The interaction between suction feeding performance and prey escape response determines feeding success in larval fish

Abstract

The survival of larval marine fishes during early development depends on their ability to feed before depleting their yolk reserves. Most larval fish capture prey by expanding their mouth, generating a 'suction flow' that draws the prey into it. These larvae dwell in a hydrodynamic environment that impedes their ability to capture even non-evasive prey; however, the marine environment is characterized by an abundance of evasive prey, predominantly copepods. Copepods sense the hydrodynamic disturbance created by approaching predators and perform high-acceleration escape maneuvers. Using a 3D high-speed video system, we characterized the interaction between Sparus aurata larvae and prey from a natural zooplankton assemblage that contained evasive prey, and assessed the factors that determine the outcome of these interactions. At 8-33 days post hatching, larvae preferentially attacked large prey that was moving prior to the initialization of the strike; however, feeding success was lower for larger, more evasive prey. Thus, larvae were challenged in capturing their preferred prey. Larval feeding success increased with increasing Reynolds numbers, but decreased sharply when the prey performed an escape maneuver. The kinematics of successful strikes resulted in a shorter response time but higher hydrodynamic signature available for the prey, suggesting that strike success in our experiments was determined by brevity rather than stealth: executing a fast strike eliminated a potential escape response by the prey. Our observations of prey selectivity reveal that larval performance, rather than preferences, determines their diet during early development.

Rapid adaptive evolution of scale-eating kinematics to a novel ecological niche

“…Understanding hybrid kinematics, especially in the context of ecological novelty, is informative because: (1) impaired performance in hybrids is a form of extrinsic post-zygotic isolation between species (McGee et al, 2015;Higham et al, 2016) and (2) it can allow the decoupling of morphology, behavior and kinematics, making it easier to identify causative traits underlying performance (Holzman and Hulsey, 2017). Finally, few studies connect observed variation in kinematics to variation in whole organism feeding performance (but see: Svanbäck et al, 2002;Takeuchi et al, 2012;China et al, 2017;Sommerfeld and Holzman, 2019;Whitford et al, 2019). Making this connection is important because it can identify kinematic traits associated with performance tasks relevant to evolutionary fitness rather than simply describing phenotypic variation in kinematic traits, most of which may not be relevant to performance or fitness (Arnold, 1983;Hu et al, 2017).…”

The hydrodynamic regime drives flow reversals in suction-feeding larval fishes during early ontogeny

“…Similarly, PIV studies on adult fish have indicated a broad variation in peak flow speed for repeated strikes by the same individuals ( Day et al, 2015 ; Holzman et al, 2008 ; Jacobs and Holzman, 2018 ). Such variation was not factored into our modeling, but could contribute to explaining performance differences between similar-sized larvae ( China et al, 2017 ; Sommerfeld and Holzman, 2019 ).…”

“…Furthermore, the probability of executing successful prey-acquisition strikes increased with increasing Re ( China et al, 2017 ). Transition into higher Re also improves larval ability to capture highly evasive prey such as copepods ( Jackson and Lenz, 2016 ; Sommerfeld and Holzman, 2019 ; Yaniv et al, 2014 ).…”

Longer development provides first‐feeding fish time to escape hydrodynamic constraints

“…where l is length (in m), u is velocity (in m/s) and is kinematic viscosity (in m 2 /s). As is commonly used in the larval fish feeding literature (Krishnan, Nafi, Gurka, & Holzman, 2020;Sommerfeld & Holzman, 2019) and in our previous research on prey capture in guppies (Dial, 2016), we use swimming velocity to calculate Reynolds number.…”