Laubenstein, Taryn Diane (2019) Relationships between behavioral and physiological performance under elevated CO₂ in marine fishes. PhD thesis, James Cook University.

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Abstract

Over the past decade there has been a concerted effort to determine how ocean acidification will affect a range of fitness-related traits in marine fishes, with studies often finding negative impacts on either behavioral or physiological performance. Until recently, most studies have focused on the mean responses of the sampled populations to ocean acidification. However, there is a growing recognition of the value in examining individual variation in responses. This can highlight individuals that are best suited to survival in future conditions. Identifying these individuals, however, can be challenging, because performance is not always consistent across all traits. Indeed, correlations can exist between traits that could either help or hinder survival at the individual level, and even affect the ability of marine fishes to adapt to ocean acidification. For instance, if two traits are negatively correlated with respect to the fitness landscape, then selection on one trait will diminish the other, slowing the rate of adaptation, and vice versa. Thus, identifying correlations among key traits is a crucial step towards understanding the potential of marine species to adapt to future climatic conditions. This thesis seeks to identify such correlations by examining the relationship between behavioral and physiological performance in marine fishes and determining how environmental conditions and parental effects might alter this relationship.

Theory predicts that environmental stressors can alter relationships between behavioral and physiological traits, either revealing or masking significant relationships. While both ocean acidification and warming have been found to affect behavioral and physiological performance in marine fishes, they can often interact in complex, non-additive ways, making it difficult to predict their combined impacts on marine fishes. Therefore, in Chapter 2 I explored the relationship between behavioral and physiological performance in a juvenile reef fish, Acanthochromis polyacanthus, reared in a full crossed design of current-day control and predicted future ocean CO₂ and temperature levels. Behaviorally, elevated CO₂, but not elevated temperature, disrupted the fish’s response to an alarm odor. Physiologically, aerobic scope was diminished under elevated temperature, but not elevated CO₂. A significant negative correlation was observed between these behavioral and physiological traits in the combined elevated CO₂ and temperature treatment. These results suggest that correlations between behavior and physiology may only be evident when fish are exposed to multiple stressors. Importantly, the negative correlation between these traits could slow the rate of adaptation to climate change.

Chapter 2 revealed a negative correlation between behavioral and physiological performance in a coral reef fish, but this relationship might not hold for other fishes. It has been hypothesized that different sensitivities of marine fishes to elevated CO₂ may derive from their life styles and the variation in seawater pCO₂ they naturally experience. For example, pelagic fishes could be more susceptible to elevated CO₂ than coral reef fishes due to the relatively stable CO₂ conditions they experience in the open ocean. Therefore, in Chapter 3 I tested the relationship between behavioral and physiological performance in a large pelagic fish, the yellowtail kingfish Seriola lalandi, in a full crossed experimental design of current-day control and predicted future CO₂ and temperature levels. In contrast to the juvenile reef fish, larval kingfish exhibited no behavioral changes in elevated CO₂ conditions. They did, however, exhibit increased resting oxygen uptake (ṀO₂Rest) at elevated CO₂, and also at higher temperature. Correlations between behavioral and physiological performance were observed, which were inversely related based on the temperature treatment; ṀO₂Rest and boldness were negatively correlated at ambient temperature, but positively correlated at elevated temperature. These results show that higher water temperature can alter the relationship between behavioral and physiological performance, potentially altering the direction and pace of adaptation.

Most ocean acidification experiments to date have employed elevated CO₂ treatments that are stable through time. Yet shallow-water habitats such as coral reefs can experience substantial diel cycles in CO₂, and the magnitude of these cycles is predicted to increase as the buffering capacity of the oceans decreases. Diel CO₂ cycles have been shown to reduce the negative effects of elevated CO₂ on behavioral traits in marine fishes, but their effect on physiological traits remains unknown. Nor is it known if diel CO₂ cycles will interact with elevated temperature, or how they might affect relationships between behavioral and physiological performance. In Chapter 4, I compared physiological performance of juvenile A. polyacanthus under stable elevated CO₂ (1000 μatm) to a diel-cycling elevated CO₂ treatment (1000 ± 500 μatm) at both current-day control and elevated (+2 °C) temperatures. The ṀO₂Rest of fish reared at stable elevated CO₂ was higher than that of fish reared in control conditions. By contrast, ṀO₂Rest of fish in the diel-cycling elevated CO₂ treatment was comparable to controls, suggesting that diel CO₂ cycles mitigated the negative effect of elevated CO₂. This mitigating effect was not observed at elevated temperature. In the stable elevated CO₂ and temperature treatment, a positive correlation was observed between ṀO₂Rest and routine activity. However, as A. polyacanthus will likely be subjected to fluctuating, rather than stable, elevated CO₂ in the future, this correlation will not likely influence selection or adaptation. Furthermore, because these fish live in shallow environments exposed to warming, they may not benefit from the mitigating effects of diel CO₂ cycles. These findings highlight the importance of considering the habitats that fishes experience when designing experimental treatments to test the effects of elevated CO₂.

