PUBLICATIONS Water Resources Research RESEARCH ARTICLE Life in a fishbowl: Prospects for the endangered Devils Hole 10.1002/2014WR015511 pupfish (Cyprinodon diabolis) in a changing climate Special Section: Mark B. Hausner1,2,3, Kevin P. Wilson4, D. Bailey Gaines4, Francisco Suarez 2, G. Gary Scoppettone5, Eco-hydrology of Semiarid and Scott W. Tyler1 Environments: Confronting Mathematical Models with 1Department of Geological Sciences and Engineering, University of Nevada, Reno, Nevada, USA, 2Departamento de Ecosystem Complexity Ingenierıa Hidraulica y Ambiental, Pontificia Universidad Catolica de Chile, Santiago, Chile, 3Division of Hydrologic Sciences, Desert Research Institute, Las Vegas, Nevada, USA, 4Pahrump Field Office, Death Valley National Park, Pahrump, 5 Key Points: Nevada, USA, Western Fisheries Research Center, United States Geological Survey, Reno, Nevada, USA Numerical simulations predict habitat temperatures under climate scenarios Abstract The Devils Hole pupfish (Cyprinodon diabolis) is a federally listed endangered species living Combining CFD with ecological solely within the confines of Devils Hole, a geothermal pool ecosystem in the Mojave Desert of the Ameri- modeling quantifies impacts of climate change can Southwest. This unique species has suffered a significant, yet unexplained, population decline in the Devils Hole is an indicator of changes past two decades, with a record low survey of 35 individuals in early 2013. The species survives on a highly expected in similar arid ecosystems variable seasonal input of nutrients and has evolved in a thermal regime lethal to other pupfish species. The short lifespan of the species (approximately 1 year) makes annual recruitment in Devils Hole critical to the Correspondence to: persistence of the species, and elevated temperatures on the shallow shelf that comprises the optimal S. W. Tyler, [email protected] spawning habitat in the ecosystem can significantly reduce egg viability and increase larval mortality. Here we combine computational fluid dynamic modeling and ecological analysis to investigate the timing of Citation: thresholds in the seasonal cycles of food supply and temperature. Numerical results indicate a warming cli- Hausner, M. B., K. P. Wilson, D. B. mate most impacts the heat loss from the water column, resulting in warming temperatures and reduced Gaines, F. Suarez, G. Gary Scoppettone, buoyancy-driven circulation. Observed climate change is shown to have already warmed the shallow shelf, and S. W. Tyler (2014), Life in a fishbowl: Prospects for the and climate change by 2050 is shown to shorten the window of optimum conditions for recruitment by as endangered Devils Hole pupfish much as 2 weeks. While there are many possible reasons for the precipitous decline of this species, the (Cyprinodon diabolis) in a changing changing climate of the Mojave region is shown to produce thermal and nutrient conditions likely to reduce climate, Water Resour. Res., 50, 7020– 7034, doi:10.1002/2014WR015511. the success of annual recruitment of young C. diabolis in the future, leading to continued threats to the sur- vival of this unique and enigmatic species. Received 25 FEB 2014 Accepted 7 AUG 2014 Accepted article online 11 AUG 2014 Published online 27 AUG 2014 1. Introduction Global climate change is expected to cause major shifts in distributions of flora and fauna [Warren et al., 2013]. However, endemic species in very restricted and specialized environments are unable to move to more favorable climatic conditions and must therefore adapt or die in their respective restricted habitats. One such habitat is Devils Hole (36.42N, 115.28W), a groundwater-fed pool ecosystem in the Mojave Desert of the American Southwest that is home to the only extant population of Devils Hole pupfish (Cypri- nodon diabolis)[Wales, 1930]. C. diabolis is a federally listed endangered species [U.S. Department of the Inte- rior, 1973] that is believed to occupy the smallest known habitat of any vertebrate [Moyle, 2002] and has evolved to endure elevated water temperatures, depressed dissolved oxygen (DO), and significant climate changes. This enigmatic species and its ecosystem has been at the center of a wide range of debates, from questions on the how it came to occupy Devils Hole (there is no known surface water connection, nor has there likely been one since the fish first populated Devils Hole) [Szabo et al., 1994; Riggs and Deacon, 2004], the disposition of federal verses state water rights [Deacon and Williams, 1991; Riggs and Deacon, 2004], the drivers of glacial/interglacial transition [Winograd et al., 1988], and finally, questions regarding the role of genetics in conservation biology [Martin et al., 2012]. Despite extensive conservation efforts in Devils Hole, C. diabolis now appears to be facing its second threat of extinction in less than 50 years, without a clear cause for the population decline. The focus of over 40 years of management and conservation efforts, C. diabolis was first threatened with extinction in the 1970s when groundwater withdrawals reduced the water level on the 14 m2 shallow shelf [Deacon and Williams, 1991] that provides its primary spawning habitat [James, 1969]. After litigation HAUSNER ET AL. VC 2014. American Geophysical Union. All Rights Reserved. 