Effect of Morphological Fin-Curl on the Swimming Performance and Station-Holding Ability of Juvenile Shovelnose Sturgeon

Researchers have used morphological characteristics of Acipenseriformes such as body size (Peake et al. 1997), the presence of a heterocercal caudal fin (Liao and Lauder 2000), and bony scutes (Webb 1986) to explain variation in swimming performance for sturgeon species. Sturgeon pectoral fins also play an important role in regulating swimming performance by generating lift (Wilga and Lauder 1999) and facilitating station-holding behavior (i.e., pressing of the abdomen and pectoral fins to the ground in order to conserve energy; Adams et al. 2003; Deslauriers and Kieffer 2012; Qu et al. 2013). As such, variations in the functional morphology of pectoral fins have the potential to impede the ability of a fish to cope with its environment (Schoenfuss and Blob 2007) and can ultimately lead to a reduction in recruitment for the species (Wolter and Arlinghaus 2003).

Sturgeon pectoral fin morphology can be influenced by tagging or extracting tissue for aging (Parsons et al. 2003), by erosion induced in high-density rearing environments (Latremouille 2003), by a lack of adequate nutrition, or by exposure to contaminants (Kruse and Webb 2005). Additionally, young sturgeon can develop a condition termed fin-curl (i.e., bending of the distal portion of the pectoral fin towards the body; Oldenburg et al. 2011; see Figure 1 as an example). Although we do not know the specific causes of fin-curl (K. Kappenman, USFWS, Bozeman Fish Technology Center, personal communication), its presence acts similarly to fin erosion by diminishing the total area of the pectoral fin, potentially reducing the fish's ability to station-hold or maneuver within the water column. Researchers have used altered morphology of pectoral fins (e.g., removal, clip, erosion) to explain dispersal and survival variability of various stocked salmonid species (Nicola and Cordone 1973; Mears and Hatch 1976; Petersson et al. 2013). Similarly, wider pectoral fins can enhance navigation in habitats with higher currents for fish that use labriform-type propulsion (Wainwright et al. 2002; Fulton et al. 2005).

Oldenburg et al. (2011) linked the presence of fin-curl in age-1 pallid sturgeon Scaphirhynchus albus to a reduced ability to station-hold, which in turn increased downstream dispersal since these fish were more likely to become entrained by the current. Pectoral fin deformities can develop both in hatchery (lake sturgeon Acipenser fulvescens, D. Dembkowski, University of Wisconsin-Stevens Point, personal communication) and natural environment settings (lake sturgeon, Doyon et al. 1999; white sturgeon Acipenser transmontanus, Kruse and Webb 2005). Incidences of pectoral fin deformities have been shown by Murphy et al. (2007) to affect 4% of juvenile and adult pallid and shovelnose sturgeon Scaphirhynchus platorynchus in the middle and lower Mississippi River. Fish used by Oldenburg et al. (2011) were hatched and reared at the Bozeman Fish Technology Center (BFTC 2007), where fin-curl is frequently observed among sturgeon (K. Kappenman, personal communication) and becomes apparent as soon as the fish develop pectoral fin rays (21–26 mm; Snyder 2002). Because of the ecological and social importance of sturgeon species, it is important to know if fin-curl affects the swimming performance and behavior of the fish.

The objectives of this study were to assess fin-curl severity and determine if variations in this phenotype affect the aerobic swimming performance of shovelnose sturgeon. In addition, swimming trials were conducted to explore the relationship between fin-curl severity and station-holding ability of individual fish. We hypothesized that fish with higher levels of fin-curl would have more difficulty station holding and would thus fatigue faster than fish that display milder fin-curl phenotypes.

