1. Introduction
American shad
(Alosa sapidissima) are an anadromous, highly migratory species native to the Atlantic coast of the United States and Canada, which historically had shad runs consisting of millions of individuals, supporting valuable commercial and recreational fisheries [
1,
2,
3,
4,
5]. The American shad is a moderately compressed fish with large green to greenish blue scales on the back, to silvery on the sides, and white on the belly. Shad have supported important fisheries in every costal state along the Atlantic coast of the United States, with the Potomac and Delaware rivers accounting for some of the largest catches [
5]. They were introduced to Pacific coast rivers, including the Sacramento, Columbia, Snake, and Willamette, as early as the 1870s [
6,
7]. Within the native range, American shad spend most of their lives (3–6 years) in the ocean, with adults migrating upstream into coastal rivers and tributaries to spawn during the spring and early summer months. Returning adults generally reach a length of 55 cm, with females usually larger than males. In late summer and fall, the recently hatched juveniles migrate downstream to the ocean, at which point they typically range in size from 7 to 15 cm [
6]. Most of these fish are iteroparous, so healthy population dynamics rely heavily on the successful downstream migration of both juveniles and adults [
6,
8].
Today, Pacific coast populations of American shad are very abundant, such as in the Columbia River where the average run in the last decade exceeded 3 million individuals and was the highest on record in 2019, with nearly 7.5 million returning adults [
9]. However, most Atlantic coast populations are declining [
10,
11,
12]. As a result, many states on the Atlantic coast have restrictions or moratoriums on American shad fishing, which prompted the development of an interstate fisheries management plan [
13,
14,
15]. Factors contributing to the decline of east coast American shad populations include overfishing, habitat loss from hydropower facilities, and pollution [
1,
6,
11,
16,
17,
18]. Low passage efficiency, impassable barriers, and delays experienced at hydropower facilities during migration may add additional energetic costs, increase avian and aquatic predation, and have significant negative effects on survival and fitness [
19,
20,
21,
22].
In addition to habitat loss, fragmentation of populations, and impeded migration, hydropower facilities can lead to injury and mortality of fish during dam passage [
23,
24]. Migrating American shad may become disorientated, and incur significant injuries, or even mortality, from passing through turbines at hydropower facilities as they travel between freshwater and marine environments [
1,
4,
19,
25]. Migratory fish species that navigate these facilities during migrations, such as American shad, are of particular concern, since they frequently encounter hydropower facilities as they travel between freshwater and marine environments [
26]. During downstream migrations, fish that become entrained in hydropower turbines may be exposed to several physical stressors including strike, rapid decompression, and shear forces [
26].
Fluid shear occurs when fish pass the interface of two masses of water moving in different directions or at different velocities. Naturally occurring shear forces pose little threat of injury to fish; however, shear forces resulting from operations of hydropower facilities, in which water velocities can change significantly over short distances, may lead to injuries including descaling, tearing or bruising of tissues, and decapitation [
27]. Locations within a hydropower facility where shear forces can exceed those naturally occurring within the river are spillways and turbines [
28], two of the more common downstream fish passage routes available for out-migrating fish. When passing through a turbine, exposure to fluid shear can vary greatly, ranging from no exposure to strain rates or acceleration events exceeding 600 s
−1 or 600 m s
−2, respectively [
29,
30]. Rapid decompression occurs when fish are exposed to a rapid decrease in pressure as fish pass the turbine runner or exit from underneath a sluice gate. The pressure through the turbine typically increases until the backside of the turbine blade is reached, at which point the pressure rapidly (<0.5 s) decreases before gradually increasing to surface pressure as fish enter the downstream channel [
31]. Pressures can range considerably between different turbine designs and even within a single turbine, depending on where the fish passes through the turbine. These pressures have been observed to range considerably, from <10 kPa absolute to well above atmospheric pressure [
29,
32]. The sudden decrease in pressure may lead to a variety of barotraumas to the fish, including swim bladder rupture, exophthalmia, and emboli or emphysema throughout the organs and tissues of the fish [
31,
33,
34]. Barotrauma injuries can result from gasses expanding within the body (explained by Boyle’s Law) or bubble formation in the blood and tissues when gas comes out of solution (explained by Henry’s Law) and can vary depending on the operating conditions of the hydropower facility and the species of fish [
31,
33,
35]. Juvenile Chinook salmon (
Oncorhynchus tshawytscha) have been observed to sufer mortality at pressure reductions as low as 50% [
31], where American eel suffered very few injuries at much greater decompression (≈90% pressure reduction) [
36] and lamprey (western brook lamprey,
Lampetra planeri and Pacific lamprey,
Entosphenus tridentatus) exhibited no physiological or behavioral response to extreme rapid decompression (>90% pressure reduction) [
24].