7020 Water Resources Research 10.1002/2014WR015511 600 Spring Count reaching as far as the U.S. Autumn Count 500 Recovery Supreme Court halted nearby Stable Decline groundwater pumping (U.S. v. 400 Cappaert 1974; Cappaert v. U.S. 300 1976) [Deacon and Williams, 1991], the population recov- 200 Relative Abundance ered (Figure 1) as the water 100 table rose [Andersen and Dea- 0 con, 2001]. Since 1995, how- 1970 1975 1980 1985 1990 1995 2000 2005 2010 2015 ever, the C. diabolis population Figure 1. Population surveys of C. diabolis in Devils Hole, showing both the earlier recovery has, for reasons not yet under- (1970–1980) and the recent (post-1995) unexplained decline of the population. stood, been in a second decline [Riggs and Deacon, 2004]. By 2013, the annual population count had reached its lowest level, with only 35 individuals recorded. A number of different hypotheses have been advanced to explain the recent decline in the C. diabolis population, including inbreeding depression [Wilcox, 2001], shifts in the microbial and algal community [Riggs and Deacon, 2004; Bernot and Wilson,2012],orsedimentdynamics[Lyons,2005],and the loss of a key prey species from the primary feeding habitat [Herbst and Blinn, 2003]. In this study, we consider whether ongoing climate change may have negatively affected the annual recruitment of C. diabolis. The species’ 10–14 month lifespan [James, 1969] makes successful annual recruitment critical to the survival of the species, and this recruitment requires (among other factors) the coincidence of water temperatures suitable for successful egg hatching [Shrode, 1975; Shrode and Gerking, 1977] and sufficient food for newly hatched larvae. In spite of its ability to survive in a very harsh environment, past efforts at breeding C. diabo- lis in captivity or maintenance of satellite populations in refuges have been largely unsuccessful. The repro- ductive life stages of Cyprinodon spp., especially developing embryos [Shrode, 1975], are strongly influenced by water temperatures [Shrode and Gerking, 1977]. For closely related Cyprinodon nevadensis nevadensis, the optimal range of water temperatures for embryo development is between 24 and 30C, and hatching suc- cess drops quickly in warmer environments—in C. n. nevadensis, hatching success drops from 80% to approximately 10% when incubation temperatures increase from 30 to 32C[Shrode and Gerking, 1977]. A successful hatch, though, does not guarantee survival. Although the rate of embryo development is rela- tively independent of temperature, warmer eggs hatch earlier and are often underdeveloped [Shrode, 1975] and thus unlikely to survive to reproduce. Embryos spawned by Cyprinodon spp. acclimated to a fluctuating temperature (like that seen on the shallow shelf of Devils Hole) had greater success at higher temperature ranges than embryos spawned under constant temperatures [Shrode and Gerking, 1977]. Adult C. diabolis, though, maintain constant temperatures by using the constant-temperature deep pool of Devils Hole to escape daily peak temperatures observed on the shallow shelf [Baugh and Deacon, 1983a]. Historically, the C. diabolis population has cycled annually, with spring lows and autumn highs [Riggs and Deacon, 2004]. Spring and autumn surveys in 2013 counted 35 and 65 individuals, respectively, whereas pre-1995 surveys averaged 200 (spring) and 400 (autumn) individuals (Figure 1). Although C. diabolis spawn year-round [Miller, 1961; La Rivers, 1962], the majority of recruitment typically occurs in the spring- time [Hausner et al., 2013], when a seasonal shift from a predominantly allochthonous winter to a predomi- nantly autochthonous summer food web begins [Wilson and Blinn, 2007]. In autumn, simultaneous decreases in solar-driven primary productivity and allochthonous contributions lead to a food-limited winter and annual mortality [Minckley and Deacon, 1975]. The bulk of annual recruitment occurs during the period each spring after the seasonal increase in food availability begins, but before water temperatures reach their seasonal peaks [Hausner et al., 2013]. The Mojave Desert’s increasing temperature is suspected to have negatively influenced recruitment success, contributing to the present population decline [Hausner