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Nolan Et Al. – 2019 Journal of Plankton Research academic.oup.com/plankt Downloaded from https://academic.oup.com/plankt/advance-article-abstract/doi/10.1093/plankt/fbz021/5537583 by Washington State University Libraries user on 30 July 2019 J. Plankton Res. (2019) 00(00): 1–17. doi:10.1093/plankt/fbz021 ORIGINAL ARTICLE Diverse taxa of zooplankton inhabit hypoxic waters during both day and night in a temperate eutrophic lake SEAN NOLAN1,*, STEPHEN M. BOLLENS1,2 AND GRETCHEN ROLLWAGEN-BOLLENS1,2 1school of the environment, washington state university, 14204 ne salmon creek ave, vsci 230 vancouver, wa, usa 98686 and 2school of biological sciences, washington state university, 14204 ne salmon creek ave, vsci 230 vancouver, wa, usa 98686 *corresponding author: [email protected] Received October 20, 2018; editorial decision May 2, 2019; accepted May 2, 2019 Corresponding editor: Xabier Irigoien As the frequency and intensity of hypoxic events increase in both fresh and marine waters, understanding the ecological effects of hypoxia becomes more important. The extant literature reports varying effects of hypolimnetic hypoxiaon the vertical distribution and diel vertical migration (DVM) of zooplankton, with some but not all taxa reported to avoid hypoxic waters. We studied the vertical distribution and DVM of diverse zooplankton taxa throughout three seasons over 2 years (2014 and 2015) in Lacamas Lake, WA, USA. We observed hypoxia (<2mgL−1 dissolved oxygen) in the hypolimnion of Lacamas Lake during five of six sampling periods, with zooplankton populations often exhibiting ‘h-metric’ values (defined as the proportion of a zooplankton population residing within hypoxic waters) ranged from 0.14 to 1.00, with an overall mean of h = 0.66. Moreover, we observed a lack of DVM in most zooplankton taxa on most occasions. Our findings indicate both community-level and taxon-specific zooplankton tolerances to hypoxia, although the exact mechanisms at play remain to be fully elucidated. Nevertheless, the common residency in hypoxic waters and the lack of DVM by diverse zooplankton taxa that we observed likely have implications for food web dynamics in Lacamas Lake and other water bodies. KEYWORDS: vertical distribution; diel vertical migration; h-metric; hypolimnetic hypoxia; freshwater available online at academic.oup.com/plankt © The Author(s) 2019. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: [email protected] JOURNAL OF PLANKTON RESEARCH VOLUME 00 NUMBER 00 PAGES 1–17 2019 INTRODUCTION decline throughout the summer, reducing hypolimnetic Downloaded from https://academic.oup.com/plankt/advance-article-abstract/doi/10.1093/plankt/fbz021/5537583 by Washington State University Libraries user on 30 July 2019 oxygen concentrations to hypoxic levels (Diaz, 2001; Hypoxia [defined as dissolved oxygen (DO) < 2mgL−1] Jenney et al., 2016). Cooler temperatures in the autumn in subsurface waters of lakes, reservoirs and coastal result in the collapse of the thermocline and allow for oceans is becoming increasingly common as eutrophi- vertical mixing of the water column over winter months. cation and rising global temperatures increase chemical Whereas DO concentrations below 2 mg L−1 can and thermal stratification in aquatic systems (Helly act to exclude large planktivorous predators, for many and Levin, 2004; Mallin et al., 2006; Ficke et al., 2007; zooplankters such exclusion often occurs at lower DO Jenny et al., 2016). Strong oxygen and temperature concentrations, allowing hypoxic waters to be utilized stratification of the water column can result in bottom as predation refugia. Indeed, several zooplankton taxa water hypoxia, which can act as a sub-lethal displacement have been observed occupying hypoxic waters during mechanism, thereby forcing vertebrate (Roberts et al., periods of high predation (Lass et al., 2000; Vanderploeg 2009; Arend et al., 2011) and invertebrate taxa (Eby and et al., 2009b; Goto et al., 2012), often exhibiting species- Crowder, 2002) with relatively high oxygen demands into specific DO tolerances (Stewart and George, 1987; shallower depths where DO concentrations are more Kizito and Nauwerck, 1995; Galkovskaya and Mityanina, favorable and may alter predator–prey interactions and 2005; Goto et al., 2012). For example, in Lake Erie, food web dynamics (Ekau et al., 2010). Bottom water Daphnia mendotae consistently avoided hypoxic waters hypoxia has been associated with large fish kills or (Goto et al., 2012), whereas Daphnia longiremis regularly ‘dead-zones’ (Rabalais et al., 2002; Stauffer et al., 2012), utilized hypoxic hypolimnetic waters during daylight and planktivorous and piscivorous fishes have been periods when oxygen concentrations were as low as observed to avoid hypoxic waters in marine