The objective of this study was to model the dose–response relationships for American Shad exposed to fluid shear and rapid decompression associated with downstream passage through hydropower turbines. These models make it possible to (1) estimate injury and mortality rates at hydropower facilities where the magnitude and frequency of these stressors are known, (2) provide guidelines or threshold values for turbine development and modification, and (3) guide turbine operations to reduce the likelihood that American shad are exposed to fluid shear or rapid decompression at levels likely to cause injuries or mortality. Specialized laboratory apparatuses were used to simulate exposure to fluid shear and rapid decompression on live fish. To ensure application to a wide range of known turbine designs, the apparatuses were set to expose fish to a wide range of magnitudes of each stressor. Results from exposure to fluid shear and rapid decompression were modeled to develop dose–response relationships for each stressor.
4. Discussion
Juvenile American shad were found to be susceptible to both fluid shear and rapid decompression associated with passage through hydropower turbines. Chinook salmon also migrate to the ocean as juveniles and are the only species to have been examined extensively and similarly for susceptibility to both fluid shear [
30,
37] and rapid decompression [
31]. When compared to juvenile Chinook salmon, juvenile American shad, such as those used in this study, are more susceptible (
Figure 4). Juvenile American shad tested in this study are also more susceptible to effects of shear and rapid decompression than other fish species, such as silver and yellow phase American eel (
Anguilla rostrata), juvenile lamprey (
Lampetra spp.), juvenile rainbow trout (
Oncorhynchus mykiss), and a few Australian species, which have been examined similarly [
24,
30,
34,
36]. This suggests that measures (i.e., turbine designs or operational modifications) taken to protect juvenile salmonids, or other fish species at hydropower facilities may not be sufficient to protect juvenile American shad.
Considerable progress has been made in the design of fish-friendly hydropower turbines [
26,
42]. Dose–response relationships to turbine stressors, such as those developed as part of this study, have been used to guide the development of new turbines [
43,
44]. Additionally, by providing managers and operators with these dose–response relationships, operating conditions for currently installed turbines may be set within certain parameters in hopes of reducing injury or mortality for passing fish.
Along the Atlantic Coast of the United States, within the native range of American shad, there are 343 hydropower projects located in areas in which American shad are present [
45]. The Northeast region of the United States alone has 275 of these hydropower projects, many of which are nearing the end of a Federal Energy Regulatory Commission (FERC) License [
45]. The 343 hydropower plants account for 945 turbines with an installed capacity of 11,058 MW [
45]. Though currently not federally listed, in many areas along the East Coast, American shad numbers are well below historical numbers and some runs are considered to be at an all-time low [
10,
11,
12]. If populations continue to decline, there is potential that American shad could be added to the federal list of endangered and threatened wildlife, at which point they would fall under the protection of the Endangered Species Act. If American shad become listed, the FERC licensing process for any of the hydropower projects within the East Coast would be greatly affected as FERC could potentially become liable in the result of the injury or death of any listed species as the result of a license [
46].
4.1. Fluid Shear
Scale loss and damage to the eyes and operculum are three of the most common injuries inflicted on fish exposed to fluid shear [
30] and juvenile American shad are particularly susceptible to these injuries. It is no surprise that juvenile American shad were susceptible to scale loss, as the proportionally large deciduous scales are easily shed with minimal handling. Juvenile American shad also have a relatively large operculum, which spans vertically across approximately 80% the fishes’ head. The physical shape of shad, laterally compressed with the maximum body depth occurring just posterior to the operculum, makes the operculum easily affected by fluid shear, particularly when flow velocities relative to the fish increase in a tail-to-head direction. Additionally, juvenile American shad have relatively large eyes, which protrude slightly from the head, making them easily affected by fluid shear.
4.2. Rapid Decompression
The susceptibility of a fish species to rapid decompression is greatly dependent on the type of swim bladder they possess [
31,
40]. American shad and other clupeoids are physostomous, meaning that they have a pneumatic duct that connects the swim bladder with the esophagus, which allows for the rapid expulsion of excess gas from the swim bladder. However, even physostomous fish may not be capable of venting excess gas in response to the rapid pressure reductions that occur during turbine passage [
47] When excess gas is not expelled, fish can incur mortal injuries such as swim bladder rupture, exophthalmia, and emboli and hemorrhaging in tissues [
31]. Swim bladder rupture was also classified as a mortal injury for Chinook salmon, another physostome, and the difference in susceptibility between the two species is likely a result of different swim bladder morphology, particularly a unique feature of the shad swim bladder.
The swim bladder often improves hearing capabilities in most teleost fish [
48]. This is particularly the case for American shad and other clupeids, which have an offshoot of the swim bladder that connects with the utricles of the inner ear [
49]. This morphological trait may be the reason that juvenile American shad are more likely to rupture their swim bladder as compared to juvenile Chinook salmon, and why swim bladder rupture is likely to cause mortality of American shad. If an American shad survives a swim bladder rupture, or if damage to the swim bladder occurs without rupturing, the fish may be severely impaired. The unique swim bladder appears to be specifically tuned to detect ultrasound in the range emitted by dolphins, which are a major predator of shad [
49,
50,
51,
52,
53]. Therefore, any damage to the swim bladder from rapid decompression may result in an increased susceptibility to predation.