1. Introduction
Fish kills caused by anthropogenic activities are commonplace in a range of aquatic habitats worldwide [
1,
2,
3]. Kills can range from minor with little to no observable effect on aquatic ecosystems, to extreme, decimating stream and river communities over vast distances [
3,
4]. Concern over fish kills is amplified when they affect valuable commercial and recreational fisheries [1–3, 5].
In many fish kill events, most of the fish killed are non-game species, including cyprinids (e.g., minnows, shiners, dace, chubs), catostomids (suckers), clupeids (shad), percids (darters), cottids (sculpin), and others [
3,
4,
6]. Although not as highly valued by the general public, these species serve important roles in community stability and energy transfer to higher trophic levels [
7,
8,
9]. Their recovery after a fish kill is just as important for overall ecosystem function as the recovery of the top-level piscivorous game fishes [
4].
Many fish species are highly mobile, and can quickly recolonize defaunated reaches after a fish kill if nearby source populations are present [
4,
5,
10,
11]. However, some species are much less mobile, greatly extending the time required for recolonization after a fish kill [
12]. Many small-bodied, non-game fish in streams and rivers are considered largely non-mobile or sedentary [
13,
14,
15], especially bottom-dwelling species such as darters and sculpins [
16,
17,
18,
19]. Individuals of these species may spend their entire lives within a short stream reach, with home ranges often spanning <30 m of stream length [
19].
The slimy sculpin (
Uranidea cognata) has the largest geographic distribution of any sculpin species in North America, spanning the breadth of Canada and extending into the northern United States and Alaska [
20,
21]. The species is restricted to coldwater streams, rivers, and lakes, often co-occurring with brook trout (
Salvelinus fontinalis) and brown trout (
Salmo trutta) [
22,
23]. In streams, it prefers clean, coarse substrates and shallow (<40 cm) water with slow (<20 cm/sec) current velocities [
24]. Due to its wide geographic range, sensitivity to a variety of anthropogenic disturbances, relatively high abundance, short life span, high reproductive output, and easy to measure biological parameters, the species has been recommended for use as a sentinel species for monitoring studies throughout the northern regions of North America [
19,
25]. Although generally considered as non-migratory with low mobility and strong site fidelity [
18], slimy sculpin can display long-range movements under certain conditions [
26,
27].
During September 2019, a fish kill resulting from organic-rich runoff after a rain event [
28,
29] occurred in a 2-km-long, spring-fed headwater reach of Garvin Brook, a coldwater trout stream in southeastern Minnesota, USA [
5]. All brook trout, brown trout, and slimy sculpin were killed, an estimated 1440 fish total [
29]. After the fish kill, brown trout within the kill reach were allowed to recover naturally via migration from downstream, unimpacted sections and reproduction by those in-migrants. Brown trout quickly repopulated the kill area, spawning within the entire kill zone less than two months after the kill [
5]. However, it was not known if the slimy sculpin population would respond similarly post-kill, given its absence of any defined spawning migration and its presumed general lack of mobility overall [
19].
The present study was initiated to examine the recovery of slimy sculpin in Garvin Brook after the September 2019 fish kill. Specifically, I examined the abilities of slimy sculpin (1) to recolonize the kill zone via upstream movements only from unimpacted downstream reaches (no unimpacted upstream source of potential colonizers), and (2) to reproduce successfully within the kill zone. These were assessed by a series of five, relative-abundance electrofishing surveys spanning three spawning seasons over a 42-month period post-kill. Surveys were conducted both within the kill zone and a similar, unimpacted reference zone downstream from the kill zone.
4. Discussion
After slimy sculpin were eliminated from a 2-km headwater reach of Garvin Brook by a fish kill in September 2019, recovery was driven by upstream movement of fish of all ages into the defaunated reach within six months after the kill, reproduction by the adult segment of the in-migrant group, and good survival of the 2020 and 2021 year classes of sculpin. Abundance recovery relative to a reference reach was achieved within six months of the kill, but age structure recovery was not accomplished until 28 months post-kill.
Instream movements by slimy sculpin usually have been characterized as minimal, with individual fish residing within a short section (<30 m) of stream for much of their lifetimes [
18,
19,
33]. Adults (especially males) move very little due to being territorial [
18,
34,
35], so instream movements usually are made by subadults seeking suitable, unoccupied habitat [
26]. However, even those movements may be very limited if habitat is plentiful and food resources are abundant [
36,
37].
