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Species-Specific Effects of Turbidity on the Physiology of Imperiled Blackline Shiners Notropis Spp. in the Laurentian Great Lakes

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Species-Specific Effects of Turbidity on the Physiology of Imperiled Blackline Shiners Notropis Spp. in the Laurentian Great Lakes Vol. 31: 271–277, 2016 ENDANGERED SPECIES RESEARCH Published November 28 doi: 10.3354/esr00774 Endang Species Res OPENPEN ACCESSCCESS Species-specific effects of turbidity on the physiology of imperiled blackline shiners Notropis spp. in the Laurentian Great Lakes Suzanne M. Gray1,4,*, Laura H. McDonnell1, Nicholas E. Mandrak2, Lauren J. Chapman1,3 1Department of Biology, McGill University, Montreal, QC H3A 1B1, Canada 2Department of Biological Sciences, University of Toronto Scarborough, Toronto, ON M1C 1A4, Canada 3Wildlife Conservation Society, Bronx, NY 10460, USA 4Present address: School of Environment and Natural Resources, The Ohio State University, Columbus, OH 43210, USA ABSTRACT: Increased sedimentary turbidity associated with human activities is often cited as a key stressor contributing to the decline of fishes globally. The mechanisms underlying negative effects of turbidity on fish populations have been well documented, including effects on behavior (e.g. visual impairment) and/or respiratory function (e.g. clogging of the gills); however, the long- term physiological consequences are less well understood. The decline or disappearance of sev- eral blackline shiners Notropis spp. in the Laurentian Great Lakes has been associated with increased turbidity. Here, we used non-lethal physiological methods to assess the responses of 3 blackline shiners under varying degrees of threat in Canada (Species at Risk Act; pugnose shiner N. anogenus: endangered; bridle shiner N. bifrenatus: special concern; blacknose shiner N. het- erolepis: common) to increased turbidity. Fish were exposed for 3 to 6 mo to continuous low levels of turbidity (~7 nephelometric turbidity units, NTU). To test for effects on respiratory function, we measured both resting metabolic rate (RMR) and critical oxygen tension (the oxygen partial pres- sure at which the RMR of fish declines). No change in RMR was detected across species or in clear versus turbid treatments. However, critical oxygen tensions were negatively affected by long- term exposure to low levels of sedimentary turbidity in the 2 imperiled species, viz. pugnose and bridle shiner, but not in the more common blacknose shiner. Variation in effects of turbidity on res- piratory performance suggests differential sensitivity to turbidity, which may contribute to the cur- rent conservation status of the 3 species. KEY WORDS: Sedimentary turbidity · Critical oxygen tension · Resting metabolic rate · Conservation physiology · Pugnose shiner · Bridle shiner · Blacknose shiner INTRODUCTION agriculture, and urbanization are pushing turbidity (suspended particulates) levels over natural ranges The loss of aquatic biodiversity globally is ubiqui- for prolonged periods (Kemp et al. 2011). Increased tous, but the underlying mechanisms driving species turbidity, and associated stressors on aquatic systems declines are not always well understood. This knowl- such as decreased dissolved oxygen and increased edge is necessary for assessing critical habitat needs temperature, have been correlated with the loss of of imperiled species to facilitate their conservation many freshwater fishes (Ricciardi & Rassmusen 1999, and restoration (Rosenfeld & Hatfield 2006). In Donohue & Garcia Molinos 2009); however, less is aquatic habitats, increases in sediment flux associ- known about the ways in which increased turbidity ated with human activities including deforestation, influences fitness. Sublethal behavioral and physio- © The authors 2016. Open Access under Creative Commons by *Corresponding author: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 272 Endang Species Res 31: 271–277, 2016 logical experiments can be used to determine the ration. In the endangered pugnose shiner, fish accli- direct effects of environmental stressors, such as tur- mated to turbid waters had a lower critical swimming bidity, on individual fish (Newcombe & MacDonald speed relative to clear-water-acclimated fish, suggest- 1991), providing managers with the evidence needed ing a decline in aerobic capacity (Gray et al. 2014). to implement recovery actions. Spotfin chub Erimonax monachus juveniles held at Increased sedimentary turbidity can directly affect ~55 NTU displayed extensive gill damage and re- fish through changes in behavior associated with re- duced specific growth rate after only 21 d of exposure duced visual abilities (e.g. foraging and predator− to sedimentary turbidity (Sutherland & Meyer 2007). prey relationships, reviewed by Collins et al. 2011); The mechanism of reduced growth