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Title:Effects of environmental warming on lentic freshwater communities and the behavioral and physiological responses by fishes to warming
Author(s):White, Dalon Paul
Director of Research:Wahl, David H
Doctoral Committee Chair(s):Wahl, David H
Doctoral Committee Member(s):Colombo, Robert E; Paige, Ken N; Ward, Michael P
Department / Program:School of Integrative Biology
Discipline:Ecol, Evol, Conservation Biol
Degree Granting Institution:University of Illinois at Urbana-Champaign
Subject(s):largemouth bass
Abstract:Climatic changes are occurring across the globe and warming is a pervasive issue for ectotherms across all habitats. Freshwater ecosystems are threatened by anthropogenic warming, and with projected increases in global temperatures, understanding the impacts of warming on aquatic communities and organism success is important. Many studies have examined the effects of future climate warming using a variety of experimental methodologies. Findings support a multitude of direct and indirect factors that will shape biotic communities. These responses provide broad expectations of the impacts of warming, such as increased nutrient loading, phytoplankton dominance, earlier phenological timing of reproductive events, shifts toward smaller body sizes, physiological constraints, and changes in behaviors. Warming temperatures can affect aquatic ecosystems through multiple mechanisms simultaneously. Temperature can affect ecosystems through ecological interactions, including both abiotic and biotic factors, such as changing physicochemical water conditions and phenological timing events, which can affect trophic cascades and cause differential species success. In ectotherms, rising environmental temperatures directly impact physiological mechanisms, influencing growth and metabolic costs that alter how individuals allocate energetic resources or how predators interact with prey. Some reproductive and life history strategies may be more beneficial in warmer temperatures, such as small body sizes and rapid growth. Species-specific thermal tolerances may further affect how organisms utilize habitats with lakes. Behaviors such as foraging, thermoregulation, and predator avoidance allow individuals to balance ecological conditions and physiological constraints with energetic demands but changing ecological and physiological conditions may mean some behaviors may be more successful than others in warming conditions. Importantly, there is some evidence of rapid adaptive responses to selective pressures that may alleviate some temperature effects, but examples are in only a handful of species in natural systems. Such multi-faceted effects interact in complex ways that are not easily predictable. Further, responses to climate change can be population-, species-, and/or system-specific, and even the capacity to adapt varies between species. Currently it is unclear how environmental changes of warming may impact important abiotic and biotic variables in lakes, as well as phenological timing of reproduction, population structures, life histories, behaviors, and physiological processes of ecologically and recreationally important fishes such as bluegill sunfish (Lepomis macrochirus) and largemouth bass (Micropterus salmoides). Previous experimental methodologies are often limited in spatial or temporal scale, in ecological relevance, and do not test climate change in replicated independent systems. There remains a need for manipulative experiments that observe the effects of increased temperatures in lake systems in situ over an ecologically relevant timeframe and in a replicated manner. I used power plant cooling lakes within central Illinois, USA as a proxy for future climatic warming to assess the impact of warming on aquatic organisms and lake ecosystems. Power plant cooling lakes are heated through thermal effluent and have remained at elevated temperatures for three to five decades. Heated lakes are warmed 5 – 7 °C year-round with temperature changes similar to projected climatic warming. Such systems offer the unique benefit of integrating myriad direct and indirect responses across all species and trophic levels to establish coherent ecological responses to climate change. From genes to ecosystems, I utilize these systems to address how warming affects aquatic communities, how community changes affect fish phenology and behavior, and how fish populations alter life histories and physiological processes to cope with persistently warmer environmental conditions. To address changes in physicochemical water quality, primary producers, and important invertebrate food sources, I quantified ecological differences between abiotic and biotic variables in ambient and heated lakes. To ensure differences observed in lakes were appropriately associated with temperature, I also quantified these variables in a more controlled mesocosm design with higher replication. To understand if ecological changes brought about by increased temperature may affect ecologically important centrarchids, I assessed the population structure and life history of bluegill sunfish in ambient and heated lakes. Because the success of behaviors associated with foraging and predation risk depend on both temperature and ecological context, which are both changed in heated lakes, I considered whether fishes inhabiting heated lakes exhibited altered behaviors. Finally, to address physiological constraints observed on largemouth bass in above-ambient temperature regimes, I quantified metabolic processes associated with energetic demands and determined if they may be adaptive in populations that have been exposed to warmer environments for decades. I found that total phosphorous and chlorophyll a are unchanged in the summer period in both lakes and mesocosms, and warming did not lead to excessive nutrient loads, algal blooms, or anoxic conditions, as has been predicted elsewhere. However, the availability of phosphorous is altered during the winter time in heated lakes, likely due to changes in physical processes such as diffusion rates, thermal stratification, and decreased ice cover. Dissolved oxygen content in heated lakes was significantly decreased during early winter and mid-summer in lakes, but significantly higher in late fall. In mesocosms, O2 content (percent saturation) was diminished during the