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(Myoxocephalus Scorpius) in Reduced Salinity

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Journal of Comparative Physiology B (2021) 191:301–311 https://doi.org/10.1007/s00360-020-01336-8 ORIGINAL PAPER Energetic savings and cardiovascular dynamics of a marine euryhaline fsh (Myoxocephalus scorpius) in reduced salinity Erika Sundell1 · Daniel Morgenroth1 · Andreas Ekström1 · Jeroen Brijs2 · Michael Axelsson1 · Albin Gräns3 · Erik Sandblom1 Received: 12 October 2020 / Revised: 18 November 2020 / Accepted: 12 December 2020 / Published online: 4 February 2021 © The Author(s) 2021 Abstract Few studies have addressed how reduced water salinity afects cardiovascular and metabolic function in marine euryhaline fshes, despite its relevance for predicting impacts of natural salinity variations and ongoing climate change on marine fsh populations. Here, shorthorn sculpin (Myoxocephalus scorpius) were subjected to diferent durations of reduced water salinity from 33 to 15 ppt. Routine metabolic rate decreased after short-term acclimation (4–9 days) to 15 ppt, which corresponded with similar reductions in cardiac output. Likewise, standard metabolic rate decreased after acute transition (3 h) from 33 to 15 ppt, suggesting a reduced energetic cost of osmoregulation at 15 ppt. Interestingly, gut blood fow remained unchanged across salinities, which contrasts with previous fndings in freshwater euryhaline teleosts (e.g., rainbow trout) exposed to diferent salinities. Although plasma osmolality, [Na+], [Cl−] and [Ca2+] decreased in 15 ppt, there were no signs of cellular osmotic stress as plasma [K+], [hemoglobin] and hematocrit remained unchanged. Taken together, our data suggest that shorthorn sculpin are relatively weak plasma osmoregulators that apply a strategy whereby epithelial ion transport mecha- nisms are partially maintained across salinities, while plasma composition is allowed to fuctuate within certain ranges. This may have energetic benefts in environments where salinity naturally fuctuates, and could provide shorthorn sculpin with competitive advantages if salinity fuctuations intensify with climate change in the future. Keywords Cardiovascular · Metabolic rate · Marine · Euryhaline · Salinity variability Introduction predicted to become more extreme in the future due to cli- mate change resulting in, e.g., longer periods of exacerbated Many coastal marine environments are characterized by drought and evaporation, increased freshwater run-of due to large fuctuations in water salinity, which challenges the altered precipitation patterns, and a more intensifed mixing osmotic homeostasis of animals inhabiting these environ- of water layers due to changing wind conditions (Durack ments. Moreover, alterations in environmental salinity are et al. 2012; IPCC 2019; Zika et al. 2018). This will be par- ticularly pronounced in shallow bays and estuaries, as these areas already experience pronounced variations in salinity Communicated by B. Pelster. (Bindof et al. in press; Held and Soden 2006; IPCC 2013). Supplementary Information The online version contains Since environmental salinity impacts a wide range of supplementary material available at https ://doi.org/10.1007/s0036 biological processes and physiological functions, abrupt 0-020-01336 -8. changes in salinity require aquatic animals such as marine * Erika Sundell fshes to either migrate to more favorable conditions, or to [email protected] acclimate their physiology to maintain homeostasis (Kultz 2015). Consequently, salinity changes can lead to local alter- 1 Department of Biological and Environmental Sciences, ations in species distribution, as well as changes in the struc- University of Gothenburg, Gothenburg, Sweden ture of ecosystems (Smyth and Elliot 2016). Nonetheless, to 2 Institute of Marine Biology, University of Hawai’i at Mānoa, assess how coastal marine fshes adjust to transient decreases Honolulu, USA in salinity, and to make predictions about future ecological 3 Department of Animal Environment and Health, Swedish implications of increased salinity variations, there is a need University of Agricultural Sciences, Gothenburg, Sweden Vol.:(0123456789)1 3 302 Journal of Comparative Physiology B (2021) 191:301–311 to understand the energetic consequences and underlying water (i.e., freshwater). Even so, empirical data are confict- physiological responses governing salinity tolerance of fsh. ing concerning the correlation between the energetic costs of In this study, we used the shorthorn sculpin (Myoxocephalus osmoregulation and environmental salinity (Ern et al. 2014). scorpius) as a model to evaluate the efect of reduced salinity From a metabolic point of view, this knowledge gap com- on cardiorespiratory function in a marine euryhaline teleost. plicates predictions about the success of