The study population of shovelnose sturgeon hatched at the Bozeman Fish Technology Center (BFTC; U.S. Fish and Wildlife Service [USFWS]) in June 2012. We transported approximately 1,000 fish in an oxygenated tank to the Fisheries Research Unit at South Dakota State University in September 2012. We observed less than 1% mortality during transportation. Upon arrival, we placed the fish (range: 6–9 cm fork length) in a 3,000-L raceway containing recirculating, dechlorinated city water (pH ∼ 7) and reared them there for 4 mo. During this period, we observed mortality of < 5%. We fed fish ad libitum daily rations of Chironomidae larvae. Two months prior to the experiment, we randomly selected 25 fish and acclimated them to individual 40-L tanks with water at 20°C. We removed four fish from the experiment since they appeared to be sluggish and were not feeding. Thus, we performed the swimming trials using a total of 21 fish. We reared all animals used in this study according to animal use and care guidelines established by South Dakota State University (Animal Welfare Assurance no. A3958-01).

The swimming protocol followed methods established by Adams et al. (2003). We starved the fish for 48 h prior to the swimming trial to ensure a postabsorptive state. We then introduced individual fish into the swim chamber (SWIM-90, Loligosystems.com) and allowed them to acclimate for a period of 1 h. We kept water temperature within the swim chamber at 20°C using a submersible heater. Throughout the swimming trials, we never observed dissolved oxygen to decrease below 90% saturation. We set water velocity at 5 cm/s for the first 30 min, and increased it to 10 cm/s for the remainder of the acclimation period. These velocities did not induce active swimming against the current. The critical swimming test (Brett 1964) began with a 15 cm/s water velocity. We then increased water velocity by 5 cm/s increments every 30 min. We halted the trial once the fish could not hold its position and became impinged against the downstream grid for 10 s. We calculated the critical swimming speed (U_crit in cm/s) as follows:

where u₁ is the highest completed velocity throughout the test, u₂ is the velocity increment (i.e., 5 cm/s), t₁ is the time spent by the fish swimming at the fatigue velocity (i.e., time spent swimming at the noncompleted interval), and t₂ is the time interval between velocity changes (i.e., 30 min). Unlike Adams et al. (2003), we did not prod fish to encourage swimming when station holding was observed. Rather, we measured the time spent station holding (min) during each interval. Station-holding behavior began when the fish rested its abdomen and pectoral fins on the bottom of the swimming chamber while the caudal fin was not actively undulating. The behavior concluded when the fish started swimming actively against the current. Occasionally, high water velocities pushed fish downstream while station holding. We considered the station-holding behavior to end once the fish made contact with the downstream screen. We converted the critical swimming speed to a relative value by dividing U_crit by the fork length of the fish (U_crit in body lengths per second; BL/s). Once the fish had fatigued, we measured weight (to nearest 0.01 g), fork length (to nearest 1 mm), and fin-curl severity (see below) before returning the fish to the holding tank. We also calculated Fulton's condition factor (Ricker 1975) for each fish (K = weight/fork length³ ×100). We replaced water from the swim chamber after each swimming trial to avoid the accumulation of waste products.

We quantified the severity of fin-curl using the pectoral fin index (PFI; Kindschi 1987). In the absence of fin-curl, shovelnose sturgeon of a given size class display low variability in pectoral fin lengths (coefficient of variation = 7%; Murphy et al. 2007). Consequently, the PFI should adequately reflect fin-curl variability without having pectoral fin length as a cofounding factor. We calculated this index by measuring the length of the pectoral fin perpendicular to the body at the center line of the fin, then dividing the length by the fork length and multiplying by 100. To measure pectoral fin length, we took a dorsal photograph of the fish following the swimming trial. We then imported the photograph into ImageJ (Abràmoff et al. 2004), where we measured the length of both pectoral fins. We calibrated all photographs using a ruler that we had placed in proximity to the pectoral fins on the bottom of the tank.