In the present study, all age groups of slimy sculpin were present throughout the lower 900 m of the kill zone by the first survey date, six months post-kill. However, decreasing adult sculpin CPE with increasing distance upstream (60% decline in CPE between lowermost and uppermost sites) within the kill zone suggests that adult sculpin may still have been actively moving into that section from downstream six months after the kill. Fewer than half as many adult fish had reached the upstream site compared to the downstream site. In fact, adult sculpin continued moving into the kill zone after March 2020, with adult CPE in the kill zone nearly doubling between March and August 2020, then remaining constant through March 2021. There was no obvious dominance of one sex over the other in the adult sculpin that moved into the kill zone. In contrast, juvenile sculpin CPE did not differ throughout the kill zone, indicating that young sculpin may have been more migratory than older fish, achieving relatively similar abundances throughout the 900 m of the kill zone. These observations appear to contradict previous studies that reported very limited movements of sculpin within streams [
18,
19,
33]. However, those studies were conducted in streams with intact sculpin populations, not a system that had experienced a fish kill. Many small-bodied fishes that normally display limited mobility can quickly repopulate kill zones [
38,
39], so it should not be surprising that slimy sculpin can quickly repopulate stream habitats lacking any sculpin. In fact, even in studies where sculpin have been found to move very little, some individuals exhibited movements exceeding several hundred meters during the study periods [
18,
19,
33], suggesting that sculpin are capable of extensive movements even within more crowded habitats. Reduced movements of adult versus juvenile sculpin lend support to previous studies [
26,
27] indicating greater movement by sculpin during their first year or two followed by greatly reduced movements as adults.
There is additional support for the observation that slimy sculpin can quickly populate a stream reach where they previously were extirpated. Beginning in 2003, the Minnesota Department of Natural Resources initiated a slimy sculpin reintroduction program to stock sculpin into nine coldwater trout streams where they were lacking (likely eliminated many decades prior due to historic poor water quality), to restore an ecologically important native species and provide additional forage for existing wild trout populations [
40]. Sculpin dispersed rapidly both upstream and downstream from their reintroduction sites, and several studies subsequently examined various aspects of the reintroductions [
41,
42,
43]. Sculpin recently were reintroduced to an additional eight streams in 2022/2023 [
44]. Coincidentally, Garvin Brook (specifically the reference reach) served as one of three donor streams from which sculpin were collected to stock elsewhere [
40].
Alternatively, it is possible that slimy sculpin may not have needed to move into the kill zone to repopulate it. Instead, the September 2019 fish kill may not have been a complete kill, leaving some survivors to gradually repopulate the kill zone via subsequent reproduction. The fish kill investigation estimated that only 172 sculpin died throughout the 2-km-long kill zone [
28], an estimated density of <0.02 sculpin/m
2. Based on previous work in Garvin Brook that found sculpin present at densities >2 fish/m
2 (N. Mundahl, unpublished data), a complete fish kill may have killed over 18,000 sculpin in the identified kill zone, 100 times higher than the official count. The sculpin’s small size, cryptic coloration, and preferred rocky habitats [
19,
24] likely caused most of the dead fish to be missed during the kill count. But those rocky interstices also may have provided reduced- or no-flow microhabitats that protected some sculpin from short-term toxic stream flows moving past overhead during the September 2019 kill event [
45], allowing fish to survive an otherwise catastrophic event. However, lacking any electrofishing survey data immediately after the kill event to support these speculations, it cannot be stated with any degree of certainty that some sculpin may actually have survived the kill.
Although adult slimy sculpin CPE in the kill zone was less than 40% of that observed in the reference zone in March 2020 shortly before the onset of sculpin spring spawning, production of juvenile sculpin by those adult fish was high. During August surveys, juvenile sculpin CPE in the kill zone was two to three times greater than in the reference zone. Some of this difference may have resulted from a greater proportion of large (>100 mm TL) adult sculpin, with greater potential fecundity [
46], in the kill zone compared to the reference zone. But greater fecundity in the kill zone could have been counteracted by the significantly skewed sex ratio of adult sculpin (more females than males) within the reference zone. However, much of the higher juvenile CPE in the kill zone simply may have resulted from better survival of young sculpin due to reduced mortality from fewer potential predators (i.e., adult sculpin, brown trout) within that zone [
5,
46]. In fact, reduced numbers of potential predators of young sculpin (i.e., adult sculpin, adult brown trout) continued through the March 2021 survey period [
5]. Much of the recovery of the slimy sculpin population within the kill zone of Garvin Brook was directly the result of reproduction by the adult sculpin that migrated into the kill zone, and the subsequent growth and maturation of the 2020 and 2021 year-classes of sculpin.