and estuarine 1.0 mg L−1 (Field and Prepas, 1997; Vanderploeg et al., systems such as the Gulf of Mexico (Rabalais et al., 2009b). Additionally, the copepod Diacyclops thomasi and 2002; Pierson et al., 2009; Zhang et al., 2009) and Puget the cladoceran Bosmina longirostris in Lake Erie and Daphnia Sound, WA (Parker-Stetter and Horne, 2009), as well as pulex and B. longirostris in Amisk Lake (Alberta, Canada) freshwater lakes such as Lake Erie (Vanderploeg et al., have been observed to inhabit hypoxic waters with DO 2009a, b). concentrations as low as 1.2 mg L−1 (Field and Prepas, The effects of hypolimnetic hypoxia on zooplankton 1997; Vanderploeg et al., 2009b). vertical distribution and migration have also been Diel vertical migration (DVM) of zooplankton is reported; however, much of this information concerns widespread in both freshwater and marine systems marine and estuarine taxa, with relatively few studies of and may be affected by a range of extrinsic factors freshwater zooplankton. For instance, during seasonal including predation, prey availability, light, temperature hypoxia events in Chesapeake Bay and the northern or chemical gradients, turbulence and advective flows (e.g. Gulf of Mexico, the lack of DO in near-bottom waters Bollens and Frost, 1989a, b; Lampert, 1993; Williamson compressed the vertical distribution of zooplankton, et al., 2011). Normal DVM, in which zooplankton reside pushing zooplankters to shallower depths (Kimmel et al., at deeper depths during the day and shallower depths 2009; Elliot et al., 2012; Roman et al., 2012; Pierson et al., during the night, can have important implications for 2017). Similar avoidance of hypoxic waters has been predator–prey interactions and the vertical flux of observed in some demersal and pelagic fishes in a number material and energy in pelagic ecosystems (Bollens of freshwater systems subject to seasonal hypoxia (Ludsin et al., 2011). DVM may also be affected by the upward et al., 2009; Zhang et al., 2009; Breitburg et al., 2018). Yet, expansion of hypoxic conditions in the hypolimnion, in other instances, some species of zooplankton have been reducing the vertical extent of DVM to the point that observed occupying hypoxic waters [e.g. Gulf of Mexico some zooplankton populations are in direct contact (Zhang et al., 2009) and Puget Sound, WA (Sato et al., with predators for extended periods (Galkovskaya and 2016)]. Mityanina, 2005; Pothoven et al., 2009; Vanderploeg Hypolimnetic hypoxia is relatively common in tem- et al., 2009a, b; Goto et al., 2012). The reduction of perate lakes and reservoirs and often follows a seasonal optimal habitat can have detrimental effects on individual pattern, whereby DO levels in deep waters begin to growth rates, survival and reproduction of zooplankton diminish in early spring due to increased biological oxy- by reducing foraging opportunities, increasing predation gen demand near the lake bottom (Diaz, 2001). Thermal and increasing metabolic rates, which in turn may lead to stratification, often beginning in late spring/early sum- significantly lower population growth rates and thus lower mer, increases surface temperatures and inhibits vertical abundances of zooplankton in regions that experience mixing of the water column, exacerbating hypolimnetic moderate to severe hypoxia (Goto et al., 2012; Elliott et al., oxygen reduction. DO concentrations often continue to 2013). 2 S. NOLAN ET AL. DIVERSE TAXA OF ZOOPLANKTON INHABIT HYPOXIC WATERS Thus, the extant literature reports varying results Downloaded from https://academic.oup.com/plankt/advance-article-abstract/doi/10.1093/plankt/fbz021/5537583 by Washington State University Libraries user on 30 July 2019 regarding the effects of seasonally variable hypolim- netic hypoxia on zooplankton distribution and vertical migration in temperate lakes, reservoirs and coastal waters. Our study attempted to shed further light on this issue through a multi-year, multi-season examination of the vertical distribution and DVM patterns of a diverse freshwater zooplankton community in response to seasonal hypolimnetic hypoxia in a temperate, eutrophic lake (Lacamas Lake, WA, USA). Our investigation addressed the following overarching research question: what effect, if any, does hypolimnetic hypoxia have on the vertical distribution and DVM of diverse zooplankton taxa? Specifically, we tested the two following hypotheses in our study: 1) Hypolimnetic hypoxia in Lacamas Lake causes ver- tical compression of the habitable range of the water column such that most zooplankton avoid the hypolimnion, and 2) Hypolimnetic hypoxia leads to reduced amplitude of DVM by zooplankton within the epilimnion and metalimnion. METHOD Study site Fig. 1. Map of Lacamas Lake, located in southwestern
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