We used relative U_crit (BL/s) instead of absolute U_crit (cm/s) to standardize for potential fish size effects. We calculated mean PFI from both fins and used this for the analysis. We performed multiple linear regression using fork length, condition factor, and PFI as independent variables and relative U_crit as the dependent variable. We did not use fish weight in the analysis due to its high level of correlation with fork length. We analyzed factors that were found to have a significant effect on relative U_crit separately, using a simple linear regression analysis. We assessed normality and homogeneity of variance using the Shapiro-Wilk and Breusch-Pagan tests, respectively. Finally, we used a random intercept linear mixed effect model (lme4 package, Bates et al. 2014) with arcsine-transformed values (percentage of time spent station holding) to assess the effect of fin-curl on station-holding ability. Water velocity, fork length, condition factor, and PFI were fixed effects while individual fish were random effects to account for repeated measures. We obtained model significance through the use of a likelihood ratio test of the full model compared to a model version without the fixed effect (fork length, condition factor, and PFI). We performed analyses using R software (R Core Team 2014).

Mean (± SD; n = 21) fish length, weight, condition factor and U_crit (absolute and relative) were 17.49 ± 1.13 cm, 15.91 ± 3.08 g, 0.30 ± 0.03 g/cm³ × 100 (condition factors were similar to those observed by Kappenman et al. 2009) and 29.80 ± 5.23 cm/s or 1.71 ± 0.29 BL/s, respectively. Multiple regression analysis showed that PFI (t-value = 2.674; P = 0.016) was the only factor significantly influencing relative U_crit (Figure 2), with fork length (t-value = −0.445; P = 0.662) and condition factor (t-value = 0.801; P = 0.434) found to have no significant effect. As such, we used a simple linear regression model to predict relative U_crit based on the PFI, which provided an increasing slope (Figure 2; F_1,19 = 8.632; P = 0.008), implying that fish displaying smaller PFI values generally swam for shorter periods of time. Lastly, the station-holding ability of shovelnose sturgeon was not impaired by fin-curl severity, fork length, or condition factor but was significantly influenced by water velocity (Figure 3; χ²(1) = 20.758, P < 0.001).

The swimming ability of juvenile shovelnose sturgeon varied with the degree of pectoral fin deformation. In fish with mild pectoral fin-curl (i.e., PFI > 8%), swimming ability, as indexed by U_crit (n = 6; 1.89 ± 0.20 BL/s), was similar to that reported by Adams et al. (2003; 1.90 BL/s) and to results for juvenile sturgeon of other species (Peake 2004; Deslauriers and Kieffer 2011). Shovelnose sturgeon in the Adams et al. (2003) study were not subjected to fin-curl because these fish originated from the Gavins Point National Fish Hatchery, where fin-curl has never been observed (J. Powell, USFWS, Gavins Point National Fish Hatchery, personal communication). Fish that had a PFI < 8% (n = 15) displayed lower U_crit values (1.64 ± 0.30 BL/s), which could result in a reduced ability to reach optimal habitat in a fragmented environment (Schoenfuss and Blob 2007). Similarly, fish displaying severe fin-curl might be more susceptible to entrainment (Hoover et al. 2011) and require additional energy to compensate for their lack of swimming ability, which in turn might lead to decreased growth rates (Rennie et al. 2005).

Station holding has been shown by Deslauriers and Kieffer (2012) to enhance swimming performance in shortnose sturgeon Acipenser brevirostrum as it is believed to act as an energy-saving mechanism. We thus hypothesized that fish with greater fin-curl severity would have more difficulty station holding (Oldenburg et al. 2011), which would then lead to a decrease in swimming performance. Contrastingly, our results indicated that station holding was similar across all fish, regardless of fin-curl severity. It would appear that the differences observed in swimming performance occurred while the fish were displaying a free-swimming behavior. It has been shown by Wilga and Lauder (1999) for white sturgeon that the angle of attack displayed by the pectoral fins significantly influences the orientation of the body, which in turns generates lift. Based on this knowledge, it is possible that shovelnose sturgeon with low PFIs have difficulty orienting their fins in order to generate lift efficiently, resulting in the early onset of fatigue. It can be hypothesized that the presence of fin-curl might limit behavioral adaptations in fluctuating energy landscapes such as a large river system (Hintz 2014), and thus act as a selective pressure against these fish.

