actinotrichia (fin rays) in each of the bilateral pectoral fins. This is accompanied by the differentiation of pectoral fin-associated muscles and neurons (Thorsen and Hale, 2005, 2007; Green and Hale, 2012). In addition to these changes in the appendicular skeleton and associated musculature, the jaw is also gaining new function: premaxillary protrusion is facilitated by the ossification of the kinethmoid bone during late larval developmental (Hernández, 2000; Hernández et al., 2002; Staab and Hernández, 2010). Moreover, the body form is becoming more streamlined (McHenry and Lauder, 2006).

Bottom Line: At 5 days post-fertilization and 4 mm in length, zebrafish larvae are successful predators of mobile prey items.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Natural Sciences, North Shore Community College Lynn, MA, USA.

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.

Show MeSH
Related in: MedlinePlus