Predatory strategies and behaviours in cephalopods are altered by elevated <scp>CO</scp><sub>2</sub>

Spady, Blake L.; Munday, Philip L.; Watson, Sue‐Ann

doi:10.1111/gcb.14098

Cited by 25 publications

(29 citation statements)

References 85 publications

(150 reference statements)

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“…Blood acid-base disturbance from environmental hypercapnia has been shown to increase cuttlebone calcification in cuttlefish (Gutowska et al, 2010b). OA has also been demonstrated to alter behavior in marine animals (Clements and Hunt, 2015), including squid (Spady et al, 2014(Spady et al, , 2018. Additionally, OA has been found to have negative impacts on embryonic growth rates and hatching success (Zakroff, 2013;Kaplan et al, 2013).…”

Section: Impact Of Ocean Acidification On O 2 Supply In Squidmentioning

confidence: 99%

Ocean acidification does not limit squid metabolism via blood oxygen supply

Birk

McLean

Seibel

2018

Journal of Experimental Biology

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Ocean acidification is hypothesized to limit the performance of squid owing to their exceptional oxygen demand and pH sensitivity of blood-oxygen binding, which may reduce oxygen supply in acidified waters. The critical oxygen partial pressure ( ), the below which oxygen supply cannot match basal demand, is a commonly reported index of hypoxia tolerance. Any CO-induced reduction in oxygen supply should be apparent as an increase in In this study, we assessed the effects of CO (46-143 Pa; 455-1410 μatm) on the metabolic rate and of two squid species - and - through manipulative experiments. We also developed a model, with inputs for hemocyanin pH sensitivity, blood and buffering capacity, that simulates blood oxygen supply under varying seawater CO partial pressures. We compare model outputs with measured in squid. Using blood-O parameters from the literature for model inputs, we estimated that, in the absence of blood acid-base regulation, an increase in seawater to 100 Pa (≈1000 μatm) would result in a maximum drop in arterial hemocyanin-O saturation by 1.6% at normoxia and a increase of ≈0.5 kPa. Our live-animal experiments support this supposition, as CO had no effect on measured metabolic rate or in either squid species.

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Section: Impact Of Ocean Acidification On O 2 Supply In Squidmentioning

confidence: 99%

Ocean acidification does not limit squid metabolism via blood oxygen supply

Birk

McLean

Seibel

2018

Journal of Experimental Biology

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“…ref. 16 ); activity, defensive 17 , and predatory 18 behaviour in cephalopod molluscs; and foraging behaviour (e.g. ref.…”

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confidence: 99%

Near-future ocean warming and acidification alter foraging behaviour, locomotion, and metabolic rate in a keystone marine mollusc

Horwitz

Norin

Watson

et al. 2020

Sci Rep

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Environmentally-induced changes in fitness are mediated by direct effects on physiology and behaviour, which are tightly linked. We investigated how predicted ocean warming (OW) and acidification (OA) affect key ecological behaviours (locomotion speed and foraging success) and metabolic rate of a keystone marine mollusc, the sea hare Stylocheilus striatus, a specialist grazer of the toxic cyanobacterium Lyngbya majuscula. We acclimated sea hares to OW and/or OA across three developmental stages (metamorphic, juvenile, and adult) or as adults only, and compare these to sea hares maintained under current-day conditions. Generally, locomotion speed and time to locate food were reduced ~1.5-to 2-fold when the stressors (OW or OA) were experienced in isolation, but reduced ~3-fold when combined. Decision-making was also severely altered, with correct foraging choice nearly 40% lower under combined stressors. Metabolic rate appeared to acclimate to the stressors in isolation, but was significantly elevated under combined stressors. Overall, sea hares that developed under OW and/or OA exhibited a less severe impact, indicating beneficial phenotypic plasticity. Reduced foraging success coupled with increased metabolic demands may impact fitness in this species and highlight potentially large ecological consequences under unabated OW and OA, namely in regulating toxic cyanobacteria blooms on coral reefs. Rising atmospheric carbon dioxide (CO 2) levels may lead to continued and accelerated global warming over the coming century 1. The resulting elevated sea surface temperature (SST) (i.e. ocean warming; OW) is accompanied by increased partial pressure of CO 2 (pCO 2) in the ocean, thus rapidly changing the marine environment by increasing acidity (i.e. ocean acidification; OA) at unprecedented rates 2. The Intergovernmental Panel on Climate Change (IPCC) has indicated that, by year 2100, global mean SST will increase by 2-4 °C and seawater pH decrease by 0.14-0.43 units 3 , with concomitant effects on marine ecosystems. Marine invertebrates are critical