Researchers have suggested that fin-curl could develop as a result of nutrient deficiencies, water quality attributes, or bacterial infection in hatchery settings (BFTC 2005). It is important to mention that similar phenotypes might be displayed by fish that exhibit fin erosion, which also occurs in captive settings (Latremouille 2003). Shovelnose and the closely related pallid sturgeon (i.e., Scaphirhychus spp.) are both reared for stocking purposes and are typically released as juveniles (Koch and Quist 2010; Steffensen et al. 2012). Scaphirhynchus spp. have also been released to investigate dispersal (Braaten et al. 2008) and habitat use (Jordan et al. 2006). Regardless of the release purpose (management or research), the current study has demonstrated the importance of pectoral fin integrity. Fin-curl is not typically quantified in sturgeon stocking programs although there are some indications that this phenotype is occurring in species other than pallid or shovelnose sturgeon (e.g., lake sturgeon). It is thus important that future studies take this result into consideration and avoid the release of fish demonstrating deleterious pectoral fin phenotypes.

Please note: The Journal of Fish and Wildlife Management is not responsible for the content or functionality of any supplemental material. Queries should be directed to the corresponding authors for the article.

Data S1. Raw data file containing juvenile shovelnose sturgeon Scaphirhynchus platorynchus weight (g), length (mm), condition factor (weight/fork length³ × 100), pectoral fin index, and absolute and relative critical swimming speed (cm/s and body lengths/s) used in the regression analysis. Data were collected at the Fisheries Research Unit at South Dakota State University (Brookings, South Dakota) in March 2013.

Found at DOI: http://dx.doi.org/10.3996/092015-JFWM-087.S1 (49 KB XLSX).

Data S2. Raw data file containing juvenile shovelnose sturgeon Scaphirhynchus platorynchus station holding time (% of time at a given water velocity spent station holding), along with the pectoral fin index, weight (g), length (mm), and condition factor (weight/fork length³ ×100) associated with individual fish. These data were used in the linear mixed model analysis and were recorded at the Fisheries Research Unit at South Dakota State University (Brookings, South Dakota) in March 2013.

Found at DOI: http://dx.doi.org/10.3996/092015-JFWM-087.S2 (45 KB XLSX).

Reference S1. Bates D, Maechler M, Bolker B, Walker S. 2014. lme4: Linear mixed-effects models using eigen and S4.

Found at DOI: http://dx.doi.org/10.3996/092015-JFWM-087.S3; also available at https://cran.r-project.org/web/packages/lme4/lme4.pdf (360 KB PDF).

Reference S2. [BFTC] Bozeman Fish Technology Center. 2005. Pallid sturgeon pectoral fin-curl evaluation results. Bozeman, Montana: Bozeman Fish Technology Center.

Found at DOI: http://dx.doi.org/10.3996/092015-JFWM-087.S4 (3429 KB DOC).

Reference S3. [BFTC] Bozeman Fish Technology Center. 2007. Pallid sturgeon fin-curl assessment for all year classes stocked from the Bozeman fish technology center. Bozeman, Montana: Bozeman Fish Technology Center.

Found at DOI: http://dx.doi.org/10.3996/092015-JFWM-087.S5 (45 KB PDF).

Reference S4. Hintz WD. 2014. Behavior, ecology, and conservation of Scaphirhynchus sturgeon. Doctoral dissertation, Carbondale: Southern Illinois University Carbondale.

Found at DOI: http://dx.doi.org/10.3996/092015-JFWM-087.S6 (2539 KB PDF).

Reference S5. Kruse G, Webb M. 2005. Upper Colombia white sturgeon contaminant and deformity evaluation and summary. Upper Colombia White Sturgeon Recovery Team, Contaminants Sub-Committee.

Found at DOI: http://dx.doi.org/10.3996/092015-JFWM-087.S7 (2164 KB PDF).

We thank Matt Toner and the Bozeman Fish Technology Center for providing us with the fish for this experiment. We also thank Dr. Mark Pegg for making his swim chamber available for the duration of the experiment. Lastly, we thank Kevin Kappenman, Bill Hintz, and three anonymous reviewers for providing comments that improved the manuscript.

Funding for this project has been provided by the U.S. Army Corps of Engineers (MIPR #W59XQ611641574).

Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government.