On the edge of death: Rates of decline and lower thresholds of biochemical condition in food-deprived fish larvae and juveniles

Meyer, Stefan; Caldarone, Elaine M.; Chı́charo, Maria Alexandra; Clemmesen, Catriona; Faria, Ana M.; Faulk, Cynthia K.; Folkvord, Arild; Holt, G. Joan; Høie, Hans; Kanstinger, Philipp; Malzahn, Arne M.; Moran, Damian; Petereit, Christoph; Støttrup, Josianne; Peck, Myron A.

doi:10.1016/j.jmarsys.2011.09.010

Cited by 40 publications

(27 citation statements)

References 66 publications

(78 reference statements)

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“…For example, selection for larger larvae, larvae with larger mouths, and the use of smaller prey should increase larval feeding rates, and perhaps reduce starvation-induced mortality. Mortality during the critical period, identified by Hjort (1914) a century ago (1), was originally attributed to the inability of the larvae to find food in sufficient quantities, leading to larval starvation (1,8,30,31). Although alternative hypotheses have been suggested to explain the variability seen in larval survival and recruitment, starvation is still widely considered a major agent of mortality in larval fishes (5,30,32).…”

Section: China and Holzmanmentioning

confidence: 99%

Hydrodynamic starvation in first-feeding larval fishes

China

Holzman

2014

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

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: 99%

Hydrodynamic starvation in first-feeding larval fishes

China

Holzman

2014

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

113

102

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“…Nucleic acid ratios however provide a point-in-time and potentially unbiased measure of individual condition and growth. Moreover, RNA:DNA ratios are strongly related to starvation across a variety of larval fish species (e.g., Meyer et al, 2012) and could potentially provide an index of imminent starvation mortality, a primary source of natural larval mortality.…”

Section: Introductionmentioning

confidence: 99%

A review and assessment of the potential use of RNA:DNA ratios to assess the condition of entrained fish larvae

Foley

Bradley

Höök

2016

Ecological Indicators

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a b s t r a c tIn rivers, lakes, and other aquatic systems throughout the world, intake pipes withdraw huge volumes of water for industrial purposes, including power plant cooling. During this process, large numbers of small-bodied, early life-stages of fish are pulled into pipes (i.e., entrained) and may be subjected to physical, thermal and chemical stress. As a result of such entrainment, these organisms can suffer direct or indirect mortality. However, given that the vast majority of larval fish are likely to die during early life due to natural processes, it is not obvious that entrainment-related mortality will have a strong influence on subsequent adult population sizes. The ability to evaluate if larval fish are dead on arrival, moribund, or in poor condition (i.e., likely to die through natural processes) at the time of entrainment could shed light on likely population-level impacts. To this end, we review the potential use of RNA:DNA ratios to index condition of entrained larval fish. Through a meta-analysis of published research studies, we demonstrate that RNA:DNA ratios of larval fish are responsive to starvation stress, with effect size increasing with duration of starvation. We relate these results to a surrogate measure of irreversible long-term negative impacts to fish populations, and demonstrate that the timescale over which RNA:DNA ratios respond to stress may not be long enough to reflect before-and-after entrainment stress. We also highlight the diverse factors contributing to variation of RNA:DNA ratios, including methodological, ontogenetic, and thermal influences. We believe that the need to account for these influences when comparing among RNA:DNA values limits the utility of broadly using RNA:DNA ratios to evaluate entrainment effects. However, the method shows promise as a quick and efficient means of determining fish condition and, used in proper context (e.g., specific to a given set of environmental conditions; in conjunction with other assessment techniques), may provide a powerful tool in assessing the effects of entrainment on fish populations. Assuming that researchers can account for sources of background variation, RNA:DNA analyses may be most useful for assessing the condition of fish larvae susceptible to entrainment (i.e., physically in the vicinity of the water intake) and/or evaluating whether fish larvae are likely to die from natural processes independent of entrainment.

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“…Embryos hatching asynchronously to this natural increase in food supply may therefore experience low survival. Under typical incubation temperatures of between 0.5 and 1.58C, growth stimulation in the range of the 8-10% we observed would be equivalent to hatching several weeks early (31), a meaningful difference given the vulnerability of lake whitefish hatchlings to starvation (43)(44)(45).…”

Section: Discussionmentioning

confidence: 80%