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“…The effects of elevated CO 2 on GABA A also appear to be responsible for a wide range of altered behaviours, such as in anti-predator responses in molluscs (Watson et al, 2014) and anxiety, lateralisation, and olfactory preference in fishes (Nilsson et al, 2012;Hamilton, Holcombe & Tresguerres, 2014;Heuer & Grosell, 2014;Lai, Jutfelt & Nilsson, 2015;Schunter et al, 2018). Previously demonstrated effects of elevated CO 2 on behaviour in S. lessoniana include increased activity and altered predatory behaviours (Spady, Munday & Watson, 2018), but the mechanism responsible for these changes has not been investigated. The importance of GABA A receptors for learning in squid (Conti et al, 2013), and evidence of the lack of inhibited learning at elevated CO 2 in the current experiment, suggests that previously demonstrated altered behaviours in S. lessoniana at elevated CO 2 (Spady, Munday & Watson, 2018) may be due to a mechanism other than altered functioning of GABA A receptors.…”

Section: Discussionmentioning

confidence: 99%

“…The genus Sepioteuthis has been noted for their complex learned social and mating behaviours (Moynihan & Rodaniche, 1982;Hanlon & Messenger, 2018;Sugimoto & Ikeda, 2012). Furthermore, the previously demonstrated effects of elevated CO 2 on activity levels and predatory behaviours (Spady, Munday & Watson, 2018) make S. lessoniana an ideal subject for this study.…”

Section: Introductionmentioning

confidence: 98%

“…The two-toned pygmy squid, Idiosepius pygmaeus, responds to elevated CO 2 with altered escape responses (Spady et al, 2014). Furthermore, I. pygmaeus and bigfin reef squid (Sepioteuthis lessoniana) respond to elevated CO 2 with altered predatory behaviours, such as increased latency to attack prey, and increased activity (Spady et al, 2014;Spady, Munday & Watson, 2018). Both in their predatory and anti-predator responses, these species displayed altered body pattern choice at elevated CO 2 (Spady et al, 2014;Spady, Munday & Watson, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Bigfin reef squid demonstrate capacity for conditional discrimination and projected future carbon dioxide levels have no effect on learning capabilities

Spady

Watson

2020

PeerJ

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Anthropogenic carbon dioxide (CO2) emissions are being absorbed by the oceans, a process known as ocean acidification, and risks adversely affecting a variety of behaviours in a range of marine species, including inhibited learning in some fishes. However, the effects of elevated CO2 on learning in advanced invertebrates such as cephalopods are unknown. Any impacts to the learning abilities of cephalopods could have far-reaching consequences for their populations and the communities they inhabit. Cephalopods have some of the most advanced cognitive abilities among invertebrates and are one of the few invertebrate taxa in which conditional discrimination has been demonstrated, though the trait has not been demonstrated in any species of squid. Here, we tested for the first time the capacity for conditional discrimination in a squid species (Sepioteuthis lessoniana). Furthermore, we investigated the effects of projected future CO2 levels (1,084 µatm) on conditional discrimination and learning more generally. A three-task experiment within a two-choice arena was used to test learning and conditional discrimination. Learning was measured by improvements in task completion in repeated trials over time and the number of trials required to pass each task. Squid exhibited significant learning capabilities, with an increase in correct choices over successive trials and a decrease in the number of trials needed to complete the successive tasks. Six of the 12 squid tested successfully passed all three tasks indicating a capacity for conditional discrimination in the species. Elevated CO2 had no effect on learning or on the capacity for conditional discrimination in squid. This study highlights the remarkable cognitive abilities of S. lessoniana, demonstrated by their capacity for conditional discrimination, and suggests that ocean acidification will not compromise learning abilities. However, other behavioural traits in the species have been shown to be altered at comparable elevated CO2 conditions. It is not clear why some ecologically important behaviours are altered by elevated CO2 whereas others are unaffected. Future research should focus on the physiological mechanism responsible for altered behaviours in squid at elevated CO2.

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Predatory strategies and behaviours in cephalopods are altered by elevated CO₂

Cited by 25 publications

References 85 publications

Ocean acidification does not limit squid metabolism via blood oxygen supply

Ocean acidification does not limit squid metabolism via blood oxygen supply

Near-future ocean warming and acidification alter foraging behaviour, locomotion, and metabolic rate in a keystone marine mollusc

Bigfin reef squid demonstrate capacity for conditional discrimination and projected future carbon dioxide levels have no effect on learning capabilities

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Predatory strategies and behaviours in cephalopods are altered by elevated CO2

Cited by 25 publications

References 85 publications

Ocean acidification does not limit squid metabolism via blood oxygen supply

Ocean acidification does not limit squid metabolism via blood oxygen supply

Near-future ocean warming and acidification alter foraging behaviour, locomotion, and metabolic rate in a keystone marine mollusc

Bigfin reef squid demonstrate capacity for conditional discrimination and projected future carbon dioxide levels have no effect on learning capabilities

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Predatory strategies and behaviours in cephalopods are altered by elevated CO₂