Slow swimming, fast strikes: effects of feeding behavior on scaling of anaerobic metabolism in epipelagic squid

Many pelagic fishes engage prey at high speeds supported by high metabolic rates and anaerobic metabolic capacity. Epipelagic squids are reported to have among the highest metabolic rates in the oceans as a result of demanding foraging strategies and the use of jet propulsion, which is inherently inefficient. This study examined enzymatic proxies of anaerobic metabolism in two species of pelagic squid, Dosidicus gigas and Doryteuthis pealeii (Lesueur 1821), over a size range of six orders of magnitude. We hypothesized that activity of the anaerobically poised enzymes would be high and increase with size as in ecologically similar fishes. In contrast, we demonstrate that anaerobic metabolic capacity in these organisms scales negatively with body mass. We explored several cephalopod-specific traits, such as the use of tentacles to capture prey, body morphology and reduced relative prey size of adult squids, that may create a diminished reliance on anaerobically fueled burst activity during prey capture in large animals

The thermal stress response to diel vertical migration in the hyperiid amphipod Phronima sedentaria

The hyperiid amphipod Phronima sedentaria experiences a temperature change of 15 °C during diel migration in the Eastern Tropical North Pacific (ETNP) from 8–10 °C at depth to 25–27 °C at night in the surface waters. The aim of this study was to determine if the natural temperature gradient experienced by P. sedentaria results in a thermal stress response. Individuals were initially exposed to their night time temperatures (23 °C) and subsequently subjected to temperatures within and above the range they typically experience. In the Eastern Tropical North Pacific P. sedentaria tolerates its normal night-time temperature (~ 23 °C), but only for the duration of its stay there (~ 9 h). Longer exposures (24 h) result in elevated heat shock protein (hsp) expression. 29 °C results in hsp expression, increased lactate production and 50% mortality at all exposure durations. This represents an upper critical temperature. Understanding the adaptations of pelagic amphipods to their current environment will help predict the physiological impacts of global warming for amphipods and their predators

Energetic Plasticity Underlies a Variable Response to Ocean Acidification in the Pteropod, \u3cem\u3eLimacina helicina antarctica\u3c/em\u3e

Ocean acidification, caused by elevated seawater carbon dioxide levels, may have a deleterious impact on energetic processes in animals. Here we show that high PCO2 can suppress metabolism, measured as oxygen consumption, in the pteropod, L. helicina forma antarctica, by ~20%. The rates measured at 180–380 µatm (MO2 = 1.25 M−0.25, p = 0.007) were significantly higher (ANCOVA, p = 0.004) than those measured at elevated target CO2 levels in 2007 (789–1000 µatm, = 0.78 M−0.32, p = 0.0008; Fig. 1). However, we further demonstrate metabolic plasticity in response to regional phytoplankton concentration and that the response to CO2 is dependent on the baseline level of metabolism. We hypothesize that reduced regional Chl a levels in 2008 suppressed metabolism and masked the effect of ocean acidification. This effect of food limitation was not, we postulate, merely a result of gut clearance and specific dynamic action, but rather represents a sustained metabolic response to regional conditions. Thus, pteropod populations may be compromised by climate change, both directly via CO2-induced metabolic suppression, and indirectly via quantitative and qualitative changes to the phytoplankton community. Without the context provided by long-term observations (four seasons) and a multi-faceted laboratory analysis of the parameters affecting energetics, the complex response of polar pteropods to ocean acidification may be masked or misinterpreted

Flight of the Vampire: Ontogenetic Gait-Transition in \u3cem\u3eVampyroteuthis Infernalis\u3c/em\u3e (Cephalopoda: Vampyromorpha)

