Hypoxia as a Mediator of Food Web Interactions and ...

Hypoxia as a Mediator of Food Web Interactions and Energy Flow in Reservoir Ecosystems Kathryn J. Lang1, Kevin L. Pangle1,2, Joseph D. Conroy3, Senaka Goonewardena1, and Stuart A. Ludsin1 Ohio State University Aquatic Ecology Laboratory, Department of Evolution, Ecology, and Organismal Biology, Columbus, OH 2Current Address: Central Michigan University, Department of Biology, Mount Pleasant, MI 3Ohio Department of Natural Resources – Division of Wildlife, Inland Fisheries Research Unit, Hebron, OH

 Nutrient pollution (eutrophication) threatens aquatic ecosystems world-wide by shaping the formation of hypoxic (“dead”) zones or areas of low dissolved oxygen (DO) availability.  In most ecosystems, hypoxia occurs seasonally, peaking during summer and late fall when temperatures are warm and the water column is thermally stratified.  Hypoxia alters species interactions via lost habitat that modifies species movement and foraging behavior.  Species at different trophic levels of the food web vary in their tolerance to hypoxia; invertebrates show greater tolerance to low DO than their fish predators, as well as an ability to use the hypoxic zone as a refuge from predation.  No previous study has quantified how this hypoxia-driven spatial disconnect between predator and prey affects energy flow from lower trophic levels to fish.  In freshwater ecosystems with an abundance of phantom midges (Chaoborus spp.; Fig. 1), which are invertebrates that (1) are highly tolerant of low DO and have been shown to use the hypoxic zone as a refuge from predation during the day, (2) prey on smaller mesozooplankton taxa, and (3) can serve as prey for planktivorous fish, seasonal hypoxia likely drives variability in energy flow to planktivorous fish by modifying their spatial overlap with Chaoborus and their mesozooplankton prey.

 We sampled two sites in Hoover Reservoir (Westerville, OH) during both day and night before (May), during (August), and after (November) peak hypoxia in 2011.  Temperature, DO, and light levels (photosynthetically active radiation, PAR) were measured throughout the entire water column.  Mesozooplankton (prey) biomass density and daily production were quantified using day and night sampling in surface (epilimnion) and bottom (hypolimnion) watercolumn layers, and the middle transition zone (metalimnion) during hypoxic August.  Zooplanktivorous fish (i.e., gizzard shad, bluegill, white crappie, white bass) were sampled in the epilimnion and hypolimnion during day and night, using replicate trawling.  Chaoborus distribution and density were quantified using discrete-depth sampling, during both day and night, and vertically-integrated net tows, conducted only at night.  Chaoborus diets were analyzed in the laboratory to quantify consumption of mesozooplankton prey. - Daily consumption was calculated from individual crop biomass, total density, and crop evacuation rates. - Non-conservative (unscaled) and conservative (scaled) estimates of consumption were made. For the former, only individuals with non-empty crops were used in estimates; for the latter, we assumed individuals with empty crops never fed in that day.

Hypothesis  Chaoborus larvae reduce energy available to planktivorous fishes in freshwater food webs during hypoxic periods by: (1) consuming mesozooplankton in oxygenated surface waters at night, when low light levels limit Chaoborus’ vulnerability to visual fish predators; and (2) vertically migrating into dark, hypoxic bottom waters during the daytime, where they are unavailable to fish predators that are intolerant of low DO and that require light to feed.

Fig. 1. A phantom midge (Chaoborus punctipennis) larva. Maximum larval size is ~ 9 mm. Photo source: http://cfb.unh.edu/CFBKey/html/Organisms/otherarthropod s/GChaoborus/chaoborus_punctipennis/.

Results  Temperature, DO, and PAR varied among sampling months, with bottom hypoxia (DO < 2 mg/L) present only during August sampling (Fig. 1).  Vertical distributions also varied across months. - In May and November during day, fish and Chaoborus mainly were found in the dark, oxygenated hypolimnion and mesozooplankton in the oxygenated epilimnion. - In August, fish, Chaoborus, and mesozooplankton avoided hypoxic bottom waters during day and night, residing in the oxygenated epilimnion instead (Fig. 2).  Chaoborus consumption of mesozooplankton varied through time, likely as an indirect response to hypoxia. - During non-hypoxic months, when spatial overlap between predator and prey in the water column was low, Chaoborus crops were mostly empty (>93% in May, >87% in November) during the day. - During August, when spatial overlap during the daytime was high in the epilimnion, >44% of the Chaoborus larvae contained mesozooplankton.  Daily Chaoborus consumption rates varied among sampling months (Fig. 3) with estimated consumption of total mesozooplankton production being high during May (scaled, unscaled: 77%, 148%) and August (53%, 100%).

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Fig. 3. Calculated crustacean mesozooplankton production and daily consumption of it by Chaoborus during each sampling month. See text for more details on consumption estimation.

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Fig. 1. Daytime temperature (˚C), dissolved oxygen (DO; mg/L), and light (PAR; µmol photons/m2/s) in May (top), August (middle), and November (bottom).

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 Hypoxia has the ability to significantly alter energy flow through ecosystems by altering species distributions and movement behavior. In our study system, hypoxia caused increased spatial overlap between mesozooplankton prey and their fish and Chaoborus predators. In turn, Chaoborus feeding behavior changed, resulting in reduced energy (mesozooplankton prey) available in the epilimnion.  The results herein also support the idea of Chaoborus acting as a driving force of food web dynamics. However, no clear evidence exists to indicate that Chaoborus serve as a net energy “sink” through transfer of energy from the epilimnion into the hypolimnion during hypoxia, as Chaoborus unexpectedly remained in the epilimnion during both day and night during peak hypoxia.  The effect of Chaoborus on planktivorous fish is still unclear. Chaoborus clearly act as a competitor by consuming shared mesozooplankton prey. Use of the hypoxic zone as a prey refuge, however, was less than expected. Thus, Chaoborus may be accessible to fish as prey as well. Clearly, further study is needed to fully understand the net impact of hypoxia and Chaoborus on fish assemblages.

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Fig. 2. Percentage of crustacean mesozooplankton, Chaoborus larvae, and planktivorous fish biomass found in each water-column layer during August.

 We thank R. Briland for technical assistance in mesozooplankton enumeration and many members of the Aquatic Ecology Lab, as well as C. Fullard, C. Goings, M. Hangsleben, T. Sindt, and X. Yang, for help in the field. Financial support was provided by OSU’s Dept. of EEOB (to SAL) and an OSU Mayers Summer Research Scholarship (to KJL).