Effects of projected near-future carbon dioxide levels on cephalopod physiology and behaviour

Spady, Blake L. (2018) Effects of projected near-future carbon dioxide levels on cephalopod physiology and behaviour. PhD thesis, James Cook University.

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Oceanic uptake of anthropogenic carbon dioxide (CO₂) is causing changes to seawater chemistry, a process known as ocean acidification. This has the potential to negatively affect a wide variety of marine organisms. To date, most studies into the effects of elevated CO₂ on marine organisms have focused on highly calcified invertebrates and fishes, with a variety of effects observed, including impacts on early life history development, respiration, behaviour, and learning. Despite their importance in marine ecosystems, comparatively little is known about the possible effects of rising CO₂ levels on cephalopods. In this thesis, I investigate the effects of CO₂ levels projected for the end of this century on the aerobic scope, reproduction, development, predatory behaviours, and learning in two species of tropical cephalopod from different taxonomic orders, the two-toned pygmy squid (Idiosepius pygmaeus) and the bigfin reef squid (Sepioteuthis lessoniana).

In Chapter 2, I investigate the effects of elevated CO₂ on the minimum and maximum oxygen uptake rates, and aerobic scope of both I. pygmaeus and S. lessoniana. Due to the pH sensitive oxygen transport of cephalopods, I expected adverse effects on oxygen uptake rates. However, there were no effects of elevated CO₂ exposure on oxygen uptake rates or aerobic scope. This suggests a level of tolerance to elevated CO₂ in both species. The ability of these two cephalopod species to cope with long-term exposure to elevated CO₂ without detriment to their aerobic scope suggests that the energy available to partition to other important tasks, such as reproduction and growth, may remain optimal at elevated CO₂.

One of the more commonly observed effects of elevated CO₂ on marine molluscs is altered reproduction and early life history development. In Chapter 3, I test the effects of elevated CO₂ on reproduction and the potential for effects after parental exposure on early development in I. pygmaeus. Despite the lack of effects of elevated CO₂ on the aerobic scope of adults observed in Chapter 2, there were adverse effects of elevated CO₂ on reproduction and development. Parents held at elevated CO₂ produced clutches with 40% fewer eggs compared with parents in ambient control conditions. Embryo area, measured directly after spawning, was significantly reduced in the elevated CO₂ treatment compared to controls, and remained smaller throughout development. There was no effect of elevated CO₂ on fertility, time to hatch, or hatching success. Lastly, female squid laid eggs >40% closer together at elevated CO₂ compared with the controls, indicating a possible effect of elevated CO₂ on egg laying behaviour. The negative effects observed here appear to be predominately a response to parental exposure to elevated CO₂ rather than exposure of the eggs themselves. As the potential for adaptation is strongly influenced by reproductive success, these effects could have consequences to the capacity of I. pygmaeus to cope with future ocean conditions.

In Chapter 4, I investigate the effects of elevated CO₂ on the predatory behaviours of both I. pygmaeus and S. lessoniana. Both species exhibited an increased latency to attack prey and displayed altered body pattern choice during the attack sequence at elevated CO₂. I. pygmaeus also exhibited a 20% decrease in predation rate, an increased striking distance, and reduced preference for attacking the posterior end of the prey at elevated CO₂. The effects of elevated CO₂ on predatory behaviours and strategies seen here could have far-reaching consequences in marine ecosystems due to the important role of squid in marine food webs as both predator and prey.

Cephalopods have some of the most advanced learning capabilities among invertebrates. In Chapter 5, I investigate the effects of elevated CO₂ on the learning and capacity for conditional discrimination in S. lessoniana. Here, individuals were subjected to a three-task training and learning experiment within a two-choice maze containing visual cues. Performances throughout these three tasks were compared to determine the effects of elevated CO₂ on learning and conditional discrimination. Fifty percent of squid from both CO₂ treatments demonstrated conditional discrimination, and time to exit the maze as well as rate of correct choice was unaffected by elevated CO₂. These findings demonstrate conditional discrimination for the first time in a squid and suggest that the learning and memory capabilities of S. lessoniana will not be affected by future elevated CO₂ conditions.

This thesis demonstrates for the first time in any cephalopod species, the effects of elevated CO₂ on aerobic recovery, reproduction, predatory behaviours, and learning. The results show that while tolerant in some aspects of physiology and behaviour, other important traits are adversely affected by elevated CO₂. However, cephalopods have short lifespans, fast growth rates, large populations, and a high intrinsic rate of population increase - all traits that favour potential adaptation to changes in their natural environment. Future studies should investigate the capacity for these animals to adapt to elevated CO₂ and determine their potential to cope with future changes in ocean conditions over the timescale at which they are predicted to occur.

Item ID: 58868
Item Type: Thesis (PhD)
Keywords: activity, anti-predator behaviour, avoidance, cephalopod, escape, Idiosepius pygmaeus, ocean acidification, predator–prey interaction, predatory behaviour, squid, startle response, Sepioteuthis lessoniana
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Copyright Information: Copyright © 2018 Blake L. Spady.
Additional Information:

Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 4: Spady, Blake L., Munday, Philip L., and Watson, Sue-Ann (2018) Predatory strategies and behaviours in cephalopods are altered by elevated CO2. Global Change Biology, 24 (6). pp. 2585-2596.

Spady, Blake L., Watson, Sue-Ann, Chase, Tory J., and Munday, Philip L. (2014) Projected near-future CO2 levels increase activity and alter defensive behaviours in the tropical squid Idiosepius pygmaeus. Biology Open, 3 (11). pp. 1063-1070.

Date Deposited: 09 Jul 2019 02:17
FoR Codes: 06 BIOLOGICAL SCIENCES > 0699 Other Biological Sciences > 069902 Global Change Biology @ 40%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060808 Invertebrate Biology @ 30%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060801 Animal Behaviour @ 30%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 50%
96 ENVIRONMENT > 9603 Climate and Climate Change > 960399 Climate and Climate Change not elsewhere classified @ 50%
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