Vampyroteuthis infernalis is a cosmopolitan cephalopod that lives in the oxygen minimum layer between 600 and 800 m depth. Morphometric and physiological studies have indicated that V. infernalis has little capacity for jet propulsion and has the lowest metabolic rate ever measured for a cephalopod. Because fin swimming is inherently more efficient than jet propulsion, some of the reduction in energy usage relative to other cephalopods may result from the use of fins as the primary means of propulsion. V. infernalis undergoes a rapid metamorphosis which consists of changes in the position, size and shape of the fins. This suggests that there are changes in the selective factors affecting locomotion through ontogeny. The present study describes these changes in relation to models for underwater ‘flight’. Citrate synthase (CS) and octopine dehydrogenase (ODH) activities, indicative of aerobic and anaerobic metabolism, respectively, were measured in fin, mantle and arm tissue across a range of body size of four orders of magnitude. The low enzymatic activities in both posterior and anterior fin tissue and the relatively high activity in mantle muscle prior to metamorphosis indicate that jet propulsion using mantle contraction is the primary means of propulsion in juvenile V. infernalis. The increase in CS activity with size after metamorphosis suggests an increased use of the fins for lift-based propulsion. Fin swimming appears to be the primary means of propulsion at all adult sizes. The negative allometry of CS activity in mantle and arm muscle is consistent with the scaling of oxygen consumption previously measured for V. infernalis and with the scaling of aerobic metabolism observed in most animals. The unusual positive allometry of fin muscle CS activity suggests that the use of fins is either relatively more important or more costly in larger animals. Positive scaling of ODH activity in all tissues suggests that fin propulsion, jet propulsion and medusoid ‘bell-swimming’ are all important for burst escape responses. Enzyme activities in Cirrothauma murrayi are consistent with finswimming observed from submersibles, while those in Opisthoteuthis californiana suggest a strong reliance on medusoid swimming using the arms. The transition from jet propulsion to paired-fin ‘flight’ with increasing body size in Vampyroteuthis infernalis appears functionally to be an ontogenetic ‘gait-transition’

The metabolic response of pteropods to acidification reflects natural CO2-exposure in oxygen minimum zones

© The Author(s), 2012. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 9 (2012): 747-757, doi:10.5194/bg-9-747-2012.Shelled pteropods (Thecosomata) are a group of holoplanktonic mollusks that are believed to be especially sensitive to ocean acidification because their aragonitic shells are highly soluble. Despite this concern, there is very little known about the physiological response of these animals to conditions of elevated carbon dioxide. This study examines the oxygen consumption and ammonia excretion of five pteropod species, collected from tropical regions of the Pacific Ocean, to elevated levels of carbon dioxide (0.10%, 1000 ppm). Our results show that pteropods that naturally migrate into oxygen minimum zones, such as Hyalocylis striata, Clio pyramidata, Cavolinia longirostris and Creseis virgula, were not affected by carbon dioxide at the levels and duration tested. Diacria quadridentata, which does not migrate, responds to high carbon dioxide conditions with reduced oxygen consumption and ammonia excretion. This indicates that the natural chemical environment of individual species may influence their resilience to ocean acidification.Funding of the National Science Foundation (grant OCE-0526502 to Wishner and Seibel, OCE – 0526545 to Daly, and OCE – 0851043 to Seibel), the University of Rhode Island, and the Rhode Island Experimental Program to Stimulate Competitive Research Fellowship Program

Temperature compensation of aerobic capacity and performance in the Antarctic pteropod, \u3cem\u3eClione antarctica\u3c/em\u3e, compared with its northern congener, \u3cem\u3eC. limacina\u3c/em\u3e

In ectotherms living in cold waters, locomotory performance is constrained by a slower generation of the ATP that is needed to fuel muscle contraction. Both polar and temperate pteropods of the genus Clione, however, are able to swim continuously by flapping their parapodia (wings) at comparable frequencies at their respective habitat temperatures. Therefore, we expected polar species to have increased aerobic capacities in their wing muscles when measured at common temperatures. We investigated muscle and mitochondrial ultrastructure of Clione antarctica from the Southern Ocean (−1.8°C) and populations of a sister species, Clione limacina, from the Arctic (−0.5 to 3°C) and from the North Atlantic (10°C). We also measured oxygen consumption and the activity of the mitochondrial enzyme citrate synthase (CS) in isolated wings of the two species. The Antarctic species showed a substantial up-regulation of the density of oxidative muscle fibers, but at the expense of fast-twitch muscle fibers. Mitochondrial capacity was also substantially increased in the Antarctic species, with the cristae surface density (58.2±1.3μm2μm−3) more than twice that found in temperate species (34.3±0.8μm2μm−3). Arctic C. limacina was intermediate between these two populations (43.7±0.5μm2μm−3). The values for cold-adapted populations are on par with those found in high-performance vertebrates. As a result of oxidative muscle proliferation, CS activity was 4-fold greater in C. antarctica wings than in temperate C. limacina when measured at a common temperature (20°C). Oxygen consumption of isolated wing preparations was comparable in the two species when measured at their respective habitat temperatures. These findings indicate complete compensation of ATP generation in wing muscles across a 10°C temperature range, which supports similar wing-beat frequencies during locomotion at each species\u27 respective temperature. The elevated capacity in the wing muscles is reflected in the partial compensation of whole-animal oxygen consumption and feeding rates

Oxygen supply capacity breathes new life into critical oxygen partial pressure (Pcrit)