Parental effects can modify the performance of offspring in elevated CO₂, yet it is unknown if they also alter the relationship between behavioral and physiological performance in marine fishes. In Chapter 5, I exposed adult pairs of A. polyacanthus to either current-day control or elevated CO₂ conditions. I split their offspring equally between control and elevated CO₂ conditions and measured their behavioral and physiological performance (response to an alarm odor for behavior, and aerobic scope for physiology). Offspring exposed to elevated CO₂ displayed an impaired response to alarm odors, regardless of their parental treatment. However, maximal oxygen uptake rates (ṀO₂Max) were higher in offspring with CO₂-exposed parents, regardless of offspring treatment, and ṀO₂Rest and aerobic scope showed significant differences between some treatments. These results demonstrate that parental effects can ameliorate some negative effects of ocean acidification, but not others. There were no correlations observed between behavioral and physiological performance. This result, along with Chapters 2 and 4, suggests that relationships between traits may only arise when fish are exposed to both warmer and more acidic conditions.

This research is among the first to examine the relationship between behavioral and physiological performance of marine fishes in a climate change context. The results demonstrate that correlations between behavioral and physiological performance do exist, but can shift depending on complex interactions between stressors, traits, and parental effects. Importantly, significant correlations between behavior and physiology were only observed under elevated CO₂ and temperature conditions, which supports the hypothesis that tradeoffs between behavior and physiology can be strengthened under environmental stress. These relationships are important because they have the potential to alter the direction and pace of future adaptation to climate change. Future studies could investigate the causal mechanisms for these relationships and extend this research beyond marine fishes to examine changes to adaptation rates in short-lived organisms. This research underscores the importance of looking beyond the mean to understand individual variation and relationships between different types of performance in order to predict the effects of climate change on marine ecosystems.

Item ID:	63887
Item Type:	Thesis (PhD)
Keywords:	behavior, climate change, CO2 cycles, CO2, ocean acidification, oxygen uptake, physiology, reef fish, seriola lalandi, temperature, yellowtail kingfish, pelagic fish
Related URLs:	https://researchonline.jcu.edu.au/57835/ https://researchonline.jcu.edu.au/56763/ https://researchonline.jcu.edu.au/63785/
Copyright Information:	Copyright © 2019 Taryn Diane Laubenstein.
Additional Information:	Three publications arising from this thesis are stored in ResearchOnline@JCU, at the time of processing. Please see the Related URLs field. The publications are: Chapter 2: Laubenstein, Taryn D., Rummer, Jodie L., McCormick, Mark I., and Munday, Philip L. (2019) A negative correlation between behavioural and physiological performance under ocean acidification and warming. Scientific Reports, 9. 4265. Chapter 3: Laubenstein, Taryn D., Rummer, Jodie L., Nicol, Simon, Parsons, Darren M., Pether, Stephen M.J., Pope, Stephen, Smith, Neville, and Munday, Philip L. (2018) Correlated Effects of Ocean Acidification and Warming on Behavioral and Metabolic Traits of a Large Pelagic Fish. Diversity, 10 (2). 35. Chapter 4: Laubenstein, Taryn D., Jarrold, Michael D., Rummer, Jodie L., and Munday, Philip L. (2020) Beneficial effects of diel CO₂ cycles on reef fish metabolic performance are diminished under elevated temperature. Science of the Total Environment, 735. 139084.
Date Deposited:	27 Jul 2020 02:46
FoR Codes:	05 ENVIRONMENTAL SCIENCES > 0501 Ecological Applications > 050101 Ecological Impacts of Climate Change @ 35% 06 BIOLOGICAL SCIENCES > 0608 Zoology > 060806 Animal Physiological Ecology @ 30% 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 35%
SEO Codes:	96 ENVIRONMENT > 9603 Climate and Climate Change > 960305 Ecosystem Adaptation to Climate Change @ 50% 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 50%
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