Spawning Allis shad exhaust their energy stores before their egg stock

Alose-vraie
Allis shad (© Ifremer)

Semelparous animals breed once, then die. But what does “once” mean? Some species comply with the so-called big bang reproduction, such as the well named Ephemera (mayflies), which lay one clutch of eggs and die within the same night. However, many species are considered semelparous while breeding several times within a single breeding season. Semélê herself mated several times with Zeus before being thunderstruck, admittedly after (in fact before) giving birth for the first time. Allis shad is such a semelparous species. It is also a capital breeder with determinate fecundity, which means that these fish start their one-month long spawning season with finite stocks of energy and eggs. They face an optimization challenge: matching egg and energy exhaustion. It would not be adaptive for them to either squander their energy and die with unlaid eggs, or survive long after having laid their last eggs. This challenge exists for every living organism, but it is probably more meaningful to species like Allis shad, which face a particularly steep rate of energy and egg exhaustion until death.

With this in mind, we documented the schedule of spawning acts and energy consumption of a few Allis shad in the field. For this, we caught them at the Uxondoa dam on the Nivelle River (Basque Country), at the end of their upstream migration, and tagged them with accelerometers that logged data (3D acceleration + temperature + pressure) until the fish’s death. Four kinds of information were obtained from these data (Fig. 1).

Figure 1. (a) shad spawning and (b) the corresponding 3D acceleration (xyz: red, green, blue) and pressure (pink) signal. (c) Tail beats and the corrsponding wave on the z-axis. (d) Tag verticality as an indicator of fish’s roundness.

First, as the spawning act consists in the fish pair spinning for a few seconds in approximately five one-meter diameter circles while thrashing the water surface with their tail, the corresponding pattern of acceleration and hydrostatic pressure was detected to assess the number and timing of spawning acts. Second, average tail beat frequency and temperature were computed for every minute and transformed in energy expenditure, using a model built for American shad1,2. Third, the gravitational component of acceleration was used to regularly compute the angle between the tag and the vertical, an indicator of fish’s roundness. Fourth, the exact timing of death was detected as both a null dynamic acceleration indicating immobility, and a shift in gravitational acceleration indicating the fish rolled on its flank. Dead fish were retrieved, in order to collect the accelerometers and their data, and weigh the fish and their remaining oocytes.

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Fig. 2a
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Fig. 2b
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Fig. 2c

Figure 2. The schedule of spawning and energy consumption. (a) Timing of shad spawning acts in the season – each colour is a different individual. (b) Cumulated energy consumed, estimated from temperature and tail beat frequency. (c) Change in tag verticality.

On average, a shad female performed 16 spawning acts distributed in six nights each separated by four nights without spawning (Fig. 2). The timing of spawning seemed to be influenced by both the physical and social environment, since the probability of spawning during one night increased with temperature, and spawning acts within a night were temporally aggregated both intra- and inter-individually. The metabolic model fed with temperature and tail beat frequency predicted a very steep energy consumption: on average 0.19kJ.min-1, summing to 7193kJ for 26 days of spawning activity, more than American shad during their 230km and seven-week long upstream migration in the Connecticut River2. Accordingly, shad thinned rapidly, especially during nights, and lost up to 53% of their initial weight. They died on average four days after their last spawning act, retaining 80g of ovaries, while the initial weight must have been around 200g.

So, shad females seem to rapidly expend their energy while spawning, and die with a significant amount of remaining eggs. Yet, shad in the Nivelle only have to ascend 13km to reach spawning grounds. How would they manage their spawning energy after a long upstream migration in a dammed river, with warming water? This management of egg and energy stock might be crucial for population conservation3. Methodologically, this study is a further step towards the monitoring of spawning activity and related energy expenditure in the field, and the field is where we (at least some of us) like to be!

 

Read the full story on BioRXiv: https://doi.org/10.1101/436295

 

 

Cited literature:

(1) Castro-Santos, T., & Letcher, B. H. (2010). Modeling migratory energetics of Connecticut River American shad (Alosa sapidissima): implications for the conservation of an iteroparous anadromous fish. Canadian Journal of Fisheries and Aquatic Sciences, 67 (5), 806–830. doi:10.1139/F10-0
(2) Leonard, J. B. K., Norieka, J. F., Kynard, B., & McCormick, S. D. (1999). Metabolic rates in an anadromous clupeid, the American shad (Alosa sapidissima). Journal of Comparative Physiology B, 169 (4–5), 287–295. doi:10.1007/s00360005022

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