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Volume 4 2016 10.1093/conphys/cov063Research articleChristine E. Verhille1, Theresa F. Dabruzzi1, Dennis E. Cocherell1, Brian Mahardja2, Frederick Feyrer3,Theodore C. Foin4, Melinda R. Baerwald2 and Nann A. Fangue1,*1Departmentof Wildlife, Fish, and Conservation Biology, University of California, Davis, CA 95616, USAof Animal Science, University of California, Davis, CA 95616, USA3US Geological Survey, California Water Science Center, Sacramento, CA 95819-6129, USA4Department of Plant Sciences, University of California, Davis, CA 95616, USA2Department*Corresponding author: Department of Wildlife, Fish, & Conservation Biology, University of California Davis, One Shields Avenue, Davis,CA 95616, USA. Tel: 1 530 752 6586. Email: [email protected] Sacramento splittail (Pogonichthys macrolepidotus) is a minnow endemic to the highly modified San Francisco Estuary ofCalifornia, USA and its associated rivers and tributaries. This species is composed of two genetically distinct populations,which, according to field observations and otolith strontium signatures, show largely allopatric distribution patterns asrecently hatched juveniles. Juvenile Central Valley splittail are found primarily in the nearly fresh waters of the Sacramentoand San Joaquin rivers and their tributaries, whereas San Pablo juveniles are found in the typically higher-salinity waters (i.e.up to 10‰) of the Napa and Petaluma Rivers. As the large salinity differences between young-of-year habitats may indicatepopulation-specific differences in salinity tolerance, we hypothesized that juvenile San Pablo and Central Valley splittail populations differ in their response to salinity. In hatchery-born and wild-caught juvenile San Pablo splittail, we found upper salinity tolerances, where mortalities occurred within 336 h of exposure to 16‰ or higher, which was higher than the uppersalinity tolerance of 14‰ for wild-caught juvenile Central Valley splittail. This, in conjunction with slower recovery of plasmaosmolality, but not ion levels, muscle moisture or gill Na ,K -ATPase activity, in Central Valley relative to San Pablo splittailduring osmoregulatory disturbance provides some support for our hypothesis of inter-population variation in salinity tolerance and osmoregulation. The modestly improved salinity tolerance of San Pablo splittail is consistent with its use of highersalinity habitats. Although confirmation of the putative adaptive difference through further studies is recommended, this mayhighlight the need for population-specific management considerations.Key words: California, cyprinid, osmoregulation, salinity, splittail, wildEditor: Steven CookeReceived 13 July 2015; Revised 17 November 2015; accepted 26 November 2015Cite as: Verhille CE, Dabruzzi TF, Cocherell DE, Mahardja B, Feyrer F, Foin TC, Baerwald MR, Fangue NA (2016) Inter-population differences insalinity tolerance and osmoregulation of juvenile wild and hatchery-born Sacramento splittail. Conserv Physiol 4: doi:10.1093/conphys/cov063.IntroductionThe Sacramento splittail (Pogonichthys macrolepidotus) is aminnow endemic to the San Francisco Estuary and its associatedrivers and tributaries in California, USA (Fig. 1). It is the onlyextant member of the Pogonichthys genus (Moyle, 2002; Moyleet al., 2004) and is composed of two genetically distinct populations referred to as the San Pablo and Central Valley populations The Author 2016. Published by Oxford University Press and the Society for Experimental Biology.This is an Open Access article distributed under the terms of the Creative Commons Attribution License h permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.1Downloaded from 4/1/cov063/2951303 by guest on 26 June 2019Inter-population differences in salinitytolerance and osmoregulation of juvenile wildand hatchery-born Sacramento splittail

Researcharticle(Baerwald et al., 2007, 2008). Although gaps remain in ourknowledge of the geographical distribution, preferred habitatand physiology of splittail, preliminary findings suggest that SanPablo larvae often hatch in higher salinities than Central Valleylarvae (Feyrer et al., 2010).Sharp declines in the abundance of many San FranciscoEstuary fish species over the last two decades have been linkedto ecosystem-wide modifications (Moyle, 2002; Feyrer et al.,2003; Kimmerer, 2004; Sommer et al., 2007; Thomas et al.,2010). These modifications include the intrusion of salinityfrom the San Francisco Bay as a consequence of climatechange and anthropogenic water consumption (Knowles andCayan, 