An integrative modeling approach to elucidate suction-feeding performance

Holzman, Roi; Collar, David C.; Mehta, Rita S.; Wainwright, Peter C.

doi:10.1242/jeb.057851

Cited by 76 publications

(122 citation statements)

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“…In addition to prey concentrations, other factors appear to have critical consequences for the hydrodynamic interaction between prey and predator. These factors include the following: the size distribution of the prey and larvae (specifically their mouth size), prey escape response, and prey shape and density (mass/volume) (16,18,27). Our findings are also of relevance to the mariculture industry, where in addition to focusing on the food's nutritional properties (28, 29) the physical properties of both food and larvae should also be considered.…”

Section: China and Holzmanmentioning

confidence: 79%

“…(A) The effect of dynamically scaled size on larval feeding rates. Feeding rate (rotifers consumed per hour) significantly increased with the dynamically scaled size of the larvae [F (2,18) = 79.4, P < 0.0001], whereas no significant effect of age was observed [F (2,18) = 79.4, P > 0.40]. (B) Feeding rates generated by an encounter rate model (dashed lines) were compared with measured feeding rates (solid lines) for all dextran treatments in the three larval age groups (8 DPH, red; 13 DPH, blue; 23 DPH, green).…”

Section: Methodsmentioning

confidence: 99%

“…Analysis of covariance (ANCOVA) indicated a strongly significant dependence of feeding rate on scaled size [continuous variable; F (2,18) = 79.4, P < 0.0001, R 2 = 0.89]. However, larval age (factor) had no significant effect on feeding rate [F (2,18) = 79.4, P > 0.40]. This result remained robust to alternative calculations of the scaled size and Re numbers (SI Appendix, Table S2).…”

Section: Significancementioning

confidence: 99%

“…To mechanistically answer this question, a model describing the force exerted on prey in the suction flow was used to quantitatively define the effect of mouth size on the ability to capture escaping prey (full description of model is provided in SI Appendix). This approach [hereafter referred to as suction-induced flow field (SIFF)] treats the aquatic predator-prey encounter as a hydrodynamic interaction between a solid particle, corresponding to the prey, and the unsteady suction flows around it (18). SIFF served to quantitatively assess feeding performance for each larval size, which we define as the maximal escape force that a prey can exert and still be captured by the striking larva.…”

Section: Term Definitionmentioning

confidence: 99%

“…The expansion of the mouth generates a strong inward flow of water. This flow exerts a force on the prey, drawing it into the predator's mouth while at the same time countering possible escape responses (15)(16)(17)(18). Because of the changes in Re throughout the various stages of larval ontogeny, the hydrodynamic interaction between a solid particle (the prey) and the unsteady suction flow produced by the predator is also expected to change.…”

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confidence: 99%

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Hydrodynamic starvation in first-feeding larval fishes

China

Holzman

2014

Proc. Natl. Acad. Sci. U.S.A.

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113

102

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Larval fishes suffer prodigious mortality rates, eliminating 99% of the brood within a few days after first feeding. Hjort (1914) famously attributed this "critical period" of low survival to the larvae's inability to obtain sufficient food [Hjort (1914) Rapp P-v Réun Cons Int Explor Mer 20:1-228]. However, the cause of this poor feeding success remains to be identified. Here, we show that hydrodynamic constraints on the ubiquitous suction mechanism in first-feeding larvae limit their ability to capture prey, thereby reducing their feeding rates. Dynamic-scaling experiments revealed that larval size is the primary determinant of feeding rate, independent of other ontogenetic effects. We conclude that first-feeding larvae experience "hydrodynamic starvation," in which low Reynolds numbers mechanistically limit their feeding performance even under high prey densities. Our results provide a hydrodynamic perspective on feeding of larval fishes that focuses on the physical properties of the larvae and prey, rather than on prey concentration and the rate of encounters.larval ecology | suction feeding | biomechanics | stable ocean hypothesis S tarvation is often considered a major cause of larval fish mortality (1-6). Therefore, the ability of larvae to find and capture food is critical for their survival. Newly hatched fish subsist on a limited supply of yolk and must encounter and successfully capture food before their energy resources become depleted (3, 7). In larval fishes, prey capture success is low at first feeding [occurring 2-4 d post hatching (DPH)] but increases rapidly during early development (3, 8). Correspondingly, larvae undergo a "critical period" of high mortality rates (of up to 99%) after which survival rates increase dramatically (2, 3, 7). The critical period commonly starts at first feeding and lasts 7-10 d, although the duration may vary among species and cohorts. Despite its impact on larval growth and survival, very little is known of the mechanism that underlies this mass mortality, especially during the critical period (1-6).As a larval fish matures, the concomitant increases in its body length and swimming speed alter the outcome of the interaction between the larvae's body and the fluid around it (9, 10). In general, at small body sizes and slow flow speeds organisms experience a hydrodynamic regime of low Reynolds numbers (Re), in which viscous forces (such as drag) dominate. Larger body size and faster flow facilitate a transition into a hydrodynamic regime of higher Re, where inertial forces dominate (see glossary in Table 1 for the Re equation; ref. 10). In larval fishes, this transition was shown to affect fundamental biological processes, such as respiration, metabolism, and swimming (11)(12)(13)(14). Like many adult fishes, larval fish capture their prey using "suction feeding" (Fig. 1): they swim toward it and, when in close proximity, open their mouth while expanding the mouth cavity. The expansion of the mouth generates a strong inward flow of water. This flow exerts a force on ...

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Section: China and Holzmanmentioning

confidence: 79%

Section: Methodsmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Section: Term Definitionmentioning

confidence: 99%

mentioning

confidence: 99%

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Hydrodynamic starvation in first-feeding larval fishes

China

Holzman

2014

Proc. Natl. Acad. Sci. U.S.A.

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113

102

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References

2016

Tarpons

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Morphology of the tongue dorsal surface of gilthead seabream (Sparus aurata)

Abbate

Guerrera

Montalbano

et al. 2012

Microscopy Res & Technique

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The gilthead seabream is a food fish, one of the most frequently used in aquaculture. In the species of commercial interest, feeding in captivity is very important and this process is strictly related to the morphological characteristics of the oral cavity. The aim of this study is, using the standard procedures for light and scanning electron microscopy, to analyze the morphology of the tongue dorsal surface to show if relationships are present between the tongue morphology and the nutritional habits and choices of this farmed species. The main characteristic of the gilthead seabream oral cavity floor is the presence of an apical pouch, with, probably, a protective role mainly for the apical, free part of the tongue. Three zones, like in other teleosts, an apex, a body and a root, can be clearly distinguished. In the pouch foliate-like papillae were observed, while the whole tongue is characterized by the presence of two types of papillae, respectively with a fungiform and cylindroid aspect, both randomly distributed throughout the whole dorsal surface of the tongue. Scattered and numerous taste buds, with the typical pear-onion shape, together with small and numerous taste pores are also present, distributed throughout the tongue surface. Our results demonstrate that in the gilthead seabream important mechanic and sensory roles are carried out by specific anatomical structures. Our anatomical data could give, together with further biochemical and physiological data, an important support with the aim of improving the nutrition of aquaculture species.

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An integrative modeling approach to elucidate suction-feeding performance

Cited by 76 publications

References 67 publications

Hydrodynamic starvation in first-feeding larval fishes

Hydrodynamic starvation in first-feeding larval fishes

References

Morphology of the tongue dorsal surface of gilthead seabream (Sparus aurata)

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