rate was specu- loss of mating opportunities (e.g. Candolin et al. lated to be associated with reduced feeding efficiency 2007); gill damage (e.g. Sutherland & Meyer 2007); and impaired respiration. A decrease in respiratory and reduction in swimming performance (Gray et al. efficiency may also be reflected in changes in meta- 2014), growth (e.g. Sutherland & Meyer 2007), and bolic rate and the ability to regulate metabolism in re- survival (e.g. egg-smothering, Gray et al. 2012). sponse to changes in the environment. In fishes, rest- However, less is known about the direct influence of ing or routine metabolic rate (RMR; measured when long-term exposure on the underlying physiological the fish is completely at rest; Brett 1964) is an indicator processes that might hinder growth and survival, of the amount of energy required for maintenance; such as oxygen uptake and metabolism. Here, we thus, an elevated RMR results in a higher energy de- investigated effects of long-term (>3 mo) exposure to mand for any activity in addition to maintenance. low levels (~7 nephelometric turbidity units, NTU) of RMR varies inter- and intra-specifically in ectothermic sedimentary turbidity on 3 blackline shiner species fishes experiencing different environmental condi- (Notropis spp.) from the Laurentian Great Lakes, 2 of tions (e.g. McDonnell & Chapman 2015, Metcalfe et which are imperiled (Gray et al. 2014) and have dis- al. 2016). For example, under hypoxic conditions (i.e. appeared from historically clear, but now turbid, low dissolved oxygen concentration), some fishes re- waters (Holm & Mandrak 2002). duce their metabolic rates to decrease oxygen de- Several blackline shiners have declining or extir- mands (Chapman 2015). Therefore, if suspended sed- pated populations: these small, rare minnows are typi- iments cause abrasion or clogging of the gills, fish cally found in clear, heavily vegetated, shallow areas may reduce their metabolic rate to compensate for re- and are notably absent from sites with increased tur- duced efficiency of oxygen uptake. Many fish are bidity (Trautman 1981, Holm & Mandrak 2002). Pug- oxyregulators, maintaining a stable rate of oxygen nose shiner N. anogenus is listed as ‘endangered’ un- consumption (VO2) over a wide range of dissolved der the Canadian Species at Risk Act (Holm & oxy gen (DO) levels until reaching their critical oxy - Mandrak 2002), and the bridle shiner N. bifrenatus is gen tension (Pcrit) beyond which VO2 becomes oxy- considered of ‘special concern.’ The congeneric black - gen-dependent, decreasing as DO declines (Ultsch et nose shiner N. heterolepis is considered threatened in al. 1978). If respiratory function is compromised (e.g. several US states but is not imperiled in Canada. Pug- due to gill clogging or damage), then we expect Pcrit to nose and bridle shiners are typically found in water be higher, reflecting increased cost of oxygen uptake. with <2.0 NTU (Gray et al. 2014) and are absent from Here, we provide a direct test of the influence of more turbid waters (Trautman 1981, Trebitz et al. prolonged exposure to low levels of sedimentary tur- 2007). In a previous study (Gray et al. 2014), we found bidity on the physiology of 2 imperiled, and 1 more significant differences in schooling behavior between common, blackline shiners. We acclimated wild- clear- and turbid-acclimated fish, with fewer pugnose caught fish to either clear or low turbidity conditions and bridle shiners schooling as turbidity increased for several months and then tested for differences in compared to no change in behavior in several other RMR and Pcrit between and among treatments and species, including blacknose shiner. Additionally, we species. found species-specific variation in swimming per- formance, an indicator of aerobic metabolism (Brett 1964), associated with turbidity acclimation only in the MATERIALS AND METHODS 2 most imperiled shiners. The ability of fishes to uptake dissolved oxygen over sensitive gill structures Fish collection and maintenance is essential to their survival; therefore, damage to gills caused by abrasive particulates or clogging of the gills Adults of 3 species (n ~40 of each species) were is expected to decrease the efficiency of aerobic respi- collected from the St. Lawrence River, between Gray et al.: Physiological responses to turbidity 273 Gananoque (44° 24’ 42’’ N, 75° 53’ 37’’ W) and Corn- and a separate temperature regulation unit. The wall (45° 0’ 4’’ N, 74° 41’ 8’’ W), Ontario, Canada, be - glass chamber was 149.0 ml in volume, 4.5 cm in tween September and November 2011. Pugnose and diameter and 7.8 cm in length, contributing to a total bridle shiners were collected from a clear (<2.0 NTU system water volume of 157.0 ml. When the system is over 3 sampling years; Gray et al. 2014), heavily veg- open (on ‘Flush’ setting) the glass chamber is
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