fshes in a future The shorthorn sculpin is a relatively stationary demersal with more intense salinity fuctuations (Kultz 2015; Morgan species that inhabits a variety of coastal habitats, including and Iwama 1998). estuaries (Bone and Moore 2008; Coad and Reist 2004), The cardiovascular system drives tissue convection of and is known to tolerate salinities down to at least ~ 11.5 ppt water, ions, respiratory gases, nutrients, waste products and (Foster 1969; Oikari 1978a, b). The population of shorthorn hormones (Sandblom and Gräns 2017). Changes in cardio- sculpin examined here were collected from an area on the vascular physiology are, therefore, crucial for coping with Swedish west coast where the salinity regularly fuctuates changing salinities. In rainbow trout, both acute exposure between full-strength seawater of ~ 33 ppt and down to ~ 20 and chronic acclimation to increased salinity coincides with ppt within a few hours (Fig. 1). a suite of marked cardiovascular adjustments. Importantly, a Previous studies on other euryhaline fshes such as rain- twofold increase in gut blood fow occurs in seawater (Brijs bow trout (Oncorhynchus mykiss) have shown that a trans- et al. 2015, 2016a), which likely serves to increase the con- fer from freshwater to seawater involves an upregulation of vective transport of absorbed ions and water away from the active intestinal ion transport mechanisms and increased intestine to their respective sites for utilization or excretion drinking rates to sustain the elevated demand for intesti- (Brijs et al. 2015, 2016a; Farrell et al. 2009). The elevated nal water absorption, which is necessary to compensate for gut blood fow is likely explained by a reduced gut vascular osmotic water loss to the hypersaline environment (Brijs resistance (Sundell et al. 2018), and a sustained increase in et al. 2015; Fuentes et al. 1997; Grosell 2013). This pro- cardiac output and stroke volume (Brijs et al. 2015, 2016a; cess involves increased intestinal epithelial Na+/K+-ATPase Sundell et al. 2018). These responses are associated with a activity that creates a trans-epithelial Na + gradient driving plastic restructuring of the heart, where the proportion of osmotic uptake of water into the blood (Grosell 2010; Whit- compact myocardium of the ventricle increases (Brijs et al. tamore 2012). Increased trans-epithelial transport of ions 2016b). Thus, while the cardiovascular responses of eury- has been suggested to be refected in an elevated standard haline fshes to increased salinity has been extensively char- metabolic rate (SMR), which is typically defned as the acterized (Brijs et al. 2015, 2016a, b; Maxime et al. 1991; minimal aerobic energy required by an animal to maintain Morgenroth et al. 2019; Olson and Hoagland 2008; Sundell basal homeostatic processes (Chabot et al. 2016; Ern et al. et al. 2018), virtually nothing is known about the cardiovas- 2014). Thus, the magnitude of the overall energy expendi- cular mechanisms governing tolerance to reduced salinity ture associated with osmoregulation should depend on the in marine teleosts. Indeed, knowledge about the combined osmotic gradient between the fsh and its environment, and cardiovascular and metabolic responses would shed light thus theoretically, osmoregulation in water iso-osmotic to onto how marine fshes cope with transient reductions in the blood plasma (i.e., ~ 10ppt) should be less energetically salinity, as well as potential physiological benefts and trade- costly than both hyper- (i.e., seawater) and hypo-osmotic ofs when environmental salinity fuctuates. Animal collection 35 25 a b 20 Te mperature ) 30 ppt 15 ( 25 10 ( ° Salinity 20 C) 5 150 0 Oct-17 Jan-18 Apr-18Jul-18Oct-18Jan-19 Fig. 1 Geographical location and environmental characteristics of ity (solid pink line) and temperature (hatched gray line) of the water the Gullmarsforden area where shorthorn sculpin (Myoxocephalus body within Gullmarsforden measured at 6 m depth between October scorpius) were collected. a The specifc area from which shorthorn 2017 and January 2019 near to where shorthorn sculpin were caught sculpin were caught within the Gullmarsforden (hatched ellipse) (the period for animal collection is indicated by the horizontal bar in on the Swedish west coast (square within inset map). b Mean salin- panel b). Logged data were unavailable during the two blank periods 1 3 Journal of Comparative Physiology B (2021) 191:301–311 303 In the present study, we measured routine metabolic rate Table 1 Morphological characteristics of Shorthorn sculpin (Myoxo- (RMR) and cardiovascular responses (i.e., cardiac output, cephalus scorpius) heart rate, stroke volume and gut blood fow) in shorthorn Experiment 1 Experiment 2 sculpin surgically instrumented with blood fow probes in full- 33 ppt 15 ppt 33 ppt 15 ppt strength
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