initial two weeks as organisms rapidly colonized the new environments likely due to faster ecosystem respiration rates, but this effect did not extend beyond the initial bloom period. Warming consistently and dramatically reduced zooplankton abundances in both lakes and mesocosms. These effects were negative in all taxa observed in lakes, though lessened in smaller zooplankton (i.e. rotifers, bosmina). Mesocosms showed that rotifers were increased due to warming, which may be a difference based on ecological scale. There were taxa-specific interactions between warming and the addition of fish in mesocosms, indicating that fish and fishless systems may not respond similarly to warming. Changes in the phenological timing of some zooplankton taxa was apparent, with earlier/shorter blooms of daphnia and calanoid copepods in lakes. There were not changes in the abundance of larval gizzard shad or larval Lepomis spp., but there were species-specific adaptive responses. Larval gizzard shad matched phenological shifts in daphnia but larval Lepomis showed evidence of delayed spawning, which may affect both predators who feed on bluegill young of year and populations of their common prey source. In mesocosms, fish did not grow faster during the summer period but were estimated to consume more, indicating that more prey biomass would be required to sustain the same amount of fish. Overall, benthic invertebrates were resilient to warming in mesocosms, but showed strong shifts due to the presence of fish. Therefore, any changes in fish communities due to warming, such as changes in population structure and feeding regimes, may be expected to indirectly alter benthic invertebrate communities. Due to the difficulty of establishing long-term heating studies on whole lake systems, there is little empirical evidence addressing the potential changes in life history strategies of fish in situ in response to future climate warming trends. Here, I study early growth rates, size-at-maturation, maximum adult size, and lifespan of bluegill populations in heated lakes compare those populations to populations in three nearby ambient lakes. I find evidence that life history strategies and population demographics are substantially affected by warmer environments. Heated populations exhibited faster first-year growth, shorter lifespans, smaller size-at-maturation, and smaller maximum adult sizes. Changes in life history strategies, including lifespan and maximum sizes, will be evident across many fish species under warmer conditions in the future. Given changes in the temperature regimes and ecological conditions in heated lakes, it may be expected that fish exhibit altered behaviors and physiological processes. I compared behavioral responses of juvenile largemouth bass collected from the three ambient and three power plant cooling lakes to both a potential predator and prey resource. I found that there was high intra-lake variability of bold and aggressive behaviors and of locomotor activity, which may indicate population-specific responses to stressors other than warming, but these differences did not correlate to warming. However, explorative behaviors differed consistently in heated lakes which I attribute to changes in food source. The findings of this work identify that large ecological changes associated with warming environments, such as food availability, may drive changes in some aspects of behavioral expression in largemouth bass but that other aspects of behavioral expression may remain driven by lake-specific factors not related to warming. Lastly, I investigated the physiological burden that above-optimum temperatures place on fish populations. I investigated metabolism, growth, and thermal tolerance of largemouth bass populations inhabiting heated lakes and compare these traits to populations from ambient lakes. Largemouth bass from ambient and heated groups were spawned in an ambient, common garden pond environment, then acclimated to either a normal summertime temperature (24 °C) or a supra-optimum temperature (30 °C). Relative to ambient populations, fish from heated populations had significant reductions in the resting metabolic rate at both temperatures and markedly increased growth rates at 30 °C. By comparing pond-raised fish to fish removed directly from heated lakes, I show that developmental plasticity played little role in establishing the metabolic rate. A lower resting metabolic rate contributed to an increase in the conversion efficiency of food to biomass of largemouth bass from heated lakes, regardless of temperature. Despite inhabiting heated lakes for many decades, neither critical thermal maximum nor minimum were altered in heated populations when raised in a common garden environment. These results suggest that largemouth bass can lessen sub-lethal effects of environmental warming by altering physiological processes that preserve aerobic scope and that these changes are generationally transient, but that changes in maximum thermal tolerance in response to warming is limited to phenotypic plasticity. Overall, I found that power plant cooling lakes are viable study systems to use as proxies for climate change. These lakes exhibit many overarching patterns of change that are expected with climate change, such as reduced zooplankton abundance and altered timing of fish spawning, but not all. Differences may be due to the spatial, temporal, and ecological scale limitations of previous studies, or due to the underrepresentation of similar turbid, intra-continental, warm-water systems in previous studies regarding freshwater lake ecosystems and climate warming. Warming was related to evident changes in life history traits of bluegill with little intra-lake variability, and in exploratory behaviors, but there remains considerable intra-lake variability in other behaviors. Further, fishes such as largemouth bass have the capacity to cope with warming through physiological regulation via epigenetic or genetic mechanisms, but, even after decades of warming, are not able to adapt higher thermal tolerances. While physiological changes may benefit individuals in warmer environments, they may also have trade-offs that have yet to be quantified.
Issue Date:2019-07-12
Rights Information:Copyright 2019 Dalon White
Date Available in IDEALS:2019-11-26
Date Deposited:2019-08

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