2002; Cayan et al., 2008; Cloern and Jassby, 2012).Evidence of declines in splittail population numbers (Mengand Moyle, 1995; Feyrer et al., 2003; United States Fish andWildlife Service, 2003) resulted in federal listing of splittail asthreatened under the US Endangered Species Act (UnitedStates Fish and Wildlife Service, 1999). Although the federallisting status was remanded in 2003, splittail retain classification as a species of Special Concern by the CaliforniaDepartment of Fish and Wildlife.2Defining conservation and management plans for splittailis complicated by their complex semi-anadromous life historyand the existence of two genetically distinct populations(Baerwald et al., 2007, 2008). Highly fecund spawning adultsof both populations undergo an annual migration from thebrackish, food-rich waters of the bays and marshes of the SanFrancisco Estuary to the spawning habitats (Feyrer andBaxter, 1998). Genotyping of age-0 splittail captured in theNapa and Petaluma Rivers (i.e. putative San Pablo population) and Suisun Marsh and the Sacramento–San JoaquinDelta (i.e. putative Central Valley population) suggests a primarily allopatric spawning distribution. Spawning and yearling rearing locations of the Central Valley splittail population(Fig. 1) are thought to be restricted to the freshwater tributaries and floodplains of the Central Valley draining theSacramento and San Joaquin Rivers into the San FranciscoEstuary, including San Pablo Bay (Daniels and Moyle, 1983;Sommer et al., 1997; Moyle et al., 2004; Baerwald et al.,2007, 2008). For the San Pablo population, spawning (Fig. 1)primarily occurs in the relatively brackish Napa and PetalumaRivers (Baerwald et al., 2007, 2008). The hypothesizedspawning distributions are supported by otolith strontium signatures of splitttail captured in San Pablo vs. Central Valleyspawning locations, which show Central Valley splittail exclusively to inhabit water with salinities below 1‰ and San Pablosplittail to inhabit water of salinities up to 10‰ during thefirst 3 months of life (Feyrer et al., 2010). The differences insalinity between primary spawning/rearing habitats may suggest population-specific differences in salinity tolerance.Fish in fresh water are hyperosmotic relative to thehypoosmotic water and approach isosmotic conditions at 10‰ (reviewed by Evans, 2008). As fish enter increasinglysaline waters, they are faced with an osmoregulatory challenge where water is lost from their relatively hyposmoticblood across their gills into the hyperosmotic water (Evans,2008). Water loss, which can be compensated for throughdrinking salt water, results in increased plasma osmolalityand reduced muscle moisture; however, the ions gained mustbe excreted from the body to the external environment viathe gills and kidneys. Ionocytes, called mitochondria-richcells, are the main sites of sodium and chloride excretion infish gills (Foskett and Scheffey, 1982; Perry, 1997; Evanset al., 2005). Na ,K -ATPase (NKA) establishes the electrochemical gradients driving Na and Cl excretion at the mitochondria-rich cells and the kidneys of marine teleost fishes(Perry, 1997; Marshall, 2002). Other fish species, for exampleAtlantic killifish (Fundulus heteroclitus), distributed along anenvironmental salinity gradient display intraspecific plasticityin gene expression, plasma osmolality and ion responses toosmotic stress (Scott et al., 2004; Whitehead et al., 2011).Furthermore, salinity tolerance and physiological responsesto osmotic stress vary ontogenetically in anadromous fishes(McCormick, 1994). Thus, fish exposed to increasingly salinewaters experience ionic and osmotic disturbances, for whichthe capacity to compensate is limited and varies among lifestages and populations.Downloaded from 4/1/cov063/2951303 by guest on 26 June 2019Figure 1: The San Francisco Estuary (in California) and its associatedrivers and estuaries, with sampling locations and putative spawninglocations for the wild San Pablo and Central Valley populations ofSacramento splittail (Pogonichthys macrolepidotus). The putativespawning locations for the San Pablo splittail population are the Napaand Petaluma Rivers. The putative spawning locations for the CentralValley splittail population are Suisun Marsh, the Sacramento andAmerican Rivers and tributaries of the San Joaquin River. San Pablosplittail collections occurred in Napa and Petaluma Rivers. CentralValley splittail were collected at sites between the confluence of theAmerican and Sacramento Rivers and Suisun Marsh.Conservation Physiology Volume 4 2016