Author Posting. © Company of Biologists, 2021. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 224(8), (2021): jeb242210, https://doi.org/10.1242/jeb.242210.The critical oxygen partial pressure (Pcrit), typically defined as the PO2 below which an animal's metabolic rate (MR) is unsustainable, is widely interpreted as a measure of hypoxia tolerance. Here, Pcrit is defined as the PO2 at which physiological oxygen supply (α0) reaches its maximum capacity (α; µmol O2 g−1 h−1 kPa−1). α is a species- and temperature-specific constant describing the oxygen dependency of the maximum metabolic rate (MMR=PO2×α) or, equivalently, the MR dependence of Pcrit (Pcrit=MR/α). We describe the α-method, in which the MR is monitored as oxygen declines and, for each measurement period, is divided by the corresponding PO2 to provide the concurrent oxygen supply (α0=MR/PO2). The highest α0 value (or, more conservatively, the mean of the three highest values) is designated as α. The same value of α is reached at Pcrit for any MR regardless of previous or subsequent metabolic activity. The MR need not be constant (regulated), standardized or exhibit a clear breakpoint at Pcrit for accurate determination of α. The α-method has several advantages over Pcrit determination and non-linear analyses, including: (1) less ambiguity and greater accuracy, (2) fewer constraints in respirometry methodology and analysis, and (3) greater predictive power and ecological and physiological insight. Across the species evaluated here, α values are correlated with MR, but not Pcrit. Rather than an index of hypoxia tolerance, Pcrit is a reflection of α, which evolves to support maximum energy demands and aerobic scope at the prevailing temperature and oxygen level.This project was supported by National Oceanic and Atmospheric Administration grants NA18NOS4780167 and NA17OAR4310081 and National Science Foundation grant OCE-1459243 to B.A.S., the Jack and Katharine Ann Lake Fellowship to A.A., the Anne and Werner Von Rosenstiel Fellowship and Garrels Memorial Endowed Fellowship to A.W.T., the Hogarth Fellowship to C.J.W., the Southern Kingfish Association Fellowship to A.L.B., and a National Science Foundation postdoctoral fellowship (DBI-1907197) to M.A.B.2022-04-3

Climate Change and invasibility of the Antarctic benthos

Benthic communities living in shallow-shelf habitats in Antarctica (<100-m depth) are archaic in their structure and function. Modern predators, including fast-moving, durophagous (skeleton-crushing) bony fish, sharks, and crabs, are rare or absent; slow-moving invertebrates are the top predators; and epifaunal suspension feeders dominate many soft substratum communities. Cooling temperatures beginning in the late Eocene excluded durophagous predators, ultimately resulting in the endemic living fauna and its unique food-web structure. Although the Southern Ocean is oceanographically isolated, the barriers to biological invasion are primarily physiological rather than geographic. Cold temperatures impose limits to performance that exclude modern predators. Global warming is now removing those physiological barriers, and crabs are reinvading Antarctica. As sea temperatures continue to rise, the invasion of durophagous predators will modernize the shelf benthos and erode the indigenous character of marine life in Antarctica

Metabolic suppression in thecosomatous pteropods as an effect of low temperature and hypoxia in the eastern tropical North Pacific

Author Posting. © The Author(s), 2011. This is the author's version of the work. It is posted here by permission of Springer for personal use, not for redistribution. The definitive version was published in Marine Biology 159 (2012): 1955-1967, doi:10.1007/s00227-012-1982-x.Many pteropod species in the eastern tropical north Pacific Ocean migrate vertically each day, transporting organic matter and respiratory carbon below the thermocline. These migrations take species into cold (15-10ºC) hypoxic water (< 20 µmol O2 kg-1) at depth. We measured the vertical distribution, oxygen consumption and ammonia excretion for seven species of pteropod, some of which migrate and some which remain in oxygenated surface waters throughout the day. Within the upper 200 meters of the water column, changes in water temperature result in a ~60-75% reduction in respiration for most species. All three species tested under hypoxic conditions responded to low O2 with an additional ~35-50% reduction in respiratory rate. Combined, low temperature and hypoxia suppress the metabolic rate of pteropods by ~80-90%. These results shed light on the ways in which expanding regions of hypoxia and surface ocean warming may impact pelagic ecology.This work was funded by National Science Foundation grants to K. Wishner and B. Seibel (OCE – 0526502 and OCE – 0851043) and to K. Daly (OCE – 0526545), the University of Rhode Island, and the Rhode Island Experimental Program to Stimulate Competitive Research Fellowship program.2013-06-3