Conservation Physiology Volume 4 2016 Materials and methodsExperimental fishCapture of wild fishTwo age classes of splittail were collected at sites dispersedthroughout the habitat range (Fig. 1). Young-of-year (after50 dph) splittail were captured in beach seines or otter trawlsfrom spring to summer of 2012 and 2013. When these fishexceeded 1 year of age, they are referred to here as ‘juvenilewild splittail’. Adult splittail, referred to here as ‘adult wildsplittail’, were caught by gill netting or beach seining throughout the entire year in 2012, and spawned at the University ofCalifornia, Davis (UCD) to produce hatchery-born splittailfor salinity exposure experiments. All wild fish collections fellunder California Department of Fish and Wildlife ScientificCollecting Permit SC-11901. All wild-captured splittail wereacclimated to fresh water at UCD for at least 30 days beforesalinity exposures or spawning. Wild-captured fish were alsogenotyped to confirm their population of origin. See onlinesupplementary material for details on wild capture, transportto UCD, acclimation to UCD laboratory conditions and genotyping. All fish handling, rearing and salinity tests were performed in agreement with the UCD Institutional Animal Careand Use Committee protocol no. 16788.Larval/young-of-year hatchery-born offspringof wild-caught splittailAdult wild splittail, caught in 2012, were genotyped to confirm their population of origin and spawned at UCD following the protocols of Deng et al. (2012). Spawning attemptswere made with both San Pablo and Central Valley wildadults, but egg fertilization was only successful for the SanPablo population. The offspring of these hatchery spawns arereferred to as larval (0–49 dph), YOY (50–360 dph) orj uvenile hatchery-born San Pablo splittail, depending on theage at the time of experiments.The fertilized eggs were incubated in tanks supplied withaerated, flow-through well water at 18.5 0.5 C, with deadeggs being removed several times each day to prevent fungalinfections. Larvae were fed a continuous supply of liveArtemia salinia from 6 dph (i.e. at completion of yolk sacabsorption) until 50 dph, when they were transitioned to amix of HBH Baby Bites (HBH Pet Products Inc. Springville,UT, USA) and Artemia salinia. At 60 dph, fish were transitioned onto a mixture of HBH Baby Bites and Rangen SalmonStarter Diet, also supplied continuously throughout the day.Effects of salinity on splittail growthThe effects of salinity on growth of larval/YOY hatchery-bornsplittail of the San Pablo population were assessed from 13 to69 dph. At 12 dph, 200 splittail were randomly allocatedbetween four (50 fish per tank) 50 l static, aerated treatmenttanks equipped with a sponge filter and maintained at18.5 0.5 C. After a 24 h adjustment period in the treatmenttanks, water of two of the four tanks was gradually raised to12‰ over 6 h at a rate of 2‰ h 1 by dissolving aquarium salt(Instant Ocean, Blacksburg, VA, USA) into the tank water. The6 h salinity increase was consistent among all salinity exposures performed here, except for chronic lethal maximum andcritical salinity maximum determinations. This duration ofsalinity increase was chosen to mimic a tidal cycle of SanFrancisco Bay, where the transition from low to high tidetends to occur in 6 h. Salinity was monitored in all experiments using a calibrated light refractometer and hand-heldYSI 556 MPS (YSI, Yellow Springs, OH, USA). After the 6 hincrease, salinity was maintained at 12‰ for 56 days (untilfish reached the age of 69 dph), while the remaining two tankswere maintained at a salinity of 0.4‰ (fresh water). In orderto maintain water quality, 30% of the water volume of bothtanks was replaced daily with water of the appropriate salinity. Every 2 weeks, six fish were removed from each tank andterminally sampled for measurements of mass (in grams) andstandard length (in millimetres).Splittail salinity tolerance experimentsChronic lethal maximum of salinityThe chronic lethal maximum of salinity was assessed for YOYhatchery-born San Pablo splittail according to the protocol ofYoung and Cech (1996). At 59 dph, 150 juvenile splittail ofmean mass 0.156 0.009 g were randomly allocated betweenthree 150 l tanks (one control and two salinity test tanks) andallowed to adjust to the new tanks for 24 h. The control tankwas supplied with flow-through, aerated well water throughout the duration of the salinity test. The salinity test tanks wereconnected with a recirculation system to allow for manipulation of salinity, and both systems were maintained at 18–19 C.Beginning at 60 dph, the water salinity